I^Bl / WHO) Woods M*rb,e Bfoloeic, :** U MA /n ""■■' '-''Jivafory OoBanographJc [tftution JOURNAL OF SHELLFISH RESEARCH VOLUME 17, NUMBER 1 JUNE 1998 The Journal of Shellfish Research (formerly Proceedings of the National Shellfisheries Association ) is the official publication of the National Shellfisheries Association Editor Dr. Sandra E. Shumway Natural Science Division Southampton College, Long Island University Southampton, NY 11968 Dr. Standish K. Allen, Jr. (1998) School of Marine Science Virginia Institute of Marine Science Gloucester Point, VA 23062-1 1346 Dr. Peter Beninger (1999) Laboratoire de Biologie Marine Faculte des Sciences Universite de Nantes BP 92208 44322 Nantes Cedex 3 France Dr. Andrew Boghen (1999) Department of Biology University of Moncton Moncton, New Brunswick Canada El A 3E9 Dr. Neil Bourne (1999) Fisheries and Oceans Pacific Biological Station Nanaimo, British Columbia Canada V9R 5K6 Dr. Andrew Brand (1999) University of Liverpool Marine Biological Station Port Erin, Isle of Man Dr. Eugene Burreson (1999) Virginia Institute of Marine Science Gloucester Point, Virginia 23062 Dr. Peter Cook (1998) Department of Zoology University of Cape Town Rondebosch 7700 Cape Town, South Africa EDITORIAL BOARD Dr. Simon Cragg (1998) Institute of Marine Sciences University of Portsmouth Ferry Road Portsmouth P04 9LY United Kingdom Dr. Leroy Creswell (1999) Harbor Branch Oceanographic Institute US Highway 1 North Fort Pierce, Florida 34946 Dr. Lou D'Abramo (1998) Mississippi State University Dept of Wildlife and Fisheries Box 9690 Mississippi State, Mississippi 39762 Dr. Ralph Elston (1999) Battelle Northwest Marine Sciences Laboratory 439 West Sequim Bay Road Sequim, Washington 98382 Dr. Susan Ford (1998) Rutgers University Haskin Laboratory for Shellfish Research P.O. Box 687 Port Norris, New Jersey 08349 Dr. Raymond Grizzle (1999) Randall Environmental Studies Center Taylor University Upland, Indiana 46989 Dr. Robert E. Hillman (1998) Battelle Ocean Sciences New England Marine Research Laboratory Duxbury, Massachusetts 02332 Dr. Mark Luckenbach (1999) Virginia Institute of Marine Science Wachapreague, Virginia 23480 Dr. Bruce MacDonald (1997) Department of Biology University of New Brunswick P.O. Box 5050 Saint John, New Brunswick Canada E2L 4L5 Dr. Roger Mann (1998) Virginia Institute of Marine Science Gloucester Point, Virginia 23062 Dr. Islay D. Marsden (1998) Department of Zoology Canterbury University Christchurch, New Zealand Dr. Kennedy Paynter (1998) 1200 Zoology Psychology Building College Park, Maryland 20742-4415 Dr. Michael A. Rice (1998) Dept. of Fisheries, Animal & Veterinary Science The University of Rhode Island Kingston. Rhode Island 02881 Dr. Tom Soniat (1998) Biology Department Nicholls State University Thibodaux, Louisiana 70310 Susan Waddy (1998) Biological Station St. Andrews, New Brunswick Canada, EOG 2X0 Dr. Gary Wikfors (1998) NOAA/NMFS Rogers Avenue Milford, Connecticut 06460 Journal of Shellfish Research Volume 17, Number 1 ISSN: 00775711 June 1998 JcniriHil of Slu'llfish Keseanh. Vol. 17, No. I. 1-2, 1998. SHELLFISH MARICULTURE IN THE BENGUELA SYSTEM: Results of a Cooperative Project To Determine Carrying Capacity of Saldanha Bay Mussel Culture SPONSORED BY SEA FISHERIES RESEARCH INSTITUTE RHODES UNIVERSITY UNIVERSITY OF CAPE TOWN EDITED BY PETER COOK Zoology Department University of Cape Town Rondebosch. South Africa SHELLFISH MARICULTURE IN THE BENGUELA SYSTEM PETER COOK' AND JON GRANT" ' Zoology Department University of Cape Town Rondebosch 7700, South Africa 'Department of Oceanography Dalhousie University Halifax. Nova Scotia. Canada Although traditional fisheries decline through overharvesting and environmental degradation, bivalve aquaeulture continues to grow worldwide. In most countries, access to suitable sheltered water sites is a major limiting factor to the growth of aquaculture, there being intense competition for the use of such sites for rec- reational or industrial purposes, hi addition, bivalve aquaculture carries with it an inherent financial risk, and a pressing need exists, therefore, for management of shellfish aquaculture through pre- dictive modeling. It is clear from current research in this area that bivalve aquaculture represents a manipulated oceanographic sys- tem, designed to achieve optimal transfer of primary production (largely phytoplankton) to shellfish production. Because food de- livery to suspension feeders is so dependent on water movement, understanding the interaction between physical oceanography and biological processes is central to the success of management models. The following five articles deal with these aspects in relation to the management of mus.sel culture in Saldanha Bay, South Africa, one of the largest embayments on the country's West Coast, and the most important mariculture site in the country. There are few protected bays on the South African coastline, and it is not sur- prising, therefore, that Saldanha is a multiple-use bay, providing for recreation, tourism, fishing, fish processing, ore transport, and aquaculture. This multiple use requires optimal provision of water access and preservation of water quality. Saldanha Bay is highly valued as an aquaculture site for the mussel Mytilus galloproviiicialis. The Benguela upwelling system fuels rich primary production in the bay, which allows growout of mussels in less than I year. Upwelling coasts are well known for their productive shellfish culture, the Spanish rias being a prime example. Worldwide experience has shown, however, that over- stocking of bays with cultured bivalves can lead to reduced growth rate, increased mortality, and negative effects from biodeposition. As greater demands are placed on Saldanha Bay for increased access to mussel culture sites, it will become increasingly impor- tant to predict what effects this could have. As the lead agency respon.sible for regulation of culture in ihe bay. the Sea Fisheries Research Institute (SFRI) sought to determine the mussel culture density that could be sustained by new primary production in Saldanha Bay. In order to more fully understand the Saldanha Bay ecosystem and its relationship to physical forcing from the shelf, an extensive study was undertaken by SFRI in collaboration with Rhodes Uni- versity and the University of Cape Town. An instrumented buoy was placed into the culture area in the inner part of the bay, and this was supplemented by baywide water samples and other hy- drographic and biological measurements, carried out on the scale of the whole bay. individual farms, and individual mussel rafts. In the articles that follow. Monteiro et al. examine the upwelled input of nitrate to the bay and its forcing of primary production, based on temperature and nutrient measurements. Pitcher and Calder use direct measurements of chlorophyll and primary pro- duction to relate new to total production and to quantify potential food for mussels and its spatial distribution in the bay. Within the scale of an individual farm. Boyd and Heasman determine the frictional effect of mussel rafts on waterflow through them, whereas Heasman et al. examine seston removal by mussel sus- pension feeding and its effect on growth. The latter two articles thus both consider Ihe effects of local scale phenomena on the delivery of food from the larger Saldanha Bay system. Finally. Grant et al. calculate a carbon budget for consumption of new production in the bay at both far and bay scales. Several features of the approaches taken in this study are unique. First, an emphasis on new production rather than total primary production considers shellfish harvest as a form of export production that can be removed without running down nutrient recycling in the bay. Second, it is rare that such a strong physical oceanographic effort has been directed toward studies of bivalve growth and carrying capacity. Third, production and consumption have been examined on several scales including bay. farm, and raft. Together, these articles are a significant contribution to aqua- culture management based on the mechanisms and modeling of an entire oceanographic system. Joiiriwl of Shellfish Research. Vol. 17. No. 1. .1-13. 1998. SHELLFISH MARICULTURE IN THE BENGUELA SYSTEM: ESTIMATES OF NITROGEN-DRIVEN NEW PRODUCTION IN SALDANHA BAY USING TWO PHYSICAL MODELS P. M. S. iMONTEIRO,' * B. SPOLANDER." G. B. BRl NDRIT," AND G. NELSON' ^Sea Fisheries Research Institute Private Bag X2 Roggeluiai 8012. South Africa '^Department of Oceanography Universin.- of Cape Town Rondebosch 7700. South Africa ABSTRACT This study uses two independent physical models, based on entrainment and turbulent diffusion, to estimate nitrate- driven new production rates in Saldanha Bay. South Africa. The t» o modelmg approaches use yearlong w ind and therinistor chain data sets that spanned a coinplete upwelling season in the southern Benguela System. The nitrate tlux estimates from the two approaches were found to be in good agreement where the entramment-based value was 9.40 mmol of N nr-d"' and the turbulent diffusion-based value was 6.47 mmol of N m"-d"'. This provided a mean value of 7.94 mmol of N m"-d"' which converts to a carbon-based new production estimate of 0.63 g of C nr-d"'. The resulting F ratio of 0.19 is in close agreement with average 0.2 for the southern Benguela System. The estimates of new production driven by the natural NOj flux were also compared with potential contributions from anthropogenic sources. Only one anthropogenic input, from a pelagic fish factory, was found to be numerically equivalent to the natural flux (8.24 mmol m"^d"'). However, the biogeocheinical pathway for the regeneration of this fish waste flux precluded it from having more than a 209c effect in the overall estimate of new production in the bay. It was concluded that the nitrate flux that drives new production in Saldanha Bay is limited principally by physical factors, namely thermocline dynamics. The estimate of new- production provides an upper limit to the carrying capacity, the real value of which is subject to better understanding of shelf-bay coupling dynamics. KEY WORDS: Shellfish, mariculture. new-production, entrainment. diffusion, Saldanha, Benguela INTRODUCTION Saldanha Bay is one of the few inshore marine systems along the South African coastline suitable for large-scale and economi- cally viable shellfish mariculture. It combines a number of suitable attributes, which include inter alia, relative protection from the high-energy coastline (Shannon and Stander 1977. Weeks et al. 1991). a physical coupling with the highly productive southein Benguela upwelling system (Shannon and Stander 1977. Monteiro and Brundrit 1990) and a high internal rate of phytoplankton pro- ductivity (Pitcher and Calder 1998). These factors give rise to some of the highest recorded growth rates (50 mm in 6 mo) for the mussel Mytilus galloprovijicialis. which forms the anchor species for the small (production -3.000 tons in 1995) but fast-growing mussel-farming sector (Hecht and Britz 1993. Heasman 1996). The scientific program, of which this study is part, aimed to assess and understand the mechanistic basis of the carrying capacity of Saldanha Bay for mussel farming (Monteiro et al. 1996). For the purposes of this study, carrying capacity is defined as the mussel biomass that could be held in the system without affecting the existing high mussel growth rates. This approach focuses the effort on rates and mechanisms of food supply in the form of seston and phytoplankton as a means to reach a bottom-up estimate of carry- ing capacity (Newell and Shumway 1993. Grant et al. 1998). Two physically driven mechanisms were initially suggested to drive food supply to mussels in Saldanha Bay: • Phytoplankton biomass and seston. including kelp detritus *Present address: Council for Scientific and Industrial Research, P.O. Box 320. Stellenbosch 7599, South Africa. E-mail: pmonteir@csir.co.za could be imported into the bay by the advection of surface water from the highls productive coastal shelf environment (Brown and Henry 1985, Brown et al. 1990), and • Phytoplankton biomass w ithin the bay could also grow from an external source of nitrogen that drives new production (Dugdale and Goering 1967, Eppley and Peterson 1979). The extent to which food supply is regulated by one or both op- tions is clearly dependent on the physical processes that drive exchange between the bay and the coast, as well as the rate of supply of external nitrogen that governs new production w ithin the bay. The physical transport of water between Saldanha Bay and the adjacent coastal system is hypothesized to be driven by synoptic scale oscillations. Stratification dynamics appear to be remotely forced by subsurface inflows and outflows of cold (9-1 TC) up- welled water on time scales of 6-10 days (Monteiro et al. 1996). During the active phase of these oscillations, the warm and nutri- ent-depleted surface layer in the bay (22°C > t > 15'^C) is undercut by a subsurface inflow of NO^-rich (-20 |jlM) upwelled water, resulting in the formation of strongly stratified conditions within the bay. Conversely, duiing the relaxation phase, there is an out- flow of the cold subsurface water, and the bay water column acquires an isothennal nutrient-depleted character. Phytoplankton, which are mostly restricted to the surface layer, depend on the NOJ inputs through the thermocline during the active phases of the cycle to drive new production and an associated increase in bio- mass (Pitcher and Calder 1998). Such a reciprocating inflow -outflow system should, depending on the degree of mixing with bay water, serve both to import coastal biomass into the bay (during the relaxation phase) and to MONTEIRO ET AL. supply NO3 to drive new production (during the active phase). This synergism could have a positive effect on the carrying ca- pacity of the system. However, the first option has been largely discounted because recent understanding of shelf-bay exchange arising from the incorporation of an entrainment mechanism pre- dicts that, on the event scale (6-10 days), the net transport of water in the surface layer is out of Saldanha Bay (Spolander 1996). The corresponding net transport of subsurface water is from the coast into Saldanha Bay (Spolander 1996). Furthermore, the very low incidence (three occurrences in 20 y) of otherwise ubiquitous coastal toxic phytoplankton blooms within Saldanha Bay (Pitcher et al. 1996) provides additional support for the notion that the net outflow of surface water exists and provides an effective barrier for the import of coastal production in the surface layer. This prediction suggests that bay-scale new production alone holds the key to the carrying capacity of Saldanha Bay for mussel farming. Linking the carrying capacity assessment to new produc- tion rather than biomass or total production also ensures that the phytoplankton biomass within the bay will be sustainably used, hence minimizing potential risks of ecosystem modification (As- mus and Asmus 1993, Dame 1993. Dankers 1993). The Benguela upwelling system is a nitrogen-limited ecosys- tem (Andrews and Mulchings 1980), where new production is driven by NO7 advected to the surface by pulsed events of equa- torward winds (Hutchings et al. 1993). These events give rise to large postupwelling phytoplankton blooms, where chlorophyll concentrations commonly reach 10-30 mg of chlorophyll m"' (Brown and Hutchings 1987). The main difference between Saldanha Bay and the coastal system is that in the former, the NOj-rich cold water wedge never outcrops. This means that NO3 supply to drive new production in the surface layer has to be injected through the therniocline (Anderson et al. 1995, Monteiro et al. 1996). Saldanha Bay is similarly NO3 limited, as shown by the subsurface biomass maxima that develop at or above the ther- mocline (Pitcher and Calder 1998). The approach of this study is based on two hypotheses: • that nitrogen (natural and anthropogenio-driven new produc- tion within Saldanha Bay is the key factor limiting the carrying capacity for large-scale mussle farming. • that the physical characteristics of Saldanha Bay are largely driven by the dynamics of the adjacent southern Benguela Sys- tem and that, by extension, estimated new production rates within the bay will be similar to ineasured rates outside the southern Benguela System. The objective is to define and quantify all of the potential sources of "new" nitrogen. Results of two physical models are used to quantify the natural NO,-driven new prodtictioii. These are com- pared with other potential contributions Irom anthropogenic inputs to provide an overall magnitude anil a mechanistic basis for new production in Saldanha Bay. MKTIIOnOI OGY Study Area Saldanha Bay is a coastal embayment located in the southern Benguela System (33'S, 18"E) approximately 100 km north of Cape Town. Its physiography was altered in 1975 by the construc- tion of a 4-km-long jetty and the Marcus Island causeway (Weeks et al. 1990) (Fig. 1 ). These modifications divided the bay into two parts that ha\e been connnonly referred to as Small Bay (14.3 x 10'' m-) and Big Bay (42.2 x 10" m") (Fig. 1). Saldanha Bay is linked to the Benguela System to the west and a large, shallow tidal lagoon (Langebaan Lagoon) to the south. The boundaries between Saldanha Bay and adjacent systems ai'e marked in Figure 1 . Iiipiil Data The two approaches used to calculate the natural nitrate tlux into the surface layer in Saldanha Bay make use of a yearlong time series spanning the upwelling season of 1994 to 1995 in the south- ern Benguela System. The first approach is via a process model of the entrainment that occurs during an upwelling event. It requires information about the strength of the wind event and the mean stratification. The second approach, via a turbulent eddy diffusion model, makes use of an hourly thermistor chaui temperature record to quantify changing stratification strength. Wind Data Wind data for the period from August 1 , 1994 to May 31 . 1995, were obtained from a record maintained by the lighthouse keepers at Cape Columbine, approximately 50 km north of Saldanha Bay. Readings were taken intermittently on the hour, and these readings were used to calculate a mean wind speed for each day. The temporal distribution of the recording can be seen in Figure 2. which shows that the overwhelming majority of the readings were taken between 3:00 and 7:00 a.m. and between 3:00 and 7:00 p.m. The wind readings, therefore, probably incorporate a component of the land-sea breeze cycle that is not properly resolved. The data are, however, likely to be adequate for bulk estimates. Lack of data made it impossible to calculate a mean on 10 occasions, with one instance of no data for two consecutive days. Linear interpolation was used to fill in these data gaps. The wind vectors were then rotated through an angle of -35° in order to align them with the general orientatiiin of the coastline, which is also the axis along which the winds tend to be polarized. Distinct wind events were defined as beginning each lime the longshore wind component started blowing in an upwelling-faxorable direction (that is. from the south), and the events ended when the longshore wind reversed direction. Wind speed was converted into a wind stress according to the formula of Large and Pond ( 1981 ), and a mean wind stress was then calculated for each wind event (Fig. 3 1. Thermistor Chain Data The Ihermisior chain record was obtained from an environmen- tal monitoring .station located at MSI (Fig. 1), where the water column was between 1 I and 1 2 m deep, and provided hourly records at 1-m intervals over the whole water column. The equip- ment was serviced at 10- to 14-day intervals when the data were also downloaded from the data logger. The period covered by the data set is from .luly 1994 to .luiic U)95. which spans the 1994 to 1995 upwelling season in the southern Benguela System (August 1994 to May 1995). CALCULATIONS Entrainment Model .\pproaeh The simplest model that captures the primary physical pro- cesses that occur during an upwelling event consists i)f a two-layer llat-botlomed ocean that is bounded on one side by an infinitely Nitrogen-Driven New Production s 33° MSO SALDANHA PRj- SSF Small Bay MSI Marcus Is 3; # /f Big Bay Malgas Is, Southern Benguela Upwelling System 56' C~' Jutten Is Peninsula 58' Langebaan Lagoon 18 Figure 1. Map showing the spatial layout of Saldanha Bay comprising the two subsections of Big and Small Bays artificially separated by the ore jettv. a western boundary to the coastal zone at the narrows between Marcus Island and the peninsula (A), and a southern boundary into Langebaan Lagoon (B(. Also shown are the positions of the monitoring station (MSI), the Pelagic Fish Factory (PFF), the Stock Fish Factory (SFF), and the Municipal Sewage Outflow (MSO). long coastline. The two layers slide freely over one another and are separated by a strong-density discontinuity such as a themiocline. When an upwelling-favorable wind blows over this ocean, the mean Ekman transport in the upper layer is directed at right angles away from the coast. This offshore flow decreases exponentially toward zero as the coast is approached, because no flow is possible across the coastal boundary. In order to conserve mass, there is a compensatory onshore flow in the lower layer of the water column, and an upwelling of the therniocline that separates the two layers. Thermocline upwelling is most vigorous at the coast, resulting in a thermocline that deepens exponentially away from the coast with pressure gradients that drive a vertically sheared longshore flow. If there were no mixing, this longshore flow would steadily increase toward infinity, and the thermocline would eventually reach the surface of the ocean. However, the vertical shears accompanying the upwelling process result in entrainment of water across the thermocline to prevent outcropping. Pollard et al. ( 1973). in a model of the upper-layer dynamics of the open ocean, applied the idea that vertical entrainment across a density discontinuity (in this instance, a thermocline) is driven by the velocity shear across the thermocline. According to their model, entrainment will occur if turbulence induced by velocity shear can overcome turbulence-suppressing effects of stable strati- fication. A measure of these effects of shear and stratification is the Richardson number: gH, Ap P (Au)' + (A\ )- (1) where R, is the Richardson number, g is the gravitational constant, H, is the depth of the upper mixed layer. Ap is the density dis- continuity across the thennocline, p is the typical density of sea- water in the system, and u and v represent the vector velocity shear across the thermocline. If this Richardson number reaches a critical value (a value of I in the model of Pollard et al. 1 1973], water will be entrained across the thermocline into the upper layers of the water column. This has the effect of increasing the stratification terms (the numerator of the Richardson number) and decreasing the velocity shear, thereby increasing the Richardson number away from its critical value. The model of Pollard et al. (1973) assuines, therefore, that entrainment will act to ensure that the Richardson number is never reduced below its critical value. For instance, if the shear across the ther- mocline increases, the rate of entrainment must increase in order to prevent the Richardson number from becoming subcritical. In an upwelling situation, the Richardson number will be infinitely large at the instant that the wind is switched on. and there will be no entrainment. Thereafter, the steady upwelling of the thermocline will reduce the numerator of the Richardson number at the same time that the establishment of the offshore and longshore shear increases the denominator of the Richardson number. Upwelling will thus reduce the Richardson number towards its critical value, when entrainment will begin, and entrainment will proceed at a rate that ensures that the Richardson number does not become subcritical. A simple two-dimensional model of entrainment during an up- welling event was presented by .Spolander ( 1996). This model can be used to investigate the entrainment that occurs during a wind event of constant intensity blowing parallel to a straight coastline. MONTEIRO ET AL. Temporal Distribution of Wind Records Turbulent Diffusion Model Approach 100 90 80 70 60 50 40 30 20 10 nil.. Hour of the Day Figure 2. The temporal distribution of wind recordings made at Cape Columbine represented as a percentage of the total possible number of recordings (350). Normally, coastlines are not straight, and upvvelling is very defi- nitely a three-dimensional process. The two-dimensional model should, however, capture the fundamental physics of entrainmeni during an upwelling event and, with suitable tuning, can be used to provide a bulk estimate of the tlux of nutrient across the ther- mocline in Saldanha Bay. The events that were identified in the wind record were used as input for this model, together with ap- proximations concerning the stratification of Saldanha Bay. It was assumed that the undisturbed depth of the upper layer in the bay is 15 m, an estimate that is based on observations that the cold lower layer is present in the bay during the relaxation phases of the upwelling cycle at a depth greater than the thermistor chain data presented here. The seasonal variation in the teinperature of the two layers can be inferred from Figures 6-9. The temperature of the upper layer increases from approximately 14°C in July to ap- proximately 20°C in January. At the same lime, the lower-layer temperature falls from about MT to approximately \\"C This seasonal variation in temperature was crudely simulated by func- tions of the form: tunper= l4 + 6sin ttT 365 . ttT tiower= l4--'^sin ^ ^^^^ (2) (3) where t„p|,^,^ and t|„^„^ are the upper- and lower-layer temperatures, respectively, and where 7' is time in days Irom July 1. Using these inputs, the model was able to produce estimates of the entrainment that occurred during each of the wind events, as well as an estimate of the total amount of entrainment thai would have occurred during the l'W4 to 1995 season along a straight coastline. This value can then be tuncil lo a hulk \.ikic appropriate for Saldanha Bay. The turbulent diffusion model used in this study was adopted from the approach of King and Devol (1979) approach. This method has two main assumptions; • first, that the NOT eddy diffusion coefficient (K^^^). which is difficult to measure, can be approximated by the thermal diffu- sion coefficient (K,,), which can be estimated relatively easily from high-resolution thermistor chain data. This is supported by the close similarity of temperature and nitrate profiles at the monitoring station (see Figures 8 and 9 in Pitcher and Calder submitted). • second, that advective heat tlux terms are small compared with the vertical seasonal fluxes. The estimated magnitude of the advective heat flux is 16-32 W m"- (velocity-0. 1 m s"' and 2°C horizontal temperature gradient across the bay), about 10% of the insolation heat tlux (150-3.50 W nr") (Guastella 1992) and 15-209f of the entrainment heat loss ( 140 W m"") (Spolander 1996). This estimate of the advective heat flux is thought to be an upper limit because the chosen horizontal temperature gradient is con- servative compared with the typical 0.5-1 °C. This gradient typi- cally characterizes the difference in the mean temperatures of the surface layers in Big Bay and Small Bay (Monteiro et al. 1990). Horizontal heat advection is therefore likely to be a minor source of uncertainty in the estimates below. Calculating the Thermal Diffusion Coefficient (K„) The thermal diffusion coefficient (K^, ) is calculated by the expression: Longshore Wind Stress 025 02 15 1 05 -005 -0 1 -0.15 1 ! iM 1 ' i'\-'' 1 :;'•;;•; i. !; « ( ; ■ 1 -0 2 -025 cQ S C O) "^ ^ ID O) - ^ ID CO Days Figure 3. The longshore wind .stress (units, N m"'') record from Augu.sl 1, WiA to May 31. m'>.=;. The record is divided up into distinct wind events lluil each ha\c ii mean wind stress. Ihe dolled line Is liic actual dail\ Muaii wind stress, and Hie solid line represents Ihe mean stress of wind c\enls thai tterc used in the entrainmeni model. NlTRf)GEN-DRIVEN Nf.W PRODUCTION K„ = - Cp- P dt dZ (4) Nitrate - Temperature Relationship for the Benguela System where Q, is the average net heat flux (W nr"), dt/dz Is the tem- perature gradient at the thennocUne inaxiinuni. and C^, and p are the specific heat (4, ISO J Kg^"'C"') and average density of sea- water ( 1.025 Kg m"') respectively. The heat flux term was estimated by a regional climatology approach based on a heat budget study in the vicinity of Saldanha Bay (Guastella 1992) and a 13-y data set of solar radiation along the Benguela System coastline (A. Tegen unpubl. data). The esti- mated heat fluxes for each of the four periods considered by this study are summarized in Table 1. These four periods span the upwelling season in the southern Benguela System and exclude the two full winter months (June and July) when upwelling ceases. The u.se of steady-state heat flux values makes the assumption that short-term variations of heat flux balance each other out to an average close to the chosen fluxes. The temperature gradient term (dl/dZ) was obtained from the thermistor chain data by finding the maximum of the derivative of a spline function through each of the hourly profiles. This provided a more reliable measure of the stratification maximum within the thermocline rather than a bulk gradient through the thermocline region. By using these inputs, hourly values of thermal turbulent diffusion coefficient K.,, can be calculated and used as the input to calculate the nitrate flux. Calculating the NO3 Concentrations From Temperature Data The lack of high temporal resolution NO3 values corresponding to the thermistor chain data set made it necessary to estimate nitrate concentrations from a relationship between temperature and NO3 concentration for the Benguela System (Fig. 4) (Monteiro 1996). The relationship is defined by; |NO;] = -2.73t + 44.27 (5) where r = 0.72 (n = 1.920) and nitrate concentrations are (j.mol L"'. This functional relationship was used to convert the thermis- tor chain temperature data to corresponding nitrate concentration values. The nitrate flux Qf^ was calculated by the expression (King and Devol 1979): K^ dNO, dZ (6) where K^,^; is the NO^ eddy diffusion coefficient and dNO^/dZ is the nitracline maximum, calculated from the derivative maximum of a spline function through the hourly NO3 concentration profiles. The use of eq. 6 assumes that K^^ = K^, (King and Devol 1979). This assumption implies that the rate of upward NO^ transport is TABLE 1. The estimated average net heat fluxes (\V m ') over the four periods of the upwelling season at the latitude of Saldanha Bay (from Guastella 1992). Spring (August to Seplemher) Summer I (October to December) Summer II (January to March) Autumn (April to May) no 170 130 90 Nilfificalion Input 0) 2000 n Z 15 00 10 00 Temperature Figure 4. .A relationship between temperature and nitrate concentra- tion for the whole Benguela System. It allows high-resolution tempera- ture data to be used to generate equivalent nitrate concentrations. approximated by the rate of downward heat transport. Because this could not be verified specifically in Saldanha Bay. the predicted NO7 flux from the turbulent diffusion approach was compared with that nidependently calculated with the entrainment model. The final output of both approaches was the nitrate flux in mmol m~"d"' which was then used to estimate the carbon based new production, assuming a Redfield ratio of 6.6 for carboninitro- gen uptake stoichiometry (Redfield et al. 1963). RESULTS Results From the Entrainment Model Approach Tuning the two-dimensional entrainment model to give an ap- propriate entrainment value for Saldanha Bay can be done by deciding what length of straight coastline is represented by the bay. An appropriate scale would appear to be the width of the channel connecting the bay to the upwelling system, which is approxi- mately 2,500 m. This length scale is undoubtedly correct to within a factor of two, which is sufficient for a bulk estimate. The en- trainment occurring in the 30 wind events identified in the wind record were, therefore, spatially integrated for 2.500 m in a long- shore direction and for 6,000 m in the offshore direction, which is the length of the channel connecting the bay to the shelf. Over the 10-month upwelling season, the total volume of water entrained in this area was 6.40 x 10'' m\ This implies a daily mean entrainment rate of 2.13 x 10' m-'day"'. The entrainment will not just occur over the area of the channel, however, but will be spread out over the entire area of the bay where the warm surface layer overlies a cold bottom layer. This area is approximately 44.8 x 10*" m"^. The mean entrainment flux for the bay is thus 0.47 m day"'. This value is one-third of the entrainment flux that would be found in the shelf upwelling system. Examination of Figures 5a-8a shows that the mean temperature difference between the upper and lower layers for the 10-nionth upwelling season is approximately 6°C. The mean entrainment flux is thus equivalent to a mean entrainment heat flux into the upper layer of the bay of -140 W M"". This is comparable in magnitude with the seasonal heat fluxes found by Guastella ( 1992) in St. Helena Bay. maintaining a MONTEIRO ET AL. Thermistor Chain Temperatures: 1-Jul-94 - 20-Sep-94 18 00 I 16 00 re 0} Q. i 14 00 (- 12 00 Surface /ifiTf SV< Jft% "^ J^ ■.i/: , '"if] v 1 Event 1 V 5 6 Time: weeks (mmddhh) Time Series of Stratification IVIaximum 1-Jul-94-20-Sep-94 9 00 8 00 7 00 5 00 5 00 Event 1 Start of upwelling season Winter weak strat Time: weelfs (mmddhh) Figure 5. Time series plots of (a) the surface and bottom temperature records and (f)l the correspondinjj stralillcallon (Strat.) maximum (Max.) for the first quarter of the 1944 to 1W5 upwelling year in Saldanha Bay. Each inflow of cold water is numbered, and Event 1 marks the beginning of the upwelling season, mmddhh: ni-month; d-day: h-hour. balanced heat bu(Jget for the upwelling season and increasing con- fidence in the use of the dimensions of the channel as the appro- priate scales for tuning the entrainmenl niodcl. The entrainment flux can be converted, in a siinplified way, into a nutrient tlux by assuming that biological productivity in the upper layers of the bay maintains a negligible cimcentration of nutrients in that layer. If it is further assumed that the concentration of nitrate in the cold lower layer is reasonably constant at INO, | = 20 |jLmol L ', then the mean entrainment flux converts into a mean nitrate tlux of 9.4 mmol of N m'" day"'. Results From the Tiirbiileiil Difjusion Miidel Approach within the thermocline. The four plots correspond to four conve- niently defined phases of the upwelling year: Winter to spring, summer I, summer II. and autumn to winter. Missing data mostly correspond to the I- to 3-day servicing and calibration periods. There is a larger gap in the surface record spanning the month of January 1995, when the surface thermistor failed. The same gap is not reflected in the stratification time series because the spline function can still use the remaining points, and the thermocline is normally not shallower than .S m. The main features of the time series, below, provide the nec- essary background of the processes that modulate NO;^ supply to the surface layer in Saldanha Bay. The upwelling season extends from August to May and is characterized by periodic inflows of cold NO^-rich water. The temperature record shows that in accor- dance with the conceptual model formulated by Monteiro et al. (1996), the stratification dynamics of Saldanha Bay during the upwelling sea.son are largely modulated by two forcing processes: \ Thermistor Chain Temperatures: 23-Oct-94 - 31-Dec-94 22 00 - £ 14 00 CM rM CM OJ Time: weeks (mmddhh) Time Series of Stratification Maximum 23-Oct-94-31-Dec-94 Thermistor Chain Data The surface and lO-m-depth hourly records fiom the thermistor chain at the environmental monitoring station in Saldanha Bay are graphically depicted in Figures 6a-9a and span the period between July 1994 and June I99.'i. Also depicted (Figs. 6b-9b) are the corresponding time .series of the stratification maximum (°Cm"') Time: weeks (mmddhh) Figure 6. Time .series plots of (a) the surface and bottom temperature records and (b) the corresponding slratificalicm (.Strat.) maximutii (Max.) for the second i|uarler of the 1W4 to IWS upwelling year in Saldanha Hay. Each inllow of cold water is numbered, and it can be seen that the amplitude of the bottom temperature excursions in- creases as the surface layer warms up into midsummer. Nitrogen-Driven New Production 9 Thermistor Chain Temperatures: 1-Jan-95 - 31-Mar-95 Time: weeks (mmddhh) Time Series of Stratification Maximum 1-Jan-95-31-Mar-95 period oscillations that characterize the iipweMing season. The transition from winter to upweliing season is evident in the stratification maximum time series (Fig. 5b). • In this early phase of the upweliing season, the period for the event cycle is 9.3 days per event, resulting in a total of six events between August and September. • During this phase, the net solar heat tlux has not significantly warmed the surface layer and stratification is largely governed by cold water inflows. Summer I Phase (Fig. 6al • Increased net solar heat flux (170 W m"") and intensity of upweliing water inflows increa.se the amplitude (~IO°C) of the temperature oscillations at 10 m, which is also reflected by changes in the magnitude and variability of the stratification maximum (6-7°C m"') (Fig. 6b). • This period was characterized by 13 events (Events 7-19) and an event period of 5.4 days. There are also a number of higher frequency peaks that could be driven by tidal ( 12 h) and inertial (-22 h at this latitude) oscillations. Thermistor Chain Temperatures; 8-Apr-95 - 30-Jun-95 Time: weeks (mmddhiti) Figure 7. Time series plots of (a) the surface and bottom temperature records and )b) tlie corresponding stratification (Strat.) maximum (Max.) for the third quarter of the 1994 to 1995 up\velMng year in Saldanha Ba>. Each infioiv of cold water is numbered, and the ampli- tude of the bottom temperature excursions begins to decrease « ith the end of summer, mmddhh: m-month; d-day; h-hour. • synoptic scale events (6- to 10-day period) that drive subsurface inflows of cold (9-1 r"C) upwelled water into the bay. • seasonal scale changes to the solar heat flux that affects surface water temperatures. Stratification characteristics are governed by the relative intensity of these two forcing factors at different times of the year. The bay water column oscillates between a strongly stratified (active phase) condition (Figs. 6a-9a), and passive phases when the external forcing relaxes, the cold water flows out. and the whole water column acquires the characteristics of the warm surface layer. The teiTiperature time series plot also provide the following additional insights into the physical characteristics of Saldanha Bay; Winter to Spring Phase (Fig. 5a) • The boundary between the winter of 1994 and the start of the 1994 to 1995 upweliing season is given by the first strong "active" event (Event 1 ). This event ends the very weakly strati- fied (13-1 5°C; stratification < 5 00 S 15 4 00 5 3 00 l\ UHiJ liJLjtU MmlJM Time: weeks (mmddhh) Figure 8. Time series plots of (a) the surface and bottom temperature records and (b) the corresponding stratification maximum for the fourth quarter of the 1994 to 1995 upweliing year in Saldanha Bay. Each inflow of cold water is numbered, and Event 40 marks the end of the 1994 to 1995 upweliing season in Saldanha Bay. 10 MONTEIRO ET AL. Plot of NH4 (uM) with depth in Saldanha Bay 3 4 NH4Concn(i.M| Figure 9. A water column protlle showing the changes in NHj con- centration (pmol Ir'l on either side of the therniocline in Small Bay. The sample at m is } m helow the surface. Summer II Phase (Fig. 7a) • This part of the time series shows that midsummer conditions persist until late February, when decreasing solar heat flux and upwelling wind stress result in a reduction of the amplitude of the variability and a convergence of the surface and lO-m tem- perature records. This has a coiTesponding effect on the strati- fication maximum (Fig. 7b). which also showed a weakening trend in late March. • Over this period, there were 14 events (Events 20-33) with a period of 7 days. Autumn to Winter Phase (Fig. 8a) The continued reduction in the intensity of the forcing pro- cesses is clearly evident, with surface temperatures dropping to below I5°C and the termination of cold nutrient-rich water inflows after Event 40, which coincided with the end of May. This marks the end of the upwelling season in Saldanha Bay. The subsequent record has typical winter characteristics with a well-mixed water column of 13-14°C. as was earlier observed for July 1994 (Fig. 5a). With the onset of winter, the stratification maximum declined (Fig. 8b) to below 0.2°C m"' after Event 40. This final quarter of the upwelling season was marked by seven events (Events 34^0) over a period of 54 days, conesponding to 7.7 days per event. Natural NO, Flux Modeled by the Turbulent Diffusion Appniaeh Average quarterly and annual NO, fluxes into the surface layer calculated from the thermistor chain data using the approach of King and Devol ( 1979) are summarized in Table 2, where the net heat fluxes are used to calculate K„. The calculations exclude the two winter nonupwelling months (June and July). DISCUSSION Estimating New Production in Saldanha Hay The entrainmcnt model and the lurhulenl dillusion method give average nitrate fluxes over the lO-mo upwelling season of 9.40 mmol of N m^'day"' and 6.47 mmol of N rn "day ', respectively. This agreement to within 30% is remarkable, considering the widely disparate approaches taken to arrive at the estimates. Al- though the two models make use of the same seasonal heat fluxes, their estimates of new production are independently driven by hourly wind records in the case of entraininent and hourly tem- perature profiles in the case of turbulent diffusion. Therefore, any eiTors arising from the two approaches are likely to accumulate independently, making the likelihood of coincidence very small. It inust. of course, be remembered that the 9.40 mmol of N m"'^day~' from the entraininent method is a spatially averaged value over the part of the bay that is stratified. The 6.47 mmol of N m~"day"', however, is a mean value at one particular point in Saldanha Bay. This point should, however, be reasonably repre- sentative of all of the stratified portions of the bay, because of the spatial hoinogeneity in the bay (Pitcher and Calder 1998). A further agreement between the two methods concerns the surface heat flux. The large surface heat flux from the atmosphere to the upper layer of Saldanha Bay would result in far higher equilibrium teinperature for the layer, were it not for the input of cold water across the thermocline. The turbulent diffusion ap- proach makes use of this fact by balancing the atmospheric heat flux with the flux of cold (and nitrogen-rich) lower-layer water. The entrainment model takes a different approach by considering the physics that causes the cold lower-layer water to be entrained into the upper layer. Encouragingly, the entrainment that occurs over the area perpendicular to the channel in Saldanha Bay results in a mean net heat flux of -140 W m^~, which is very close to balancing the 130 W m"" seasonally weighted average flux from the atmosphere used in the turbulent diffusion approach. A par- ticular advantage of using these two different methods to deter- mine the flux of nitrogen into the upper layer is that they depend on diffei-ent data sets. In the case of Saldanha Bay, the wind record is considerably longer than the temperature record from the therm- istor chains. The entrainment model approach may therefore be used to determine the interseasonal range in nitrate flux v\ ithiii the bay. The two approaches provided an average natural NO, flux into Saldanha Bay during the upwelling season of 7.94 mmol of N m""day~'. Assuming that the NO, is completely used to drive new production (Dugdale and Goering 1967. Eppley and Peterson 1979). the annual average caibon-based new production rate is 0.63 g of C nr-day"' (7.94 x 6.6 x 12/1,000 = 0.63). This is calculated al.so assuming that carbon uptake is governed by the Redfield C:N molar stoichiometry of 6.6 (Redfield et al. 1963). Although recenl work has raised some questions about this as- sumption (Monteiro 1996). it is still reasonable to link the Redfield ratio to particulate export production. This is what is consumed by the filter feeders. TABLE 2. Calculated NO7 fluxes (mmol of N m"^day"') across the thermocline o\er (he upwelling season in Saldanha Ray. the quarUrl) and annual mean \alues are shown with the corresponding net heat I1u\ \ulues l\\ m "). Season Quarter Heat NO3 Spring (August 10 September) IK) 6.10 Summer 1 (October to December) 170 S.71 Summer II (January to March) 1 "^0 .'^,.';7 Auliinin (April 10 May) W 4.S.'i Nitrogen-Driven New Production 11 TABLE 3. A comparison of the ne« production and / ratio values obtained from this slud> with a range of values measured hy '"^N uptake from the southern Benguela System. NevN Production f Area (gof C m-day-') Ratio Source Coastal Benguela 0.42 0.24 Probyn et al. in press Agulhas Bank 0.24 0.17 Probvn et al. 1995 St. Helena Buy 0.44 0..32 Waldron and Probyn 1991 Saldanha Bay 0.63 0.19 This study An average estimate of the /ratio for Saldanha Bay in suinmer can be made (eq. 8) (Eppley and Peterson 1979. King 1987) by combining the calculated new production rate value with the av- erage total net production rate (3.40 g of C m^'day"' ) (Pitcher and Calder 1998) obtained from ;;( situ '""C uptake measurements. /ra new production 0.63 0.19 (8) '"•''" total production 3.40 The calculated /' ratio for Saldanha Bay of 0.19 indicates that production is mostly driven by regenerated nitrogen (~809f ). Thus, only -20<7r of the total phytoplankton production is potentially available in a long-term sustainable basis to mussels in the bay. How Realistic Is This Sew Production Estimate? Earlier physical data suggest that physical characteristics in Saldanha Bay are largely driven by coastal dynamics. This would suggest that phytoplankton production characteristics in Saldanha Bay should bear some similarities to the surrounding southern Benguela System. There is good agreement between the calculated new production estimate from Saldanha Bay and //; situ '^N-based measurements from the Benguela System (Table 3). The Saldanha Bay values are the highest in the system, although the correspond- ing/ratio is relatively low. The Agulhas Bank System, like Saldanha Bay. is a stratified environment where new production is driven by NO^ transport across the thermocline, resulting in a subsurface chlorophyll maxi- mum (Probyn et al. 1995). St. Helena Bay is also a largely strati- fied environment but is located in the vicinity of Cape Columbine, one of the major coastal upwelling cells in the southern Benguela System (Waldron and Probyn 1991). Here, a higher/ratio (0.32) has been linked to NO3 supply, attributable to both cross-shelf advection of newly upwelled water and turbulent diffusion across the thermocline (Waldron and Probyn 1991 ). For the inner shelf of the southern Benguela System (32°S). where NOJ from upwelled waters outcrop at the surface, new production rates are higher but the/ratio remains close to 0.2 (Table 3). Low /ratios (0.17-0.32) suggest that in the Benguela System, phytoplankton production is unexpectedly and largely dominated by regenerated production. In this respect, the estimated new production rate and associated / ratio for Saldanha Bay indicate that Saldanha is not significantly different from the surrounding southern Benguela System. We argue that this provides further confidence in our new production estiinate. Nevertheless, the comparison of these values must take into account differing sampling scales. The Benguela System (southern Benguela. Agulhas Bank) values are averages of a few spatially distributed instantaneous ''^N measurements, and the St. Helena Bay samples are an average of a series of four daily samples (Waldron and Probyn 1991 ). By contrast, the Saldanha Bay value is the average of hourly data over a whole upwelling season from a single but spatially representative point. Globally, the disagree- ments in estimates of in situ and bulk measurements of new pro- duction are attributed to the scale mismatch between the two ap- proaches (Piatt et al. 1989). In situ measurements, unless per- formed as a high-resolution time series, could provide results biased toward the stage of the upwelling cycle at which measure- ments are taken. This is particularly important in upwelling sys- tems where the / ratio changes with the nitrate concentration and the stage of the 6- to 10-day upwelling cycle (Probyn 1992). The same difficulties could arise with respect to the use of in situ '""C total production measurements used to calculate the av- erage /"ratio (eq. 8). However, because the '''C average is based on six 10-day field trips over 2 y. where at least three measurements were taken on each field trip (Pitcher and Calder 1998), the tem- poral averaging is likely to be representative for those years and proN'ides some confidence in the estimated /ratio. It should be noted that this new production estimate is likely to be subject to significant interannual (e.g.. El Nino Southern Os- cillation (ENSO)) variability linked to changes in the intensity of remote equatorward winds, which drive shelf scale upwelling, and local winds, which drive entrainment and local stratification dy- namics. The importance of this variability to estimates of carrying capacity should be assessed as a matter of some importance. Other Sources of New Nitrogen in Saldanha Bay In the absence of any significant natural freshwater runoff points into Saldanha Bay. the main anthropogenic nitrogen inputs are the two fish-processing factories and a minor contribution from the treated effluent from the sewage plant (Monteiro et al. 1996). The magnitudes of each of these nitrogen inputs are shown in Table 4. where the natural NO7 flux is also included for compari- son. These data show that the calculated flux from the pelagic fish factory is of the same magnitude as the natural flux; the flux from the stock fish factory is <10% of this magnitude, and the contri- bution from the sewage outflow is insignificant. Given that the main sources of nitrogen loading are located in Small Bay (Fig. 1). these data suggest that this part of the system should manifest the effects of enhanced new production in the form of elevated primary producer biomass relative to Big Bay. A symptom of this enrichment was observed in the summer of 1993 to 1994 in the form of an Ulva bloom under the "■footprint" of the pelagic fish factory plume and the nitrogen source of which was TABLE 4. Natural and anthropogenic fluxes of nitrogen into Saldanha Bay. The latter fluxes are calculated assuming a distribution over the whole bay area of 56.5 km"; it shows that the nitrogen flux from the pelagic fish factory waste is comparable to the natural NOJ flux but that other potential inputs are small. Nitrogen Flux Input (mmol m"-day ') Sources Natural 7.94 This study Pelagic Fish Waste 8.24 CSIR 1991 Stock Fish Waste 0.56 Sea Harvest Fishing Co. Sewage 1.2 X K)--* Saldanha Municipality MONTEIRO ET AL. isotopically linked to the same effluent (Anderson et al. 1996, Monteiro et al. in press). The same effect has not been observed in the phytoplankton, where contrary to expectations, the biomass in the surface layer is 10-159r lower in Small Bay than in Big Bay (Pitcher and Calder submitted). This suggests that anthropogenic nitrogen flux is not dis- charged directly into the surface layer, where it would add on to the natural nitrate flux through the thermocline and result in an approximate doubling of the phytoplankton biomass (Monteiro et al. in press). Rather, the nitrogen waste, which is largely associated with a particulate (<1 mm) fraction, is deposited in the benthic environment, where it is remineralized into NH4 (Fenchel and Blackburn 1979). The resulting benthic flux of remineralized NH4 enriches the natural subthermocline reservoir of Dissolved Inor- ganic Nitrogen (DIN) by an estimated 2-3 |jlM. This is supported by a high-resolution profile of NH4 from Saldanha Bay. It shows that concentrations of NHj below the thermocline are enriched by 4-5 |xM relative to the nitrogen-depleted surface layer (Fig. 9). This 209(: enrichment of the subthermocline waters will increase the magnitude of the nitrogen gradient and result in a increased nitrogen flux and ultimately on the measured phytoplankton bio- mass. This is consistent with the observed average difference in phytoplankton biomass between Big Bay and Small Bay (Pitcher and Calder 1998). CONCLUSIONS This study has provided an estimate of average annual new production for Saldanha Bay of 0.63 g of C m"~ day"' based on two independent physical models for the transport of NO3 across the thermocline. This average value, when combined with the mea- sured total net production rate of 3.40 g of C m"" day"' (Pitcher and Calder 1998) yields an /ratio of 0.19 which is close to the range that characterizes '"'^N-based estimates from the southern Benguela System. Anthropogenic sources of new nitrogen into the system were shown to be significant in the magnitude of their fluxes but, because of their pathway, to have little effect on the overall new production estimate. It was therefore hypothesized that new production in Saldanha Bay is physically controlled by the stratification dynamics rather than by the total load of new nitro- gen introduced into the bay. In this respect, both physical models are suggested to provide satisfactory estimates of new production in Saldanha Bay in the period of the study. However, the extent to which the estimated new production is available to mussels in the system will depend on the as yet un- known extent to which it is retained within the bay system or exported with the predicted net outflow of surface layer water. This is a critical unknown that is the subject of the next stage of the work. LITERATURE CITED Anderson. R. J.. P. M. S. Monleiro & G.J. Levitt. 1996. The effect of localised eutrophication on competition between Ulva lactuca (Ul- vaceae, Chlorophyta) and a commerical resource of Gracilaria verru- cosa (Gracilariaceae, Rhodophyta). Hydmbiologia. 326/327:291-296. Andrews, W. R. H. & L. Hatchings. 1980. Upwelling in the Southern Benguela Current. P 101^1. Oceunogr. 9:1-81. Asmus, H. & R. M. Asmus. 1993. Phytoplankton-inusscI bed interaction in intertidal ecosystems. In: R. F. Dame (ed.l. Bivalve Filter Feeders m Estuarine and Coastal Ecosystem Processes. NATO ASl Series. Series G: Ecological Sciences. 31:57-84. Brown, P. C. & J. L. Henry. l9iS.5. Phytoplankton production, chloro- phyll-a and light penetration in the southern Benguela region during the period between 1977 and 1980. In: L. V. Shannon (ed.). South African Ocean Colour and Upwelling Experiment. Sea Fisheries Research In- stitute, Cape Town. 270 pp. Brown, P. C. & L. Hutchings. 1987. The development and declme of phytoplankton blooms in the .southern Benguela upwelling system: 2. Nutrient relationships. In: A. I. L. Payne, J. A. Gulland, and K. H. Brink (eds.). The Benguela and Comparable Ecosystems. South African Journal of Marine Science. 5:393^10, Brown. P. C, S.J. Painting & K. L. Cochraiie. 1991. Estimates of phy- toplankton and bacterial biomass and production in the northern and southern Benguela ecosystems. S. Afr. J. Mar. Sci. 1 1:537-564. CSIR. 1991. Evaluation of the discharge of selected fish factory effluents and the impact on the adjacent marine environment. CSIR Report. EMA-C 91171, Council For Scientific and Industrial Research. Preto- ria, South Africa. 49 pp. and appendices. Dame, R. F. 1993. The role of bi-valve tiller feeder nuitenal lluxes 111 estuarine ecosystems. In: R. F. Dame (ed). Bivalve Filter Feeders in Estuarine and Coastal Ecosystem Processes. NATO ASI Series, Series G: Ecological Sciences. 31:245-270. Springer-Verlag, Heidelberg. Dankers, N. 1993. Integrated estuarine management — obtaining a sustain- able yield of bivalve resources while malnluining environmental qual- ity. In: R. F. Dame (ed). Bivalve Filler Feeders in Estuarine and Coastal Ecosystem Processes. NATO ASI Series. Series G: Ecological Sciences. 31:57-84. Springer-Verlag, Heidelberg. Dugdale, R. C. & J.J. Goering. 1967. Uptake of new and regenerated forms of nilrogen m primary productivity. Liiiuiol. Occanogr. 12: 196- 206. Eppley. R. W, & B. J. Peterson. 1979. Particulate organic matter tlux and planktonic new production in the deep ocean. Nature. 282:677-680. Fenchel, T. & T. H. Blackburn. 1979. Bacteria and Mineral Cycling. Aca- demic Press. London. 225 pp. Grant, J., J. Stenton-Dozey. P. M. S. Monteiro. G. Pitcher & K. Heasman. 1998. A carbon budget of Saldanha Bay (South Africa) for raft culture of Mytilus galloprovincialis. J. Shellfish Res. 17:41-49. Guastella, L. A. 1992. Sea surface heat exchange at St Helena bay and implications for the southern Benguela upwelling system. In: A. 1. L. Payne, K. H. Brink. K. H. Mann, and R. Hilborn (eds). Benguela Trophic Funclil Slu-llfi.sh Research. Veil. 17. No. I. 15-24. I^WX. SHELLFISH MARICULTURE IN THE BENGUELA SYSTEM: PHYTOPLANKTON AND THE AVAILABILITY OF FOOD FOR COMMERCIAL MUSSEL FARMS IN SALDANHA BAY, SOUTH AFRICA G. C. PITCHER AND D. CALDER Sea Fisheries Research Insriliile Private Bag X2. Rogge Bay. 8012. South Africa ABSTRACT Saldanha Bay is a semi-encK).sed enibaynient with a strong link to the highly productive Benguela upwellnig system. Almo.st all of the South African mussel indu.stry is located in this bay, where the mussel Mylilus i^alliipwviiuicili.s is cultivated on ropes suspended froin rafts. This study provides an estimate of phytoplankton biomass and pnmary productivity within the bay. parameters that are neces.sary for prediction of mussel growth rate and assessment of carrying capacity. It further examines the underlying mechanisms controlling phytoplankton population variability, placing emphasis on the changing physical and chemical environment so important in establishing conditions for rapid phytoplankton growth and in regulating the advective renewal of seston for suspension feeders. A mean water column chlorophyll a concentration of 8.62 mg m"' was measured, and daily rates of production ranged from 0.38 to 5.92 (mean. 3.40 g of C m~" day"'). Phytoplankton variability was controlled primarily by changes in the physical state of the bay as determined by inputs of energy at the interfaces with the coastal upwelling system and the atmosphere. At the coastal-bay interface, upwelling processes on the shelf determine the advective transport of phytoplankton and the input of nutrients from the coastal upwelling system. These horizontal exchanges ;ire dictated by event-scale fluctuations in wind stress and barotropic shelf waves. At the atmosphere-bay interface, wind stress at the water surface determines the rate of entrainment that provides the nutrient input into the euphotic zone. Enhanced vertical mixing of the upper water column breaks down stratification, thereby redistributing the phytoplankton population within the water column, and in some cases resuspends bottom sediments, thereby altering the turbidity and light environment. The prominence of a sometimes intense and sharply defined subsurface chlorophyll maximum during periods of thermal stratification was established. Lateral transports within the bay are also determined predominantly by wind-driven circulation, which dominates tidally driven flow in most instances. KEY WORDS: Phytoplankton biomass. primary production, mussel farms, Saldanha Bay INTRODUCTION Saldanha Bay is a semi-enclosed embayment on the western coast of South Africa (Figure 1 ) with a maximum depth of 30 m at the entrance to the bay. In 1975. it was separated into two smaller bays. Small Bay and Big Bay. by the construction of an iron-ore jetty. Saldanha Bay is linked to the Benguela upwelling system on its western side and feeds Langebaan Lagoon, a shallow tidal body of water, situated at the southern end of the bay. Few sites are suitable for mariculture on the South African coast, and practically the entire mussel industry is located in this bay. where the mussel Mylilus gallciprovincialis is cultivated on ropes suspended from rafts. In 1994, the marketable mussel yield in Saldanha Bay ex- ceeded 2,500 tons (Heasman 1996), and the potential for growth of the mussel industry is in contrast with that of the fishing industry, which is faced with static or reduced quotas (Du Plessis 199.3). Saldanha Bay is suitable for this type of mariculture, not only because it offers the protected waters necessary for raft cultivation, but also because of its strong link to the highly productive West Coast upwelling system (Shannon and Pillar 1986). Marine bivalves are cultured throughout the world, and in many places, the culture of mussels has grown exponentially in the last decade. Acceptable culture sites are. however, limited by habitat suitability, access, and competing recreational or commercial use (Grant et al. 1993). Suspension feeders, such as mussels, have a remarkable capacity to filter the water column and to deplete the water of seston. such that they are food limited at high culture density (Navan'o el al. 1991). As available culture space becomes filled with stock, there may be a depression of individual bivalve growth rate and an increase in mortality caused by several factors associated with overcrowding (Grant et al. 1993). Experience in several major shellfish production centers has shown that exceed- ing the carrying capacity leads to retarded growth rates, slower recoveries after spawning, and lowered resistance to disease, all of which can threaten the economic viability of mariculture ventures. Research has demonstrated major site differences in mussel growth rate, confirming that environmental conditions can regulate shellfish production and that bivalve growth can be predicted as a function of the environment (Grant et al. 1993). A means to predict the ability of Saldanha Bay to sustain mussel culture was therefore considered essential to the continued development of the shellfish industry, and a research program was initiated to determine the carrying capacity of the bay for economic mussel farming. In our approach to the assessment of carrying capacity, the limiting re- source for filter-feeding bivalves was ultimately assumed to be suspended food. This article exainines the underlying inechanisms controlling phytoplankton population variability in Saldanha Bay, placing considerable emphasis on the changing physical and chemical environment so important in establishing conditions for rapid phytoplankton growth and in regulating the advective re- newal of seston for suspension feeders. The study also provides an estimate of phytoplankton biomass and primary productivity within the bay necessary for prediction of mussel growth rate and assessment of carrying capacity. DATA Data were collected from a monitoring buoy and from six field studies conducted during winter, spring, or autumn during the period 1993 to 1995. The monitoring buoy, anchored in 12 m of 15 16 Pitcher and Calder s m- S.'; SALDANHA si hr^ Or SOUTH AFRICA (T/ J,^ Sawaww Say / ISO soo KHOTMIres ___' ' ■ Meeu Is Skaapeiland/- ^ ^^^^^^ --': r.';- V /■:;J Figure 1. Saldanha Bay: monitoring buoy (MB) and sampling Stations SI to S28. water, was located in Small Bay, and samples for the analysis of chlorophyll (Chi) a were collected daily at 1,6, and 10 m for the period from July 1993 to December 1994 (Fig. I ). Water samples for qualitative assessment of the phytoplankton composition were also collected daily at this buoy. These samples were fixed in neutralized formalin and examined by means of an inverted mi- croscope. During each of the field studies, phytoplankton spatial distributions were surveyed by sampling a grid of 28 stations (Fig. 1 ). At each of these stations, profiles of temperature and in situ Chi fluorescence were obtained by means of a submersible Chelsea Instruments Aquapack. and samples for the analysis of Chi a were collected from l-m depths. Aquapack profiles were also conducted daily at the monitoring buoy during selected field studies. For the final field study, samples for the analysis of Chi a were collected daily at 0.5-m intervals by means of a fine-scale discrete water sampler (Waldron and Probyn 1989). Productivity stations were undertaken at the site of the monitoring buoy on 3 days during each field study. These comprised '''C uptake experiments at dis- crete depths, corresponding to the 100, 50, 10. and 1* light levels. Sample depths were calculated from secchi disc measurements (Par.sons et al. 1977). Samples for NO, and Chi u analysis were also collected at these depths. Samples for NO3 were analyzed with a Technicon Auto Analy- ser II (Mostert 1983), and Chi a was measured nuromelrically in 90% acetone extracts with correction for phaeopigments (Holm- Hansen et al. 1965). Primary productivity was measured by the '^C technique of Strickland and Parsons (1972). Three light and one dark sample were inoculated with 10 ixCi of NaH'"'CO^ and in- cubated in situ at each light depth. At the 50 and lOOf light depths, duplicate samples were incubated for estimation of nanoplankton productivity. After 4 h, samples were filtered onto Whatman GF/F filters and air dried. The duplicate samples at the 50 and ]()% light depths were first filtered through a l()-|xm-pore-sizc filler, thereby providing estimates of nanoplankton productivity. Labeled inor- ganic C was removed by fuming over concentrated HCI for 20 niin before the filters were placed in vials. Instagel scinlillalum lluor was added, and the vials were vigorously shaken and stored in the dark for counting on a Beckman Scintillation Counter. RESULTS Chi a Time Series Monthly mean concentrations of Chi a were calculated from daily means derived from water column integrals of Chi n at the monitoring buoy for the period from July 1993 to December 1994 (Fig. 2). There was a general increase in biomass during the up- welling season, with the highest Chi a concentrations being re- corded during the latter part of the upwelling season. For the period from September to December, mean Chi a concentrations ranged between 4 and 8 mg m''', and for the period from January to June, concentrations ranged between 10 and 14 mg m"\ The winter period during which phytoplankton biomass was lowest and mean Chi a concentrations were <4 mg m"' was confined to the month of July. The mean water column Chi a concentration for the entuc period sampled was 8.62 mg m""\ Blooms of the photosyn- thetic ciliate Mesodiniuni lubrum were responsible for dramatic increases in phytoplankton biomass during August in both 1993 and 1994. Diatoms were a common component of the netplankton in spring and early summer, but dinotlagellates dominated in late summer and autumn. Phytoplankton biomass during the upwelling season, although generally high, was accompanied by considerable variability (Fig. 2), the frequency of which implicated synoptic scale forcing. A lime series of daily profiling of temperature and //; ,v///( tluores- cence at the monitoring buoy for the period from November 21 to December I 1994 (Fig. 3). and a similar time series of temperature and Chi a concentration for the period March 16-24. 1995 (Fig. 4). provided insight into the hydrography responsible for this variabil- ity. Upper mixed-layer dynamics and the intrusion of cold bottom water into Saldanha Bay after intermittent upwelling events on the shelf were of paramount importance. A sometimes intense and sharply defined subsurface Chi maximum (Chl^,;,^) was estab- lished during periods of thermal stratification. During the first time series (Fig. 3). the entire water column was initially (November 21-23) characterized by warm water of relatively low phytoplankton biomass. However, a subsurface bio- mass maximum was found to develop (November 24 to December I ) with the establishment of vertical stratification subsequent to the penetration of cc)ld bottom water into the bay and the sun warming * i F M A 1993-94 Kigui-e 2. Montlily means of C'hl a calculated from daily means de- rived frnni «aler eolumn inteyrals at the monitoring buoy for the period hom ,Iuh IW.< to December l'W4 (means are presented as points inside the box. standard errors are presented as the box, and standard deviations around the mean are presented as whiskers I. Ph^toclankion Availability for Mussel Farms 17 Figure 3. Daily time series of (al sea temperature ( C) and (h) in silii Chi fluorescence as profiled with a Chelsea Instruments Aquapack at the monitoring buov for the period from November 21 to December 1, 1994. of surface water. This biomass maximum appeared to increase with shoaling and intensification of the thermocline (November 30 to December 1 ). During the second time series (Fig. 4), a well-established sub- surface Chl,,,^^ was initially (March 16-17) observed during a period of thermal stratification. Subsequent (March 18-19) cooling of the surface water and warming of bottom water indicated mix- ing, thereby eroding the subsurface Chl,,,.,^ and redistributing the phytoplankton population within the upper mixed layer. The sub- surface Chl,,,^^ reestablished (March 20-24) in the region of the thermocline, as the water column again stabilized, after the intru- sion of cold bottom water and warming of the surface water. Spatial Distribution of Chi a Sampling of Stations SI to S28 often revealed considerable spatial variation in the phytoplankton biomass within Saldanha Bay. Temperature and in situ Chi fluorescence profiles conducted at these stations on November 29, 1994. depict a typical spring or summer situation when winds from the south predominate along the long axis of the bay (Fig. 5). Small Bay was characterized by warmer water and lower phytoplankton biomass. The southeastern Figure 4. Daily time series of (a) sea temperature (°C') and (b) Chi a at the monitoring buoy for the period from March 16 to 24, 1995. Figure 5. Spatial distribution of (a) sea surface temperature, (b) sur- face in situ Chi fluorescence, and (c) in situ Chi fluorescence at the subsurface maximum as measured with a Chelsea Instruments Aqua- pack on November 29, 1994. parts of Big Bay were, on the other hand, characterized by cooler water and higher phytoplankton biomass. The higher biomass in Big Bay was particularly evident in the subsurface layer. A vertical section, extending from the northern to the south- eastern shores of Saldanha Bay. of temperature and in situ Chi fluorescence on November 29. 1994, further demonstrated the as- sociation of the subsurface Chl,,,,^ with the thermocline (Fig. 6). An accumulation of warm water and a deepening of the ther- mocline in Small Bay was associated with reduced /(( situ fluores- cence. In Big Bay, a shallowing of the thermocline and enhanced mixing in the upper water column was responsible for higher phy- toplankton biomass. A composite of surface Chi a concentrations obtained from the 17 occasions on which the grid of Stations SI to S28 was sampled indicated that the shallows of Small Bay and the entrance to Langebaan Lagoon were characterized by lower biomass (Fig. 7). For the remainder of the bay, mean surface Chi a concentrations varied between 5 and 1 1 mg m"''. Although Small Bay was domi- nated by Chi a concentrations <9 mg nr\ a considerable portion of Big Bay was characterized by concentrations >9 mg m"^. Phytoplankton productivity Productivity measurements were undertaken on 3 days during each of the six field studies. 18 Pitcher and Calder Figure 6. A vertical section extending from the northern shore to the southeastern shore ofSaldanha Bay of la) sea temperature ( C) and lb) in situ Chi fluorescence as profiled with a Chelsea Instruments Aqua- pack on November 29, 1994. 1993 to 1994 During the first year of study, typically winter conditions were encountered during the July to August field study iFig. 8). The water column was well mixed with little vertical structure. Inter- mediate temperatures, between 14 and 15°C. were evident throughout the water column, and NO, concentrations exceeded 8 mmol m"''. Chi a concentrations were all less than 4 nig m"\ and the highest productivity estimates approximated 27 ms of C m~' ir'. During the December field study, the water column was strati- fied. Surface water temperatures exceeded 1 VC and were depleted of nutrients. Bottom water temperatures declined below IO°C. and NO, concentrations in excess of 20 mmol m"' were measured. Chi a concentrations and productivity estimates were generally hjgher. with maximum values approximating 18 mg m"' and 92 mg of C m""* h~', respectively. There was a tendency for these maxima to be subsurface. In March, during the latter part of the upwelling season, the entire water column was warmer; bottom temperatures exceeded 13°C and surface waters attained 18°C. NO, concentrations were <1 mmol m"'. Chi a and productivity estimates were high, with maxima of 19 mg m"' and 1.^8 mg of C m"' h"', respectively, both of which were subsurface. 1994 to 1995 During August of the second year ol study ll'ig. 9), surface temperatures between \?i and I4"C and bottom temperatures as low as I I C indicated early stratification. NO, concentrations ex- ceeding 4 mmol m"' and Chi a concentrations as high as 26 mg m ' were responsible for the highest single productivity estimate of 181 mg of C m ' h '. By November, surlace waters had warmed considerably to >I8"C and intrusions of cold bottom water of producti\itv iPPi as relaled to temperature, NO, concentration, and t'lil a concentration. V\iihin the upper photic zone, P" ratios from discrete depths t)tten approached the theoretical maximuiTi of 25 mg of C mg of Chi ^r' h"' (Falkowski 1981 1. These particularly high P" values of >15 mg of C mg of Chi o"' h ' were recorded during spring blooms of small diatoms. The P-I equation of Piatt et al. ( 1980) was used to model the results; P. (1 (e i-pi/p.i (1) where P," is the instantaneous rate of photosynthesis normalized to Chi a at irradiance I: P., is the maximum rate of photosynthesis; a is the initial slope of the P-I curve, and 3 is a parameter to char- acterize photoinhibition. An average P^ estimate of 9.24 mg of C mg of Chi (/ ' h ' for the photic zone was established from the 20 Pitcher and Calder PRIMARY PRODUCTIVITY (mg C • m-3 • h') 30 60 90 120 160 180 210 30 60 90 120 150 180 210 30 60 90 120 150 180 210 9 f I I I I I ." Temp, 6 Aug. 94 , ^^ O 10 ^M 8 Aug. 94 1 ^^ t^^ m ...■■ 28 No« 94 10 Aug. 94 i^!y':Mi 17 Mar. 95 19 Mar. 95 TEMPERATURE ( X) 10 12 14 16 IB 20 22 Chi 3 (nigTn-3) 3 6 9 12 15 18 21 NITRATE (mmol'tn-S) 3 6 9 12 15 18 21 10 12 14 16 18 20 22 3 6 9 12 15 18 21 3 6 9 12 15 18 21 10 12 14 16 18 20 22 5 6 9 12 15 18 21 3 5 9 12 15 18 21 Figure 9. Profiles of primary productivity (PP) as related to temperature, NO, concentration, and (hi a concentration. photic zone integral of productivity norniaji/ed to hiomass derived from the above P-1 equation. Daily Productivity Estimates of daily productivity, corrected for respiration, were calculated by multiplying the hourly production rate by a factor F = d - R • n. where d is the number of effective daylight hours (i.e.. davlight hours less I hour each at sunrise and sunset), R is the hourly rate of respiration (assumed to be lO'^'r of the hourly pro- duction during daylight), and n is the number of night hours. Daily rates of production calculated in this way for each of the productivity stations conducted during this study ranged from 0..^8 to 5.92 (mean. .^.40 g of C m"" day"') (Fig. 12). Although there was an apparent seasonal trend, with a tendency for lower esti- mates durinc winter, considerable variabilitv durinu most field Ph>t()pi.anki()N Avaii,ahilit^ k)r Mussel Farms 21 TABLK I. Productivity station photic depth and photic zone integrals of Chi a, priniurv prodiictl\lty. and productivity normalized to biomass. Date Photic Depth Chi a Productivitv (m) (mg m"") (mg of C m"" h"') 9.5 10.8 66.3 9.5 23.3 106.9 6.8 14.9 54.5 7.6 60.6 45S.2 7.0 22.(1 339. 1 9.8 3S.() .343.7 6.2 77.1 427.6 8.1 65.7 493.1 7.5 104.1 626.6 9.2 48.1 183.5 12.1 83.2 259.6 9.2 161.0 495.9 5.4 45.2 285.5 6.8 48.4 404.2 6.0 60.4 492.8 7.5 109.9 237.6 7.5 123.5 670.7 7.5 94.8 603.9 (mgof C mgof Chi' h"') Jul> 31, 1993 August 2. 1993 August 4. 1993 December S. 1993 Decemher 10. 1993 December 13. 1993 March 13. 1994 March 15, 1994 March 17. 1994 August 6. 1994 August 8, 1994 August 10, 1994 November 23, 1994 November 28. 1994 November 30, 1994 March 17. 1995 March 19, 1995 March 22. 1995 6.2 4.6 3.7 7.6 15.4 9.0 5.6 7.5 6.0 3.8 3.1 3.1 6.3 8.4 8.2 2.2 5.4 6.4 studie.s indicated the importance of forces at the event scale in dictating variation in primary productivity. Alternately, an hourly rate of production of 79.46 mg of C m" ' h"' for the photic zone was calculated from the P" estimate of 9.24 mg of C mg of Chi a'' h~' derived from the P-l equation of Piatt et al. (1980) and the mean water column Chi a concentration of 8.62 mg m"\ Assuming a mean photic zone depth of 8.0 m and an average daylength of 12 h. this translates to a daily rate of pro- duction of 3.48 g of C 111"" day"'. As a result of the poor corre- lation of P'* with relative surface irradiance (Fig. 1 1 ). the former estimate of daily productivity of 3.40 g of C m~" day"' was con- sidered more reliable. DISCUSSION Saldanha Bay is a semi-enclosed system exposed to a hierarchy of physical forcing functions. Although tidal influences are appar- ent under light wind conditions, Saldanha Bay is predominantly wind driven (Bilski 1996), as is the adjacent upwelling system (Shannon et al, 1990), These winds have diurnal variability (Jury et al. 19851 and an energetic synoptic scale signal (Nelson and Hutchings 1983), as well as seasonal and interannual variation (Shannon et al, 1990), In winter, the water column is vigorously mixed and therefore approximately isothermal, with high nutrient availability but little biological productivity. Under these circumstances, the suspension of particles results in a turbid habitat in which phytoplankton growth is likely to be limited by the availability of sunlight to sustain photosynthesis. During the upwelling months, however, the water column can become highly stratified, because intermit- tent upwelling on the shelf causes a cold lower layer to penetrate into the bay. which together with sun warming of surface water, enhances stratification (Monteiro et al. 1998). A nutrient-depleted W93 S'93 W94 S'94 A'95 A'94 SEASON Figure 10. Mean nano and total productivity as measured at the 50 and 10% surface irradiance levels for the winter (W), summer (S), and autumn (A) periods of study during 1993, 1994, and 1995 (ranges are presented around the mean as whiskers). ?T Pitcher and Caldkr 30 40 50 60 Percent Surface Irradiance Figure 11. Primary productivity normalized to biomass (P") as measured at tlie 100, 50, 10, and 1% surface irradiance levels. upper layer is therefore typically found overlying a nutrient-rich lower layer because the thermocline never upwells to the surface of the bay and there are essentially always two layers to the system during the upwelling season (Monteiro et al. 1998). This strong vertical stratification effectively isolates phytoplankton in a shal- low surface layer in which the mean surface inadiance is much higher than the irradiance averaged over the entire water column. Also, the 1% light penetration depth in Saldanha Bay during the upwelling season was typically deeper than the upper mixed-layer depth, indicating a stratified photic zone penetrating below the thermocline. As a result, the net growth rate of the phytoplankton in the surface layer increases after the establishment of vertical statification. The necessary flux of nutrients into the upper layer to sustain this growth will occur when the turbulent upper layer en- trains nutrient-rich lower-layer water across the thermocline (Mon- teiro et al. 1998). This process will occur when the wuid is suffi- ciently strong to deepen the upper mixed layer, thereby entraining colder water from below. The rate of this entrainment is directly proportional to the wind stress. In addition to enriching the surface water, this process redistributes the phytoplankton population throughout the water column. Local wind-induced turbulent mix- ing is therefore a key physical process determining the vertical fluxes of heat and the vertical distribution of nutrients and phy- toplankton. During the upwelling season, a sometimes intense and sharply defined subsurface phytoplankton maximum develops in associa- tion with the thermocline. The productivity maximum (P,,,.,^) in some instances con'esponded lo this biomass maximum, but in other instances, P,„ ,^ was foimd above the subsurface Chl,,,,,^. The formation and persistence of subsurface biomass maxima may be ascribed to a number of potential mechanisms, including changes in cellular Chi a, behavioral responses of motile phytoplankton, accumulation at a density interface, reduced grazing pressure, sta- bility effects, and enhanced growth at the nutricline (Jamart el al. 1977, Cullen 1982). Clearly, different mechanisms will be impor- tant under different conditions and it is highly probable that a number of factors act in concert to determine observed biomass profiles. In Saldanha Bay. it would appear that subsurface maxima 6000 ^ 5000 E o E 4000 p 3000 O a o a. 0- a. < Q. 2000 1000 — 1 1— 1 I ; : 1 1 L__ 1— : : ; ' — ; ^ ; ; ; ; W93 S'93 W94 S'94 A'95 A'94 SEASON Figure 12. Mean daily estimates of productivity for the v\inter (W), spring (S), and autumn (A) periods of study during I'W.^. 1994, and IW5 (ranges are presented around the mean as whiskers). PH'iroi'l.ANKl'ON AVAII.AHII ir^' I(1R Ml'SSHL FARMS 23 are established as a result of accumulation in the region of the thermocline after a reduction in local wind stress and turbulent mixing. The location of the Chl,,,,^ at the nitracline. above the \^,i light level, establishes the potential for ;/) siiii growth as a mecha- nism for sustaining the Chl,,,.^.^. Under these circumstances, pri- mary productivity in the subsurface Chl„,,^ could account for a significant proportion of the total water column production and winild therefore be an important site for nitrate-based new produc- tion, as defined b\ Dugdale and Goering ( 1967). In this instance, the Chl,„,^ will function as an effective nutrient trap (.lamart et al. 1977), restricting the diffusive invasion of nutrients into the mixed layer, while continually eroding the nitracline downward, provid- ing sufficient light is available. After upwelling on the shelf and the penetration of cold bottom water into Saldanha Bay. the shallowing of the thermocline results in an outflow of surface water and an advective loss of phytoplank- ton from the bay (Monteiro et al. 1998). On the other hand, during periods of relaxation, the wedge of cold bottom water retreats, favoring the advective introduction of coastal blooms into the bay. The relaxed phase of the upwelling cycle therefore serves as a mechanism by which coastal surface red-tide blooms, a serious threat to (he mussel-farming industry, can be lapidly imported into the bay (Pitcher et al. 1996a). Previous measurements of Chi a concentrations in Saldanha Bay reported by Henry et al. (1977) and Monteiio and Brundrit (1990) are within the range of jiieasurements made during this study. However, the mean water column concentration of Chi (( (8.62 mg m"-') calculated in this study is considerably higher than the mean levels of 2.86 and 2.15 mg m""* reported by Brown and Cochrane (1991) and Brown et al. (1991). respectively, for the adjacent coastal upwelling system. These studies, however, re- ported mean Chi a concentrations for the upper 30 m of the water column and were not confined to the inshore region, but included all measurements within the 500-m depth contour. The daily rates of production calculated during this study (range. 0.38-5.92; mean. 3.40 g of C m~- day"' ) are notably higher than the estimates of Henry et al. ( 1977) for Saldanha Bay. which ranged from 0.86 to 3.30 (mean, 1.75 g of C m"" day"'). Our estimates are. however, similar to most other estimates of produc- livity in the southern Benguela ecosystem. For example, off the Cape Peninsula, in waters ranging from recently upwelled to aged upwelled water, daily production rates varied between 0.94 and 7.50 g of C m"" day"' (mean. 3.47 g of C m"" day"') (Brown et al. in press). In a time series study conducted over 27 days in St. Helena Bay. daily productivity ranged from 0.99 to 7.85 g of C m^~ day"' (jiiean, 3.27 g of C m"" day"') (Mitchell-Innes and Walker 1991). and in Elands Bay. a small exposed bay situated north of Saldanha Bay. a phytoplankton biomass nutrient con- sumption equation provided a production estimate of 3.92 g of C m"~ day"' (Pitcher et al. 1996b). Our mean estimate of daily phytoplankton productivity in Saldanha Bay is almost identical to the mean of 3.47 g of C m"" day"' reported by Brown et al. (1991) and is derived from all production measurements conducted on the West Coast of the southern Benguela. CONCLUSION Saldanha Bay is a highly productive system providing a food environment and temperature regime optimal for the farming of the mussel M. galloprovincialis. Mussel growth rates measured in Saldanha Bay are therefore presently among the highest in the world (Heasman et al. 1998). The proximal agents of phytoplankton dynamics in Saldanha Bay are changes in the physical state of the bay as determined by inputs of energy at the interfaces with the coastal upwelling system and the atmosphere. Two physical forcings and the interaction of these forcings are of primary inipo)'tance in controlling phy- toplankton population variability in Saldanha Bay (Fig. 13). At the coastal-bay interface, upwelling processes on the shelf determine the advective transport of phytoplankton and the input of nutrients from the coastal upwelling system. These horizontal exchanges are dictated by event-scale fluctuations in wind stress and barotropic Figure 1.1. .\ diagram of the physical forcings that operate at the interface between Saldanha Bay and the coastal upHclling system and the atmosphere during the upwelling season: (A) wind-dominated circulation responsible for the lateral transport of phytoplankton blooms; (B) rcsuspension of bottom sediments and a resultant modification of turhiditv : ((') turbulent mixing and erosion of the thermocline responsible for the entrainment of nutrients and the vertical redistribution of phytoplankton populations; (D) advective import/export of phytoplankton blooms; and (E) the flux of nutrient-rich bottom water. 24 Pitcher and Calder shelf waves that may or may not be in phase with these wind events (Nelson pers. comm.). At the atmosphere -bay interface, wind stress at the water surface determines the rate of entrainment that provides the nutrient input into the euphotic zone of Saldanha Bay. Enhanced vertical mixing of the upper water column breaks down stratification, thereby redislributint: the phytoplankton popu- lation within the water column and. m some instances, resuspend- ing bottom sediments, therefore altering the turbidity and light environment. Lateral transports within the bay are also determined predominantly by wind-driven circulation, which dominates tid- ally driven flow in most instances. Although this study places great emphasis on the changing physical and chemical environment as a mechanism of phy- toplankton population changes, it is important to remember that the plankton species in .Saldanha Bay show behavioral, biochemical, and life-history adaptations to the physical and chemical variabil- ity characteristic of this bay. It is these capabilities of adaptation that are responsible for the seasonal dominance of particular taxo- nomic groups and, for example, the high biomass blooms of the photosynthetic ciliate M. nihniiu in August each year. ACKNOWLEDGMENTS We thank Pedro Monleiro. convenor of the Working Group of the Sea Fisheries Research Institute liueniaioiis between Maricul- liire caul the Eiivironnieiit. for initiating and coordinating the Saldanha Bay Research Programme and Kevin Heasman for col- lecting daily phytoplankton and Chi o samples. LITERATURE CITED Bllski, S. 1996. The characterisation of synoptic circulation patterns in Saldanha Bay. MSc. Thesis. University of Cape Town, South Africa. 95 pp. Brown, P. C. & K. L. Cochrane. 1991. Chlorophyll a distribution in the southern Benguela, possible effects of global warming on phytoplank- ton and its implications for pelagic tlsh. S. Afr. J. Sci. 87:2,^3-242. Brown. P. C. J. G. Field & L. Hatchings. In press. Primary production during five phytoplankton blooms following upwelling. S. Afr. J. Mar. Sci. Brown, P. C. S. J. Painting & K. L. Cochrane. I99I. Estimates of phy- toplankton and bacterial biomass and production in the northern and southern Benguela ecosystems. S. Afr. J. Mar. Sci. 1 1:5.37-564. CuIIen. J. J. 1982. The deep chlorophyll maximum: comparing vertical profiles of chlorophyll a. Can. J. Fi.sh. Aqiiat. Sci. 39:791-803. Du Plessis. A. J. 1993. Mussel culture in South Africa: current status and future commercial prospects. In: T. Hecht and P. J. Britz (eds.). Aqua- culture '92. Proc. Aquacult. Assoc. Sihn. Afr. 1:92-96. Dugdale. R. C. & J.J. Goering. 1967. Uptake of new and regenerated forms of nitrogen in primary productivity. Lininal. Occanogr. 12:196- 206. FaIkow.ski. P. G. 1981. Light-shade adaplalion and assimilation numbers. / Plank. Res. 3:203-216. Grant. J.. M. Dowd. K. Thompson. C. Emerson & A. Hatcher. 1993. Perspectives on held studies and related biological models of bivalve growth and carrying capacity. In: R. F. Dame (ed.). Bivalve Filler Feeders in Fstuarine and Coastal Ecosystem Processes. Springer- Verlag, Beriin. NATO AS! Series. 33:371-420. Heasman, K. G. 1996. The influence of oceanographic conditions and cul- ture methods on the dynamics of mussel famiing in Saldanha Bay. South Africa. MSc. Thesis. Rhodes University, Grahamstown, South Africa. 99 pp. Heasman, K. G., G. C. Pitcher. C. D. McQuaid & T. Hecht. 1998. Shellfish mariculture in the Benguela system: raft culture of Myiilus gallopri>- vincialis and the effect of rope spacing on food extraction, growth rate. production and condition of mussels. J. Shellfish Res. 17:33-39. Henry. J. L., S. A. Mostert & N. D. Christie. 1977. Phytoplankton produc- tion in Langebaan Lagoon and Saldanha Bay. Trans. Roy. Soc. S. Afr. 42:383-398. Holm-Hansen, O.. C. Lorenzen. R. W. Holmes & J. D. H. Strickland. 1965 Fluorometric determination of chlorophyll. J. Cans. Int. E.xplor. Mer. .30:.V|5. Janiart. B. M.. D. F. Winter. K. Banse, G. C. Andei-son & R. K. Lam. 1977. A theoretical study of phyloplanklon growth and nutrienl distribution in the Pacific Ocean oft die noithwesleni LIS. coasl. Deep-Sea Res. 24:75.3-773. Jury. M. R., F. Kamstra & J. Taunton-Clark. 1985. Diurnal wind cycles and upwelling off the northern portion of the Cape Peninsula in summer. 5. Afr. J. Mar. Sci. 3:1-10. Mitchell-Innes. B. A. & D. R. Walker. 1991. Short-term variahihty during an anchor station study in the southern Benguela upwelling system: phytoplankton production and biomass in relation to species changes. Pro.i^. Oceanogr. 28:65-89. Monteiro, P. M. S. & G. B Brundrit. 1990. Interannual chlorophyll vari- ability in South Africa's Saldanha Bay system. 1974-1979. S. Afr. J. Mar. Sci. 9:2X1-287. Monlerio. P. M. S., B. Spolander. G. B. Brundrit & G. Nelson. 1998. Shell- fish mariculture in the Benguela system: nitrogen driven new produc- tion in Saldanha Bay. ./. Shellfish Res. 17:3-13. Mostert, S. A. 1983, Procedures u.sed in South Africa for Ihc automatic photometric determination of micronutrients in sea water. S. Afr. J. Mar. Sci. 1:189-198. Navarro, E.. J. I. P. Iglesias, A. Perez Camacho. U. Labarta & R. Beiras. 1991. The physiological energetics of mussels (Mytihis galloprovin- cialis Lmk) from different cultivation rafts in the Ria de Arosa (Galicia. N. W. Spain). Aqnucuhure. 94:197-212. Nelson, G. & L. Hutchings. 1983. The Benguela upwelling area. Prog. Oceanogr. 12:333-356. Parsons. T. R.. M. Takahashi & B. Hargrave. 1977. Biological Oceano- graphic Processes. 2nd ed. Pergamon, Oxford. 489 pp. Pitcher. G., D. Calder. G. Davis & G. Nelson. 1996a. Harmful algal blooms and mus.sel farming in Saldanha Bay. In: P. A. Cook and W. Uys (eds.). Aquaculture '94. Proc. Aquacult. Assoc. Sthn. Afr. 5:87-93. Pitcher, G. C, A. J. Richardson & J. L. Korrubel. 1996b. The use of sea temperature in characterizing the mesoscale heterogeneity of phy- toplankton in an embayment of the southern Benguela upwelling sys- tem. ./. Plank. Res. 18:643-657. Piatt. T., C. L. Gallegos & W. G. Harrison. 1980. Photoinhibilion ol pho- tosynthesis in natural assemblages of marine phytoplankton, ./, Mar. Res. 38:687-701. Shannon, L. V., J. R. E. Lutjeharrns & G. Nelson. 1990. Causative mecha- nisms for inlra-annual and interannual variability in the marine envi- ronment around southern .M'rica. S. .\f. J. Sci. 86:356-373. Shannon, L, V. & S. C, Pillar, 1986. The Benguela encosyslem. Part III. Plankton. Oceanogr. Mar. Biol. .Ann. Rev. 24:65-170. Strickland. J. D. H. & T. R. Parsons. 1972 A Practical Handbook of Sea- water Analysis. 2nd ed. Bull. Fish. Res. Bd. Can. 167:310 pp. Waldron. H. N. & T. A. Prohyn. 1989. A discrete water sampler to exannnc fine-scale hydrochemical properties in the water column at sea. S. Afr. J. Mar. Sci. 8:357-361. Jtnmmt of Shellfish Kesccinh. VdI. 17. No. 1. 25-32. m^S. SHELLFISH MARICULTLRE IN THE BENGUELA SYSTEM: WATER FLOW PATTERNS WITHIN A MUSSEL FARM IN SALDANHA BAY, SOUTH AFRICA A. J. BOYD' AND K. G. HEASMAN^ Sea Fisheries Research liistitiiw Private Bag X2 Roggebaai, Cape Town. South Africa Rhodes University Grahamstown, South Africa ABSTHiCT The water flow rates w ilhin mussel rafts in Saldanha Bay were measured and related to hydrodynamic forcing (in terms of ambient flow in the farm) and raft specifications. Currents within and in the vicinity of the mussel farm were highly variable in speed and direction and were subject to wind and tidal forcing, as well as bay resonances. The rafts affected the water flow in three ways: most of the flow diverged around a raft: within a raft, the flow tended to align along one of its major axes; and within the raft, the water was retarded. Retardation appeared to depend on ambient flow speed and was statistically related to mussel rope spacing. Velocities of 7.5 cm/s and 1.25 cm/s within the farm and rafts, respectively, are suggested as the most appropriate values for calculating the food supply rates required by associated studies. The effect of a similar farm on downstream advection velocities is modeled considering a uniform flow, and possible future ad\ection limitations on a designated new lease area are discussed. KEY WORDS: Manculture, mussels. South Africa, hydrodynamic. flow. raft, model INTRODUCTION Saldanha Bay is a largely enclosed embayment of 66 km" on South Africa's West Coast (Fig. 1 ). It is connected on its western side to the energetic, productive Benguela upwelling system (Shannon 1985) by a mouth 2 km wide. 5 km long, and 30 m deep through which there is a net input of cool, nutrient-rich water at depth (Monteiro and Spolander submitted). This water is mixed upward within the bay and is responsible tor high levels of primary productivity there (Pitcher and Calder submitted). At its southern end. Saldanha Bay feeds Langebaan Lagoon, a shallow expanse of approximately 20 km". The bay itself was divided into two parts by the construction of a 3-km-long industrial jetty in 1975 (Small Bay in the north with an area of 14 kin"^ and Big Bay to the south with an area of 52 km" [Fig. 1]). Flow through the final kilometer of the jetty is only partially restricted. Saldanha Bay is subject to physical forcing on various scales. Strong bay resonances of between 20 and 90 min have been mea- sured (this study; see Fig. 3), and there is a diurnal tidal forcing the amplitude of which varies considerably depending on location. The strongest tidal currents are found adjacent to Langebaan La- goon (1 m/s) and in the mouth (0.3 m/s) (Shannon and Slander 1977. Boyd and Spolander unpubl.). However, wind forcing is dominant over most of the bay (Weeks el al. 1991. Bilski 1996). Because of the strong stratification that is present in most months (Heasman 1996). the surface layer is most affected. The winds are mainly orientated along the long axis of the bay and have diurnal variability (Jury 19S5). as well as an energetic synoptic scale sig- nal (Nelson and Hutchings 1983). A further forcing factor is the passage of barotropic shelf waves southward along the coast that may or may not be in phase with the local wind forcing (Nelson pers. comm.). There is also the periodic advection of surface water from the coastal regions through the mouth of Saldanha Bay (Lam- berth and Nelson 1987). Such intrusions could bring chlorophyll- rich water into the bay (consistent with the Costal Zone Colour Scanner (CZCS) images of Shannon et al. 1985) but also toxic red tides, as occurred in March 1994 (Heasman 1996. Pitcher and Calder submitted). The site of this study, the Sea Harvest mussel farm, is located close to the mouth of the bay, yet in a relatively sheltered location (Fig. 1), and would be subject to all of the above influences. The basic design of the farm is shown in the inset in Figure 1 and consisted of 60 rafts spread over 50 ha in 10 rows of five to seven rafts each. The initial distance between rows was approximately 100 m and between rafts in each row was 60 m. but this was modified in time by rafts dragging their anchors during major storms. The rafts consist of wooden lattices supported by hollow as- bestos-cement floats. The rafts were mainly 14 x 11 m or else 22 X 1 1 m in size, and mussel ropes 6 m in length were supported from wooden crossbeams 60 cm apart (Fig. 2). Thus, the spacing between ropes in the long axis direction was always 60 cm. but some rafts had a 60-cm distance between ropes along a crossbeam, whereas others had a 90-cm spacing. This spacing, together with the maturity of the raft, determined the amount of "free water" between ropes. Additional details are provided by Heasman ( 1996) and Heasman et al. (1998). This study aims to bridge the gap that would otherwi.se have existed between the sy.stem^ay scale studies that were being un- dertaken and the mussel biology studies within the farm (Heasman et al. 1998). Specific objectives include: • measuring flow rates through the mussel rafts and mussel farm to provide food supply rates (see Grant et al. 1998), • relating internal flow rates to external hydrodynamic forcing and to different specifications/attributes of the mussel rafts, and • evaluating the effect that mussel farms may have on flow pat- terns in temis of constraining the carrying capacity of a body of water. The importance of the latter was stressed by Van Stralen and Dijkema (1994) and also by Hickman ( 1992); Better understanding of water movement through and around the culture system, and any alterations to the pattern that result from changes in mussel density, mussel size, longline or raft density, may hold the key to optimising mussel production for either the individual farmer or the mussel industrv as a whole. 25 26 Boyd and Heasman Figure 1. Map of Saldanha Bay showing the position of the mussel farming areas, 1 in Small Bay and 2 in Big Bay. The layout of rafts in the Sea Harvest mussel farm in 1993 is shown in the inset. METHODS Data were collected on five field trips between July 1993 and December 1994. All of the within-raft measurements were made by means of tracking small drogued drifters with reference to the superstructure of the raft, with a handheld compass and tape mea- sure as necessary. The drogue consisted of a 2-L white plastic bottle (weighted to be slightly negatively buoyant) attached via a length (generally 2 m) of brightly colored monofilament nylon line to a small lOO-niL float. The line seldom snagged on the mussel ropes, and when it did. it was freed immediately. These drogues, developed during the first field study, were also used to measure small-scale ambient flow in the farm because they were easy to deploy and had minimal windage. In order to measure the flow at various sites within the farm, the following methods were also used: tetrahedral drogues (Boyd 1982, Bilski 1996) were deployed between rafts and tracked by an optical (split-image) range finder and handheld compass. All di- rections displayed are therefore relative to magnetic north. 24°W of true north. Flow below a raft at 10-ni depth was also measured on two occasions by a diver and dye. In August 1994, a Valeport current meter with 1 cm/s sensitivity giving water speed and di- rection (also magnetic) averaged over 5 min was deployed at 2-m depth at appropriate sites between rafts. Whenever possible, am- bient fiow and within-raft flow were measured as pairs of values. However, because of the variability of the ambient flow within the farm and also because flow within the rafts was found to depend on the angle between ambient flow and the physical raft axis, two essentially separate data sets were obtained: I. those in which we waited for the flow to align with an axis, generally the long axis, and for a downstream pluine of clear water to develop before making measuremenls. This was a prerequisite for food extraction studies (Heasman et al. sub- mitted); and 2. experiments comparing external flow and internal flow in any direction in rafts of different specifications. RESULTS .4ND DISCUSSION Flow Through the Mussel Farm Unfortunately, no long-term records of flow through the mussel farm were obtained. Flow through (or in the vicinity of the farm) at 2- and 8-m depth was measured on seven occasions by Bilski (1996). These measurements give an average drogue speed of 7.5 cm/s at 2-m depth. This value of 7.5 cm/s can be contrasted with a mean of 1 1 cm/s for Small Bay using Bilski's data. Weeks et al. (1991) show that surface current speeds for Saldanha Bay as a whole were mainly between 4 and 1 2 cm/s. w ith a mean of 8 cm/s, but observations were biased to low wind speeds. The drogue experiments conducted as part of this study show a mean value of approximately 6 cm/s for ambient flow at 2-m depth in different parts of the farm, and data frnni the Valeport cunent meter show 7.6 cm/s (n = 282 1. Using the current meter data only, there is evidence of consistently stronger flow at the exposed southeast corner (and southwest corner) of the farm, in contrast to the more sheltered northwest corner, yet clearly, "surges" or "resonances" in current velocity were experienced at all sites (Fig. 3). Mean current speeds for these three sites are shown in Table 1. Results for the southwest corner clearh show that five substantial surges occuned over 6 h. during a period of high speed, whereas shorter time-scale fluctuations were more proininent dur- ing lower ambient speeds. The presentation of these currents vec- torial ly (together with flow through the rafts) highlights the vari- Wati-.r Flow Pattrrns in a Mussel Farm 27 Figure 2. A photograph of a typical raft during the di\ergence experiment (Fig. 4). The small floats of the drogues used in the investigation are highlighted white. The causeHay is shown in the background. ability even further because rapid changes in direction are not always reflected in the current speed plots (see Fig. 6a for an example of variability on the 20-min time scale). Qualitative Description of the Effect of Mussel Rafts on AmhienI Flow and Aspects of Through Flow Early experiments showed the propensity of the water to choose the path of least resistance when approaching a raft at an angle by flowing through the raft parallel to its short axis. The periodic prevalence of ambient flow across the isobaths increased such flow through the raft. Countering this effect was the general alignment of the bathymetry (and dominant flow direction) with the long axis of the rafts. In practice, this leads to a relatively even mix of flow along either axis, or sluggish flow while new patterns were being established. Furthermore, on several occasions, the inertia of the whole raft system was observed, where a large, mature raft with 60-cm rope spacing would move as a whole on its anchors by a few meters over a period of minutes, whereas near- zero velocities in the raft suggested that it was trapping the water. This would also create a lag between forcing and flow through. The other major effect of raft flow patterns was in diverging the near-surface flow around a raft. On one occasion, divergence of two closely spaced drogues, after a period of parallel flow, was measured every few minutes over a period of ().."> h (Fig. 4). In this instance, the flow did not converge after passing the raft; the difference in ambient cross-shelf flow as a function of their greater separation probably caused this. Such near-surface divergence ahead of a raft resulted in surprisingly few entanglements when 2-m drogues were tracked through the fann in contrast to 8-m drogues. The latter result is in keeping with two experiments car- ried out by a diver and dye that suggested little or no retardation of ambient flow below the raft. Flow-Through Rafts in Relation to Ambient Flow and Rope Spacing Experiments conducted before August 1994 concentrated on measuring the ratio of within-raft and ambient velocities based on established flow patterns. Data from December 1993 and March 1994 showed that flow in immature rafts could periodically reach speeds as high as 5 cm/s (or40'7r of ambient), but such values were not maintained for long. Heasman (1996) combined the results of all of those established flow experiments dunng which samples were also taken for food extraction, and the results are given separately for rafts with 60- and 90-cm spacing in Figure 5. Apart from two outliers with faster through-flow in the 60-cm rafts, there are indications of nonlinearity in the relationships, with through- flow velocities reaching a maximum of 1 .2-1 ..'> cm/s. This was not seen in the experiments with 90-cni spacing, which had a bias toward lower ambient speeds. The greatest number of observations was recorded in August 1994, when the Valeport curtent meter was deployed between rafts and flow patterns within one or two adjacent rafts were all mea- sured simultaneously. For practical reasons, within-raft flow rates measured by the small drogues were only measured every 10 min in comparison to the 5-min averages from the curtent meter. Figure 6 illustrates the variability in ambient flow being im- posed on the flow through two 22 x 1 1 m rafts on two separate days. The latter part of the record in Figure 6a shows the flow alternating every 20-.30 min, a pattern that can be seen in the rafts with greatly reduced velocities. Figure 6b shows stronger currents, but again with short-term variability. Flow rates of 2-3 cm/s dur- ing forcing of 10-L'i cm/s were regularly measured, through flow thus being approximately 20% of ambient. A time series of ambient and within-raft current speeds (sepa- rately for 60- and 90-cm spacing) corresponding to Figure 6a is shown in Figure 7. Flow speeds within the 90-cm raft can be seen to be equal to or greater than those in the 60-cm raft in most instances. The previously mentioned descriptions have outlined the vari- ability and complexity of the real situation and, thus, the difficulty in analyzing the data numerically in a representative manner. In addition, short time leads and lags sometimes occurred, so that if simple simultaneous ratios were calculated, these could combine slow ambient with fast raft flow and vice versa. Figure 8 shows the wide range of ratios between internal and external flow from the August 1994 experiments. Despite the above reservations, we tested statistically for the difference between the means of the ratios of simultaneous through flow to ambient for the rafts with 60- and 90-cm rope spacing. This Boyd and Heasman Figure 3. Time series of ambient current speeds at three sites in the farm in August 1994 showing short-term variability. was done by arcsin transforming the data and then testing for the difference between two means from normal populations with un- equal variances. Using data from the combined experiment only (Fig. 7). the mean ratios for the 6()-cm raft and the 9()-cm raft were found to be significantly different only at the 5* level with a TABLE 1. Mean ambient current speeds (cni/sl at different sites in the Sea Harvest farm measured v\ith the Valeporl current meter. Site Date No. of Observations Means SD NW corner 6/8/94 67 3.67 1.35 NW corner 8/9/94 73 4.0 2.0 SW corner 9/8/94 65 I(l..'i7 3.37 SE corner 7/8/94 77 I2.SI 2.92 Overall 6-9/8/94 282 7.6 N 0' 13h23. 3t42 180' • • • I3K35. 13h04. • 12h52. ^ START 12h52« * ■ 13h04* , • • 13h24. tt40 20 40 m SCALE 13h33. 1 Figure 4. Divergence of near-surface flow around a raft. Experiment conducted on December 12, 1993. Times are given next to the droque positions. one-tailed Mest. For the August 1994 data set as a whole (Fig. 8), the differences between the ratios of internal to external flow were significant at the 2.5% level with the same test for the rafts of different specification. Such a difference is in keeping with the different food extraction and mussel growth rates found for such rafts (Heasman et al. submitted). The influence of maturity of the mussel ropes on food extrac- tion was clearly shown by Heasman (1996) and Heasman el al. (submitted), but quantitative differences of maturity on flow pat- terns were not resolved. Nevertheless, rope maturity must influ- ence velocity, and with regard to extremes, the data set shows that the fastest through flows were measured on relatively immature rafts. SUMMARY STATISTICS The effective upper bounds of flow rates through the rafts come from examples of steady-state flow, which were measured over the entire study period from both smaller and larger rafts. The data corresponding to food extraction experiments conducted during field Ambient = no retardation 60cm Winds were low. except on August 9. 1994, when Iherc were 15-20 knots. 6 8 10 12 14 Ambient water speed (cm/s) Figure .^. .Speeds of water flow through mussel rafts with 6(1- and y(l-cni rope spacings in relation to ambient speeds during sleadv-slate conditions when food extraction experiments were done. Wati;r Flow Paiti-rns in a Mussel Farm 29 ArovtncI rait ^^ ^rJlu V\ l\_ 6hrs lOmin Scale Raft. Axis Direction Tlirough raft Through raft ^> -. \ \ Scni/se Ropes spaced at 90cni \.-.. Ropes spaced at 60cm Around raft 5hrs 20min Through raft North Raft Axis Direction Scale 5cni/sec X-TY '\n\'^ \A\ Figure 6. (a I The speed and direction of water currents taken simultaneously outside and through rafts with 60- and 90-cm rope spacing on August 8, 1994. (hi The speed and direction of water currents taken simultaneously outside and through rafts with 60-cm rope spacing on August 9, 1994. trips (Fig. 5) show an approximate relation for through flow relative neous" ratios shown in Figure 8 cannot be used together with average to ambient of 13% for 60-cm rafts and 25% for 90-cm rafts. The values for ambient flow because of lags, which cause a bias, former average value, combined with 7.5 cm/s average ambient flow The August 1994 data set (collected on the large 11 x 22 m for the farm, gives a mean through flow of 1.0 cm/s for the more rafts) provides mean raft speeds of 1.4 cm/s from the southwest common 60-cm rafts and 1.9 cm/s for 90-cm rafts. The "simulta- and southeast comers to 0.9 cm/s for the sheltered northwest cor- Figure 7. Water through-flow speeds in rafts with 6(l-cm (dark shading! and 90-cni (light shading) rope spacing in relation to the speed of the ambient flow on August 8, 1994. 30 Boyd and Heasman 1UU + „ 5 o 80 c + 0) 0) 60 1*- ■ + + + + -5 + + ? 40 ■ + + o : f t* -+ u. + ■++«- 90cm - + , „ 20 E + ■ ; + 60cm ■ ._ ■- ■ a ■ Si .■ -. - • ■ I ■ 60cm sp acin g + 90cm spacing | Figure 8. Individual ratios of internal to external flow for rafts with 90- and 60-cm rope spacing. ner (see Fig. 3). Comparing Tables 1 and 2 shows that the overall relation to ambient flow is of the order of 1 5'^/< for these large rafts, with proportionally lower values at higher ambient speeds, sug- gesting some nonlinearity. From the above summary, and supported by the various de- scriptions provided earlier, a "'working value'" of mean through- flow speed for all rafts in the Sea Harvest farm is suggested to be 1.25 cm/s (17% of mean ambient flow). In terms of volume (or area) of water flowing through a raft of 11x14 m (154 nr) along the long axis, this amounts to three rafts per hour or 77 rafts per day (i.e., approximately 1.2 Ha). The ambient flow speeds in Saldanha Bay were found to be dependent on depth (Weeks et al. \'~)9\. Bilski 1996) because of the dominant influence of wind forcing. At 5-m depth, currents were 509c of those al 1- or 2-m depth. This factor is not quantified further in this study, but rather is offset against the unavoidable undersampling in high wind conditions, noted by all previous stud- ies and also applicable here. THE REQUIREMENT FOR FOOD: THE IMPORTANCE OF ADVECTION The food requirements of a mussel raft within the Sea Harvest farm (Heasman et al. 1998, Grant et al. 1998) appear to be barely met in the rafts by a mean advection velocity of 1.25 cm/s and the measured phytoplankton food concentrations of Pitcher and Calder (1998). This marginal food balance is also consistent with the better growth of the 90-cm rafts with their higher tlow-through rate, because the primary limitation is How through the raft, not ambient advection. Heasman et al. (1998) estimate that the Sea TABLE 2. Mean speeds of the water flowing through the rafts at different sites In the Sea Harvest farm measured with mini-drogues (data set includes non-steady-state mea.surements). Site/Raft Date No. of Observations Means SD NW (90 cm) 6/8/44 23 0.88 0.50 NW (90 cm) X/X/94 27 1.19 0.77 NW (60 cm) 8/8/94 35 0.73 I) 4(1 SW (60 cm) 9/8/94 27 114 0.78 SE (90 cm) 7/8/94 35 161 0.92 Overall 6-9/8/94 147 I.I 1 Harvest farm extracted between 1 6 and 35% of the plankton pass- ing through it. suggesting that subsequent farms (if screened by others) would receive substantially less food concentration. They would also receive it more slowly through reduced ambient flow speeds. The effect would be cumulative on each farm as the num- ber of suiTounding famis increases. In order to illustrate this nu- merically, a simple model was developed to show how a fami similar to Sea Harvest, but in a more uniform flow environment, could affect ambient flow speeds. This enabled results from this study to be used, and also, there is likelihood that similar technology may be used as mariculture in Saldanha Bay expands (Appendix A). The conclusion that can be drawn from this model are. first, that ambient upper-layer flow would be reduced by approximately 3% by each row of rafts within the farm, or 30% for the whole farm if flow through the farm was constrained on its sides by, for example, immediately adjacent farms. Second, it suggested that, for rafts of the same size, those that allow greater through-flow speeds would actually retard the ambient flow more (up to a cer- tain maximum) than those with slower through flow. In terms of advection, the new lease Site 2 appears well situated to receive near-surface advection from the south, driven by the dominant southerly winds. Away from the vicinity of the jetty, the data of Weeks et al. ( 1991 ), Bilski ( 1996), and Boyd and Spolander (unpubl.) show velocities of the order of 10-15 cm/s northward. However, with the expansion of mussel farming in Site 2, and the resulting slower water speeds, there may be an extension of the pressure gradient force from north to south ( see Fig. I ), which would oppose advection over the lease area, lower advection being accompanied by a further reduction of food concentrations. This would not affect the '"potential production" of the bay but could result in declining yields in Site 2. In turn, this could lead to requests for new lease sites to make the bay-scale production es- timates possible. The highly productive waters of the Ria de Arosa in northern Spain (Navano et al. 1991) show a widespread distribution of mussel farms. Nevertheless, with regard to variations in food avail- ability, the authors acknowledge "...the farmer's empirical knowledge that mussels from rafts on the borders of a grouping grow faster than those from the inner part . . .". This effect is related explicitly to food availability and quality by the authors, but advection would also play a role. Very few field studies of hydrodynamics in relation to mussel farming could be found in the literature. Gibbs et al. (1991) ex- amined water column properties and flow rates for the farming areas of Pelorus Sound. South Island, New Zealand, and identified the characteristics of different regions. Sheltered embayments showed longer flushing times than did regions closer to the main channel, and tides and freshwater inflow were the main forcing factors in a two-layer system. Saldanha Bay is also a two-layer system, but wind is the main factor, complemented by tides, and '"sheltered" regions have yet to be positively identified. An ac- celerated flow immediately below the mussel curtain was observed by Gibbs el al. (1991) but still with stronger flow at depth than within the ropes. They reported an approximate reduction in the flow within farms (composed of long lines of ropes parallel to the current) to 30% of ambient, with ""the rest of the flow being forced below the farm or around it." The flow beneath rafts (and farms) in Saldanha Bay will be- come nunc importanl as the number of farms increases, but water velocities at 10-m depth are much less than those near the surface, being not directly affected by winds, which are the dominanl forc- ing factor over most of the bay (Bilski 1996). The conlnhulion by Wathr Flow Patterns in a Mussel Farm 31 hori/oiUal adxection of the upper layer sht)uld not be reduced to the extent where areas with long flushing times are created. A general slowing of circulation would also have ad\erse effects regarding build up of deposits on the bottom belov\ the rafts. It is therefore essential to commence baseline studies on both food concentration and mean adveclion velocities (as well as the use of appropriate models that have recently become available locally I P. M. S. Monteiro and S. A. Luger. CSIR pers. comm.]) together with the development of Site 2. An initial restriction on development to 300 Ha (Monteiro pers. comm.) is appropriate in order to provide time for the optimal use of Saldanha Bay's waters to be formulated, including the maintenance of the present high growth rates for mussel mariculture (Heasman 1946). APPENDIX A: CONCEPTUAL MODELING OF THE FLOW WITHIN A MISSEL FARM The objective of this model was to estuiiate the retardation of ambient water movement due to a mussel farm by considering an idealized farm using raft technology similar to that used at the Sea Harvest site. The following description and assumptions are with reference to Figure 9. and consider long a.\is flow constrained on the sides of the farm. 1 . The effect of each raft is to diverge the flow around it (Fig. 9a). 2. The flow reconstitutes before the next row of rafts (Fig. 9a). 3. If there v\ere frictionless streamlines around each raft, there would be no retardation of flow (Fig. 9b). 4. If the flow did not diverge, it would be slowed considerably (Fig. 9c). It is clear that the real situation will lie between the extreme cases described by Points 3 and 4. In order to solve for the overall retardation due to each row of mussel rafts, consider first the special case in which the time taken for ambient flow to move a distance L„ from one row of rafts to the next is the SAME as that taken for water to move a distance ( from just in front of a raft to recombine with the ambient flow several meters behind it. as shown in Figure 9d. Thus, the turnover rate is the same for the approximately 0.6 Ha of water surrounding the raft and that within the en\ elope of the raft itself. Expressed numerically: { hi v„ (1) where \\, is the ambient \elocity and \ is the internal velocity. This implies ( 20 m ■v„ (2) for the Sea Harvest farm v 100 m .5 cm/s X 7.5 cm/s (3) This implication is consistent with steady-state measurements. The retardatory effect of each row of rafts perpendicular to the flow will also be dependent on the raft density and width across the flow ; in this case, the flow envelope around rafts of 1 2-m width occupied about 20% of the crosstlow space, as shown in Figure 9d. and the resultant reduced speed can be estimated by the following method. Let the baseline case described in Figure 9b have a uniform velocity V„, ahead of the first row of rafts and also behind the rafts when the velocity flow field has recombined. This implies that, although the flow around the obstruction will be accelerated, the Figure 9(a) ambient uniform flow I ) ( i 1 1 W I 1 *( Row 1 flow effectively uniform before row 2 Figure 9(c) Row 2 boundary to constrain ; flow ' ' frictionless streamlines, no retardation hypothetical non- divergent flow Figure 9(d) y Lc Special cose: D [d = 0.2D] Figure 9. Conceptual modeling of steady-state flow through a mussel farm with water flow constrained on the sides. mean momentum of fluid mo\'ing through a distance L„ in a time Momentum = V,, x (D x L„ x h] x p (4) where h = "height" of ropes and p = water density. If part of the water is moving through a mussel raft of effective dimensions d and (. then the transport will replace an area d x f moving at V^^, with an area d x ( moving at v. Momentum = [V„ x D x L„ - V„ x d x < + v x d X f ] p X h (5) where v = (t/LJ V„ in this special case. The difference between the momentum in these two instances is: (V„- V) X dfph. or V„ diph (6) In order to consider the reduction of momentum in proportion to that of the volume D x L x h. take D = 1 . L^, = 1 . V^, = 1 : h = 1, p = 1; and the d and f values as fractions: d = 0.20; and ( = 0.2 giving v = 0.2. 32 Boyd and Heasman The difference in momentum amounts to 0.032 or 3.2% retar- dation for each row of rafts. If this is extended to 10 rows of rafts, and assuming that each row is constrained on its sides, the rows will act cumulatively to retard the overall flow, leading to retar- dation through the farm of -28%. The field study values of -7.5 cm/s within the farm and -1 1 cm/s outside the farm are consistent with the model estimate of retardation due to the farm, but given the variability of flow patterns in the Sea Harvest farm, this can be regarded as fortuitous. The dependence of Eq. 6 on ( as a variable should also be considered. The value of ( has not been measured, but its mini- mum value is obviously the size of a raft and 0.2 x L„ is viewed as a good estimate during steady internal flow. If I is increased to 0.3 L^^ with an appropriate increase in v (in order to maintain the special case) and all other values are constant, we get an increase in retardation to 0.042 (cf. 0.032). Taking Eq. 6 and differentiating with respect to ( . we find a maximum retardation of 0.050 occur- ring at (' = 0.5 L^, and v = 3.75 cm/s. The latter is not regarded as a realistic average velocity from measurements, or dimension in terms of the model, but suggests that the 90-cni rafts would slow the ambient flow more than those with a 60-cm spacing between ropes because of faster through flow, despite their having fewer ropes. This model was also examined without the special case that f ( : — V,,; and we let v = a — V^., (7) thus allowing faster (or slower) through flow at the same distance f. The momentum difference was formulated and differentiated with respect to a in order to find the maximum. The results were the same as for the previous case: indeed, what the new model substituted for a "single transfer" of a body of water of length 0.5 L„ moving at 3.75 cm/s, was 2.5 separate bodies of water of length 0.2 L„ moving at 3.75 cm/s. Note that the dependence of retardation (Eq. 6) on d/D is cru- cial, but only valid so long as d « D. thereby allowing space for accelerated flow around the rafts. Brundrit (UCT, pers. comm.) suggests that each raft may have a relatively fixed " 'critical"' through-flow velocity, which will tend to be maintained, provided that d « D such to allow for accelerated flow around the raft. The strong dependence of through flow on approach angle and forcing speeds suggests that such a fixed critical velocity was not generally operational here but could be during faster, more unifonn ambient flow. The above method could not be used with lines of mussel ropes across a current. In this case, each rope would apply friction to the flow, proportional to the square of the velocity past it. Because of the higher velocities associated with each mussel rope, and the possible lack of large open areas such as between rafts, the reduc- tion in ambient velocity could be greater than for the rafi situation and requires a separate investigation. ACKNOWLEDGMENTS We thank Sea Harvest for their support, Ms Lieze Swart for technical assistance. Professor G. B. Brundrit of the University of Cape Town for feedback on the model, and the two anonymous reviewers for their valuable criticisms. LITERATURE CITED Bilski. S. 1996. The characterisation of synoptic circulation patterns in Saldanha Bay. MSc Thesis. University of Cape Town, South Africa. 95 pp. Boyd, A. J. 1982. Small-scale measurements of vertical shear and rates of horizontal diffusion in the Miiithern Benguela Current. Fish. Bull. S. Afr. 16:1-9. Gibbs, M. M., M. R. James. S. E. Pickmere, P. H. Woods, B. S. Shake- speare, R. W. Hickman & J. lUingworth. 1991. Hydrodynamics and water column properties at six stations associated with mussel farming in Pelorus Sound. 1984-85. N. Z. J. Men: Freshwal. /?alloprovincialis make it a preferred culture species over the indigenous Choromytilus ineridionalis. Over the last 10 y. mussels in Saldanha Bay have been farmed on both longlines and rafts. Although several local and New- Zealand longline designs have been tried and tested, because of the high-energy nature of the bay during the early winter months, the longline farming method has been discarded in favor of rafts. The rafts, originally based on a Spanish design, have been modified considerably to cope with the high-energy environment. Two sizes of raft are currently used, both of which consist of wooden lattices supported by hollow asbestos cement floats. The larger rafts are 22 X 1 1 m with 29 crossbeams, whereas the smaller rafts are 15 x II m with only 19 crossbeams. The crossbeams are spaced 60 cm apart. The inussel ropes, which are suspended to an average depth of 6 m. are spaced, on the crossbeams, at either 60 or 90 cm. Spaced at 60 cm, the smaller rafts carry a total of 323 ropes, whereas the larger rafts carry 493 ropes (i.e., approximately two ropes per square meter). At a spacing of 90 cm. the smaller rafts carry 245 ropes and the larger rafts carry 374 ropes (i.e.. approxi- mately 1.5 ropes per square meter). To prevent the mussels from dislodging and sloughing off during rough seas, a 30-cm wooden peg is inserted every 50 cm down the length of each rope. Mussel growth in Saldanha Bay is rapid, and on average, each raft is harvested twice a year (Heasman 1996). Suspension feeders such as mussels have a remarkable capacity to filter the water column and to deplete the water of seslon. such that they may be food limited at high culture density (Navarro et al. 1991). Raft culture is particularly intensive in respect to the high density of mussels grown on the structure, and studies of raft culture in the Spanish Rias have demonstrated that there is local seston depletion due to suspension feeding (Perez Camacho et al. 1991 ). As stock density increases, there may therefore be a depression of bivalve growth rates and an increase in mortality caused by factors asso- ciated with overcrowding, all of which can threaten the economic viability of mariculture ventures (Grant el al. 1993). Moreover, research has demonstrated major differences in mussel growth rate between sites, confirming that environmental conditions can regu- late shellfish production and that bivalve growth can be predicted as a function of the environment (Grant et al. 1993). A means to predict the ability of Saldanha Bay to sustain mussel culture was therefore considered essential to the continued development of the shellfish industry and to the determination of the carrying capacity of the bay for mussel farming. The principal objective of this investigation was to establish the relationship between the food removed by inussels and the growth. 33 34 Heasman et al. Saldanha Bay ^^ Small Bay '^"-? ^ Study farm ^j-i SOUTH AFRICA \ #/ J,^ Saldanha Bay y Club IMykonos V^^^..^..^—- ----^ 250 500 Kilomelres 25 I Figure 1. Map of Saldanha Bay showing the position of the study farm. condition, and production of mussels cultured at the two different rope spacings. These estimates also contribute inputs to a carbon budget to be used to estimate the level of mussel production that can be sustained in Saldanha Bay (Grant el al. 1998). METHODS The study was conducted in a farm located in Small Bay. comprising approximately 60 rafts in a 50-ha lease (Fig. 1 and 2). Mussel Feeding The removal of food by mussels was examined in terms of chlorophyll (chl) a. phaeopigment. and particle volume concentra- tion. Chi a and phaeopigment samples were analyzed according to Parsons et al. ( I9S4|. and particle volume was measured by sizing and counting particles with a Coulter Multisizer according to Shel- don and Parsons (1967). Food removal by mussels was investi- gated on three spatial scales, viz.. rope, raft, and farm scales. Particle depletion by mussels at the rope scale was investigated on rafts with 6-ino-old ropes. A 50-mL water sample was collected from within the mussel mass on the rope by inserting a 6-mm- diameter tube 10 cm into the mussels on the rope. Further water samples were taken by means of an array of syringes from the outer perimeter of the mussels and at 5-, 15-. 25-. and 35-cni from the perimeter of the mussel mass. Samples were collected from ropes on the upstream, center, and downstream side of the raft. The removal of food at the raft scale was determined by col- lecting water samples upstream of the raft and at 4-m intervals along the longitudinal axis of the raft at a depth of 2 m. The rafts suspended ropes of mussels ranging in age from I to 7 mo. Samples were collected under varying conditions and seasons, and whenever possilbe water samples were collected simultaneously from rafts with 60- and 90-cm rope spacings U 63 (a) (H) (S) (@) Figure 2. .\ plan of the layout of rafts (.\ through Fl within the mussel farm. Rait Culiuri- of M. cmjawrovinciaus 35 Food renunal at the farm scale was assessed by exariiiiiiiig chl a depletion through the farm. Samples were collected from 2-m depths at six stations 250 in apart along the long axis of the farm. The first station was approximately 100 m in tront of and the last 100 m behind the larni. Mussel GroKlh, I'mductioii, and Conditidii Mussel growth rates were estimated by conducting eight growth trials. For each trial, 1.000 seed mussels were measured and bound onto a seed rope. Eight ropes were prepared in Ibis way and placed centrally down the long axis of a raft. A sample of 25 mussels from the top and bottom meter of each rope at either end and in the middle of the rafts was collected every month and measured. Six of the trials took place on two adjacent rafts. Rafts C and D. with rope spacings of 60 and 90 cm, respectively, i.e.. three trials on each of the two rafts (Fig. 2). Two trials were conducted from September 1 993 to March 1 994. two from March to September 1994, and two from October 1994 to March 1995. The remaining two trials were carried out on Rafts E and F from April to September 1993 (Fig. 2). Newly settled cohorts were ignored, and only the seed mussels bound onto the ropes were collected and measured. The condition of mussels was determined on a monthly basis as described by Crosby and Laurence (1990). Mussels between 65 and 85 mm shell length were collected, scrubbed, and placed in fresh water. This resulted in the instantaneous closing of the two valves, avoiding further intake of water. Mussels were individually placed in a container full of water, and the overflow was collected and measured. The flesh was then extracted, dried for 48 h at 80°C, and weighed. The dry mass of mussel flesh (g) was then divided by the volume of the mussel (mL), and expressed as a percentage to give an index of condition. The effect of rope spacing on total raft biomass. production, and marketable production was also investigated by harvesting a number of randomly selected ropes down the center of the longi- tudinal axis of the raft. Biomass was defined as the total mass of mussels of any size, harvested from a rope or a raft, after a period of time. Total production was defined as the biomass minus the initial seed mass, whereas marketable production also excluded settled seed and other unmarketable mussels. To measure the above parameters, the initial seed mass was weighed and the mus- sels on each rope were si/e graded and weighed at harvesting. Adjacent rafts were chosen on the assumption that food availabil- ity would be less variable than rafts further apart. To examine differences between all possible pairs of means, multiple comparison tests were conducted using Tukey"s test. Slopes of regression models were compared by analysis of covari- ance. RESULTS Chl a and Particle Removal Rope Scale There was a substantially greater \olume of particles in the water extracted from within the mass of mussels on the ropes than outside, presumably from a build-up of particles among the mus- sels as a consequence of reduced flushing (Table 1 ). The consid- erably elevated phaeopigment concentrations within the mussel mass indicated that these particles were of detrital origin. These degradation products totally dominated the plant pigment concen- trations within the rope of mussels. Both chl a and particle volume were generally lowest at the rope surface, indicating localized depletion of food in the immediate vicinity of the rope. Phaeopig- ment values decreased rapidly away from the ropes, with the result that the ratio of chl a to phaeopigment increased to >1 at the front of the raft. Downstream, however, the ratios remained <1 some distance from the rope, indicating a general increase in the detrital load through the raft and a subsequent decrease in the quality of food available to mussels. Raft Scale Substantially higher chl a and particle volume concentrations were available to mussels on the upstream side of a raft compared with those in the middle or downstream. The percent particle vol- ume removed from the water as it passed through a raft was sig- TABLE 1. The mean chl a. particle volume, and phaeopigment concentrations found inside, at the edge, and at various distances from 6-mo-old ropes of mussels. Ropes were sampled from the upstream (front), the middle, and downstream (back) sides of the raft (n = 2 for each rope position; standard deviation is shown in parentheses). Chl a Particle Volume Phaeopigments (mg m"') (mm"' X 10' m ') (mg m •') Distance Front Middle Back Front Middle Back Front Middle Back 10 cm 5.47 1.41 1.21 22.13 5.89 4.19 213.5 34.84 31.46 into rope (0.68) (0.15) (0.54) (7.25) (1.16) (1.86) (32.5) (5.11) (6.23) Rope 3.90 0.82 1.00 4.31 1.52 1.69 8.76 4.98 12.19 surface (3.33) (0.51) (0.33) (0.60) (0.66) (0.40) (2.98) (0.74) (8.82) 5 cm 3.25 1.64 0.73 5.41 1.95 0.90 8.23 2.61 3.47 (1.51) (1.26) (0.48) (1.16) (0.59) (0.14) (3.93) (2.21) (0.67) 15 cm 5.33 1.49 1.24 5.96 1.70 1 IQ 5,69 2.21 2.66 (4.44) (0.96) (0.72) (0.64) (0.70) (0.16) (2.03) (0.86) (0.61) 25 cm 4.72 1.31 0.32 6.76 1.87 1.22 3.83 0.86 1.15 (2.65) (0.93) (0.10) (0.58) (1.00) (0.31) (1.71) (0.42) (0.63) 35 cm 4.04 1.55 0.56 7.06 2.11 1.32 2.89 1.97 3.45 (2.11) (1.18) (0,26) (0.05) (0.12) (0.16) (0.80) (0..';6) (2.36) 36 Heasman et al. 30 50 70 PARTICLE VOLUME EXTRACTED (%) Figure 3. The relationship between the volume of particles and chl a removed from the water passing through mussel rafts. nificantly correlated with the percentage of chl a removed, indi- cating little discrimination hy mussels in removing particles whether or not they contained chl a (Fig. 3). The ropes on each raft are of uniform age. but within the farm, individual rafts vary from newly seeded rafts to those available for harvesting, at 6 or 7 mo. Rafts with ropes <2 mo old removed significantly less chl ci than did rafts 3 and 4 mo old. These in turn removed considerably less chl a than did ropes that had been in the water for longer than 6 mo (Fig. 4). These experiments were all conducted on rafts with rope spacings of 60 cm, with mature rafts capable of removing in excess of 90% of the chl a from the water. The efficiency of removal of particles also varied with rope spacing. Removal of both chl a and particle volume was signifi- cantly greater for rafts with 60-cm rope spacings than for rafts of the same age with 90-cm rope spacings (Fig. 5; Tables 2 and 3). 1 90 V-- p. V. 90 cm* • L V''^---. Chl. a 90 cm • • \\ n;---.. P.V. 60 cm • • 70 ChL a 60 cm • • 50 30 ^ ■^ ^^^ 10 • 1 _L 1 1 Front of rati 6 8 10 12 DISTANCE INTO RAFT (m) 14 Back ot raft Figure 5. Particle volume (P.V.I and chl a removal through rafts with 6-mo-old nmssels spaced al 60 and 90 cm. Chi a and particle volume removal through a raft therefore in- creased with both the age of the mussel ropes suspended from it and with decreased rope spacing. Farm Scale At the farm scale, marked differences were observed between chl a levels at the front and the back of the tarm (Fig. 6). Chl (/ distributions within the farm reflect phytoplankton spatial hetero- geneity resulting from several processes, including the effect of removal by mussel feeding. On the basis of current speed data in and around rafts of 1.2,'i and 7.5 cm s.~' respectively (Boyd and Heasman l4i-)8). and the rate of food removal by the rafts, it was 16 20 4 Back of raft Front of raft DISTANCE INTO RAFT (m) 16 20 Back of raft Figure 4. The percentage of chl a removed from water passing at 2-ni depth through rafts with mussels ranging in age from <2 mo to >6 mo. Rope spacing on all rafts was M) cm. \ eriical bars signify standard deviation. RAFI' CULTLIRK oh M. GALI.OPKOMNCIAUS 37 TABLK 2. Tlu' pi'ici'iil chl (f rt'iiKiiniii<: in thi' \\:itur on |);issin^ thniii^h 6-nu)-old mussel rafis "ilh 6(1- and y(l-cni rope spacing. DilTiTtnl superscripts indicate significant diiferences at p < U.U5. Chin (""() Chi fl ( Tf » till a ( f^f ) J I remaining at remaining at remaining at O Rope Spacing 4 m (SD) 8 m (SI)I 12 m (SD) z 60 cm 45.91" 31.73" 19.15^ < UJ ir (20.7) (9.15) (9.68) 90 cm 67.94" 52.57"'' 29.02" (32.22) (15.14) (2.88) calciiliitcd that 169f of the food particles delivered to the farm would be extracted if the water passed once through the entire fann. The observed reduction in chl a concentration of >309'<: from the front to the back of the farm may be a function of reduced flow in the more sheltered regions of the farm (Boyd and Heasman 1998). Growth and Production Mean mussel growth rates were plotted for growth trials con- ducted on rafts with 60- and 90-cm rope spacings during the period from September 1 993 to March 1995 (Fig. 7). and the slopes of the regression models of growth rate for these and the 1993 winter trials are compared (Table 4). The slopes of the regression models of growth rate from the top (Meter 1) and bottom (Meter 6) of sample ropes from both ends and from the center of the rafts tor the trials conducted between September 1993 and March 1995 are also compared (Table 5). Winter growth rates were significantly slower than those in summer, irrespective of rope spacing. Mussels on rafts with 9(}-cm rope spacing grew significantly faster than those on 60-cm spaced ropes during the winter of 1993 and the summer of 1993 to 1994. Similar observations were made during the 1994 winter and the 1994 to 1995 summer period; however, the differences were not statistically significant, possibly as a result of the masking effects of fouling (Table 4). Growth rate was also significantly affected by positon of the mussels on the ropes and by position of the ropes on the raft. However, there was no consistent trend for better growth in any one position within seasons. The mussels at the top of the center rope in the raft with 90-cm rope spacing showed signifi- cantly better growth than did the mussels at the same position in the rafts with 60-cm rope spacing during summer. Although this TABLE 3. The percent particle volume remaining in the water on passing through 6-nio-old mussel rafts with 60- and 90-cm rope spacing. Different superscripts inciate significant differences at p < 0.05. Particle Particle Particle volume (% ) volume ( % ) volume i%) remaining at remaining at remaining at Rope Spacing 4 m (SD) 8 m (SD) 12 m (SD) 60 cm 37.16*' 22.74" 20.44" (15.72) (16.01) (12.80) 90 cm 63.12" 5 1 .49"'' 29. L5" (16.02) (15.13) (2.87) 95 \ 85 > V J ^\- 75 ^ •^^ -i [ ^^ ■-^^^ ■ r 65 . ^^ 55 Water flov n^ ^ V ^ 250 Front of farm 500 750 1 000 1 250 DISTANCE INTO FARM (m) Back of farm Figure 6. The percentage of chl ii removed from water passing through the mussel farm. \ ertical bars signify standard deviation. trend was also evident in winter, the differences were not statisti- cally significant (Table 5), Biomass. production, and marketable production were found to be significantly higher for ropes spaced at 90 cm (Table 6). These differences were particularly evident for the production of medium and large mussels. From these data, it was inferred that the total harvest of marketable mussels from rafts with 90-cn'i rope spacings was greater than that from rafts with 6()-cm spacings, despite the reduced number of ropes (Table 1). Summer 10 20 Sept 14 1993 ■ South top □ Center bottom 40 50 WEEKS • Soulti bottom X Nortti top 80 Marcti 29 1995 O Center top A North bottom Figure 7. The summer and winter growth of mussels on rafts with 60- and 90-cm rope spacings. 38 Heasman et al. TABLE 4. Slopes of the regression equations for shell length as a function of time for rafts of different rope spacings (6(1 and 90 cm) over two summer periods and two winter periods. Different superscripts indicate significant differences at p < 0.05. TABLE 6. Mean mussel biomass, production, and marketable production (kg) for 6-m ropes on two adjacent rafts with different rope spacing (n = 16). The trial extended from September 1993 to March 1994 (n= 16). Season Rope Spacing (cm) /■ Regression Slope Parameter 60-cm Rope Spacing (SD) 90-cm Rope Spacing Summer 1993/4 Summer 1994/5 90 90 0.87 0.78 2.1 1-' 1 .95" (SD) Total biomass 273.87-' 326.89" Summer 1993/4 60 0.80 1.91" (35.89) (48.99) Summer 1994/5 60 0.83 1.85" Initial seed mass 20.2 r 20.2 r Winter 1993 90 0.80 1.46'-' (6.13) (6.13) Wimer 1994 90 0.81 1 .37"" To(al production 251.66'' 306.68'-" Winter 1993 60 0.82 1 .32'' (29.76) (42.86) Winter 1994 60 0.78 1.29'' Settled seed mass Marketable production 123.89' (20.77) 80.878 139.78' (24.84) 116.76" Condition Although there was a tendency fo • the con Jition of mussels to Small mussels (9.52) 18.43' (8.89) (10.93) 16.12' (4.71) be affected by the rope position within the raft of ropes, these differences were not statistica and by the spacing lly significant. The Medium mussels 39.04' (15.79) 51.33' (10.52) condition of mussels ir the center of the rafts tended to be lower Large mussels 23.4k'' 49.31' than that at either end. espeically on rafts with 60-cm rope spac- (3.88) (17.55) ings. The condition of mussels at the raft extremities not only appeared to be higher but were also less affected by rope spacing, reflecting excess food in these areas (Fig. 8). Small mussels, =65-75 mm shell length (SD; medium mussels, =76-83 mm SL; large mussels, =>83 mm SL. Marketable production = sum of production of small, medium, and large mussels. DISCUSSION Saldanha Bay is a highly productive systein providing a food environment and temperature regimen optimal for the farming of the mussel M. gallopivviiicialis. The dense culture of mussels on rafts is responsible for local limitations in food supply at the scale of the raft, requiring bay, farm, and raft scale approaches to the estimation of carbon flow through the mussels (Boyd and Heas- man 1998). The bay is characterized by subsurface nitrate input and high chl a levels for most of the year (mean water column chl a of 8.62 mg nr'; Pitcher and Calder 1998). Phytoplankton vari- ability is controlled primarily by changes in the physical state of the bay as determined by inputs of eneigy with the coastal up- welling system and the atmosphere (Pitcher and Calder submitted), and because suspended food reaches bivalves through advection, an appreciation of water circulation and exchange is also required to estimate the sustainable level of mussel production in the bay (Boyd and Heasman 1998). Water entering rafts in Saldanha Bay therefore has a high seston load, exceeding the pseudofeces threshold of mussels (Fos- ter-Smith 1975, Widdows et al. 1979, Ki(t>rboe et al. 1980, Bayne et al. 1989, Bayne et al. 1993). The situation in the raft interior, however, is different. Current speeds decay as water progresses through the raft, as does the food supply, with chl a and particle volume concentrations reduced by 67 and 77%, respectively, for rafts with rope spacings of 60 cm. The greater food removal by older seed ropes spaced at 60 cm is therefore a function of both increased feeding and greater retardation of water exchange through rafts with more mussel mass. Thus, the marginal food balance within rafts is primarily a consequence of limited flow through the rafts, rather than ambient advection. Here, mussels may compensate for lower food availability by altering their feed- ing behavior. Assuming food quality is high, the ventilation period would increase, as would filtration rates, no pseudofeces would be produced, gut passage time would be increased, and assimilation TABLE 5. Slopes of the regression equations for shell length as a function of time for different positions on a raft, i.e.. south end, center, and north end, and top and bottom of each rope, (irowth trials took place over sunmier and winter periods on rafts with different rope spacings (60 or 9(1 cm). Different superscripts indicate signiFicant differences at p < 0.05. 1993 to 1994 1993 to 1994 1994 to 1995 1994 to 1995 1994 1994 60 cm 90 cm 60 cm 90 cm 60 cm 90 em Position Summer Summer Summer Summer Winter Winter South top 1.94"^ 1 .98' l.S'' 2.18" i.,W 1..36' South bottom 1.97' 1.92'= 1 .67'' -> T^t' 1.32' 1.25' Center top 1 .97' 2.34" 1.6.3'' 1 l')^ 1.38' 1 .39' Center bottom 2.02' 1.94' 2.07"" 2.20" 1.38' l.28'8 North top 1.99' 2.35" 2.12" 1.96' 1.268 1.17*^ North bottom 2.22" 2.39" 2.19" 1 .96' Storm damage 1.47' RaKI' CULniRH OK M. CAl.l.OFROVINCIAlJS 39 TABI F 7. Mean production ol inurki'tuble mussels (kj;! for two sizes of raft, each with different rope spacing. Small Raft (15 X II ml Large Raft (22 X 11 m) 6(l-cni Rope Spacing 9((-cni Rope Spacing 6()-cni Rope Spacing 90-cm Rope Spacing Marketable Production 26.121 28.606 .^9.869 4.1.785 and absorption efficiency would improve (Bayne el al. 1989. Bayne et al. 19931. Despite possible compensation, it appears that at a rope spacing of 60 cm, insufficient food reaches the center of the raft for optimal mussel growth and production. With a rope spacing of 90 cm. the delivery of chl a and particle volume to the center of the raft increased by 14 and 26%, respectively, and this is reflected in the growth rate of mussels. At a given rope spacing, the summer growth rate is 30% faster than the winter growth rate, and during summer, mussel growth rate on ropes spaced 90 cm apart is a further 8% higher than those spaced 60 cm apart. At the time of harvesting, a 30% increase in the production of marketable mus- sels was measured from ropes suspended at the increased spacing. Consequently, the total harvest of marketable mussels was calcu- 18 1 gl6 ■ 2 O 14 H Q §12 O 60 cm- 90 cm^ '\. __; >^ ■ "" \. 10 •^ '- , South Center North Figure 8. The condition index of mussels on rafts with 60- and 911-cni spaced ropes. lated to be 9% higher from the rafts with lower rope density. The increased rope spacing also reduces the growout period to market- able size by 2-4 wk. which given the exceptionally fast growth rates of mussels in Saldanha Bay. is significant in terms of farm management and annual production. ACKNOWLEDGMENTS We thank the management of Sea Harvest Corporation and in particular Mr. Andre du Plessis for their cooperation and logistical support during the field studies. LITERATURE CITED Bayne. B. L.. A. J. S. Hawkins. E. Navarro & I. P. Iglesias. 1989. Effects of seston concentration on feeding, digestion and growth in the mus.sel Myriliis edulis. Mar. Ecol. Prog. Ser. 55:47-54. Bayne. B. L., J. 1. P. Iglesias. A. J. S. Hawkins, E. Navarro. M. Heral & J. M. Deslous-Paoli. 1993. Feeding behaviour of the mussel. Myliliis edulis: responses to variations in quantity and organic content of the seston. J. Mar Biol. Assoc. U.K. 73:813-829. Boyd. A. J. & K. G. Heasman. 1998. Shellfish mariculture in the Benguela System: water flow patterns within a mussel farm in Saldanha Bay. South Africa. / Shellfish Res. 17:25-32. Crosby. M. P. & D. G. Laurence. 1990. A review and e\ aluation of bivalve condition index methodologies with a suggested standard method. J. Shellfish Res. 9:233-237. Foster-Smith. R. L. 1975. The effect of concentration of suspension and inert material on the assimilation of algae by three bivalves. / Mar Biol. Assoc. U.K. 55:411-418. Grant. J.. M. Dowd. K. Thompson, C. Emerson & A. Hatcher. 1993. Perspectives on field studies and related biological models of bivalve growth and carrying capacity. In: R. F. Dame (ed.). Bivalve Filter Feeders in Esluarine and Coastal Ecosystem Processes. Springer- Vedag. Berlin NATO ASl Series. 33:371-420. Grant. J.. J. Stenton-Dozey. P. Monteiro. G. Pitcher & K. Heasman. 1998. Shellfish mariculture in the Benguela System: a carbon budget of Saldanha Bay for raft culture of Mytiliis galloprovincialis. J. Shellfish Res. 17:41^9. Heasman, K. G. 1996. The influence of oceanographic conditions and cul- ture methods on the dynamics of mussel farming in Saldanha Bay. South Africa. MSc. Thesis. Rhodes University. South Africa. Hecht, T. & P.J. Britz. 1992. The current status, future prospects and environmental implications of mariculture in South Africa. S. Afi: J. Sci. 88:335-,342. Ki-^ AFRICA (iiso'y /^ Club J..- SALDANHA \ BAY y Vlykofios ^V^--'^' 250 500 h MLOMETRES Moriculturc ■ Monitoring buoy 2.5 KILOMETRES Figure 1. Map of Saldanha Bay illustrating the areas of mussel ciilli>uti()n. Carbon Budget of Saldanha Bay 43 trients, a dependence on this source would ultimately graze down the standing stock and signify exceedance of carrying capacity (Wassmann 1^)8S). Annual cycles of primarv production in Saldanha Bay are closely tied into upwelling-dri\en entrainnient of nitrate into the euphotic zone, with new production being about 20<7r of total production (Monteiro et al, 1998). Studies of chlo- rophyll dynamics in the bay indicate several scales of variability including seasonal and interannual (Monteiro and Brundrit 1990. Pitcher and Calder 1998). Chlorophyll is generally high throughout the year, reaching values of >50 p,g L"', and is low only during the brief austral winter period when upwelling winds are inactive and chlorophyll declines to <.'i p.g L"' (Pitcher and Calder 1998). On shorter time scales, there are recurrent peaks in chlorophyll with 6- to 7-day periodicity due to wind events and a subsequent relax- ation phase (Monteiro et al. 1998). An annual average for new production in Saldanha Bay has been estimated from the turbulent diffusion of nitrate into the euphotic zone based on temperature profiles and nitrate-temperature relations (Monteiro et al. 1998). Application of a Redfield ratio to nitrate flux yields a new pro- duction of 0.62 g of C m " d"'. Moreover, an estimate of new production in Saldanha Bay derived from an entrainnient model of exchange across the thermocline and average nitrate concentration produced a similar value (Monteiro et al. 1998). We recognize that there may be periods during which mussels are more food limited (e.g.. winter) and that an annual estimate of primary production averages out these periods. Averaged over the 12-m water column, the standing stock of total phytoplanktoii carbon based on chloro- phyll measurements (Pitcher and Calder 1998) and C:Chl = 50 is 5.2 g of C m"-. Despite the data record for phytoplankton. the dynamics of particulate organic carbon are poorly known for Saldanha Bay. The concentration of total organic particulates is consistently high through the year at -10 nig L~' (Heasman 1996). but the nature of this material is unknown. In contrast, other sites on the Cape Peninsula have been well characterized. Previous studies of these areas indicate that there is abundant kelp detritus in the water column, which provides significant nutrition for other mussel spe- cies such as Aulacomya ater and Choromytilus meridionalis (Grif- fiths 1980. Stuart 1982. Fielding and Davis 1989). Saldanha Bay is not kelp rich, but the red macroalga Gracilaria verntcosa grows in subtidal beds and appears on the beaches in massive detrital wracks (Simons 1977). Detritus from Gracilaria sp. has a C:N = -6. similar to phytoplankton. and is known as a nutritional food source for deposit-feeding polychaetes (Tenore 1977). For the pur- poses of our carbon budget, we have assumed that all upwelled nitrogen is channeled into new phytoplankton production, leaving none for macrophytes. Although this approach accounts for all of the new production arising from new nitrogen, it allows all pro- duction to occur in a labile form (phytoplankton cells) and creates a maximal estimate of food supplies available to mussels. Exchange and Predicted Mussel Prnductinn The passage of water through the lease is used as a measure of food delivery via tidal and/or wind-driven exchange. For an aver- age flow of 7.5 cm sec ' in the upper 6 m (Boyd and Heasman 1998). the transit time of a particle through a hectare of water (assuming no impedance by rafts) would be 0..^7 h. resulting in 65 turnovers of water through a raft site per day assuming 24 h of flow. In summer, the production:biomass (P:B) ratio of the phy- toplankton in the euphotic zone based on measurements in Pitcher and Calder (1998) and C:Chl = .50 is I.I. so that the standing stock of phytoplankton responsible for estimated new production is 0.54 g of C m'. The transport tlux of phytoplankton carbon to a culture site is 65 times this value. .^5.1 g of C m"-^ day*'. Adding in the daily primary production to this value (0.62 g of C m"^ day"') results in a food supply of ~.^6 g of C m"' day"'. Despite this potentially large delivery of food, the flow through the mussel ropes reduces the ambient How by a factor of 6 to 1.25 cm sec" (Boyd and Heasman 1998). If we apply this reduction to a whole hectare containing a raft, the exchange becomes 10.8 turnovers day"'. The flux of food arising from new production and its trans- port through the rafts is thus 5.8 g of C m"" day"' + 0.62 g of C m"" day"' primary production = -6.4 g of C m"" day"', assuming that the entering water is "new" and unfiltered. Because new phytoplankton production can be exported as secondary produc- tion, this value represents an estimate of potential mussel yield arising from nitrate-driven phytoplankton production and under- scores the potential effect of culture conditions on shellfish pro- duction. Observed Mussel Production Measurements of seeded mussel biomass and seasonal harvest were obtained from data in Heasman (1996) and Heasman et al. (1998). Values expressed as shell-on wet weight were multiplied by 0.053 to convert to shell-free dry weight (Palinerini and Bianchi 1994). Tissue carbon content was assumed to be 40%. These re- sults (Table 1 ) indicate that the bulk of summer biomass is in recently seeded juveniles obtained from the summer reproductive period (van Erkom Schurink and Griffiths 1991 ) rather than from harvested adults. We expect that nonpredatory mortality in raft culture will be low (Fuentes et al. 1994), so that the seeded mus- sels, even if not harvested, also represent a net annual sink for new production. In winter, the seeding of juveniles is reduced as is harvest of adult standing stock. Summing the annual juvenile and adult production, the total carbon production of cultured mussel biomass, normalized to the culture area (i.e.. over the entire hect- are), is 175 g of C m"- y"' or 0.48 g of C m"" day"'. This value is only about 7.5% of that calculated for advected new production (6.4 g of C m"" day"'). However, other carbon sinks must be accommodated before system carrying capacity can be calculated. Oilier Carbon Sinks It should be recognized that <100% of the phytoplankton will be grazed by mussels and that some primary production will go to other grazers. Some of these groups such as deposit feeding benthos beneath the rafts are fueled by mussel feces (Tenore et al. 1982, Grant et al. 1995) and thus represent no further demand on primary production. Similarly, the microbial loop is fueled by regenerated production. In contrast, there may be net consumption of new primary production by the fouling organisms that inhabit the mussel ropes (Lesser et al. 1992). primarily the tunicates Cioiia iiuestinalis and Pxura stohmifera (Heasman 1996). Pyura tends to occur in more exposed conditions and is less common in the shel- tered waters of Small Bay. Ciona is abundant in Small Bay but is variable in depth distribution on the mussel ropes as well as hori- zontally through the rafts (Heasman 1996). On the basis of the latter sampling, a reasonable estimate of Ciona density is 9.4 x 10^ individuals per rope, with 332 ropes per raft. Our measurements indicate an average dry weight of 0.72 g per individual and a carbon content of 26.13% (Slenton-Dozey and Grant unpubl.). 44 Grant et al. TABLE 1. Seeded biomass and annual yield in Saldanha Bay raft culture of M. galluprovincialis. Wet Weight Wet Wei; ght Tissue Dry W eight Tissue Dry Weight Production Variable (kg rope"') (SD) (kg rope ' 1 (kg m~- raft y"') • g of C m- y ') Initial seed 20,2 6.1 1,1 2.9 14,2 Summer Seed 123.9 20.8 6.6 18 87,2 Yield 80.9 9.5 4.3 11.8 .56,9 Summer sum 204.8 30.3 10.9 29.8 144,1 Winter Seed 13.5 10.1 0.7 2 9,5 Yield M).5 7.7 1.6 4.4 21,5 Winter sum 34 17.8 2.3 6.4 31 Total sum .^6.2 175.1 Summer includes values from September to March, and winter includes values frcmi April In September, Initial seed is the planted juvenile biomass; summer and winter seed refers to secondary settlement of juvenile inussels; and yield is the commercial harvest of adults, SD. standard deviation. Production values in the last column are expressed over the whole culture area (1 raft ha"'). Although we do not have P;B estimates for C intestimiUs. it is well known to be an annual species, with drastic seasonal declines in population biomass and a high reproductive investment (Svane 1983). Petersen and Svane (1995) measured juvenile mortality of 70% for this species in the field over several weeks. We assume that the net production (including mortality) for C. intestinalis is annual replacement of biotnass (P:B = 1), resulting in a carbon requirement of 58.7 g of C nr" y"' or 0.16 g of C m"" day"' from advected new production. Zooplankton are the other pelagic grazers that potentially com- pete with cultured mussels (Hanson et al. 1986). Because the Ben- guela region has been extensively studied, there are estimates of zooplankton production for the coastal ocean, although not spe- cifically for Saldanha Bay, where there are only limited data (Grindley 1977). On the basis of a variety of studies including grazing experiments, growth, and egg production. Hutchings et al. (1991) estimated that copepods and euphausiids in the southern Benguela had a production of 45 g of C m ~ y"' (range = 1 1-79), equivalent to 0.12 g of C m~" day"'. Benthic suspension feeders such as clams and natural mussels are abundant in many culture locations, including Saldanha Bay (van Erkom Schurink and Griffiths 1993). Christie and Moldan (1977) sampled a transect of benthic macrofauna leading away from a fish plant in Saldanha Bay. A single station containing the mussel C. meridionalis had 75.44 g ash-free dry weight m"" of bivalves, among the highest biomass in their survey. Applying a P:B ratio of 2 for adults of this species (Griffiths 1981) and an organic carbon content as 50% of ash-free dry weight yields 75.4 g of C m"" y"' as annual production, or 0.21 g of C m""' day"'. Although this extrapolation is based on a limited area, C. meridi- oiudis is locally dense in the vicinity of Saldanha Bay (van Erkom Schurink and Griffiths 1990). This value is less than half of mussel production in the culture area, but the calculation is highly depen- dent on the biomass of benthic suspension feeders in the bay. Exchange and System Carbon Prodmlinn Knowledge of consumer production and primary production may be used to derive an exchange rale necessary to deliver the required phytoplankton carbon to a hectare of culture area; Mussel production + other carbon sinks = phytoplankton standing stock * exchange + primary production (I) Using a phytoplankton standing stock of 0.54 g of C iii"^, primary production of 0.62 mg of C m"" day"', and the terms for mussel, fouling, zooplankton. and benthic production calculated abcwe yields an exchange rate = 0.65. almost an order of magnitude lower than the observed exchange rate based on current meter measurements through the rafts. A bottom-up approach indicates that there is more food available through continuous advection of new production than is required by the demands of secondary production estimated in a top-down approach. Furthermore, the calculated exchange rate necessary to provide advective renewal of phytoplankton is less than the estimated exchange rate derived from flow through the rafts. System New Prodmlinn In the above calculations, we have allowed new production to be delivered to our hypothetical lease with no limitation on the supply of external phytoplankton. However, an upper limit on mussel production in the bay would ultimately be controlled by total new production, in our case, calculated over an area of 4,480 ha. The exchange required for the food from 4,480 ha to be avail- able to mussels cultured in the leased area of 1,000 ha is simply the ratio of the two areas, resulting in a turnover of 4.5 day"', less than half the exchange calculated to occur through the rafts. These calculations provide even ftirther evidence that there is not a local limitation of food delivery and that our estimates of water ex- change and food delivery are reasonable. Sedimentation Rate Sedimentation rate of particulate organic matter from mussel biodeposition reflects the ingestion and the processing of organic carbon by the cultured animals. Collection of feces in the field can be used to accurately assess bivalve absorption (Cranford and Har- grave 1994). and sedimentation measurements in the vicinity of the culture area provide a crude check on the carbon budget calcula- tions that \vc ha\c made. Monteiro (unpubl.) used sediment traps beneath a rail in Small Bay to measure a sedimentation rate of 13.3 X 10' kg of POM raft ' y '. Assuming that POM is 50% particu- Carbon Budget of Saldanha Bay 45 late organic carbon (POC). that phytoplankton arc absorbed with an efficiency of 40-80% (van Erkom Schurink and Griffiths 19')2; Rosenberg and Loo I'JS.'?). and that all of the sedimentation is due to mussel feces, the daily ingestion required to supply the resulting biodeposition rate of 1.82 g of C m"' day"' is 3.03-9.10 g of C m~- of lease area ( 1 ha). With a 30"^ gross growth efficiency, this ingestion would support a production of 1-3 g of C m~" day '. larger than the observed mussel production (0.48 g of C m"" day''). However, the estimate based on sedimentation must be considered a maximum production estimate because all of the deposition does not arise from mussels. Grant et al. (1995) showed that longline culture of Mytiliis ediilis increased sedimentation rate by a factor of 2 over a background value at a similar control site. DISCUSSION Exchange as a IJmiling Factor It is apparent that in addition to the bay-scale input of nitrate that affects food production for mussels, there is a raft-scale ex- change rate that may limit their secondary production. The fric- tional effects of the hanging mussels and their proximity to adja- cent mussel ropes cause restricted flow of water through the raft compared with the ambient unimpeded flow (Boyd and Heasman 1998). The magnitude of this flow reduction may be assessed with an approach used by Jackson and Winant (1983) to look at flow through kelp forests. The drag (D) exerted by individual mussel ropes is described as D = Cu Qvr dl (2) where C,-, = drag coefficient (0.5 for flow approaching a cylin- der), Q = seawater density ( 1.03 g cm"'), u = ambient velocity, d = diameter of the cluster of mussels surrounding the rope (-50 cm), and 1 = rope length (5 m). For a culture density of three ropes per square meter (Heasman et al. 1998), drag per unit area of the raft is thus 0.43 u". In comparison, Jackson and Winant (1983) found a value of 0.15 u" for a kelp forest, or about 1 times greater drag than on a sandy bottom. The drag of the mussel ropes is about three times greater than the kelp forest value, and therefore 30 times greater than over a bare bottom. Because drag scales as u~, current reduction should thus be on the order of 30"^^ or 5.5. This agrees well with the observed current reduction for Saldanha Bay culture of six times (Boyd and Heasman 1998). As the water progresses through the interior of the raft, the speed will decay successively, as will the food supply and potentially, mussel growth (Grant 1996, Boyd and Heasman 1998). These calculations do not account for the interaction of the adjacent ropes, which will be a function of the boundary layer and wake region associated with each one. Wind tunnel experiments with adjacent cylinders (Bearman and Wadcock 1973) indicate that a spacing of one cylinder diameter or less causes instability in the wake region of the flow , and more or less drag than an isolated cylinder depending on how close they are. At a 60-cm rope spacing and with a 25-cm radius surrounding the rope due to the mussel shell layer, the mussel culture units are far less than one diameter apart, covering -50% of the raft area. Studies by Eckman et al. (1981) suggest that in bottom boundary layer flow, coverage by roughness elements >8% may induce skimming flow such that the water goes around rather than through the obstruction. It is appar- ent that the dense culture of rafts will limit water exchange, al- though this factor does not necessarily present a limitation to mus- sel growth, as calculated above. Our carbon budget suggests that the total secondary production in the vicinity of the rafts requires 0.65 exchanges per day, and so a reasonable guideline would be that new rafts he located where exchange is at least one per day. Comparison With Other Studies The harvest production of mussels in Saldanha Bay may be compared with that from other studies of raft culture to assess the carbon tluxes in relation to yield (Table 2). Detailed studies of mussel production have been carried out in both Ireland (Rodhouse et al. 1985) and the Galician Rias of Spain (Perez Comacho et al. 1991), the latter among the world's highest production. Many of the differences in production may be attributed to the biomass seeded, similar in Ireland and South Africa, but an order of mag- nitude less in Spain. Although the absolute harvest (per square meter of raft) is less in Spain, the efficiency of production (bio- mass/harvest) is highest there (Table 2). Ropes increase in wet weight by a factor of 9 in only 6 mo (Perez Comacho et al. 1991 ). each yielding three ropes for growout even after thinning. Saldanha Bay is less efficient than this, but more than twice as efficient as culture in the Irish example (Table 2) and in the Swed- ish mussel culture described in Rosenburg and Loo (1983). Har- vest efficiency is dependent on mortality as well as growth. Mor- tality figures are not available for Saldanha Bay, but a comparison between Irish and Spanish culture indicates that although the latter is -20% during the culture period (Perez Comacho et al. 1991), Irish culture mortality may be 50% of the harvest (Rodhouse et al. 1985). Mortality is partially due to mussels falling off the ropes, a factor that is related to storms and wave exposure. Despite the greater biomass seeded in Ireland compared with South Africa (Table 2), the latter is more productive, probably because of the enhanced food supplies of the upwelling system. The superior efficiency of Spanish production may also be attributed to up- welling-based primary production (Blanton et al. 1987), as well as the lower biomass per sleeve and reduced density of sleeves (1.23 ropes m~") compared with Saldanha Bay (3 ropes m~~). Ecosystem Carbon Fluxes The imposition of bivalve culture into bay ecosystems causes potentially large changes in the routing of primary production. Mussel rafts may consume more than 60% of the incoming chlo- rophyll (Rodhouse et al. 1985). with estimates of up to 88% for Saldanha Bay rafts (Heasman et al. 1998). Although values of raft consumption and fecal deposition may be normalized to a per- square-meter basis between studies, the absolute values of these rates are dependent on raft size, rope density, and stocking TABLE 2. A comparison of mussel hardest in relation to biomass seeded for tliree raft culture sites. Quantity Killary Harbour Saldanlia Bay Ria de Arousa Bioina.ss seeded 3.24 1.16 0.28 Harvest 6.9S 6.48 2.76 Yield/seed T -> 5.6 9.8 Kilfary Harbour. Ireland, data are for M. edulis (Rodliouse et al. 1985). while Saldanha Bay. South Africa, and Ria de Arousa. Spain (Perez Ca- macho et al. 1991 ). are data for M. gulloprovincialis. Saldanha Bay values are based on Table 1 data (Column 4) expressed as carbon. All values are in kg C m"" raft y"'. 46 Grant et al. density inside of socks (Table 2) and are thus difficult to compare even as normalized values. It is also useful to focus on ratios between processes, again considering a comparison of Saldanha Bay to carbon budgets of mussel raft culture based in Killary Harbour, Ireland (Rodhouse and Roden 1987, Rodhouse et al. 1985). and Galicia. Spain. There are few studies that attempt to document the competition between mussels and zooplankton. Working in the Ria de Arousa. Hanson et al. ( 1986) suggested that zooplankton clearance of water column phytoplankton could exceed 100%, even under productive upwelling conditions. Zooplankton grazing at raft culture sites has been examined in sufficient detail for comparison at several sites (Table 3). Comparing within the mussel culture areas (equivalent area for both zooplankton and mussels) for Saldanha and Ria de Arousa sites, mussel production exceeds zooplankton production by a factor of 4 and 18, respectively, despite the high zooplankton clearance rate mentioned for Ria de Arousa (Table ?'). In a system- wide context, the influence of mussels compared with most other ecosystem flows is entirely dependent on the relative extent of cultured area. In Saldanha Bay, the proposed culture area is 22% of the total area. Because of a large filtration capacity, mussels produce as much carbon as zooplankton, even on a baywide basis. At the Spanish site, mussel culture covers only 10% of the ria, yet system-wide mussel production is 43% greater than that due to zooplankton. In Killary Harbour, Ireland, the area in which rafts are deployed is apparently small (-1,200 m~), and thus in a bay- wide comparison, mussel use of phytoplankton is not large relative to zooplankton. We conclude that in bays with developing aqua- culture, zooplankton may take a significant portion of the food that TABLE 3. Comparisons of culture area and syslem-wide estimates of mussel production on rafts and zooplankton production for South African, Spanish, and Irish culture sites. Variable Saldanha Bay* Ria de Arousat Killary Harbourt Mussel culture area (ha) l.OOO 2,3U9 Bay area (ha) 4.480 23.000 729 Mussel production (culture area) (g of C m"- day-') 0.48 5.26 Zooplankton production (culture area) (g of C m'-day^') 0.12 \21A5 0.03 System mussel production (tons of C day^') 4.8 ISI.S 0.03 System zooplankton production (tons of C day-') 5.4 85.1 0.2 System-wide mussel calculations assume that mussel production is con- strained to the culture area, whereas sysleni-wide zooplankton production is extrapolated to the whole bay area. * Saldanha Bay: mussel production is derived from Table 1; zooplankton production is derived from values in Hutchings et al. ( 1991 ). t Ria de Arousa: mussel production is derived from values in Perez Ca- macho et al. (1991) assuming one raft ha-'; zooplankton consumption estimated during upwelling event from 107% clearance m-' day-' of 300 mg of C m-'. lO-m depth (Hanson et al. 1986). and 30% gross growth efficiency. i Killary Harbour: values from Rodhoiisc and Rodcn (14S7); missing val- ues not available. would otherwise be available to mussels through advection. As culture expands, mussels will consume far more food than resident zooplankton populations. The effect of epifaunal fouling on food resources available to cultured bivalves is also poorly known. In contained culture (e.g., pearl nets), there is little doubt that fouling causes physical dis- ruption to flow, which may inhibit water exchange (CUiereboudt et al. 1994). In suspended culture, there are various aspects of fouling that must be considered in order to assess its importance to mussel culture. First, mussels are often competitively superior and thus dominant members of fouling communities (e.g., Okamura 1986). especially in culture where suspended densities are so high. In terms of biomass, Rosenburg and Loo et al. (1983) indicated that mussel epifauna '"made up about 1% of the weight after 15 months and played a negligible role compared with the mussels in the transfer of energy in the community."' In a detailed study of epi- fauna on M. giilloproviniialis raft culture, Tenore and Gonzalez (1975) found that suspension-feeding epifauna (sponges, bar- nacles, sea cucumbers, sea squirts ) comprised up to 2 1 % of mussel biomass. Lesser et al. ( 1992) stated that the ascidian C. inrestiiuilis made up 25% of total biomass in rope culture. In Saldanha Bay. on the basis of the standing stock of C. intestinalis calculated above, its biomass would be 58.8 g of C m"", similar to the summer harvested biomass of mussels (Table 1 ) and markedly greater than the relative fouling biomass found in the above studies. Heasman ( 1996) states that mussel production on fouled ropes is only 25% of unfouled ropes, emphasizing the food competition due to these epifauna. Nonetheless, fouling biomass will be extremely depen- dent on recruitment patterns, temperature, water quality, and pre- dation pressure (Brault and Bourget 1985, Okamura 1986). In addition, there are spatial gradients in the distribution of fouling animals that include depth and rope position in the raft (Heasman 1996). Mus.sels clearly dominate epifauna with respect to filtration capacity. For example, in samples from a l-y-old mussel culture. Lesser et al. (1992) found that M. edidis had three times the fil- tration capacity of the solitary ascidian C. intestinalis. Petersen and Riisgard (1992) calculated that this ascidian could affect phy- toplankton populations in a Danish tjord. Our calculations suggest that fouling organisms do not represent a major net carbon sink in Saldanha Bay compared with mussels, because their biomass is turned over annually. However, more work is required to assess the importance of fouling on the carbon budget for Saldanha Bay. The influence of benthic consumption on food available for mussels is similar to that of other competing carbon fluxes in terms of the significance of suspension feeders that sequester new pro- duction. The microbial food web and smaller deposit-feeding benthos are active in recycling carbon and nitrogen and have not been included in our calculations. The benthic community beneath mussel culture has been well described and consists of opportu- nistic deposit feeders, adapted to the organic enrichment resulting from biodeposition (Tenore et al. 1982, Grant et al. 1995). In this respect, mussels decrease competition from the natural benthos by favoring a detritus-based community that is not sustained by pri- mary consumption of phytoplankton. Rodhouse and Roden ( 1987) consider that the benthos of Killary Harbour subsist entirely on detrital organic matter and biodeposition. Carrying Capacity of Saldanha Bay Our calculations indicate that the food required to support the existing production of raft culture is less than the estimated value Cakhon BuncET of Saldanha Bay 47 of food delivery based on exchange. Allhougli lliese calculations do not suggest limitation of food provision due to exchange, the levels of chlorophyll depletion measured by Heasman ( 1996). ap- proaching 9()''f . indicate that there is significant grazing pressure at the local scale. In order for carrying capacity to exceed new pro- duction, there must be import of phytoplankton from the open coast, a possibility during relaxation phases of upwelling (Pitcher et al. 1996). If the cairying capacity of Saldanha Bay is ultimately constrained by new production, then the question becomes one of culture extent and location, i.e., how much area is culti\able under a given culture method? An inipt)rtant consideration in answering this t|ueslion is that of the residence time of Small Bay. Although we can calculate that the renewal of water and phytoplankton at the raft exceeds the use of phytoplankton by grazers, this calculation assumes that the in- coming water is not particle depleted. As mussel culture increases, there is a greater probability that water passing through the raft has previously been filtered by other mussels. Small Bay (2,000 ha) has a ratio of 33: 1 to the area of the present Sea Harvest farm (60 ha). Without inhibition of flow by the rafts (average current speed = 7.5 cm sec"'), the turnover time of the bay through the farm would be 10 days. This value decreases with How inhibition. The residence time of Small Bay is on the order of 20 days (Boyd pers. comni.l. so that under conditions of How inhibition by the rafts >50'7f , Small Bay would be renewed by Big Bay and/or coastal water more rapidly than it would be filtered by the farm. In this sense, the upper limit on carrying capacity must be total new production for Saldanha Bay. Nonetheless, further insight into the comparative magnitude of these exchange processes is required. Assuming that because baywide new production is 0.62 g of C m~' for 300 days y"', and that the production area is 44.8 x 10'^ nr, annual new production for the Saldanha Bay (Big Bay and Small Bay) is 8,333 tons of C y~'. A summary of carbon sinks requiring the use of new phytoplankton production is in Figure 2. These calculations indicate that suspension-feeding benthos are the dominant carbon sink, followed by zooplankton, mussels, and fouling. There is a surplus of 654 tons of POC, about 37% of present mussel production, that is not required by pelagic or benthic secondary production. Because there is no drastic food limitation at the lease scale, production per hectare could poten- tially be increased by this percentage. However, there is unlikely to be completely efficient use of new phytoplankton production, i.e., phytoplankton may be unavailable because of advection or sedi- mentation. Moreover, there are a number of assumptions and ap- proximations in these calculations that cannot be quantified in their contribution to the "residuar' carbon. Far-field -Benguela upwelling M Advection/Diffusion- nitrate New primary production 8333 Zooplankton 1962 Mussels 1751 Fouling 587 5 Suspension-feeding benthos 3378 ..ij^^^B M^' Secjiment Figure 2. Carbon flux diagram for the routing of new primary production in Saldanha Bay. .All Hows are in tons of C y~'. Mussels and fouling occur only within the culture area, and their total production is expressed over the entire zone of new production in the bay (4,480 ha). 48 Grant et al. Nonetheless, from a management standpoint, it is worthwhile to double the number of rafts in several of the cultured hectares and compare growth with present culture levels as a test of the limits of stocking density. Beyond the calculated surplus carbon, it is possible to shift the carbon budget in favor of mussels to the detriment of other trophic groups such as zooplankton. as in the Netherlands (Van Stralen and Dijkema 1994). We recognize that the culture potential of Saldanha Bay is not uniform and that other factors besides food may limit production. For example, there are regions of Saldanha Bay with increa.sed wave exposure, leading to reduced growth of M. gallopro- viiwialis (Raubenheimer and Cook 1990). Although the carbon bud- get approach is useful, it provides only an initial and simplified estimate of carrying capacity. The most important components of the ecosystem — exchange and primary production — are averaged in both time and space. Factors such as two-dimensional circulation and win- ter lows in primary production are not included in the overall budget. There are major uncertainties that linut our understanding of carbon dynamics in the bay, and these are being approached in simulation modeling studies of Saldanha Bay. Finally, the importance of the Benguela upwelling to the car- rying capacity of Saldanha Bay for mussel culture cannot be over- emphasized. Monteiro and Brundrit (1990) documented interan- nual variability in Saldanha Bay chlorophyll as a result of warm water intrusion of nutrient-poor water that replaced nutrient-rich upwelling. The effects of this variability on mussel culture were examined by Blanton et al. ( 1987). who related upwelling intensity to mussel condition in Spanish raft culture. Because new produc- tion is a primary constraint on carrying capacity, further under- standing and prediction of phytoplankton and nutrient dynamics are at the core of managing culture density and extent in Saldanha Bay. ACKNOWLEDGMENTS Cedric Bacher provided helpful comments on the manuscript. The logistic support given by Sea Harvest Corporation and Atlas Sea Farms to K.H. is gratefully acknowledged. LITERATURE CITED Bearman. P. W. & A. J. Wadcock. 1973. The interaction between a pair of circular cylinders normal to a stream. ./. Fluid Mcch. 61:499-51 1. Blanton. J. O.. K. R. Tenore. F. Castillejo. L. P. Allcinson. F, B. Schwmg & A. Lavin. 1987. The relationship of upwelling to mussel production in the lias on the western coast of Spain. J. Mar. Res. 45:497-51 1. Boyd, A. J. & K. G. Heasman. 1998. Shellfish mariciilture in the Benguela System: water flow patterns within a mussel faini in Saldanha Bay. South Africa. J. Shellfish Res. 17:25-32. Brault. S. & E. Bourget. 1985. Structural changes in an estiiarinc subtidal epihenthic community: biotic and physical causes. Mar. Ecol. Pro,i;. Ser 2I:6.V73. Carver. C. E. A. & A. L. Mallet. 1940. Estimating the carrying capacity of a coastal inlet for mussel culture. Aquaculnire. 88:39-53. Christie. N. D. & A. G. S. Moldan. 1977. Effects of fish factory effluents on the benthic macrofauna of Saldanha Bay. Mar. Poll. Bull. 8:41—15. Claereboudt. M. R.. D. Bureau. J Cote & J. H. Himmelman. 1994. Fouling development and its effect on the growth of juvenile giant scallops {Placopecren mai^elUmicus). Aqmicidlure. 121 :327--<42. Cranford. P. J. & B. T. Hargrave. 1994. In situ time-series measurement of ingestion and absorption rates of suspension-feeding bivalves: Pla- copecten magellanicus. Limnol. Oceanogr. 39:730-738. Dame, R. F. 1996. Ecology of Bivalves: An Ecosystem Approach. CRC Press, Boca Raton, FL. 272 pp. Dugdale, R. C. & J.J. Goering. 1967. Uptake of new and regenerated forms of nitrogen in primary productivity. Liinuol. Oceanogr. 12:196- 206. Eckman, J. E., A. R. M. Nowell & P. A. Jiimars. 1981, Sediment destabi- lization by animal tubes. J. Mar. Res. 39:361-374. Fielding, P. J. & C. L. Davis. 1989. Carbon and nitrogen resources avail- able to kelp bed filter feeders in an upwelling environment. Mar. Ecol. Prog. Ser. 55:181-189. Fuentes, J., I. Rayero, C. Zapata & G. Alvarez. 1 4^*4. Inlliience of stock and culture site on growth rate and mortality of mussels iMytihis gal- loprininciulis Lmk.) in Galicia. Spain. AqiiacidtKrc. 105:131-142. Grant. J. 1996. The relationship ofhioenergetics and the environment to the field growth of cultured bivalves. J. Exp. Mar. Biol. Ecol. 200:239- 256. Grant, J., M. Dowd, K. Thompson, C. Emerson & A. Hatcher. 1993. Perspectives on field studies and related biological models of bivalve growth, pp. 371-420. In: R. Dame (ed.). Bivalve Filter Feeders and Marine Ecosystem Processes. Springer Verlag, New York. Grant. J., A. Hatcher. D. B. Scou. P. Pocklington. C. T. Schafer & C. Honig. 1995. A multidisciplinary approach to evaluating benthic im- pacts of shellfish aquaculture. Estuaries. 18:124-144. Griffiths, R.J. 1980. Natural food availability and assimilation in llie bi- valve Choromytilus meridionalis. Mar. Ecol. Prog. Ser. 3:151-156. Griffiths. R.J. 1981. Production and energy flow in relation to age and shore level in the bivalve Choroinyiilus mcntlionalis (Kr. ). Esiuar. Coast. Shelf Sci. 13:477-193. Grindley. J. R. 1977. The zooplankton of Langehaan Lagoon and Saldanha Bay. Trans. Roy. Soc. S Afr. 42:341-370. Hanson, R. B.. M. T. Alvarez-Ossorio, Cal R., M. J. Campos, M. Roman. G. Santiago, M. Varela & J. A. Yoder. 1986. Plankton response fol- lowing a spring upwelling event in the Ria de Arosa. Spain. Mar. Ecol. Prog. Ser. 32:101-113. Hatcher. A.. J. Grant & B. Schofield. 1994. Effects of suspended mussel culture (Mytilus spp) on sedimentation, benthic respiration and sedi- ment nutrient dynamics in a coastal hay. Mar. Ecol. Prog. Ser. 115: 219-235. Heasman. K. G. 1996, The infiuence of oceanographic conditions and cul- ture methods on the dynamics of mussel farming in Saldanha Bay. South Africa. M.Sc. Thesis. Rhodes University. Grahamstown. South Africa. Heasman, K. G., G, Pitcher, C. D, McQuaid & T, Hecht, 1998, Shelinsh maricultiire in the Benguela System: food delivery to mus,sel rafts in a high production environment and the effect of rope spacing on food extraction, growth rate, yield and condition of mussels. J. Shellfish Res. Henry, J. L. & S. A. Mostert. 1977. Phytoplankton production in Lange- haan Lagoon and Saldanha Bay. Trans. Roy. Soc. S. Afr. 42:383-398. Hutchings, L., S. C. Pillar & H. M. Verheye. 1991. Estimates of standing stock, production and consumption of meso- and niacrozooplankton in the Benguela ecosystem. S. Afr. J, Mar. Sci. 1 1:499-512, Jackson. G. A, & C. D. Winant, 1983. Effect of a kelp forest on coastal currents. Com. Shelf Res. 2:75-80. Lesser, M. P., S. E. Shumway. T Cucci & J. Smith. 1992. impact of hulling organisms on mussel rope culture — interspecific competition for hmd among suspension-feeding insertebrales. ,/, £'v/i. Mar. Hiol. Ecol. 165:91-102, Monteiro, P, M, S, & G, B, Brundrit, 1990. Interannual chlorophyll vari- ability in South Africa's Saldanha Bay system 1974-1979. S. Afr. ./. Mar. Res. 9:281-287, Carbon Budget of Sai.danha Bay 49 Monteiro. P. M. S.. B. Spolander. G. B. Brundiit & Ci. Nelson. In press. Shellfish mariculture in the Benguela System: nitrogen driven new production in Saldanha Bay. J. Shellfish Re\. Okanuira. B. 1986. Formation and disruptions of M\ulu\ ctliilis m ihe fouling community of San Francisco Bay, California. Mm: Emi Pnif;. Scr. .^0:27?-:s:. Palmerim. P. & C. N. Bianchi. 1994. Biomass measurements and weight- lo-weight conversion factors: a comparison of methods applied lo the mussel Mylihis gallnprovincialis. Mar. Biol. 120:273-277. Perez Coniacho, A.. R. Gonzalez & J. Fuentes. 1991. Mus,sel culture in Galicia (N.W. Spain). Aquacultun: 94:263-278. Petersen. J. K. & H. U. Riisgard. 1992. Filtration capacity of the ascidian Ciona intestinalis and its grazing impact in a shallow fjord. Mar. Ecul. Prog. Ser. 88:9-17. Petersen. J. K. & I. Svane. 1995. Larval dispersal in the ascidian Cinna iniesunalis (L). Evidence for a closed population, ./. /-.;/>. Mar. Rial. Ecol. 186:89-102. Pitcher. G. C. & D. Calder. 1998. Shellfish mariculture m the Benguela System: phytoplanklon and the availability of food for commercial mussel farms in Saldanha Bay. South Africa. / Shellfish Res. Pitcher. G. C. A. J. Richardson & J. L. Korrubel. 1996. The use of sea temperature in characterizing the mesoscale heterogeneity of phy- loplankton in an embayment of the southern Benguela upwelling sys- tem. ./. PUmkum Res. 18:643-657. Raubenheimer. D. & P. Cook. 1990. Effects of exposure to wave action on allocation of resources to shell and meat growth by the subtidal mussel. Mxtilus galloprovincialis. J. Shellfish Res. 9:87-93. Rodhouse, P. G. cS: C. M. Roden. 1987. Carbon budget for a coastal inlet in relation to intensive cultivation of suspension-feeding bivalve mol- luscs. Mar. Ecol. Prog. Ser. 36:225-236. Rodhouse. P. G.. C. M. Roden, M. P. Hensey & T. H. Ryan. 1 985. Pro- duction of mussels. Myriliis ediilis. in suspended culture and estimates of carbon and nitrogen flow: Killary Harbour. Ireland. J. Mar. Biol. As.wc. U.K. 65:55-68. Rosenberg. R. & L.-O. Loo. 1983. Energy-flow in a Mytilus cdulis culture in western Sweden. .Ai/itaciiltiire. 35:151-161. Shannon. L. V. & G. H. Stander. 1977. Physical and chemical character- istics of water in Saldanha Bav and Langebaan Lagoon. Trans. Roy. Soc. S. Afr. 42:441-460. Simons. R. H. 1977. The algal llora ol Saldanha Bay. Trans. Roy. Soc. South Afr. 42:461-477. Sluarl. V. 1982. Absorbed ration, respiratory costs and resultant scope for growth in the mussel Aiilacomya atcr (Molina) fed on a diet of kelp detritus of different ages. Mar. Biol. Leil. 3:289-.306. Svane. I. 1983. Ascidian reproductive patterns related to long-term popu- lation dynamics. Sarsia. 68:249-255. Tcnore. K. T. 1977. Growth of Cajntella capilala cultured on various levels of detritus derived from different sources. Limnol. Oceanogr. 22:936-941. Tenore. K. R.. L. F. Boyer. R. M. Cal. J. Corral. C. Garcia-Ferdandez. N. Gonzalez. E. Gonzalez-Gurriaran. R. B. Hanson. M. Krom. E. Lopez- Jamar. J. McClain. M. M. Pamatmat. A. Perez. D. C. Rhoads. G. de- Santiago. J. Tietjen. J. Westrich & H. L. Windom. 1982. Coastal up- welling in the Rias Batas. N.W. Spain, contrasting benthic regimes of the Rias de Arosa and de Muros. J. Mar. Res. 40:701-772. Tenore. K. R. & Gonzalez. 1975. Food chain patterns in the Ria de Arosa. Spain: an area of intense mussel aquaculture. lOth Eur. Symp. Mar. Biol. 2:601-619. van Erkom Schurink. C. & C. L. Gnffiths. 1990. Marine mussels in South- em Africa — their distribution patterns, standing stocks, exploitation and culture. J. Shellfish Res. 9:75-85. van Erkom Schurink. C. & C. L. Griffiths. 1991. .\ comparison of repro- ductive cycles and reproductive output in four southern African mussel species. Mar. Ecol. Prog. Ser. 76:123-134. van Erkom Schurink. C. & C. L. Griffiths. 1992. Physiological energetics of four South African mussel species in relation to body size, ration and temperature. Camp. Biochem. Physiol. 101 A:779-789. van Erkom Schurink. C. & C. L. Griffiths. 1993. Factors affecting relative growth rates in four South African mussel species. Aquaculture. 109: 257-273. Van Stralen. M. R. & R. D. Dijkema. 1994. Mussel culture in a changing environment — the effects of a coastal engineering project on mussel culture [Mytilus edulis L) in the Oosterschelde Estuary (SW Nether- lands). Hydrobiologia. 283:359-379. Wassmann. P. 1988. Primary production and sedimentation. Sed. Trap Stud Nordic Countr. 1:100-110. Joiinuil of Slwlljlsh Research. Vol. 17, No. I. 51-5S, IWX. COASTAL SHELLFISH RESOURCE USE IN THE QUIRIMBA ARCHIPELAGO, MOZAMBIQUE D. K. A. BARNKS,' A. CORRIP:," M. WHITTINGTON," M. A. CARVALHO,- AND F. GELL^ ^ Dcpailim'fit oj Zoology and Animal Ecology University College Cork Cork. Ireland 'Frontier The Society for Environmental Exploration 77 Leonard Street London. EC2A 4QS. United Kingdom Tropical Marine Research Unit Department of Biology University of York York, United Kingdom ABSTItACT The level, types, and influences of use of intertidal and subtidal molluscs and crustaceans were examined on four islands of Ihe Quirimba Archipelago in northern Mozambique. Artisanal collecting was restricted to spring low tidal periods and involved at least 5"* of the population of the study islands. Twenly-two mollusc species and tlve decapod crustascean species (.Pcilimiridae and Poruinidue) were collected, of which the large gastropods Chicoreus ramosus (Muricidae) and Fa.scii>la trapezium (fasciolaridae), were the most important on coral reef rubble shore regions. The bivalves Pinchula iiii>ra and Barbalia fii.sca were the most important species in seagrass [Hathodiile sp. and Cymodocea sp.) areas. The diversity and identity of target species and proportions of species taken by intertidal collectors differed between smdy islands. The mean length of the gastropods C. ramosus and F. trapezium collected on the larger islands of Quirimba and Quisiva have significantly decreased on the basis of examinations of previously collected middens. Those collected at Quirimba and Quisiva Islands were also smaller than current collections at the nearby smaller islands of Quilaluia and Senear. KEY WORDS: resource use, mozambique, intertidal, shellfish, fisheries INTRODUCTION Mozambique has the largest amount of coastline (2.700 km) of any country on mainland East Africa and one of the greatest de- pendencies on it (Macia and Hernroth 1995. Coughanowr at al. 19951. Toward the end of its 16-y internal conflict, in 1990. the gross national product per capita of Mozainbique was estimated at S80 U.S. (World Resources Institute 1993. Coughanowr et al. 19951. making it one of the poorest countries of the world. Ap- proximately two-thirds of the 16 million of the country's popula- tion live in the coastal zone, but there are still large coastal regions of mangrove and coral reef that are relatively undisturbed. The growth of the urban centers along the western Indian Ocean coastal zones coupled with the degree of countries" dependence on them has created inuch concern for the implementation of an Integrated Coastal Zone Management plan (Holdgate 1993. Linden 1993. Coughanowr et al. 1995). However, to date. Mozambique does not have such a plan, reflecting the overall lack of human and financial resources to perform studies on coastal management issues at the national level. The creation of strategic intertidal and marine re- serves has become an important, and arguably the most effective. management tool for preserving and boosting complex multispe- cies fisheries, not only in East Africa (Crawford and Bower 1983, Kennedy 1990. Andersson and Ngazi 1995). but throughout the world's tropical and subtropical regions (Alcala and Russ 1990. Roberts and Polunin 1991). East African coastal resource use takes a variety of forms be- sides fisheries. Many, such as live coral mining (Dulvy et al. 1995). sand inining causing coastal erosion (Semesi and Ngoile 1995). dvnamite fishing (Andersson and Naazi 1995). and man- grove deforestation (Coughanowr et al. 1995). have proved highly damaging, but in the short term are financially rewarding in often difficult socioeconomic conditions. The coastal zone of northern Mozambique is little developed, and the level of resource use is mainly limited to artisanal fisheries (local consumption), although some commercial fisheries also operate. The near-shore marine biology and resource use of northern Mozambique is poorly stud- ied, virtually unmanaged. and little known. The only coastal region of Mozambique that has approached the level of study afforded to much of the East African coastline is that of Inhaca Island (Gove 1993. Longomane 1995. Santana Afonso 1995). by virtue of its close proximity to Maputo. Studies of intertidal invertebrate re- source use have, at Inhaca Island as with virtually all other Indo- Pacific study locations, been very general in scope and focused little on the detail of species used and influences on individual species populations. In this study, we report on the level and type of use of molluscs and decapod crustaceans on four islands of the Quirimba Archi- pelago in northern Mozambique, based on interviews with artisa- nal intertidal collectors, observations of collections, and target spe- cies identifications and measurements. The findings are discussed relative to the most studied location in Mozambique. Inhaca Is- land, as well as resource use in other areas of East Africa and the Indo-Pacific states. THE COASTAL ENVIRONMENT The Quirimba Archipelago in the Cabo Delgado province of northern Mozambique consists of 27 islands of various sizes, of which Quirimba Island itself is one of the largest at 6.5 by 2.5 km (Fig. 1). The bathymetry of the marine area enclosed by the ar- 52 Barnes et al. Figure 1. Insert bottom left: the position of Mo/,unil)ique in southern Africa and the Qnirlniha Island Archipelago in northern Mozam- bique. Main map: the Quiriniba Island Archipelago with the five study islands marked (1) Quiriniba, (2) Quilaluia. (3) Senear. (4) Mefunvo,* and (51 Quisiva. The li^ht-shaded region is the intertidal /.one and shallows, with the reef edge marked as a jagged edge and sandflats marked as a smooth edge. *Only casual observations recorded. chipelago is very shallow, with intertidal zones spanning over 1 km and tidal ranges of about I m on neap tides and 4 m on spring tides. The sea temperature varied little around 25 C during the study period, but the salinity is highly variable because of the proximity of the islands to the deltaic mouths of the large Mon- tepeuz River. The eastern seaboard of the islands is coral reefs with typical associated intertidal zones consisting of reef crest, lagoons, and reef rubble areas. The intertidal of the western side of the i.slands is a mixture of sand flats, seagrass meadows (Halhodule sp. and Cyinodocea sp.). and mangroves (Avicciuiiti inmina. Ceriops lai>al. Rhizophora mncronata. and Biuiiieria fixmiuwhiza). Al- though there are extensive mangrove systems throughout the ar- chipelago, the four principal islands involved in this study. Quir- iniba. Quisiva. Quilaluia and Senear, have only isolated pockets of mangrove. The relatively large area of coastline encompasses a wide range of intertidal habitats and thus a high diversity of both molluscs and crustaceans, as well as representatives of 1."^ other phyla of animals (Barnes 1997, Barnes unpubl.). The Quirimba Archipelago has virtually no tourism, and the population of most of the islands ranges from approximately 3,000 (Quirimba) to 40 (Quilaluia). Of the study islands, only Quirimba has a freshwater supply, which is presumably the main cause of low population density ot ihc islands and relatively low fishing pressure on the intertidal and offshore water.s. Fishing and inter- tidal collecting are mostly for local consumption and constitute the main source of protein and income for the islanders, although trade is comparatively limited. One of the major anthropogenic influ- ences on the coastal environment is probably that of deforestation of the mangrove systems, principally to build homes, but no reli- able figures are available for the extent of this activity. METHODS The number of fishermen (people collecting) on the intertidal zone of the western shore of Quirimba Island was counted with binoculars daily between July 20 and September 2. 1996. The daily tidal range was calculated and noted for these dates from local tide tables. Observations were made on collection practices, including methodology, duration, location on the shore, and target species. Similar but smaller scale observations were made of subtidal zone molluscan and decapod crustacean fishing activities. Occasional counting and observations were made, in the same manner as that for Quirimba Island, on the neighboring islands of Quilaluia. Quisiva. and Senear. On most days when collections had taken place, a random sample of fishermen were asked if their collec- tions could be investigated. In all cases, permission was sought and given. The molluscan and decapod crustacean species and number of individuals collected were counted. The length (or carapace width in the case of crustaceans) of the most collected species was measured with a micrometer and recorded. The variety, frequency, and identity of target species were re- corded to examine collection differences between fishermen, dif- ferent shore types, and islands. The length frequency data obtained from the most collected species were used to investigate differ- ences, first between fishermen in length selection and then, by pooling data, between islands. The practice of deshelling most species one at a time monospeeifically in the same places for years meant that old collections long since buried in sand were easy to find. These were unearthed and measured, and although the time scale was unknown, they provided a comparison with the same species collected in 1996. Interviews with local fishermen sug- gested that shore middens were solely from collections made on those islands. Such a comparison between shell lengths was ana- lyzed to investigate effects of harvesting the populations of these species. RESULTS Collfcliiin I'nqmncy uint Efjiirl The main area, within the littoral zone, used by fishermen was between the Low Water Spring and the Extreine Low Water Spring tide levels. The frequency of mollusc and crustacean col- lection was, therefore, dictated by the tidal regime. On Quirimba Island, people harvest the intertidal zone during the daylight low- water period for about 2-3 h. about 4-6 days in a fortnight period (Fig. 2). The low-water period was slightly offset from the nominal low tide lime because of local geographic peculiarities, such as large sand bars causing "bottlenecks." Fishermen were observed to be active for an exceptional period of 8 days in one fortnight (the end of August 1996) with the timing of the lowest tide of the year. The difference in tidal range of this lowest tide was 4.2 m. just 10 or 20 cm greater than a more typical high spring tide (such as that of July I, 1996). This small vertical difference, however, resulted in a widening or additional exposure of about 50 m of the intertidal zone. The magnitude of the number of fisherman also varied with tidal height, approximately (although not exactly on Coastal Shi-li i ish Resource Use in Mo/amhique 53 July 20 Days 30 August September Figure 2. Harvest effort with magnitude of tidal rantje. Tlie numbers of intertidal harvesters on Quiriniha Island's South and West eoasts (•) are illustrated by the scale on left, and the tidal daily range ( D) is indicated by the scale on right (shown for the months from July to September I'Whl. occasion) being greatest on the lowest tides. Observations of the outlying intertidal sandbanks and Quirimba Island eastern shore suggested that the peak value of 82 fishermen observed on August 30. 1996. probably represented about half of the total collecting population of Quirimba Island (pers. obs. and interviews). A maxi- inum figure of about 150 fishemien. or 5% of the total population of Quirimba Island (Joachim Gessner pers. comm.). compared with observed maxima of 1 1 (Quilaluia Island). 13 (Senear Island), and 40 (Quisiva Island). Over 70% of the collectors on the island intertidal zones were women and children, unless weather condi- tions precluded fishing by outrigger canoes and dhows, when the proportion of men collecting on the intertidal zone would increase. Species Collected In total, this study found 22 species of molluscs and five spe- cies of crustaceans of artisanal/commercial importance in the in- tertidal (and subtidal) zones of the archipelago (see Table I). Fif- teen species of molluscs and three species of crustaceans were collected during the study period on the Quirimba Island intertidal zone. Mollu.scs were collected by 78 (93.9%) of 83 study fisher- men at Quirimba Island, and exclusively so by 71 (84.3%). Deca- pod crustaceans (palinurids and portunids). by contrast, were col- lected by 6 (7.2%) of 83 and exclusively so by Just 2 (2.4%) of 83. Several species of two other groups, holothurian echuiodcrms and fish, were collected by 7 (8.4%) of 83. I ariatiiiii in Species Selection, Collection Quality, and Quantity The species of molluscs and crustaceans selected for collection varied with indi\idual collector preference, between shore types (reef, seagrass and mangroves) within each island and between islands. Table 1 illustrates species' commercial value and the five species of greatest importance to intertidal fishermen in each of the shore types and the subtidal. On reef rubble shore regions of the Quirimba Archipelago, the large gastropod molluscs Chicureus ramosus (L.) (ramose murex) and Fasciola trapezium (L.) (tulip shell) are the two most collected species. After the 2- to 3-h period of collection, these are usually taken to be deshelled above the high-water level. Although some people had a preference for col- lecting a specific species or couple of species, notably Octopus vul,i;aris (Cuvier) or C. ramosus and F. trapezium, most intertidal reef fishermen are opportunistic and take a variety of species. Palinurid lobsters were occasionally collected from subtidal coral reef crevices, particularly at Quilaluia Island. In contrast to those on coral reefs, most intertidal fishermen on seagrass and mangrove areas were more selective, taking just one or two species. The abundant bivalve molluscs Pimtada nii^ra (Sowerby) (pearl oys- ter) and Barhatia fuscci (Bruguiere) (almond ark) were the most important species in the seagrass areas. The method of collecting arks differed from that of all of the other species listed, because it .sometimes involved fishermen locating them beneath the surface of the sand with their feet. C. ramosus and F. trapezium shells were also important collected species in seagrass beds; the last of the major five species was another very common bivalve, the pinna shell Pinna muricata. Although two other species of pinnas oc- cuiTed semiburrowed in the intertidal zone, Atrina vexiltum (L.), bemg large, was very difficult to remove from its burrow and Atrimi pectinata was rarely seen. P. muricata was highly abundant and relatively easily removed from sand but. like other pinnas, had a larger shell volume-to-edible component ratio than most mol- luscs collected. Islanders collecting pinnas, almost exclusively specialized on them but also had to remove all of the shells in order to be able to cairy them back, which in turn reduced the collecting time during low water. The mangroves of the four islands inves- tigated were rarely seen to be used for collecting, but the large portunid crab S. serrata (Forskal) (Mud Crab) was dug from bur- rows in the mangrove systems of Ibo Island. In addition, people from Quirimba Island collected about 30 sacks (50 kg) per month (about 4 sacks maximum per person) of Terebralia palustris (L.) (mangrove whelk) from the larger mangrove systems of the adja- cent mainland and Ibo Island. These whelks were crushed to form bait for fish traps. There were substantial differences in the species and propor- tions of species taken by intertidal fishermen from the four differ- ent study islands. Table 2 illustrates the proportion (percentage) of individuals of each species collected relative to the total number collected and the proportion of fishermen collecting each species. The variety of molluscs collected was greatest on Quirimba Island. Quirimba Island was also the only study island on which crusta- ceans were collected during the study period. Few species were collected to a similar degree (in terms of numbers or fishermen) on each of the four islands. Uunljis lamhis (L.) and C. ramosus were the iTiost similarly collected between islands. In contrast, P. nigra was the most important species at Quirimba Island in terms of number of fishermen collecting it and number collected and the least important (joint) on Senear Island. Effects of Collection The size ranges of individuals, measured from collections of each target species, were generally norinally distributed just below the maximum length of each species (see Fig. 3). The double, nonoverlapping. length-frequency histograms of L. lambis were the product of intertidal collection (left peak) and subtidal collec- tions (right peak). L. lamhis was an important target species for subtidal fishermen, who often snorkeled specifically for it. Obser- vation of collection habits and the small numbers of L. lamhis collected suggested that the species was only collected from the intertidal zone incidentally while fisherman were looking for more important target species such as C. ranuisus and F. trapezium. C. ramosus shells collected on Quirimba Island in August 1996 had a mean lensth of 82.7 (SD 14.3) mm, and the smallest shells 54 Barnes et al. TABLE 1. Molluscs and crustaceans harvested in the Quirimba Island Archipelago. Intertidal Scientific name English name Value Reef Seagrass Mangrove Subtidal Reef and Seagrass Molluscs Class Bivalvia Family Arcidae Baihatia fiisca Almond ark 5.000/k Family Pinnulae Atrina ve.xilltwi Giant pen shell 1.000 e Pinna muricata Pinna shell 2.000/k Family Pteriidae Pinctada nigra Pearl oyster 5.000/k Family Tridacnidae Thdania squamosa Fluted giant liam 3.000 e Class Gastopoda Family Cassidae Cassis corniita Horned helmet 1.5.000 e Cxpraecassis ntfa Bullniouth helmet L5.000 e Family Conidae Conus lilteratus Lettered cone 1.000 e Family Cymalidae Charonia tritonis Trumpet triton 120.000 e Family Cypraeidae Cypraea rigris Tiger cowrie 100 e 5 Family Fasciolaridae Fasciola trapezium Tulip shell 250 e 2 Family Harpidae Harpa major Major harp 5,000 e Family Melongenidae Volema pyrum Not sold Family Mitridae Mitra mitra Mitra shell 8.000 e Family Muricidae Chicoreus chicoreus Murex shell 10.000 e Chicoreus ramosus Ramose murex 5.000 e 1 Family Naticidae Polinices mamilla Pear moon shell Not sold Family Potamidae Terebralia palustris Mud whelk Not sold Family Strombidae Lambis chiragra Arthritic spider 10,000 e Lambis lambis Common spider 10.000 e 4 Strombus mutabdis Humpback conch Not sold Family Turbinidae Turbo coronatus Turban shell Not sold Family Turbinellidae Vasum turbinrlluni Not sold Class Cephalopoda Octopus vulgaris Common octopus 3,000/k 3 Crustacea (Decapoda) Family Palinuridae Pamdirus homarus Scalloped lobster 10.000 e Panulirus versicolor Painted lobster 10.000 e Family Portunidae Porlunus pelagicus Pelagic swimmer Not sold Scylla serrata Mud crab 5.000/k Thalamita crenata Widefront swimmer Not sold The value (in Meticais) and importance of species are .shown for three intertidal habitats and the subtidal (e = each, /k = per kilo). The five numbered species in each of the four habitats are the most important species harvested (1 being most important of these and 5 being the least). The index was calculated from an average of importance in terms of the number of specimens collected, and the number of harvesters collecting each particular species. Coastal Shellfish Resource Use in Mozambique 55 TABLE 2. The proportions of mollusc and crustacean species harvested in the Quirimha Island Archipelago. Commercial species Quirimha Island n = 16.756 (8.^) Quisiva Island n = 1.682 (77) Quilaluia Island n = 5(15 (12) Senear Island n = 65 (8l Molluscs Class Biviilvid Family AiriJtw Barhario fusca Family Piimidcie Alrina vexillum Pinna muricala Family Ptehidae Pincuida nigra Family Tridacnidae Tridacna squamosa Class Gastopoda Family Cassidae Cassis comuta Cypraecassis rufa Family Conidae Conus litleratus Family Cymaridae Charonia rritonis Family Cypraeidae Cypraea tigris Family Fasciolaridae Fasciola trapezium Family Harpidae Harpa major Family Melongenidae Volema pyrum Family Mitridae Mitra milra Family Muricidae Chicoreus chicoreus Chicoreus ramosus Family Naticidae Polinices mamilla Family Poiamidae Terebralia palustris Family Slromhidue Lombis chiragra Lambis Uimbis Slronihus mutabilis Family Turbinidae Turbo coronatiis Family Turbinellidae Vasum lurhinellum Class Cephalopoda Octopus vulgaris Total Molluca Crustacea (Decapoda) Family Palinuridae Panulirus bomarus Panulirus versicolor Family Portunidae Portunus pelagicus Scylla serrata Thalamita crenata Total Crustacea 10.3(44.3) Negligible 2.8 (8.3) 78.9(54.2) Negligible 0.1 (7.2) 0.2(13.2) 0.3(13.2) Negligible Negligible 2.6(22.9) Negligible 0.3 (6.0) 0.1 (9.6) 3.7 (2.4) 0.2(1.2) 0.1 (8.4) 99.8 (93.9) 0.1 (4.8) Negligible* Negligible 0.2(7.2) 23.8(10.4) 0.1 (1.3) 0.5 (6.5) Subtidal only 0.5 (3.9) 3.2(5.2) 0.2 (3.9) 1.8(7.8) 32.0(76.6) 22.1 (44.2) 0.2 (5.2) 2.3(13.0) 1.9(1.3) 8.5(55.8) 91.8(97.4) Subtidal only Subtidal onlv 78.8(25.0) 0.2 (8.3) 0.6(8.3) Subtidal onK 0.4(8.3) Subtidal only 2.4(8.3) 4.2 (50.0) 0.2 (8.3) 7.5(41.7) 0.8(16.6) 4.6(25.0) 99.6(81.8) Subtidal only Subtidal onlv 3.1 (12.5) Subtidal only 4.6(25.0) 18.5(37.5) 3.1 (12.5) 4.6(12.5) 6.2(12.5) 21.5(25.0) 38.5 (62.5) 96.9 (87.5) Subtidal only Subtidal only The total sample size of specimens is illustrated under each island heading together with the sample size of harvesters in parentheses. The values (percent) for each species are the proportion of total number of individual specimens harvested at each island sampled during the study period. The proportion of harvesters collecting each species is shown in parentheses. Species that were only collected subtidally are illustrated as such. The two species marked with an asterisk are imponant within the archipelago but were not collected to any great degree on any of these four islands. Dashes indicate species not collected at that site. 56 Barnes et al. Lambis lambis 200 250 300 Turbo coronatus 400 >^ u c (D Z3 C3" CD 50 40 30 - 20 10 - oCL 15 20 50 40 30 20 10 25 30 Terebralia palustris 35 ___mn 1 40 60 80 100 Pinna muricata 120 100 120 140 Length 200 mm Figure 3. Length-frequency histograms of exploited molluscs at Quir- imba Island. Samples of specimens Here measured from harvester collections to illustrate the size range of each species being used. The smaller of the two peaks seen in the /,. lambis histogram « as the result of intertidal collections, and the larger peak to the right was the result of subtidal snorkel-aided collections. collected were between 40 and (iO iiini Umg. The mean length ot'C ramosus shells from terrestrial middens, harvested on Quirimba Island from years previous was 117.3 (SD 15.6) mm. and the smallest shells collected were between 80 and 90 mm long. Al- though there was considerable overlap in the length of C. ramosus shells collected in 1996 and from previous years (Fig. 4). the average length has significantly decreased (Student I = 96.6. p < 0.001). Similarly, the average length and smallest length of F. trapezium collected on Quirimba Island have significantly de- creased (Student ; = 94.7. p < 0.001) from 130.9 to 103.9 and from over 100 to 70, respectively. Shells of F. trapezium from the other (seasonally) well-populated study island, Quisiva. illustrated a similar pattern (Fig. 5). The lengths of F. trapezium collected at Quilahua Island and Senear Island (both of which have low per- manent population) were 1 14.5 and 1 15.8 mm, respectively. These were both significantly larger than collected F. trapezium from Quirimba and Quisiva Islands (Student t = 22.1, p < 0.001 ). On Quilaluia and Senear Islands, the average length of F. trapezium had also significantly decreased from old collections on the same islands (Student t = 3.4, p < 0.01 and t = 3.0. p < 0,01. respec- tively). Within an area of the lower shore, between 20 and 80 m wide for 0.75 km, the large semiburied bivalve Pimm muricata domi- nated the seagrass benthos of Quirimba Island, averaging IS/m" but with occasionally up to 60/m" (Barnes, unpubl.). In contrast to the size reduction of intertidal representatives of the gastropod species C. ramosus and F. trapezium, length measurements sug- gested that populations of the P. muricata have so far been unaf- fected by the cuirent and previous levels of collection at Quirimba Island. The size of collected specimens was not significantly (Stu- dent t = 0.6. p > 0.05) different from the size of those found to have died of natural causes. Most adult intertidal fishermen studied or interviewed rejected or claimed to reject shells of each species below a certain size. Causal but unquantified observations suggested that this varied between adults and that children collected smaller shells. All of the species of mollusc shells found in old collections were still col- lected in 1996. but some species, notably many of the low-value species (e.g., Polinices mamilla. Turlio coronatus. Vassum tur- binellwn). were not represented in old midden collections. The mean carapace width of the portunid 5. serrata collected (mainly from the mangroves adjacent to Ibo Island) was 147.6 inm (minimum. 104 mm; maximum. 200 mm). S. serrata was rarely observed to be collected from the mangroves of any of the study islands, although those on Quiriinba Island have apparently sup- ported brief periods of collection in the past (Joachim Gessner, pers. comm.). The sizes of both populations and individuals of Quirimba Island .S'. serrata were small. August 1996 50 40 30 20 T 10 - J -1 n - ■ \\ n r^ FlHi 1 1 ; , n III Hn' 40 60 80 100 120 140 160 180 Previous 50 40 30 20 10 40 60 140 160 180 100 120 Length ( mm ) Figure 4. I.englh-frequency histograms of ('. ramiisux collections al Quirimba and yuisi\a Islands. The upper histogram represents col- lections made during the study period (iy%). and the lower histogram represents midden collections. Coastal Shellfish Resource Use in Mozambique 57 100 120 140 160 180 ^^ Quirimba middens n 12 ' r I 4 o 60 80 100 120 140 160 180 60 80 100 120 140 160 180 16 12 8 4 Quisiva middens 60 80 140 160 180 100 120 Length ( mm ) Figure 5. Lcngth-t'requcncv histograms of F. trapezium collections at Quirimba and Quisiva Islands. The darker shaded histograms repre- sent collections made during the study period (19961, and the lighter shaded histograms represent old collections dug up from now unused middens. DISCUSSION The intertidul and immediate subtidal zones of Quirimba. Quisiva. Quilaluia. and Senear Islands of the Quirimba Arehi- pelago are a vital resource for local fisheries. These are operated by between 5 and 25% of the island populations, mostly by women and children. This translates to between 2 and 10 collectors per kilometer of intertidal zone (on spring tides). Intertidal collecting was only undertaken on spring low tides, and effort in terms of number of collectors was proportional to the tidal range. Such an intensity of collection is considerably lower than that both in Tan- zania (Andersson and Ngazi 1995. Horril et al. 1996) to the north and on Inhaca Island (pers. obs.) to the south. The proportions of species and actual species of molluscs and crustaceans harvested in the Quirimba Archipelago also differed considerably from those harvested in southern Tanzania and south- em Mozambique. The number of artisanally important species was high, although a few species harvested at Inhaca Island were not collected in the Quirimba Archipelago (pers. obs.). This was be- cause of rarity in somt cases (e.g.. Modiuhts phytipinanim (horse mussel]) and probably lack of necessity (e.g.. Calappa hcpaucu I box crab I and ilea sp. (fiddler crab() because other more prized species such as Porliimis pelcifiinis {Piirlunidae) were compara- tively more abundant in the Quirimba Archipelago. Molluscs were proportionately much more imptxtant to the uitertidal collectors of the Quirimba Archipelago and Tanzanian Islands than in the more southerly Inhaca Island, where the tonnage of molluscs, decapod crustaceans, and holothurians collected per unit time was approxi- mately equal (Longomane 1995. Santana Afonso 1995. Macia and Hernroth 1995). Molluscs, particularly mussels, dominate the in- tertidal resources collected in much of South Africa (Hockey et al. 1988, Va Erkom Schurink and Griffiths 1990). The abundance of edible and search-time cost-effective mollusc species in the Quir- imba Archipelago partly explains the lesser dependence on octo- pus compared with Tanzania (Andersson and Ngazi 1995). The interpretation of the results from this study involves the assumption that changes in size distribution are due (or largely due) to fishing pressure and not other ecological factors. Although such an assumption may be an oversimplification, it has been used as the basis for studying various shell fisheries (e.g.. in East Africa by Horril et al. 1996, in South Africa by Van Erkom Schurink and Griffiths 1990, and in Belize by Azueta 1993 unpubl). The re- source/environmental effect of the artisanal intertidal fisheries in the Quirimba Archipelago does not seem particularly marked when compared with the majority of tropical or subtropical fish- eries of this type reported previously (Gomez et al. 1989. Alcala and Russ 1990. Andersson and Ngazi 1995. Coughanowr et al. 1995). There has been a significant decrease (Student / = 94.7, p < 0.001 and t = 22.1. p < 0.001 respectively) in the size of two of the most importantly collected mollusc species (F. trapezium and C. ramosus). The timeframe over which this has happened is un- known. The data collected by this study suggest that the length of harvested individuals of the.se species has decreased less on the shores of the two smaller islands (Quilaluia and Senear), where fishing pressure is lower, than on the other, larger islands of Quir- imba and Quisiva (F. trapezium. Student l = 2.03. p < 0.05 and t = 2.12. p < 0.05; C. ramosus. Student ; = 2.77. p < 0.01 and l = 2.72. p < 0.01. respectively). Although the differences are small, they may illustrate the effect of increased collection pressure on the populations of these species. The brachyuran crab P. pelagicus was the most important local crustacean fished. This species is imponant elsewhere along the East African Coast (pers. obs.). and crabs of the genus Porluims are also a major contribution of West African crustacean shellfish- eries (Manning and Holthuis 1981). Grapsid crabs, although lo- cally abundant, appear not to be collected, as in parts of West Africa, such as Ghana (Irvine 1947) and the Cape Verde Islands (Barnes unpubl.). No mention has been found of crabs of the genus Tlialamita being caught elsewhere for food, although Rathbun (1921, in Manning and Holthuis 1981) mentions their ease of capture in the Congo intertidal zone. The exploitation of the crustacean 5. serrata does not appear high in the Quirimba Archipelago. However, over 11% of col- lected individuals had carapace widths smaller than would be al- lowed by law in South Africa ( 1 14 mm minimum in Cape Province and 115 mm miniinum in Natal), and the size of individuals ob- served in the Quirimba Island mangroves was small and the spe- cies was rare. S. serrata has often been overexploited throughout its range, which spans the Indo-Pacific region (MacNae 1968). There are. however, extensive mangroves around Ibo Island and a substantial part of the northern Mozambique coastline. This region mav. therefore, be one of the more important regions globally for 58 Barnes et al. the species, both from resource supply and conservation angles. The absence of freshwater (and the hardships associated with this) from Quilaluia. Quisiva, and Senear may be an important factor in maintaining the relatively low overall current level of intertidal resource utilization (although the inshore and offshore fishing pressures may be considerably higher; Darwin/Frontier Mozam- bique Marine Research Programme unpubl.). The absence of tourism and lack of suitable diving equipment, as well as an intertidal zone on which collection is easy, have resulted in little free or SCUBA diving for lobsters or larger mol- luscs. L. lambts (spider conch) shells are one of the most important species collected to sell, but there has been no obvious size or population effect discovered by this study. Lobsters of the genus PanuUnis are often heavily exploited to the extent of catastophic population decrease, a problem being faced in both southern Tan- zania and southern Mozambique, along with many other coastal tropical/subtropical urban areas. Throughout the Quirimba Archi- pelago. PaiHilinis hoinanis and Painilinis versicolor remain com- mon in the subtidal zone (3-20 m; pers. obs.). The diversity of molluscs exploited artisanally (22 species) is one of the highest reported of any Indo-Pacific local region known to the authors and probably reflects both the local marine biologi- cal diversity and the lack of local anthropogenic disturbance. This situation can be partly attributed to the extended period of civil conflict (ending in 1992). which heavily damaged the transport and communication infrastructure and precluded tourism, but also caused population shifts into the relative safety of the archipelago. The fact that the archipelago is farther from an international airport (Maputo is 2,000 km distant) than virtually any other stretch of coastline in Africa, combined with the lack of water on many of the islands, has also restricted development. The region could be arguably regarded as one of Africa's most remote mainland sites of marine biological diversity and cultural importance, but the islands are small and increased development will bring new and additional disturbances, changing the nature of the intertidal sy,stem. One of the principal aims of the ongoing studies of the Darwin/Frontier Moi;ambique Marine Research Programme is to ultimately provide key information and suggestions that could lead to an effective management plan to sustain the archipelago. ACKNOWLEDGMENTS This study was funded by the Darwin/Frontier Mozambique Marine Research Programme. This is a collaborative venture be- tween the Society for Environmental Exploration (SEE) and the Ministepara a Coordenagao de Acjao Ambiental (MICOA) in Mozambique and is funded in part by the Darwin Initiative for the survival of Species (Department of the Environment. United King- dom). The authors thank the logistics staff and vnsequently faunal composi- tion. Simenstad and Fresh { 1 995 ) reported that the application of gravel to intertidal sediments resulted in a shift from a polychaete to a bivalve and nemertean dominated community, but emphasised that changes are likely to be site-specific. Such shifts in commu- nity compo.sition could have repercussions at other trophic levels [e.g.. changes in the abundance of certain harpacticoid copepod populations that are important prey for ju\enile salmon and flatfish species (Simenstad and Fresh 1993)]. In the United Kingdom, Parliamentary law necessitates the use of protective netting in Manila clam cultivation to prevent escape of this introduced species (Spencer et al. 1997). Spencer et al. (1996. 1997) found that the application of plastic netting to an estuarine silty sand substratum led to an immediate increase in sedimentation rate over cultivated plots that elevated the organic content of the .sediment. Within 6 mo the cultivated plots were dominated by opportunistic spionid worms. During the following 24 mo. the spionids were replaced by high abundances of larger deposit feeding worm species. The plastic netting also became ^flW" B - ^?^^ • .. 4ir , ^ ^^^ ■**'■. * * y i^flSiaSilKsttik . f^ j^v '^^^Sr ^ ^*« ^ IjQb*^!^ x^ "* '*< ' V J ■f Mt 'J, %. ■» ^ ^ C*' '^^ . i ^ -,^.15^ ■1- • ■• .*:^ V ■ > ^ f f '■ ':">■ ,-:.■ „fc^^ :i^-^ .«» '^«^^1 fe... .' ^ « D ^^ ^||' g%|r»gi assa5aiirr:j?^^'^ Figure 1. The sequence of environmental impiicls thai occur throu^liout Manila clam cullivallon (.Spencer et al. 19%. IW7, IWXi. A) flam plots covered with plastic netting become fouled with alj-ae and increase sedimentation rate. Kenular liushandrv is required to remove the alyae. Bl P'ouling al);ae attract epii'aunal species such as Lilloriiui lillh differences in the henthic conununity were apparent for a further 6 mo. Environmkni'al Impacts of Bivalvh Marichlture 63 fouled wilh Eiueroinoipha spp., which hi tiiin atliiicled gra/iiis: littorinid snails (Fig. 1 ). Hard-shcilcd clams, on-grow n in plastic bags placed directly on the sediment, had no detectable effects on the betithic inveitebiate population found in the sediment between the bags (Mojica and Nelson 1993). Although Mojica and Nelson (1993) al.so found no differences in the infauna sampled directly beneath clam poches. they expressed caution about this result because of their low num- ber of samples. Recent studies b\ Chandrasekara and Frid ( 19961 and Fletcher and Frid (1996) emphasise how repeated trampling can induce localised changes in invertebrate and plant communi- ties on tidetlats and rocky clam poches they expressed caution about this result due to their low number of samples. Relaid mussels lead to the development of mussel mud beneath the mussel bed as the filtration and feeding activities of the mus- sels increase sedimentation rate. These deposits are composed of dead shells, silt, and pseudofeces that persist in excess of 18 mo after the mussels have been removed. The cohesive nature of the mussel mud is degraded by a combination of bacterial activity and wave erosion (Davies et al. 1980). In summary, both the addition of gravel or shell substrata, the formation of mussel mud and the use of protective netting induces localized change in benthic community composition. However, while netting is easily removed and accumulated sediment is rap- idly reworked by tidal currents, waves and bioturbatory activity (Spencer et al. 1998). the addition of gravel and shell material effectively creates a new habitat leading to more persistent changes in local community composition. Suspended Raft Cultivation Superficially, suspended rope culture of bivalves has little vi- sual effect on the landscape. However, the large biomass of cul- tivated and fouling organisms suspended beneath rafts and buoys has a major effect on phytoplanktonic. benthic, and hydrographic processes in close proximity to the cultivation site. Mussels pro- vide a complex surface area on which dense epifaunal communi- ties consisting of over 100 species can develop (Tenore and Gonzalez 1976). Small portunid crabs. Pisidia hmgicornis. were found to be abundant among fallen mussels beneath rafts in the Spanish rias. These, in turn, were fed upon opportunistically by several fish species that normally consume polychaete worms (Lo- pez-Jamar et al. 1984). P. longicomis are so abundant in areas of mussel cultivation that their larvae dominate (90% of the biomass) the zooplankton community normally characterised by copepods (Alvarez-Ossorio 1977). Mussels excrete high levels of ammonia (Tenore and Gonzalez 1976), which promotes high levels of pro- ductivity in algae attached to mussel lines, that is equivalent to algal production in local intertidal systems (Lapointe et al. 1981 1. So great is the productivity associated with mussel lines in the Spanish rias. that Tenore et al. (1982) speculated that inshore fisheries were potentially enhanced by the bedload transport of organic rich sediment into coastal areas. Cultivation sites that are well flushed by tidal currents, as in the Spanish Rias, do not encourage the accumulation of pseudofaeces beneath mussel rafts which results in a favourable increase in macrofaunal biomass (Rodhouse and Roden 1987). The relatively beneficial effects that occur in the Spanish rias contrast sharply with the effects observed by Dahlback and Gunnarsson ( 1981 ) in Sweden. They demonstrated organic sedimentation rates of 2.4— 3.1 g organic C m"" d"' beneath mussel longlines. which was twice as much as found in adjacent uncultivated areas. This ex- cessive organic enrichment was associated with anoxic sediment and bacterial mats of bacteria. Reggialoa spp.. developing beneath the longlines. In this situation, the benthic infauna had low di\er- sity and biomass. which is a well documented response to polluted sites (Pearson and Rosenberg 1978). Similarly, the productivity of den.sely stocked Japanese oyster grounds was detrimentally af- fected by the generation of large quantities of pseudofaeces and high filtration rates (Ito and Imai I95.'i. Kusuki 1977). Pseu- dofaeces production was so great beneath oyster cultivation rafts that it was at least equivalent to natural sources of sedimentation (Mariojouls and Kusuki 1987). HARVESTING Harvesting of subtidally grown species occurs using towed dredges or suction pumps, the effects of which were discussed earlier and are well reviewed elsewhere (Messieh et al. 1991. Jones 1992. Dayton et al. 1995. Jennings and Kaiser 1998). The harvesting of trestle-grown and suspended bivalves has little, if any effect as they are removed without interfering directly with the environment. In contrast, the harvesting of intertidal spe- cies that are cultivated directly on or in the substratum requires various means of mechanical extraction. Physical disturbance of intertidal sediments by invasive com- mercial bivalve harvesting activities is of concern to fisheries man- agers because of direct effects on populations of target species, causing non-catch mortality, and to nature conservationists be- cause of the interference with the feeding behaviour of wading birds (Goss-Custard and Verboven 1993, Shepherd and Clark 1994). habitat degradation or the alteration of infaunal invertebrate community structure. The environmental effects of harvesting natural populafions of intertidal and shallow sublittoral bivalves has received considerable attention in the United Kingdom be- cause of the scale and intensity of operation, particularly with respect to tractor and suction dredging intertidally for cockles (Allen 1995. Cotter et al. 1997. Hall and Harding 1997). It is surprising that the environmental effects of cultivated bivalve har- vesting have been little studied to date, especially as clam beds can occupy large areas of the intertidal zone with individual commer- cial plots that usually measure 40 m" or greater. The greatest visible effect of suction dredging or mechanical raking on the sediment is the creation of depressions or trenches which may take days to months to restore depending on sediment type and location (Dyrynda and Lewis 1995. Hall and Harding 1997). These trenches may encourage larval settlement by provid- ing an environment subject to lower current velocities (Snelgrove and Butman 1994). However. Thrush et al. (1996) report that defaunated sediments become destabilized, leading to faunal emi- gration, which greatly delayed recolonization. Recolonisation rate is likely to differ between habitat-types depending on a combination of factors, including sediment stabil- ity and exposure to wave action and currents. In addition, the scale of disturbance will have important implications for recolonization rate depending whether this occurs through active/passive move- ment of adults or through larval recruitment (Hall and Harding 1997). Most studies of recolonization rate have been performed on scales of <1 m", which do not equate to the scale of commercial harvesting practices. However, more recent studies have been de- signed at a scale appropriate to examine the effects of disturbance associated with commercial harvesting activities. In Hall and Har- 64 Kaiser et al. ding's ( 1997) study of shores tractor dredging in tlie Solway Firth, they found that the benthic community within dredged plots was indistinguishable only 3 mo after harvesting regardless of the scale of disturbance, which ranged from 223 m" to 2025 m". They emphasised that the sum total of disturbed areas on a sandflat subjected to commercial harvesting would exceed that examined in their study, but that it would be patchily distributed and unlikely to extend the recovery trajectory much further. The rapid recovery in the Solway Firth was attributed to large-scale sediment movements that obliterated their treatment effects (Hall and Harding 1997). In another, similar study undertaken at a commercial Manila clam farm at Whitstable on the southeast coast of England. Kaiser et al. (1996) found that the infaunal community was restored within 7 mo after suction harvesting clam parks (each park. 40 m"). This site had an underlying sediment of cohensive mud/clay overlayed with a veneer of coarser sediments. Suction dredging removed this veneer leaving the mud/clay exposed. Tube dwelling polychaetes. such as Lanice conchilega and Euclymene lumbiicoides, burrowed down into the mud/clay fraction and were less adversely affected than more mobile species such as Macoma balthica and Scoloplos arniiger. which were found in the coarser overlying sediment. It is likely that these fauna would only recolonise harvested areas once this veneer of coarse sediment had been restored. Wave action is probably the main agent of sediment restoration at this site which is exposed to prevailing northeasterly and easterly winds. Spencer et al. (1998) conducted a similar experiment in the River Exe. Devon. England. This site was much more sheltered than those studied by Hall and Harding (1997) and Kaiser et al. ( 1996) and characterised by fine muddy sand. Although sediment structure and profile was restored ?i mo after suction harvesting (Fig. 1 ). the benthic community was not fully restored until 9 to 12 nio after harvesting occuiTed (Spencer et al. 1998). The immediate effects of suction dredging are. not suiprisingly, quite severe, as the entire upper layers of the substratum and fauna are removed. In some fisheries, bivalves are collected by hand or mechanised raking. As yet unpublished data (Kaiser and Broad) suggests that the composition of benthic fauna within hand-raked plots recovers within 54 days of initial disturbance. Unlike suction- dredging techniques, hand-raking leaves the sediment /;; situ and does not affect all the animals within the path of the rake. Soft sediments recover relatively quickly after physical distur- bance (but see Thrush et al. 1996 for a good example of an ex- ception). However, disturbance of key habitat structures, such as hard substrata or plants, particularly seagrasses, are likely to have much more severe effects. Seagrass beds are highly specialised habitats, acting as nursery grounds for juveniles of many species and they are important for the productivity of coastal areas. The effects of anthorpogenic disturbance to these habitats is excellently reviewed by Short and Wyllie-Echeverria (1996). Fishers gather- ing molluscs in the intertidal zone may cause disturbance as they walk across substrata. As a result, they suggested the use of re- stricted walkways to minimise their disturbance. MANAGEMENT CONSIDERATIONS Seed Collection Mechanical methods of harvesting bivalve seed have the po- tential to modify non-target communities associated with seed- beds. In the United Kingdom, mussel seed collection is managed by issuing licences to dredge defined areas of the seabed which will constrain the limits of habitat modification that may occur as a result of harvesting. Ovcrcxploilalion oi' seedbeds in The Neth- erlands has caused declines in bird populations that depend upon this food resource and has also caused a decline in the sustainable fishery, such that mussel seed are presently imported for relaying. The consequences of the decline of mussel stocks for other key predators of mussels such as green crabs. Carcinus maenas. and starfish. Asterias riibens. is unknown. These species have presum- ably switched to feeding on alternative prey species. The use of spat collectors in midwater has little, if any second- ary effects on the environment. The continuous relaying of cultch, however, leads to habitat modification. This may result in an in- crease in local habitat and species diversity which is more likely to be perceived as a beneficial rather than negative effect. However, any negative effects that might arise from the use of cultch in the coastal zone might be constrained by restricting its use to areas specially designated for bivalve cultivation. The introduction of alien species is generally regarded as un- desirable and their potential ecological effects are now well known (Ludyanskiy et al. 1993. Eno 1996. Minchin 1996). The risk of inadvertently introducing alien species with shipments of bivalves and via other vectors such as ballast water can be significantly reduced if Codes of Practice are adopted as part of a management plan, such as that produced by ICES (Anonymous 1994. Minchin 1996). Some of these introduced species are harmful to cultivated bivalves (e.g., starfish, green crabs) or create management prob- lems (e.g., fouling organisms). On-growing The environmental effects of mariculture during the on- growing stage will vary according to the nature of the habitat and the scale of cultivation. Problems associated with eutrophication beneath mussel lines are ameliorated in situations where tidal flow is sufficient to disperse particulate matter generated by the mussels and other epibiota (Tenore et al. 1982. Rodhouse and Roden 19< o ^ GTX1 GTX4 C4 C3 C2 01 U Q Total toxicity: 1 13,259 ug STX eq./lOOg 25 50 mole % Figure 3. Toxin profile (mol "Xr). Accumulation of PSP toxins bj- A. ater total meat during its maximal toxicity. ti s 1200 900 600 300 5 5 I S I 2 s s I I I ^ )ole% Figure 6. Comparison of averaRC toxin iimiposition (mol '''c I of tlu' three molluscs, correspondin;; to the hJKhcst toxltily reached by each one during the monlloring period. ACCLIMLU.ATION OF PSP TOXINS IN A. ATliK 73 show ih.il (Ills Miolliisi.' has a lower depuration rate than the bivalve, making this shelllish a dangerous vector of PSP toxins. In the case of ,4. nmc'llijoniu's, even when its PSP-toxin accunuilation reached highest toxicity in the digestive gland, the amount in the foot muscle tissue was always lower than the quarantine level and negligible during the total monitoring period. This feature makes this carnivorous snail potentially suitable for human consumption during PSP closures, considering that only the foot muscle tissue of this mollusc is cunently consumed. Finally, this article gives evidence supportmg the recommendation to pay attention to higher order consumers such as carnivorous gastropods as vectors of PSP toxins and to include them in surveillance programs (Shumway 1995). especially in this southern part of South America. ACKNOWLEDGMENTS This study was supported by FONDECYT 1961 122, Fundacion ANDES, and FIP 95-23B. LITERATURE CITED Benavides. H.. L. Prado, S. Diaz & J. L. Carreto 1995. An exceptional bloom of AU'xanilriiim caleneUa in the Beagle Channel, Argentina, pp. 1 13-1 19. In: P. Lassus, G. Ar/,al. E. Erard. P. Gentien, and C. Marcail- lou (eds.). Harmful Marine Algal Blooms. Intercept Ltd., Paris. Guo, X., A. Uehara, A. Ravindran, S. H. Bryant, S. Hall & E. Moczyd- lowski. 1987. Kinetic basis for insensitivity to tetrodotoxin and sax- itoxin in sodium channels of canine heart and denervaled rat skeletal muscle. Biochemisln- 26:7546-7556. Guzman. L.. I. Campodonico & M. Antunovic. 1975a. Esludios sobre un florecimiento toxico cau.sado por Gonyaula catenella en Magallanes. IV. Distrihucion y niveles de toxicidad de veneno paralitico de los mariscos (noviembre de 1972 — noviembre de 1973). Aiitilc.s. Iiisl. Pat. Piinni Arciuis {Chile) 4:209-209-223. Guzman. L. I. Campodonico & S. HermosiUa. 1975b. Estudios sobre un floreciento toxico causado por Gonyuulax cciienella en Magallanes. I. — DisUibucion espacial y temporal de G. catenella. Atiales. Inst. Pal. Pimta Arenas (Chile) 4:173-183. Guzman, L. & G. Lembeye. 1975. Estudios sobre un floreciento toxico causado por Gonaiila.x catenella en Magallanes. II. — Algunas condi- ciones hidrograficas asociadas. Anales. Inst. Pat. Piinta Arenas (Chile) 4:185-195. Hall, S., G. Strichartz. E. Moczydlowski. A. Ravindran & P. B, Reichardt. 1990. The saxitoxins; sources, chemistry, and pharmacology, pp. 29- 65. In: A. Hall and G. Strichartz (eds.). Marine Toxins: Origin, Struc- ture and Molecular Pharmacology. American Chemical Society Sym- posium Series 418. American Chemical Society, Washington, DC. Lagos, N.. D. Compagnon. M. Seguel & Y. Oshima. 1996. Paralytic shell- fish toxin composition: a quantitative analysis in Chilean mussels and dinoflagellate. pp. 121-124. In: T. Yasumoto. Y. Oshima and Y. Fukuyo (eds.). Harmful and Toxic Algal Blooms. Intergovernmental Oceanographic Commission of UNESCO. Paris. Lembeye, G.. L. Guzman & I. Campodonico. 1975. Estudios sobre un florecimento toxico causado por Gonaulax catenella en Magallanes. III. — Fitoplancton asociado. Anales. Inst. Pat. Punia Arenas {Chile) 4:197-208. Moczydlowski, E., S. Hall, S. S. Garber. G. S. Strichartz & C. Miller. 1984. Voltage-dependent blockade of muscle Na* channels by guanidinium toxins: effect of toxin charge. / Gen. Physial. 84:687-704. Mufioz, P., S. Avaria, H. Sievers & R. Prado. 1992. Presencia de dinotlage- lados tdxicos del genero Dinophysis en el seno de Aysen, Chile. Re\: Biol. Mar. Valparaiso 27:187-212. Oshima, Y. 1995. Postcolumn derivatization liquid chromatographic method for paralytic shellfish toxins. J AOAC Int. 78:528-532. Segers, P. A. 1908. Primera observacion de una causa de enfermedad del higado causando una hipertrofia y cirrosis atrdfica consecutivas por excesividad funcional, debido a absorcion de toxinas, y primera obser- vacion de esplenomegalia concomitante con hipertrofia de baso en estas infecciones. La Semana Medica (Buenos Aires) 20:1 17-1 19. Shumway. S. E. 1995. Phycotoxin-related shellfish poisoning: bivalve molluscs are not the only vectors. Rev. Fish. Sci. 3:1-31. Strichartz. G. S.. S. Hall. B. Magnani, C. Y. Hong, Y. Kishi & J. A. Debin. 1995. The potencies of synthetic analogues of saxitoxin and the abso- lute stereoselectivity of decarbamoyl saxitoxin. Toxicon. 33:723-737. Williams, S. (ed.). 1984. Paralytic shellfish poison, pp. 344-345. In: Of- ficial Methods of Analysis. 14th Ed. Association of Official Analytical Chemists (AOAC), Ariington, VA. .lourmil of Shellfish Resianh. Vol. 17, No. 1. 7,S-7,S, I')'*. IN VITRO LIFE CYCLE AND PROPAGATION OF QUAHOG PARASITE UNKNOWN STEPHEN J. KLEINSCHUSTER,' ROXANNA SMOLOWITZ/ AND JASON PARENT' ^ Haskin Slwllfish Research Lahonilory 6959 Miller Avenue Port Norris, New Jersey 08349 'Laboratory for Aquatic Animal Medicine and Puth(dogy University of Pennsylvania Marine Biological Laboratoiy 7 MBL St Woods Hole. Massachusetts 02543 ABSTRACT An important new disease of hard clams or quahogs (Mercenaria mercenaria) in the northeastern United States appears to he caused by the protist described as QPX (quahog parasite unknown). Identification of the factors that cause or promote the disease in clams and development of diagnostic methods, as well as characterization of the life cycle of the parasite, require that the organism be cultured in vitro. Using standard tissue culture techniques, we report here the long-term propagation and in vitro life cycle of QPX. KEY WORDS: QPX. in vitro culture, life cycle, proliferation, hard clam, quahog. Mercenaria mercenaria INTRODUCTION III 1995, a protistan parasite was found to be associated with high mortalities of cultured hard clams, Mercenaria ineicenaria (quahogs), from clam leases in Provincetown and Duxbury Bays. MA. Significant mortalities, anecdotally reported to be up to 80% of the clam population, occurred just before the clams reached harvest size (approximately 2 y) in some years (Smolowitz et al. 1998). Histologically, the pathogenic organisms appeared to be very similar to the Chytridiales fungus that was first described by Drinnan and Henderson (1963) when it was found in moribund clams from Neguac. New Brunswick. Canada. Drinnan and Hen- derson ( 1963) suggested that this organism was a true parasite and was instrumental in the observed periodic population collapse of hard clams in the New Brunswick area. They believed that this organism was directly infective. Whyte et al. (1994) reported that a similar organism, which they named quahog parasite unknown (QPX). was responsible for high mortalities in juvenile and adult hard clams in a shellfish hatchery on Prince Edward Island (PEI). Canada, in 1989. Whyte et al. (1994) suggested that QPX was similar to the Labyrinthuloides and Traustochytriales. Both are orders in the phylum Lcdmnthomorpha in the subkingdom Proto- zoa (Pokorny 198.'>) but were previously classified in the phylum Labinthidomycota of the kingdom Pron.sta (Porter 1990). In 1996, QPX-like organisms were identified in cultured clams from three locations along the eastern seaside shore of Virginia (Ragone- Calvo et al. 1997. L. Ragone-Calvo pers. coinm.). Drinnan and Henderson (1963) recognized the need to culture the QPX parasite but produced no report describing culture meth- ods. Whyte et al. (1994) were able to isolate QPX cells from infected clams in the PEI hatchery. When placed in sterile artificial seawater with antibiotics, some cells produced a morula-like struc- ture containing daughter cells (probably sporangia) that eventually developed into biflagellated. uninucleate stages. Since that study, no further work on the life cycle of the organism has been accom- plished. Continuous culture of the organism and infectivity studies using cultured organisms have not been accomplished. Previous attempts (Smolowitz unpubl.) to culture QPX-like organisms using methods described by Whyte et al. (1994) and others (Vishniac 1955, Liebovitz 1963) from infected Massachusetts clams have been unsuccessful. We report here the long-term and continuous in vitro culture, propagation, and passage of QPX, including zoo- spore induction, as part of an in vitro life cycle. MATERIALS AND METHODS Presumptively infected clams (M. mercenaria) were obtained from planted flats in Provincetown and Duxbury, MA, and main- tained in isolated aquaria at the Haskin Shellfish Laboratory. Clams were shucked, and extensive focal swellings or nodules were identified in the mantle edges (Smolowitz et al. 1997). Cells of the parasite were obtained by dissecting areas of inflamed mantle tissue suspected to contain the protist as aseptically as possible with a stereo-dissecting microscope. Tissue samples thus obtained were transferred to a deep Maximov slide, rinsed five times in sterile seawater, and minced into l-mm'' pieces with a scalpel blade. Minced tissue samples were transferred to a 15-mL centrifuge tube containing 10 mL of sterile seawater and antimi- crobics (penicillin. 200 U/mL; streptomycin. 0.2 mg/mL; and am- photericin B. 0.025 p-g/mL) and were incubated for 30 min at 25°C under ambient air conditions. After this treatment, the seawater was aspirated and replaced with culture medium consisting of MEM Eagle (a inodification, Sigma 0644), 5.1 g/L; CaCU x 2H,0, 1.82 g/L; KCl. 0.68 g/L; MgCL x 6H,0. 4.36 g/L; NaCl, 24.26 g/L; MgSO^ x 7H,0. 3. 16 g/L; HEPES. 5 g/L; glucose. 0.5 g/L; heat-inactivated fetal bovine serum (Hyclone), 10% by vol- ume; penicillin, 100 U/mL; and streptomycin, 0.1 mg/mL. The pH of the final medium was adjusted to 7.2 with I M HCI and filter sterilized. The contents of each centrifuge tube were transferred to a 25-cm- T-flask (Falcon) and incubated at 25"C under ambient atmosphere. After the initial seeding of flasks, the medium was exchanged every 3—4 days (50%) and cells were routinely subcul- tured over a period of 6 mo. Phase-contrast microscopy was used to routinely monitor the cells and to obtain photomicrographs. Giemsa-stained smears of the QPX organisms cultured in MEM were prepared by aspirating 0.2 mL of the organism in culture media, smearing the aspirate on a slide, drying the slide, staining with Giemsa (Luna. 1968), and cover slipping. The smears were examined with a BH-2 Olympus microscope. 75 76 Kleinschuster et al. RESULTS The clam cells comprising the infected mantle tissue degener- ated within 10 days after the seeding of the culture flasks because the growth medium did not support clam mantle tissue. However. QPX cells contained within the mantle tissue appeared to thrive quite well in this medium and in a few days began to grow and propagate, ranging in size from 5 to 120 (xm. as seen in Figure 1. QPX thalli were enveloped by mucofilamentous material within degenerated mantle tissue (Fig. 1 ). Growth and maturation of the thalli resulted in the formation of sporangia containing many veg- etative endospores (Fig. 2). When the sporangia ruptured, en- dospores were released and formed thalli, and the vegetative growth aspect of the //; vitro life cycle was repeated (Figs. 3 and 4). In the vegetative state. QPX cells appeared to be separated from each other by a clear gel-like substance. Examination of Giemsa- stained smears from MEM cultures showed a blue mucoid material surrounding and separating the QP.X organisms. If the growth medium containing sporangia was replaced by sterile seawater. endospores as morulae-like structures adhered to the bottom of the culture flask and ectoplasmic nets became evident (Fig. 5). Within 1— f days, motile zoospores formed from the adherent endospores. Shortly thereafter (24 h), the zoospores settled and became adhered to the culture vessel (Figs. 6 and 7). As noted, the formation, motile phase, and settlement of the zoospores occurred in sterile seawater. After settlement, replace- ment of the seawater with growth medium resulted in the vegeta- tive cycle beginning anew. Figures 8-10 illustrate typical parasite cultures and microfllamentous nets surrounding immature thallis. DISCUSSION Using modifled MEM and sterile seawater. we have developed methods for continuously culturing in vitni QPX cells isolated from infected hard clams. Various forms of the parasite as iden- tified in histological sections were also identified in vitro, includ- ing thalli with thick cell walls, sporangia, and endospores. i A 1 — 3 ^ — 4 5 Fij-ure 1. QPX thalli (A) in degenerated clam niiinlle tissue (B). Notice muconianienlous material IC). I'liase-conlrast microscopy; scale bar. 50.0 Figure 2. Endospores (Al in a mature .sporangium (B). Phase-contrast microscopy, scale bar, 25.0 pm. Figure 3. Rupture of mature sporangium, releasing endospores (A). Phase-contrast microscopy; scale bar. 50.0 pm. Figure 4. Immature tballi alter Ibe rupture of a sporangium (A). Phase-contrast niicroscopv; scale bar, 25.0 pm. QPX Lll-K CvCLh AND PROPAGATION 77 Figure 5. Immature thalli cultured in sterile seawater (A). Notice ectoplasmic net hyphae (B). Phase-contrast microscopy, scale bar, 25.0 (im. Figures 6 and 7. Motile zoospores (A) originating from adhered thalli (morula). Notice ectoplasmic net (Bl. Phase-contrast microscopy; scale bar, 25.0 pm. Zoospores were formed from endospores/young thalli when spo- rangia were placed in sterile seawater. QPX organisms examined by Whyte et al. (1992) also produced zoospores when placed in sterile seawater. Zoospores have not been identified in infected clam tissue. It is likely, however, that zoospores are liberated from the sporangia contained in the clam tissue after the death and disintegration of host clam tissue. Additionally, the observation of resumption of the vegetative cycle after placing zoospores back into MEM strongly suggests that direct infection via zoospores also occurs in aquacultured clams, resulting in the production of tissue vegetative forms in live clams. The ectoplasmic net, a characteristic of the Labyrinthomor- phids, is composed of branching units of cytoplasm organized into a net. In some species, such as those of the genus Labyrinthida. the cells glide within the larger units, and in other species iLcihyriii- tlndoides spp.). the units are used to pull or push the cells in generating motility. In all species, the nets appear to be involved in the absorption of nutrients from the substrate. The ectoplasmic net originates from one or more cytoplasmic organelle(s) termed a sagenogencuisome (Pokomy 1985). In sterile seawater. presump- tive ectoplasmic netlike projections were associated with the en- dospores/zoospores. Interestingly, this netlike material was not identified in foci of QPX-like infections in clams that were exam- ined either at a light or an electron microscopic level (Smolowitz et al. 1997) or in cultures of QPX in MEM. Sagenogenetosomes also have not been identified in QPX observed within the infected clam tissue foci as of this report (Frank Perkins, pers. comm.). However, it is possible that sagenogenetosomes are present in the parasite's vegetative form but may be very rare. In infected clam tissues, instead of an ectoplasmic net, a homogenous mucofila- mentous material was produced by the parasites (Smolowitz et al. 1997). Examination of Giemsa-stained smears of parasite cells cultured in MEM showed a similar mucofilamentous material present surrounding the thalli and sporangia. Such findings are unusual for this group of organisms (Pokomy 1985). The occurrence of inflammatory nodules and swellings in in- fected clams from marine waters of the northeastern United States provided rich tissue concentrations of the parasite from which in vitro cultures could originate. Culture of organisms from infected clams in other locations in which tissue nodules cannot be identi- fied will require additional isolation and concentration methods. However, the in vitrn culture of QPX cells isolated from tissues of infected clams strongly suggests that this organism is the primary infective agent. 78 Kleinschuster et al. Figures 8-10. Typical QPX organisms in growth culture medium. Notice iialos of varying degree that compose the cell wall. Phase-contrast microscopy; scale bar, 25.0 (im. The ability to produce large uncontaminated cultures of QPX cells, as described here, will provide researchers with the materials to investigate more fully the many aspects of QPX disease of hard clams, including the pathogenesis of QPX disease in clams and environmental modulations of that disease, resistant properties of the clam, virulence properties of the QPX organism (especially production of the mucofilamentous net), and detailed examination and characterization of the parasite. It is not known what pertur- bations in in vitro culture may have been induced in the observa- tions reported in this study. ACKNOWLEDGMENTS This work is identified as Hatch Project No. 32100 and Paper No. 32100-4-97 by the New Jersey Agricultural Experiment Station. LITERATURE CITED Drinnen, R. E. & E. B. Henderson. 1963. 1962 Mortalities and a Possible Disease Organism in Neguac Quahaugs. Annual Report No. Bl I, Bio- logical Station. St. Andrews, New Brunswick. Liebovitz, A. 1963. The growth and maintenance of tLssue-cell cultures ui free gas exchange with ihe almosphere. Am. J. Hvi;. 7X: 173-180. Luna, L. G. 1968. Manual of Histologic Staining Methods of the Armed Forces ln,stitute of Pathology. 3rd ed. McGraw-Hill Book Co., New York, p. 121. Pokomy, K. S. 198.'i. Phylum LabnnlhomorplKi In: }. J, Lee, S. H. Hunter, and E. C, Bovee (eds.). Illustrated Guide to Prolo/.oa. Society of Pro- tozoologists, Lawrence, KS, p. 318-321. Porter, D. 1990. Phylum Labyrinthulomycota. //;, L. Margulis, J. O. Cor- liss, M. Melkonian, and D. J. Chapman (eds.). Handbook of Protista. Jones and Bartlett, Boston, p. 388-398. Ragone-Calvo, L. M., J. G. Walker & E. M. Burreson. 1997. Occurrence of QPX, quahog parasite unknown, in Virginia hard clams, Mencnana ineixenurui. Abstracts of the 1997 .Annual Meeting, Ft. Walton Beach, FL. Nat. Sliell. Assoc. 16:334. Smolowitz, R., D. Leavitl & F. Perkms. 1998. Observations of the protistan disease similar to QP.X in Mcnenarin merccnana (hard clams) troiii Ihe coast of Massachusetts. J. Invert. Pathol. 7l:9-2.'i. Vishniac, H. S. I9. 0.998, Tukey's HSD). The Feeding Efficiency Experiment indicated that the sabellid worms were efficient at ingesting LWMs (Fig. 5). At the lowest density examined in this study (2.6 x 10"' LWMs/mL, a level barely quantifiable with a hemocytometer), 66.77r of the worms had inszested LWMs, The relative number ol LWMs inuested was. NovHL Use of Microcapsules 81 100 90 80 70 60 50 3 2.8 0-2.6 > e 2.4 o I 2.2 o 5 2 5 1.8 1.6 1.4 maximum 15 30 60 Time (min) 30 60 120 240 Time (min) Figure I. Percentage of worms feeding and rclati\e number of LWMs ingested (logl over time (mean + SE). Data from three replicates, with independent assessment of 20 worms per replicate, per treatment. Worms were exposed to approximately 1.6 million particles/mL (0.2 gm LWMs in 50 ml. seawater). however, significantly smaller than that of the other densities (Figs. 6and7)(ANOVA. pl«>k. Thailand 10330 ABSTRACT Growth and siirvn al ot liatchery-reareiJ juxcnilc spoltod hahylon, Biilnimiui aicotata, were assessed for 7 mo. Juveniles with initial mean shell length of 15.0 ± 0.8 mm (n = 25) were held in a nursery culture system with four different treatments: two substrate types and two seawater flow rates. Length and weight measurements of individual babylon were determined monthly among the four experimental treatments, and the average monthly growth was evaluated. There were significant differences in both shell and tissue growth rates among the four treatments in most months (p < 0.05). The highest growth rales occurred in the treatment with sand substrate and flow-through seawater. whereas the lowest growth was in the treatment with no sand substrate and static seawater. The iu\eniles exhibited no growth reduction in any of the treatments except the treatment with no sand substrate and static seawater. Survival exceeded 80'7f for all treatments. KEY WORDS: gastropod, Bal->ylonia aieolata. growth, survival, nursery culture INTRODUCTION The spotted babylon. Bahyloiiia areolata (Habe 1964), known as Hoy Wan in Thailand, is a marine benthic gastropod (Neoi;as- tropoda: Buccinidae) that lays egg capsules on muddy sand sub- strate, Planktonic veligers emerge from the capsules 7 days after deposition. Postmetamorphic individuals are benthic and motile and spend most of their time half-buried in the sand. These juve- niles are capable of significant movement when offered prey or confronted by predators (Munprasit and Wudthisin 1988. Shan- mugaraj et al. 1994). The exposed nature of spotted babylon make them vulnerable to overfishing. Harvests have declined, creating chronic market shortages of larger size classes. With a foreseeable increase in demand, there is concern about sustaining and protect- ing natural populations and preventing overexploitation. Thus, various concentrated efforts are needed to develop sustained uti- lization of this gastropod fishery. Knowledge of basic laboratory- rearing techniques is key in the establishment or improvement of commercially cultured gastropod species. Literature on B. areolata is scant (Munprasit and Wudthisin 1988. Singhagraiwan et al. 1989). although Baiiylonia spirata and related species have been studied in India and Hong Kong (Thirumavalavan 1987. Morton 1990, Shanmugaraj et al. 1994. Raghunathan et al. 1994. Patterson et al. 1994. Ayyakkannu 1994. Patterson et al. 1995). Attention has been focused on aquaculture of spotted babylon as a means of preventing overfishing and increasing market sup- ply. Fast growth, low feed costs, year-around breeding, and high piice and demand suggest that this mollusc may be a profitable aquaculture species. Chaitanawisuti and Kritsanapuntu (1997) have described the larval and early juvenile culture of this species. This study was aimed at evaluating growth and survival of spotted babylon juvenile. B. areohita. in four nursery culture conditions. MATERIALS AND METHODS Experimeiitnl ,1 ninuils Broodstiick spotted babylon with a mean shell length of 5.7 ± 0.04 cm were obtained from the coastal fishing grounds of Rayong Province, on the Eastern Gulf of Thailand. The broodstock were conditioned to spawn in 1.5 x 1.0 x 0.5 m tanks supplied with tlow-through seawater (5 L/min). Salinity and temperature ranged from 26 to 29 ppt and from 28 to 30°C, respectively. A 10-cm layer of fine sand was supplied as substrate in the spawning tanks. After spawning, egg capsules and larvae were reared to metamor- phosis by the modified methods of Munprasit and Wudthisin ( 1988) and Chaitanawisuti and Kritsanapuntu (1997). Spotted bab- ylon larvae metamorphosed 18 days after fertilization at a mean shell length of 1.520 ± 2.8 |xm when they started settling on the bottom of the rearing tanks. Newly settled juveniles were then harvested and placed in nursery tanks for rearing until reaching the average shell length of 15 mm. at which time they were used for the growth experiments. Experimental Nursery Culture Condition In this study, the spotted babylon were held in nursery tanks with four different treatments — Treatment 1 : sand substrate with tlow-through seawater. The juveniles were reared in duplicate con- crete tanks of 1.5-m'' capacity supplied with a flow through of natural, aerated seawater (5 L/min). The tank bottom was covered by a 10-cm layer of fine sand substrate. The tank bottom and sand were cleaned by water jet and sun dried at monthly intervals: Treatment 2: no sand substrate with tlow-through seawater. This was similar to the first treatment, but the tank bottom had no sand substrate: Treatment 3: sand substrate with static seawater. The juveniles were reared in duplicate concrete tanks of 1.5-m'' capac- ity containing filtered ( 1 |xm pore size), continuously aerated sea- water. The tank bottom was covered by a 10-cm layer of fine sand substrate. Seawater was changed twice daily. The tank bottom and sand were cleaned by water jet and sun dried at monthly intervals; Treatment 4: no sand substrate with static seawater. This was similar to the third treatment, but the tank bottom had no sand substrate. Juvenile Rearing The juveniles, with an average shell length of 15 mm, were reared in four duplicate nursery culture conditions as described 85 86 Chaitanawisuti and Kritsanapuntu above for 7 mo. The initial stocking density was 100 indi\idiials per nr { 150 per tank). Juveniles were fed lul libitum with chopped carangid fish {Selaroides leptolepis) twice daily at 9:00 AM and 5:00 PM. Growth rates were assessed by measuring change in shell length, shell width, total weight, and wet tissue weight at monthly intervals. Mean monthly growth rates (G) and standard deviations were calculated from average increments in shell size and weight according to the formula: G = (W, - W,,)/(t| - t„), where W„ and W, = shell size or weight at times t,, and t,, respectively. The number of dead individuals was recorded in each tank at monthly intervals, and an average monthly survival rate was calculated. Statistical Analysis All statistical analyses were performed with the SPSS/PC+ Sta- tistical Package for the Social Sciences. Differences in growth and survival of all treatments were determined by a one-way analysis of variance at a = 0.05 and Tukey's studentized range test to determine statistical differences among treatments in length and weight. All data on growth rate were subjected to log transforma- tion, and percent survival data were arcsine transformed before statistical analysis. RESULTS Growth and Survival Assessments Growth (Shell Length and Width) The average monthly instantaneous growth rates in shell length and width of juvenile B. areolata did not differ significantly (p > 0.05) throughout a period of 7 mo in all treatments, but growth patterns were similar among the four treatments in that length- width ratios remained fairly constant with time (Fig. i ). The av- erage monthly shell length and width increased rapidly for the first 4 mo and. thereafter, gradually decreased. Average monthly growth increiTients in shell length and width of fi. areolata did not differ significantly (p > 0.05) in all treatments. The greatest growth increments were in Treatment 1. followed by Treatments 3. 2. and 4. respectively. Growth increment in shell length ranged from 3.65 mm/mo in Treatment 1 to 2.49 mm/mo for Treatment 4 (Table 1 ). Shell width increments ranged from 2.41 mm/mo in Tieatment 1 to 1.28 mnVmo for Treatment 4. At the end of the experiment, the greatest increase in shell growth was obtained in Treatment 1 . w ith an average shell length and width of 42.08 ± 9.1 and 26.25 ± 6.1 mm, respectively. The smallest overall growth was in Treatment 4. with an average shell length and width of 35.21 ± 5.6 and 19.62 ± 3.2 mm, respectively. The final mean growth in shell length and width of spotted babylon in Treatment 1 was significantly greater than that in Treatment 4 (p < 0.05) but did not differ significantly from that in Treatment 2 or 3 (Table I). GroHth (Weisht) The average monthly instantaneous growth rates in total weight and wet tissue weight of juvenile B. arcoUila did not differ sig- nificantly (p > 0.05) throughout a period of 7 mo among all of the treatments. Growth patterns were similar among the four treat- ments (Fig. 2). The average monthly growth increments increased over the first 4 mo and. thereafter, gradually decreased. The great- est growth increments were in Treatment I, followed by Treat- ments 3, 2, and 4, respectively. Growth increment in terms of total weight ranged from 1.53 g/mo in Treatment 1 to 0.70 g/mo in A, Shell length "nme (month) - Treatment 1 - Treatment 2 - Treatment 3 - Treatment 4 B. Shell width Time (montti) -Treatment 1 -Treatment 2 ■ -Treatment 3 ■ - Treatment 4 Figure I, Growths in shell length and width of juvenile B. areolata reared under four nursery culture conditions over 7 mo. Treatment 1, sand substrate + tlowing water: Treatment 2, no sand substrate + flowing water; Treatment 3, sand substrate + static water; Treatment 4, no sand substrate + static water. Treatment 4. and wet tissue weight was 0.74 and 0.37 g/mo in Treatments 1 and 4. respectively. Average monthly grov\th incre- ments in total weight and wet tissue weight of B. areolata did not differ significantly (p > 0.05) in all treatments. The greatest in- crease in weight was obtained from Treatment 1, with an average total weight and wet tissue weight of 1 1.22 ± 5.7 and 5.57 ± 6.8 g, respectively. The smallest was in Treatment 4. with an average total weight and wet tissue weight of 5.74 ± 9.8 and 3.31 ± 5.2 g. respectively. The final mean growth in total weight and wet tissue weight of spotted babylon in Treatment 1 was significantly greater than that in Treatment 4 (p < 0.05) but did not differ significantly from that in Treatment 2 or 3 (Table 1 ). Survival Rales The average monthly survival of juvenile B. areolata did not differ significantly (p > 0.05) through the culture period of 7 mo for all treatments. Survival patterns were similar among the four treatments (Fig. 3). The average monthly survival gradually de- creased over the first 4 ino. and thereafter, no mortality took place in any of the treatments. The average monthly percentages were 0.28 ±0.1. 1.42 ± (1.2. 0.71 ± 0.2. and 1.42 ± 0.347r in Treatments I. 2. 3. and 4. respectively. The final mean survival of spotted babylon did not significantly differ (p > 0.05) among the four treatments {Table I ). Size Distribution At the end of the experiment, the harvested animals were graded into 10-mm size intervals. Treatments 1 and 3 showed the Growth anii Survival of B. areolata 87 TABLE 1. Mean growlli and survival rates of Juvenile H. areolata reared under the four nursery culture conditions; there were no si^niHcant differences in growth and survival as determined by analysis of variance. Nurserv Culture Conditions lirowth Parameters Sand Siihslrate. Flowing Water No Sand Substrate, Flowing Water Sand Substrate, Static Water No Sand Substrate, Static Water Final shell length (mm) Final shell width (mm) Final total weight (g) Final shell weight (g) Final tissue meat weight (g) Final survival (%) Growth rate in shell length (mm/mo I Growth rate in shell width (mm/mo) Growth rate in wet tissue weight (g/mo) Growth rate in total weight (c/mo) 42. OS 26.24 11.22 5.27 5.57 97.0 3.65 2.41 0.74 1.5.^ 36.50 21.73 6.81 3.44 3.84 90.5 2.83 1.70 0.58 0.89 40.27 24.52 10.27 4.99 5..54 96.5 3.38 2.13 0.76 1.35 35.21 19.62 5.74 3.52 3.31 90.0 2.49 1.28 0.37 0.78 most uniform growth and more individuals in large sizes. Treat- ments 2 and 4 showed irregular and largely variable growth (Fig. 4). By the end of the expenment, the large size classes in Treat- ments 1 and 3 were 40.0-50.0 mm at 85 and 55%, respectively. In contrast, in Treatments 2 and 4. the largest size classes were 35.0- 40.0 mm at 54 and 60%. respectively. A. Total weight 3 4 Time (month) -Treatment 1 -Treatment 2 ■ -Treatment 3 -Treatment 4 B. Wet tissues weight 2 3 Time (month) -Treatment 1 - Treatment 2 • -Treatments • -Treatment 4 Figure 2. (Irowths in total weight and wet tissue weight of juvenile B. areolata reared under four nursery culture conditions over 7 mo. See legend to Figure 1 for experimental treatments. DISCUSSION In this study, juvenile spotted babylon. B. areolata. have been successfully reared in a shore-based nursery system. The spotted babylon are capable of reaching the marketable size of 5-6 cm shell length in 7 mo with a high survival rate. The best nursery culture method tested was to use tanks with sand substrate and free flowing seawater. It is suggested that water flow and sand substrate are important factors for spotted babylon growth in nursery cul- ture. The treatments had no effect on the survival rate of the test animals. The sand substrate may play an important role in the growth and survival of spotted babylon. The effect of substrate could be manifested in numerous ways. The presence of sand substrate may cause a reduction of stocking density (thinning out) of snails in the rearing tank because a number of snails can bury in sand substrate, thus affecting a third dimension to their distribu- tion. Alternatively, lack of substrate may induce interactive energy expenditures by individuals similar to that described in queen conch. Strotnbus gigas (Siddal 1984). Average monthly growth rates of B. areolata were higher than those of the spiral babylon, B. spirata. and the giant muricid gastropod. Chicoreus ramosus. 3 4 Time (month) -Treatment 1 - Treatment 2 ■ -Treatments ■ -Treatment 4 Figure 3. Survival rates of B. areolata in tv\o size classes at the end of the experiment, reared under four nursery conditions. See legend to Figure 1 for experimental treatments. 88 Chaitanawisuti and Kritsanapuntu 100 - 1 90 < 80 - 70 - 60 50 40 30 20 - \ 10 1 \ 4 : 1 rrealment 1 Treatment 2 Treatment 3 Treatment 4 Culture condition -»- 30-40 mm. — •- 40-50 mm. Figure 4. Size distribution of B. areolata in two size classes at the end of the experiment, reared under four nursery conditions. See legend to Figure I for experimental treatments. These results are in general agreement with the study of Raghu- nathan at al. (1994), who reported that the average growth rate ol B. spirata was increased from 2.9-3.0 to 3.5-3.8 cm in shell length and from 6.5-7.8 to 11.1-14.1 g in total weight over a 10-mo period. Patterson et al. ( 1995) observed an average growth rate tor B. spiniki fed with oyster and crab 1.2 and 0.05 g/day. respec- tively, over a 30-day period. In contrast, juveniles of C. ramosii.s reared in concrete raceways averaged 2.6, 10.9, 9.2, 4.2. and 1.1 mm/mo in shell length at ages of 2, 4, 5, 8, and 1 2 ino, respectively (Nugranad et al. 1994). Kraeuter ct al. (1989) reported that the average growth rate of knobbed whelk, Biisycon carica, for the first 10 y of life in laboratory conditions was 14.4 tntWy. Growth performance of juvenile abalone, Haliotis tiihenuUilii. was im- proved by grading the animals. Growth of small abalone improved in the absence of larger conspecifics. The choice of stocking den- sity is essentially a trade-off between maximum growth, optimal biomass gain, and economic considerations. The latter may dictate densities that would result in a net reduction in growth, but a greater reduction in overall production costs (Mgaya and Mercer 1995). This study showed that B. areolata may be an anitnal with aquaculture potential. It exhibited a fast growth, enabling market- able sizes to be cultured within 7 mo with a simple hatchery technology for larviculture and juvenile growout. Further studies should concentrate on improvement of the culture technt)logy of this series for higher growth and production of juveniles in both nursery and growout phases. Additional data are required to assess the economic feasibility of the culture of this species. ACKNOWLEDGMENTS We thank the National Research Council of Thailand (NRCT) for providing funds for these re.search projects in the fiscal year of 1995. We are special grateful to Prof. Dr. Piamsak Menasveta, Director of Aquatic Resources Research Institute, Chulalongkorn University, for his encouragement and suggestions. Last, we ex- tend our thanks to Dr. Sonkiat Piyatiratitivorakulfor for assisting in the statistical analysis and the revision of the manuscript. LITERATURE CITED Ayyakkaniui. K. 1994. Fishery status of Buhvlnnia ipiniki at Porto Novo, southeast coast ot India, Phukcl. Mar. Biiil. Cent. Spec. Puhi No. I3:5.V56. Chaitanawisuti, N. & A. Kritsanapuntu. 1947. Laboratory spawning and juvenile rearing of the marine gastropod: spotted habylon. Bahylomu areolcita Link 1807 (Neogastropoda; Buccinid.ie). in Thailand. J. Shcll- fhh Res. 16:31-37. Habe, T. 1964. Shell of the Western Pacific in Color, vol 2. Hoikusha Publishing Co., Osaka. 233 pp. Kraeuter, J. N., M. Castagna & R. Bisker. 1989. Growth rate estimates for Busycon curica in Virginia. J. Shellfisli Res. 8:219-225. Mgaya, Y. D. & J. P. Mercer. 1995. The effects of size grading and stock- ing density on growth performance of juvenile abalone. Haliotis tuhei- ciilatti Linn. AiiiHunlliire. 136:297-312. Munprasit, R. & P. Wudthisin. 1988. Preliminary study on breeding and rearing of areolata babylon (Bahyli)iiiu areolata. L). Technical Paper No. 8. Eastern Marine Fisheries Development Center, Departmetit of Fisheries, Rayong Province, Thailand. 14 pp. Morton, B. 1990. The physiology and feeding behaviour of two iiiarine scavenging gastropods in Hong Kong: the subtidal Babylonia lutosa and intertidal Nassariiuis festiviis. J. Moll. Stud. 56:275-288. Nugranad. J.. T. Poomtong & K. Promchinda. 1444. Mass culture of Chicoreus rainosas (Gastropoda: Muricidae). Phuket. Mar. Biol. Cent. Spec. Puhl. No. 13:65-71. Patterson, J.. T. Shanmugaiaj & K. Ayyakkannu. 1994. Salinity tolerance of Bahyloiua spirata (Neogastropoda: Buccinidae). Phuket. Mar. Biol. Cent. Spec. Puhl. No. 13:95-97. Patterson. J. K.. C. Raghunathan & K. Ayyaknnu. 1995. Food preference, consumption and feeding behaviour of the scarvenging gastropod Bahxiouia spirata (Neogastropoda: Buccinidae). hul. ./. Mar. Sci. 24: 104-106. Raghunathan, C, J. K. Patterson & K. Ayyakkannu. 1994. Long term study on food consumption and growth rate of Babylonia spirata (Neogas- tropoda: Buccinid.ie). Phuket. Mar. Biol. Cent. Spec. Puhl. No. 13:207- 210. Shanmugaraj, T., A. Murugan & K, Ayyakkannu. 1994. Laboratory spawn- ing and larval development of Babylonia spirata (Neogastropoda: Buc- cinidae). Phuket. Mar. Buil. Cent. Spec. Puhl. No. 13:95-97. Siddal. S. E. 1984. Density-dependent levels of activity of juveniles of the queen conch Stroinbus .iiii;as Linn. ,/. Shelljish Res. 4:67-74. Singhagraiwan, T., S. Singhagraiwan & M. Sasaki. 1989. EfTeets of irra- diated sea water with ultraviolet rays on inducing to spawn of the areola babylon (Babylonia lUcolcUa Link). Technical Paper No. 12. Eastern Marine Fisheries Development Center, Department of Fisheries, Ray- ong Province, Thailand. 16 pp. Thirumavalavan. R. 19897. Studies on Babylonia spirata (Linn.) Mollusca (Gastropoda: Buccinidae) from Porto Novo waters. M. Phil. Thesis. Annamalai University, India. Joiirmil ofShiUlhh Kcscanh. Vol. 17. No. 1. 8')-')-S. l'»8. ONTOGENETIC CHANGES IN SALINITY AND TEMPERATURE TOLERANCE IN THE DOUGHBOY SCALLOP, MIMACHLAMYS ASPERRIMA WAYNE A. O'CONNOR AND MICHAEL P. HEASMAN A'SVV Fisheries Poll Stephens Researeh Centre Sahinuimler Bay. NSW. 2316. Anstralia ABSTRACT Bnihryos and larvae of the doughboy scallop. Miimiililamys usperrima. were held at lemperatiires in the range from 9 to 24°C and exposed to salinities in the range from 27.5 to 40 ppt. At each stage in ontogeny, salinity optima remained constant at 32.5 ppt: however, optimal temperatures differed and there were significant interactions between the effects of salinity and temperature. Percent development of eggs to D-veliger stage was greatest at a temperature of 17°C. whereas mean larval survival and shell length increase were greatest at 21 and 24°C, respectively. Overall, larvae were more tolerant of extremes in both salinity and temperature than embryos. Juvenile (18 mm shell height) and maturing (28 mm shell height) M. asperrima held at temperatures of 14 or 24°C and exposed to salinities in the range of 15-40 ppt grew rapidly at 24"C but exhibited salinity optima (.32.5-35 ppt) similar to those at the earlier ontoaenetic stages. Maturing scallops were, however, less tolerant of salinity reductions than were their smaller conspecitics. For both juvenile and maturing M. cisperrima. initial behavioral responses, such as byssogenesis. provided a guide to longer term growth and survival. In general, salinity and temperature optima were seen as reflecting the environmental conditions likely to be experienced by the respective ontogenetic stages within Jervis Bay. However, response of embryos in particular to reduced temperature was inconsistent with the geographic range of M. asperrima and was thought to reflect either genetic differences in stocks or preconditioning. KEY WORDS: salinity, temperature, tolerance, ontogeny, byssogenesis, scallops INTRODUCTION Autecological study of bivalves has clearly demonstrated that development, growth, and survival are affected by physical param- eters, in particular, temperature and salinity, which have been de- scribed as "master factors" for many marine organisms (Kinne 1964). Accordingly, the effects of these two factors have been described for numerous mollusc species including many pectinids. Temperature directly influences metabolic rate and survival of scallops (Nakanishi 1977. Ventilla 1982, Dame 1996) and indi- rectly influences the nutritional environment (Wallace and Rein- snes 1985, Ito 1991). Thus, seasonal temperature regimens criti- cally influence the siting and timing of hatchery, farming, and stock enhancement programs. Similarly, the distribution of scal- lops is clearly limited by salinity, with most scallops living in fully saline water (Brand 1991). In many cases, such as Argopecten gibbiis (Allen and Costello 1972), Chlamys opercularis (Paul 1980a), and Pecten maxiimis (Strand et al. 1993), scallops are not tolerant of reduced salinity and require areas of relatively high stable salinity. Equally important, but less researched are the synergistic ef- fects of temperature and salinity. It has long been recognized that the effect of one can be modified by the other and that there is a need to study their actions concurrently (Kinne 1964). Interactions in tolerance to salinity and temperature have been demonstrated in pectinids (Paul 1980a. Tettelbach and Rhodes 1981. Mercaldo and Rhodes 1982, Hodgson and Bourne 1988, Strand et al. 1993). with extremes in one factor commonly reducing tolerance to variations in the other. To illustrate this, surface contour diagrams are useful and have been used to visually represent the responses of pectinids (Paul 1980a. Tettelbach and Rhodes 1981, Mercaldo and Rhodes 1982), Through the comparison of these contour diagrams, onto- genetic changes in temperature and salinity tolerance are also eas- ily observed. Tettelbach and Rhodes (1981) found that embryonic development was limited to a narrow range of temperature and salinity, whereas larval growth and survival occur over a wider range. Similar observations have been made on Patinopecten yes- soensis. where spat were less tolerant of salinity reductions than adults (Yamamoto 1956 cited in Brand 1991), and on Pecten fu- matiis. where temperature optima increased during the early stages of ontogenetic development (Heasinan et al. 1996). Over the geographical range of Mimaehlamys asperrima (Lamarck, 1819). mean monthly sea temperatures vary from mini- muin winter values of 9-1 1°C in southern Tasmania (Hortle and Cropp 1987) to maximum summer values usually in the range of 23-25°C on the central coast of New South Wales (N.S.W.) (CSIRO 1994 unpubl.) Although there is some conjecture as to the northern extent of the species range on both the eastern and west- em Australian coasts, if it does extend to Queensland in the east (Lamprell and Whitehead 1992) or Shark Bay in the west (Wells and Bryce 1988), even greater temperature maxima could be ex- pected. With respect to salinity, M. asperrima is confined to areas of relatively high and stable salinity. Most major populations have been reported in coastal waters (e.g., Bass Strait. D'Entrecasteaux Channel. St. Vincent Gulf) or embayments in which freshwater intrusions have a limited effect (e.g.. Port Phillip Bay. Jervis Bay). The importance of temperature and salinity and their interac- tions in establishing protocols for scallop hatchery production and in determining the optimal timing of spat availability prompted an investigation of tolerance in M. asperrima. Variation in tolerance according to ontogenetic stage was also investigated. For this pur- pose, the salinity tolerance of hatchery-reared juvenile M. asper- rima was assessed at temperatures approximating the minima and maxima encountered in Jervis Bay ( 14 and 24°C). METHODS All M. asperrima embryos, larvae, and juveniles used in this study were progeny of broodstock collected from Murrays Beach. Jervis Bay. Broodstock were held in the hatchery at 14"C in sea- water (33-35 ppt) until required, usually less than 2 wk. Spawn- ings were conducted by methods described in O'Connor and Heas- 89 90 O'Connor and Heasman man (1995). and in all experiments, the progeny from a minimum of five separate pairs of adult scallops was used. Temperatures were maintained with water baths fitted with thermostatically con- trolled immersion heaters, all housed in a cool room held at a constant air temperature of 9 ± 1°C. Salinities were measured with a temperature/salinity bridge (Yeo-kal. Sydney. Australia) and ad- justed with "Ocean Nature-" salt mixture (Aquasonics Pty Ltd. Inglebum. Sydney. NSW) or rainwater. To ensure that salinities were not altered with the addition of microalgal food, algal cells were centrifuged to a concentrate before D-veligers and spat were fed at a rate of 5.000 cells/larvae per day and 10'' algal cells/mL per day, respectively. All seawater in this study was passed through l-|jim-pore-size (nominal) cartridge filters before use. Cul- tures of embryos and veligers were static and nonaerated. whereas juveniles were held in aerated aquaria for both acclimitization and experimentation. Experiment I: Embryo Salinity and Temperature Tolerance Eggs from five scallops were collected separately on a 20-(j.m- pore-size nylon mesh sieve and resuspended in 1 L of seawater (18°C ± 0.5°C, 35 ppt). Each batch of eggs was fertilized, and the suspension was mixed thoroughly with a perforated polyvinyl chloride plunger. Zygote number in each batch was estimated from four replicate 1-mL aliquots sampled while inixing and examined on a Sedgwick rafter slide at lOOx magnification. Within 30 min of spawning, equal numbers of zygotes from each batch were pooled and thoroughly mixed before aliquots of 4.5 mL of the suspension (1.500 zygotes) were collected with an adjustable au- tomatic pipette and transfen'ed to 30()-mL food-grade plastic con- tainers. In a preliminary experiment, embryos were exposed to salini- ties from to 40 ppt, increasing in 5-ppt increments. Development did not occur at salinities of 25 ppt or less. On the basis of this finding, a fully orthogonal experiment was designed, in which replicate sets of four 300-mL containers were maintained at one of six salinities (27.5, 30, 32.5. 35. 37.5. or 40 ppt) and one of five temperatures (9. 14. 17. 21. or 24°C). Hypersaline solutions (37.5 and 40 ppt) were generated by the addition of artificial sea salt (Ocean Nature*) to seawater (35 ppt). Hyposaline solutions (<35 ppt) were generated by the dilution of seawater with rainwater. D-veliger larvae can be observed as early as 30 h postfertilization (Krassoi et al. 1996). although the rate of development is tempera- ture dependent (Cragg and Crisp 1991); thus, replicates were al- lowed 56 h before sampling. At that time, the seawater in each container was thoroughly mixed and four replicate 1 0-mL samples were taken from each container. The number of zygotes having developed to D-veliger stage in each sample was determined by dispersing each sample on a Petri dish and counting larvae with the aid of a dissecting microscope (40x magnification). On the basis of these estimates, D-veliger yield (the percentage of eggs reaching D-veliger stage) was calculated. Before the commencement of Experiment 1. it was realized thai care was needed in the selection of both the salt and the diluent for salinity adjustment. In an evaluation of hypersaline solutions for detaching P.fumatus spat (Heasman et al. 1994). it had been noted that the choice of artificial salt mixture for salinity increase sig- nificantly affected spat response. To test the utility of Ocean Na- ture® and rainwater, an additional treatment was added in which embryos were placed in .seawater that had been diluted to 25 ppt with rainwater, before being returned to 35 ppt with Ocean Na- ture*. In this way. embryos were exposed to both the diluent (rainwater) and the salt mixture and development could be com- pared with that of seawater. Experiment 2: Veliger Salinity and Temperature Tolerance Batches of embryos were reared in 1.000-L polyethylene tanks containing seawater (18°C, 35 ppt) at an initial stocking density of 5 eggs/mL. After 48 h, the tanks were drained and D-veligers were retained on a 45-|xm-pore-size screen. D-veligers were resus- pended in 10 L of seawater. and their numbers were estimated from four replicate l-mL samples taken while the suspension was being mixed with a plunger. Three replicate Erlenmeyer flasks, filled with 1011 niL of sea- water and stocked with D-veligers (5/mL). were held at each of the previously tested temperature and salinity combinations (see Ex- periment 1 ). Larvae were fed daily and given complete water exchanges every second day. After 7 days, the larvae were col- lected on mesh sieves and resuspended in 10 niL of a seawater and formalin (2% by vol) solution. The numbers of larvae that had survived until Day 7 in each replicate were counted with the aid of a microscope (40x magnification), and where possible, the growth (increase in shell length measured parallel to the hinge) of 50 larvae from each replicate was determined. In replicates where fewer than 50 larvae had survived until Day 7. all surviving larvae were measured. Experiment 3: Juvenile Salinity and Temperature Tolerance Two groups of 4S hatchery-reared M. aspcrrinui juveniles, comprising small (IN. 4 ± 0.7 mm shell height, mean ± SE) and larger (28.8 ± 0.5 mm shell height, mean ± SE) scallops were collected and cleaned of biofouling. Macroscopic inspection of the gonads of the group of larger scallops indicated that they had commenced sexual maturation. Half of the scallops within each group were selected at random and placed in 14°C seawater to acclimatize for 4 days. The remainder were in seawater at 24''C for 4 days' acclimatization. Physical limitations restricted the number of temperatures tested to two. and so 14 ± 0.5 and 24 ± 0.5°C were chosen because they approximated the extremes encountered by M. aspcrrima at the site of broodstock collection. At each temperature, four repli- cate 8-L aerated aquaria were established at each of eight salinities (15. 20. 25, .30. 32.5. 35. 37.5. and 40 ± 1 ppt) generated as in Experiment I. Each scallop was placed in an individual aquarium. Seawater in each aquarium was drained thrice weekly and replaced with fresh, temperature- and salinity-equilibrated seawater. Tem- peratures and salinities were monitored daily throughout the ex- periment to ensure that they did not vary outside the prescribed ranges. The experiment was run for 10 days, during which survival was monitored daily and growth (increase in shell height) was detennined at the termination of the experiment. Byssal attachment of juveniles to the walls of the aquaria was monitored at 2, 4, 8, and 24 h poststocking. On each occasion, spat were gently pushed with an artist's brush to determine if byssal attachment had occurred. RESULTS Experiment I: limhryo Salinity and Temperature Tolerance Fertilized eggs placed in containers at 9' C extruded polar bod- ies, but development then ceased irrespective of salinity. The high- M. Asri.KHiMA. Salinity, and Tkmperature Tolerance 91 esl peicciit dc\clop[iieiU Co D-veliger stage OL'currcd at 17 and 2I°C (Fig. 1). At 17 C, development to D-veliger stage occiined at all salinities in the range from 27.5 to 40 ppt but was greatest at 32.5 ppt. In combination, the highest mean percent development to D-veliger stage (?• 34 ffi w Temperature (°C) Figure 1. The effect of temperature and salinity on the yield of M. asperrima D-veligers. Isopleths indicate the percentage of eggs devel- oping to D-veliger stage, and the circle indicates the point of maxlnuim recorded yield. Temperature (°C) Figure 2. The effect of temperature and salinity on the numbers of A/. asperrima larvae surviving to Day 7 postfertilization. Isopleths indicate the number of live larvae expressed as a percentage of the initial number stocked, and the circle indicates the point of maximum re- corded survival. peratures of 17°C or less, with the greatest increases in larval length occurring in the range from 21 to 24°C at salinities of 32.5 and 35 ppt. The highest growth recorded in this trial (33.5 |j.m) was at a temperature/salinity combination of 24°C and 32.5 ppt. Larval growth and survival at various temperatures were com- pared by two-way ANOVA. Before comparison, survival data were arcsin square root transformed and homogeneity of variance for both growth and survival data was assessed by Cochran's test (Winer 1971) (C = 0.196, p = 0.052 and C = 0.202. p = 0.042. respectively). Unlike the previous embryo development data, het- erogeneity in larval survival data was considered to be minor, and that in a design with equal sample sizes, two-way ANOVA was sufficiently robust to deal with such minor departures from homo- geneity (see Underwood 1997). Temperature and salinity signifi- candy (p < 0.05) affected both growth and survival of larvae, and there were significant interactions between temperature and salin- ity in both cases. Experiment 3: Juvenile Salinity and Temperature Tolerance Both juvenile and maturing juvenile scallops grew more rapidly when held at 24°C than at 14°C, with the greatest growth incre- ments recorded at salinities of 32.5 and 35 ppt (Fig. 4a). The greatest absolute growth increments at either I4"'C or 24°C were recorded for maturing scallops (0.7 and 1.5 mm. respectively); however, unlike juveniles, these scallops did not grow or survive at any salinities of 30 ppt or less. Some juveniles were capable of surviving up to 10 days at salinities of 25 ppt, whereas both sizes survived at 30 ppt (Fig. 4b). There were no observed differences in salinity tolerance of either juveniles or maturing scallops with respect to the two tested temperatures (Fig. 4b and c). 92 O'Connor and Heasman Growth (um) He;isman et al. 1996). Both embryos and larvae of M. asperrima demonstrated clear responses to extremes in temperature. At low temperatures (9-14°C), little to no embryonic development oc- curred and both larval growth and survival were reduced. At el- evated temperatures, embryonic development and larval survival were reduced; however, the increasing distance between isopleths above the respective optimal temperatures indicated that both em- bryos and larvae were more tolerant of temperature increases than decreases. The optimum for embryonic development in this study (17°C) was similar to that found by Krassoi et al. (1996) (18°C), beyond which they observed significant increases in larval abnor- malities. For larval growth, the optimal range began at 20' C (Fig. 3), the upper limit tor optinial larval survival (Fig. 2), and did not decrease with temperature increases within the range tested. Clear ontogenetic changes in temperature optima were ob- served for M. asperrima. Comparisons of embryonic development (yield) and larval survival demonstrate similar temperature optima. but greater tolerance by larvae. Notably, larvae grew rapidly at elevated temperatures at which embryos did not survive. However, particular care should be taken in the interpretation of embryonic temperature tolerance results. The narrow tolerance range ob- served is inconsistent with the geographical distribution of M. Temperature (°C) Figure 3. The effect of temperature and salinitv on the growth of 7-day-old M. asperrima larvae. Isopleths Indicate the mean increase in shell length measured parallel to the hinge, and the circle indicates the point of maximum recorded growth. Irrespective of the size of juvenile scallops or the temperature at which they were held, response to abrupt salinity reductions commonly involved a short period of swimming, followed by valve gaping, and then valve closure. In general, scallop responses to salinity reductions appeared more rapid and violent than did those of scallops exposed to salinity increases of similar incre- ments. There was also a trend for responses to increase in intensity with salinity reductions down to 25 ppt; however, it was difficult to discern any differences between responses to salinities of 15 and 20 ppt. The time taken by juveniles to bysally attach to the walls of the aquaria retlected, in most respects, growth and survival at that particular salinity/temperature combination (Fig. 5). Attachment did not occur at salinities lower than .^0 ppt and was most rapid at 32.5 and 35 ppt. Within the range from 30 to 40 ppt, byssal attachment commenced most rapidly at 24"C, with some scallops having attached within 2 h. The major disparity between observa- tions of byssal attachment and growth and survival data occurred at a salinity of 30 ppt. Although 507r of 1 S-mm juveniles and 75% of 28-mm M. asperrima byssally attached to aquaria walls (Fig. 5), they did not survive the duration of the trial at this salinity/ temperature combination (Fig. 4). DISCUSSION Temperalure Temperature is a key variable in scallop larval rearing, with demonstrable effects as early as the first cleavage stages of em- bryonic cell division (Zavarzeva 1981). In general, low tempera- tures reduce growth and development (Beaumont and Budd 19S2, Hodgson and Bourne 1988, Heasman et al. 1996), whereas the high temperature, mortality increases (H^)dgson and Bourne 1988, 1.5 - .-G) F 1.2 Q-' / E, 0.9 ,>- \ — ▼ , 1 0.6 ^x' ^\s-^ O U.3 A J I.--. -% ~~--J • • A A t 10 _ I- _X.-J- I l^^. 1 8 - / / /A / A A A > 3 6 4 - / / ? ^ •:>r ■<^' w *'- -r ^ inn •■■ .„ T..X- J I ^ ."" ^ X K X ^ 80 : /▼" -^ / "tS 60 - / / / > 1 40 20 T // 1 X "^ - --g a 15 20 25 30 35 40 Salinity (ppt) D 28 mnn scallops, 24 °C ^ 28 mm scallops, 14°C ▼ 18 mm scallops, 24 °C •- 18 mm Scallops, 14°C figure 4. Increase in shell height la) and survival (h and c) of M. asperrima juveniles held a( one of two temperatures and one of eight salinities. M. Asrt:f% CO 100 80 60 14°C, 18mm • 3b 32.5 30 S 1 40 - 37.5 & 40 20 t 1 J L 2 4 6 810 12 14 16 18 20 22 24 100 80 60 40 20 14°C, 28mm ^5 ^ 32.5 30 37.5 & 40 I I I 2 4 6 8 10 12 14 16 18 20 22 24 . 35. .,.. ^°°24°C,r8mm " 32.5 80 60 . ,_ 40 20 100 80 60 40 20 -.*"- 30 ''37.5 40 J L 2 4 6 8 10 12 14 16 18 20 22 24 24°C, 28mm 35 "32^5 r 37.5 .30 40 2 4 6 8 10 12 14 16 18 20 22 24 Time (h) Figure 5. Byssogenesis of M. asperrima over 24 h when held at .salini- ties within the range from 3(1 to 4(t ppt at a temperatures of 14 or 24C. Figures in each graph indicate water temperature ( C), scallop size I mm I and test salinities (ppt I. asperrima. Spawning in southeastern Tasmania occurs in Septem- ber and October (Zacharin 1994), when water temperatures are in the range from 10 to 14-'C (Hortie and Cropp 1987). At these temperatures, limited embryonic development would be expected (Fig. 1). This suggests that there are either genetic differences in tolerance (and possibly optima) across the species range or the results reflect preconditioning. Physiological responses of organ- isms can be modified by their thermal history (McLusky 197,^. Paul 1980b) and. in this case, possibly by the parental history. Broodstock (and their gametes) used here were held at 18°C, and thus, temperature shock may explain poor embryonic development at lower temperatures. However, observations in the hatchery have indicated that, irrespective of the parental holding iciiipcraturc ( 14-22"C). developnient of M. asperrima embryos decreases dra- matically at temperatures exceeding 20°C (W. A. O'Connor 1993 pers. obs.). Thus, ontogenetic changes between embryo and larval tolerances still exist. Salinity The predominantly coastal distribution of M. asperrima is re- flected in salinity tolerance of each of the ontogenetic stages tested. Salinity optima remained largely static at approximately 32.5 ppt. irrespective of ontogeny. Again, this is consistent with the observations of embryos by Krassoi et al. (1996), who found optimal salinity to be in the range from 32 to 34 ppt, with increas- ing percent abnormality outside of this range. Salinity tolerance, however, tended to increase with ontogeny from embryo to larvae to juvenile stages, only to decrease at the onset of maturity. The increase in tolerance from einbryo to larval stages has often been reported in bivalves (Tettelbach and Rhodes 1981. Dame 1996), as has a subsequent slight decrease in tolerance of C. opercidaris with increasing age (Paul 1980b). The cause for the latter is unknown, although in M. asperrima. it may retlect an additional metabolic demand due to the onset of maturation in larger juveniles. As noted earlier, care is needed in the use of salts and diluents used for salinity adjustments. Subsequent to this research, Krassoi (1995) tested a number of salts and diluents as the sole media for culture and found Ocean Nature* and Sydney municipal water to be unsuitable for the development of M. asperrima. Larval abnor- malities did not increase, but D-veliger yields were reduced. In this study, yields of D-veligers were not significantly reduced when embryos were maintained in a solution of approximately 72% seawater and 28*^ artificial seawater (Ocean Nature" and rainwa- ter). This was equivalent to the ainount of salt mixture or rainwater that would be needed to either raise or lower the salinity by 10 ppt. Although this suggests that these results were not affected by the use of Ocean Nature® or rainwater, it raises the question "At what concentration were yields affected?" and reinforces the need for care when using artificial media. Salinity Temperature Interaction As reported in several earlier studies with pectinids (Paul 1980a, Tettelbach and Rhodes 1981, Mercaldo and Rhodes 1982, Hodgson and Bourne 1988, Strand et al. 1993), there is a signifi- cant interaction between temperature and salinity in their effects on M. asperrima. In general, extremes in one factor reduce toler- ance to variations in the other, although one factor can influence responses more rapidly than the other. Tettelbach and Rhodes (1981) concluded that temperature appeared to hold dominance over salinity ior Argopeeten irradiaiis irradians. because deviation from temperature optima caused the most rapid reductions in growth. This conclusion was drawn from the proximity of isop- leths in A. irradians surface contour diagrams; however, a differ- ent pattern was observed for M. asperrima. Surface contour dia- grams of M. asperrima embryo yield differ little with respect to the separation of isopleths along temperature or salinity axes (Fig. 1 ), whereas larval growth and survival were more sensitive to changes in salinity than temperature. This sensitivity is reflected in the distribution of M. asperrima. which occurs in areas of stable sa- linity, but across a broad latitudinal range that experiences extreme temperature differences on the order of 15°C (i.e.. 9-24°C). Ecological and Farming Effects The value of short-term studies, such as this, in which envi- ronmental changes are often abrupt, is open to conjecture. Daven- 94 O'Connor and Heasman port et al. (1975) argued that such changes are unlikely to be representative of those encountered in the natural environment because they provide little opportunity for animals to acclimatize. However, Paul (1980b) has suggested that although such results are likely to be a "severe" indication of tolerance, they can still be of particular value to the mariculturist. Optima derived from such studies are applicable to hatcheries where these physicochemical parameters are controllable and can be applied in determining rearing conditions for the early ontogenetic stages of scallops. Similarly, even conservative estimates of tolerance are of value in selecting sites for nunsery rearing and grow out of scallops. Ontogenetic changes in temperature tolerance of M. aspeniiiiti are similar to those previously described for P. fiimatus (Heasman et al. 1996), with a tendency for increased tolerance and higher temperature optima with increasing age. These changes in optima appear to be reflected in the reproductive behavior in populations of M. aspenima in Jervis Bay. Peaks in reproductive condition occur in late winter and spring (O'Connor and Heasman 1996), when temperatures are increasing and generally in the range from 16 to 19°C. Gamete release at this time would increase the like- lihood of embryos experiencing optimal temperatures of about 18°C and make it unlikely that they would encounter supraoptimal temperatures of >20°C. Larval survival would also be expected to be at its greatest toward the upper end of this temperature range, although larval growth rates would increase if temperatures of 20°C were reached. Increases in water temperature with the onset of summer could accelerate the later stages of larval growth and promote spat growth. In these experiments, both juvenile and ma- turing scallops grew well at the approximate upper limit of tem- peratures in Jervis Bay (24°C). Major oceanographic events and their effects on temperature have been used to explain recruitment variation in two Australa- sian pectinids. Amusiiim balhni (Bemardi. 1861) (JoU 1994, Joll and Caputi 1995) and P. fiimatus (Heasman et al. 1996). In the latter case, the El Nifio Southern Oscillation (ENSO) and the East Australian Current, along with the hydrography of Jervis Bay, were thought to lead to periodic temperature regimens in which the temperature optima for P. fiimatus were met. The scarcity of such regimens was suggested as a factor in the infrequent nature of significant recruitment of P. fiimatus. Recruitment of M. aspenima has exhibited annual variations that reflect those seen in P. fiimatus (W. A. O'Connor 1996 pers. obs.): however, these variations have not been of the magnitude observed for P. fiimatus. This may result from the extended availability of reproductively capable M. asper- rima in Jervis Bay. which permits the exploitation of suitable temperature regimens whenever they arise. In addition, embryos of M. aspenima are more tolerant of elevated temperature than are those of P. fumatus, for which temperatures greater than 18 C led to dramatic reductions in development. On the basis of these results, fertilization, incubation, and em- bryonic development should be conducted at temperatures in the range from 17 to 20°C. Temperatures for larval rearing should be increased to 20-2 1 °C to maximize growth while maintaining high survival (Figs. 2 and 3). Juveniles and maturing juveniles grew well at 24°C, without mortality, indicating that ihcy were more tolerant of elevated temperatures than were larvae. Of the tested salinities, optima remained in the range from 32.5 to 35 ppt irre- spective of ontogeny. From a production perspective, salinity op- tima are unlikely to present difficulties; however, the seasonal timing of hatchery rearing is in some cases constrained. Most hatcheries can heat water; however, few can easily cool water. At the southern extent of the species range in Tasmania, water will rarely exceed the optima for embryonic development, but at Port Stephens Research Centre, water temperatures can reach 25°C during the summer months. Without cooling, water suitable for incubation is only available for approximately 9 mo a year, al- though these months include the peak in wild stock reproductive condition and would permit production of spat in time for a spring/ summer season of rapid growth. Behavioral Responses Behavioral changes have been found to be a useful indicator of physiocheniical stressors within a pectinid's environment (Daven- port et al. 1975. Roberts 1973 cited in Paul 1980b. Heasman et al. 1996). Most bivalves close their valves in response to salinity change to allow iso-osmotic intracellular regulation to commence (Hawkins and Bayne 1992); however, M. asperriina initially re- spond in a manner similar to that oi A. irradians (Duggan 1975) and C. opercidaris (Paul 1980a), by swimming, presumably in an attempt to escape the influence of the irritant. The magnitude of the response was observed to give some indication of its ultimate effects on growth and survival. Within several hours, further in- dications of the suitability of environmental conditions can be obtained from the number of scallops having bysally attached. Attachment was most rapid at temperature/salinity combinations at which high growth and survival occurred. However, in common with C. opcnidaiis (Paul 1980b). byssal attachment also occurred under conditions in which juveniles did not survive. At salinities of 30 ppt, juveniles held at I4°C survived, whereas those at 24°C did not. Possibly, the demands of byssogenesis, between 4 and 14% of energy budget for somatic production in Chlamys islandica (Vahl 1981), in conjunction with a metabolic rate accelerated by in- creased temperature, are too great. Regardless, behavioral obser- vations provide an additional tool in the evaluation of potential culture environments, particularly for M. aspenima. which con- tinues byssal secretion into its adulthood. In summary, ontogenetic changes in M. asperriina tolerance to both temperature and salinity were evident, as was an interaction between these two factors. However, although the temperature optima increased in later stages of development, the optimal sa- linity for all developmental stages tested remained fixed. In gen- eral, behavioral response, including byssogenesis. pro\ ided a guide to longer term growth and survival. ACKNOWLEDGMENTS The authors thank Allen Frazer, Stephen O'Connor, and Wayne Walker for assistance with this research. Thanks are also due to Geoff Allan, David Stone, Mark Booth, and the anonymous ref- erees for valuable editorial comments and assistance during prepa- ration of the manuscript. Allen, D. M. & T. J. Coslello. 1972. The (.alico scallop. Arfiopecten kHjIius. N.O.A.A. Tech. Rep. NMFS S.SRF 656. 19 pp. Miami. PL. USA. Beaumont, A. R. & M. D. Budd. 1982. Delayed growth of the mussel LITERATURE CITED (Mxiilus ediilis) and scallop Wn icn iikimiiius) veligcrs al low Icmpera- lures. Mar. Biol. 71:97-100. Brand, A. R. 1991. Scallop ecology: Distribulmn and hehavLour. pp. 517- M. ASPI.KKIMA. SaI,INIIA . AND TEMPERATURE TOLERANCE 95 ?S4. In: S. E. Shumway (ed.). Scallops; Biology, Ecology and Aqua- culture. Developments in Aquacullure and Fisheries Science, vol. 21. Elsevier. Amsterdam. Cragg. S. M. & D. J. Crisp. 1491. The biology of scallop larvae, pp. V.'i- 122. In: S. E. Shumway (ed.l. Scallops: Biology. Ecology and Aqua- culture. Developments in .'kquaculture and Fisheries Science, vol. 21. Elsevier, Amsterdam. Dame. R. F. 199(1. Ecology of Marine Bivalves: An Ecosystem Approach. CRC Press. Boca Raton. FL. 254 pp. Davenport, J.. L. D. Gruffydd & A. R. Beaumont. 197.'>. An apparatus to supply water of fluctuating salinity, and its use in the study of the salinity tolerance of the larvae of the scallop Peclen iiiaximns L. ./. Mar. Biol. As.mc. U.K. 55:391-409. Duggan. W. P. 197.'?. Growth and survival of the bay scallop. ArgD/H-cti'ii irnuiiaiis, at various locations in the water column and at various densities. Proc. Natl. Shellfish Assoc. 63:68-71. Hawkins, A. J. S. & B. L. Bayne. 1992. Physiological interrelations, and the regulation of production, pp. 171-222. In: E. Gosling (ed.). The Mussel Mytilus: Ecology. Physiology. Genetics and Culture. Elsevier. Amsterdam. Heasman. M. P., W. A. O'Connor M. asperrima A.W.J. Frazer. 1994. Detachment of commercial scallop, Pecten fitmalus. spat from settle- ment substrates. Aquaciihiire. 123:401^07. Heasman. M. P., W. A. O'Connor & A. W. J. Frazer. 1996. Ontogenetic changes in optimal rearing temperatures for the commercial scallop. Peclen fiimaliis Reeve. / Shellfish Res. 15:627-634. Hodgson. C. A. & N. Bourne. 1988. Effect of temperature on larval de- velopment of the spiny scallop. Clilamys hasiaia Sowerby. with a note on metamorphosis. J. Shellfish Res. 7:349-357. Hortle. M. E. & D. A. Cropp. 1987. Settlement of the commercial .scallop Peclen fiimatus Reeve 1855. on artificial collectors in eastern Tasma- nia. Aquacullure. 66:79-95. Ito. H. 1991. Japan, pp. 517-569. In: S. E. Shumway led.). Scallops: Bi- ology. Ecology and Aquaculture. Developments in Aquaculture and Fisheries Science, vol. 21. Elsevier. Amsterdam. Joll. L. M. 1994. Unusually high recruitment in the Shark Bay scallop (Amusium balloti) fishery. Mem. Queensland Museum. 36:351-356. Joll, L. M. & N. Caputi. 1995. Geographic variation in the reproductive cycle of the saucer scallop. Amusium balloii (Bemardi, 1861) (Mol- lusca: Pectinidae), along the Western Australian coast. / Mar. Fresh- water Res. 46:779-792. Kinne. O. 1964. The effects of temperature and salinity on marine and brackish water animals. II. Salinity and temperature-salinity combina- tions. Oceanogr. Mar. Biol. Ann. Rev. 2:281-339. Krassoi, R. 1995. Salinity adjustment of effluents for use with Marine Bioassays: Effects on the larvae of the doughboy scallop Chlamys asperrimus and the Sydney rock oyster Saccostrea commercialis. Aus- tralasian J. Ecotoxicol. 1:143-148. Krassoi. R.. D. Everett & 1. Anderson. 1996. Methods for Estimating Sublethal To.xicity of Single Compounds and Effluents to the Dough- boy Scallop Chlamys asperrima iMollusca: Pectinidae) (Lamarck). National Pulp Mills Research Program Technical Report No. 18. CSIRO. Canberra. 63 pp. Dickson. ACT. Australia. Lamprell. K. & T. Whitehead. 1992. Bivalves of Australia. Crawford House, Bathurst, NSW, Australia. 182 pp. McLusky, D. S. 1973. The effect of temperature on the oxygen consump- tion and filtration rate of Chlamys iAeijuipeclen) opercularis (L.) (Bi- valvia). Ophelia. 10:114-154. Mercaldo, R, S. & E. W. Rhodes. 1982. Influence of reduced salinity on the Atlantic bay scallop Argopeclen irradiiuis (Lamarck) at various tem- peratures. J. Shellfish Res. 2:177-181. Nakanishi. I. 1977. Studies of the effect of the environment on the heart rate of shellfishes. 1 . effect of temperature, salinity and hypoxia on the heart rate of scallops. Bull. Hokkaido Reg. Fish. Res. Lab. 42:65-73. O'Connor. W. A. & M. P. Heasman. 1995. Spawning induction and fer- tilisation in the doughboy scallop Chlamys (Miiiicuiilamys) asperrima. Aquaculture. 136:117-129. O'Connor, W. A. & M. P. Heasman. 1996. Reproductive condition in the doughboy scallop Chlamys (Mimachlamys) asperrima Lamarck in Jervis Bay. Australia. / Shellfish Res. 15:237-244. Paul, J. D. 1980a. Salinity-temperature relationships in the queen scallop Chlamys opercularis. Mar. Biol. 56:295-300. Paul. J. D. 1980b. Upper temperature tolerance and the effects of tempera- ture on byssus attachment in the queen scallop Chlamys opercularis (L.). J. Exp. Mar. Biol. Ecol. 46:41-50. Strand. 0.. P. T. Solberg. K. K. Andersen & T. Magnesen. 1993. Salinity tolerance of juvenile scallops {Pecten maxinms) at low temperature. Aquaculture. 115:169-179. Tettelbach, S. T. & E. W. Rhodes. 1981. Combined effects of temperature and salinity on embryos and larvae of the northern bay scallop Ar- gopeclen irradians irradians. Mar. Biol. 63:249-256. Underwood, A.J. 1997. Experiments in Ecology. Cambridge University Press, Cambridge, United Kingdom. 504 pp. Vahl, O. 1981. Energy transformations by the Iceland scallop, Chlamys islandica (O. F. Miiller) from 70°N. I. The age-specific energy budget and net growth efficiency. J. Exp. Mar. Biol. Ecol. 53:281-296. Ventilla. R. F. 1982. Scallop culture in Japan. Adv. Mar. Biol. 20:309-382. Wallace. J. C. & T. G. Reinsnes. 1985. The significance of various envi- ronmental parameters for growth of the Icelandic scallop, Chlamys islandica (Pectinidae), in hanging culture. Aquaculture. 44:229-242, Wells, F. E, & C, W. Bryce. 1988. Seashells of Western Australia. Western Australian Museum. Perth, Australia. 207 pp. Winer, B. J. 1971. Statistical Principles in Experimental Design. McGraw- Hill, New York, pp 205-210. Zacharin, W. 1994. Reproduction and recruitment in the doughboy scallop, Chlamys asperrimus, in the D'Entrecasteaux Channel, Tasmania. Mem. Queensland Museum. 36:299-306. Zavarzeva, E. G. 1981, A method for estimating the rate of development of mollusc embryos [Engl, transl.). DoU. Biol. Sci. 266:527-528. Jounnil nf SJirllfisb Rcscanli. Vol. 17, No, l,i»7-l()l. KWS, THE IMPORTANCE OF GONADAL DEVELOPMENT ON LARVAL PRODUCTION IN PECTINIDS MARCEL LE PENNEC,' RENE ROBERT,' AND MIGUEL AVENDANO' ^Biolofiic nuiriiw UMR CNRS 6539 Iiistitiit Universitaire Europeen de la Mcr Universite de Bretagne Occidentale 29280 — Plouzane, France -IFREMER Centre de Brest BP 70. 29280— Plouzane. France ^Facultad de Reciirsos del Mar Universidad de Antofagasta. Casilla 170 Antofagastu. Chile ABSTRACT In the natural environment and in hatcheries, development of pectinid eggs varies considerably between species, between populations of a given species, and between hatcheries. In addition, results observed in hatcheries vary considerably from one year to another and are therefore not reproducible, which is detrimental to the success of this type of aquaculture venture. On the basis of results obtained both in situ and in the laboratory for Argopeclen imrpuralus from Chile and for Pecten maximus from France, an attempt was made in this study to determine factors leading to poor quality of eggs of these pectinids. Nutrient level available in the gonad seems to be the main factor involved. In particular, absence or low levels of polyunsaturated fatty acids such as 20:4 (n-6), 22:6 (n-3), and 20:1 {n-9) appear to be delrimenlal to proper larval development. Similarly, sterols are also necessary to ensure a harmonious larval existence because this molecule is used extensively by the embryo in building cellular membranes. The addition of these compounds to anificial feed or selection of new algal feeds seems to be a prionty if the dependability of Pectinid hatcheries is to be increased. KEY WORDS: factors, quality of oocytes, larval development, Pectinids INTRODUCTION In both the natural environment and hatcheries, levels of pec- tinid egg development are extremely variable within a given spe- cies, between populations, and from one hatchery to another. Fur- ther, results obtained in nature and in experimental or private hatcheries are not reproducible from one year to the next. Evidence of this nonreproducibility can be gleaned from the literature for pectinids living in cold to temperate waters such as Plaeopeclen imigeUanicus (Naidu et al. 1989), for warm-water species such as Argopecten circularis (Felix-Pico 1991), and for strictly temper- ate-water pectinids such as Pecten maximus (Ansell et al, 1991), Fertilization rates are based on the number of normal D larvae produced from a given number of eggs (Salaiin 1994). The non- reproducibility of these fertilization rates is linked to quality of the gametes released. These gametes must possess structural (Dorange 1989) and biochemical characteristics fSoudant 1993) necessary to ensure harmonious embryonic development throughout the en- dotrophic phase (Lucas et al. 1986) and to allow subsequent proper development of larvae and successful metamorphosis. On the basis of studies by Bayne (1976) on Mytilus ediilis and Helm et al. (1973) on Ostrea ediilis. it is generally accepted that the main reason for differences in bivalve gamete quality are due to environmental conditions experienced by inaturing adults. More recent studies by Delaunay (1992) and Soudant (199.3) confirm these observations. As a result, research effort over the last 15 y has been directed toward resolving this problem. Results that have been and are being obtained should allow a significant advance in pectinid aquaculture in the near future. In this article, an attempt was made to determine precisely factors responsible for the poor quality of gametes in mature adults of two pectinid species. To this end. results obtained in situ and in the laboratory for Argopecten piirpiiratiis from Chile and P. maxi- mus from France were examined. These results were obtained by the authors or by researchers (Salaiin 1994) working in our labo- ratories at IFREMER/Brest and at the Universities of Brest and Antofagasta. It is hoped that such an approach will increase our understanding of the complex biological and reproductive aspects of these organisms. CONSIDERATION OF PAST RESULTS Spawning Levels and Quality of Gametes A. purpuratits Regrettably, results available are fragmentary and involve adults only from one area in the north of Chile. Adults were sampled by diving at maturity from the Bay of Mejillones (Region II. northern Chile) and spawned by thermal shocks in the labora- tory. Observations were made strictly after collecting (Table I). P. maximus Individual fertilization rates were examined, between 1992 and 1995. for 3- to 5-y-old animals originating from the Bay of Brest and conditioned in the IFREMER hatchery in Argenton (Brittany. France) by techniques previously described (Robert et al. 1994). Observations on fecundity (number of oocytes emitted) were re- 97 98 Le Pennec et al. TABLE 1. Relationship between size of adult A. piirpiiraliis and number of eggs spawned (Avendano 1993). Length No. of No, of Oocytes of Adults Individuals per Individual Date of Spawn (mm) That Spawned (xlO") September 27, 1992 55-6.^; 7 6.4 October 12. 1992 66-75 11 10.4 November 4, 1992 76-85 12 14.4 November 10, 1992 96-105 S 27.5 conditioned F. ijiu.xiiinis individuals was 10.59 x 10'^ ± 1.36 (mean for all spawns ±95% confidence interval), whereas the mean num- ber of D larve was 28.31 x 10'' ± 4.10. Different results were obtained with mature animals from the Bay of Brest, where a negative correlation was found between these two parameters, i.e., the greater the number of oocytes emit- ted, the lower the D larvae levels (Fig. lb). Mean fecundity of animals from the natural environment was 8.43 ± 1.40 (mean for all spawns ±95% confidence interval), and the number of D larvae was on the order of 47.45 ± 8.98. Spawiiiiif; and iMrral Development alized 1 h after spawning, whereas data on D larvae formation were obtained 48 h after egg release. Fecundity was not correlated with the number of D larvae obtained. In other words, it would appear that the number of D larvae obtained is similar regardless of the quantity of oocytes emitted (Fig. la). Average fecundity of Regression Plot 15 20 Fecundity Y = 27,6636 + .061 5 * X: R''2 = .0004 Regression Plot 25 -1 — ' — r 8 10 12 14 16 18 20 22 Fecundity Y = 66,8819 -2,3049- X; R»2 = ,1289 Fisure I, la) Regression line hetHeen the number of oocytes released (fecundity) and the number of 4S-h-old I) larvae from mature scallops taken from the natural environment, (b) Regression line between the number of oocytes released (fecundity) and the number of 48-h-old D larvae from hatchery-conditioned hroodslocks. A. purpnratiis For adults collected at maturity in the Bay of Mejillones, high- est values for the gonadal-somatic index were observed from Oc- tober to December, during which period spawning occurred in silii. This same period was also found to be favorable for larval devel- opment in the laboratory by standard techniques following those described for P. maximus (Robert et al. 1994). Larval growth rates varied between 3.5 and 7.6 p.m/day. and levels of metamorphosis, which correspond to the number of postlarvae divided by the num- ber of pediveligers, were low (Table 2). P. maximus Results from the IFREMER hatchery of Argenton for adult P. maximus. sampled from the bay of Saint-Brieuc (Brittany, France), are shown in Table 3. These results were obtained during the natural breeding period in the bay. In the experimental spawns, which were in the same period where P. maximits spawned in the bay of Brest to massive in situ spawns (in phase), the number of abnormal larvae (abnormal pro- dissoconch or abnormal velum) observed was only 4.2% of total larval number as opposed to 6.4 and 16.4% for the out-of-phase spawns. Similarly, larval growth rates, measured in fjim/day, were in the order of 4.9 |jim for in-phase spawns and between 3.8 and 2.6 (j(,m for the other cases. Finally, levels of metamorphosis (num- ber of postlarvae observed 2 wk after transfer in the micronursery produced from a given number of pediveligers ready to set) were higher for in-phase individuals (22.9%) than for other groups (0 to 18^.6%). From a biological point of view, growth of bivalves in the hatchery of Argenton was relatively problem free, with the excep- tion of July and August, at which time gonadal development could not be obtained after the initial gonadal purging of the animals. Only spawners that are already undergoing gametogenesis m the TABLE 2. •A comparison of gonadal-somatic index, larval growth rate, and level of metamorphosis in A. purpuratus reared on four occasions during the natural breeding period in the Bay of Mejillones. Ihile (Avendaiio 199.1). Gonadal- Larval Level of Somatic Growth Rate Metamorphosis Date of Spawn Index (pni/day) (%) September 27. 1992 16.9 2.8 October 12, 1992 1X.3 6.5 5.7 November 4, 1992 17.6 3.5 November 10, 1992 IS.l 7.6 2.3 Larval Production in Pix-iinids 99 TABLE 3. Results of larval rearing experiments carried out during the July 1987 reproductive season of P. maximus in relation to spawning periods recorded in situ (seawater temperature, 16"C) (from Salaiin 1994). Level of Abnormal Larval Hatchery Spawn in Relatii un Larvae on Larval Growth Survival L eve! No. of Level of to In Situ Spawn Day 2 ( % ) Rate (pm/day) (%) Postlarvae Metamorphosis In phase to* 4.2 4.9 92.3 105.846 22.9 Out of phase tO- 7 12.4 2.6 48.1 8.700 3.6 tO + 3 16.4 3.8 53.9 50.256 18.6 Out of phase by malntainins; tO + 9 6.4 3.2 24.1 the spawners at I4'C tO + 16 9.5 3.6 27.3 10,554 7.7 to + 35 12.2 3.2 12 *t0, in phase spawns: tO -7, +3, +9, +16. and +35, early or late spawns as compared with those detected in the natural environment. natural environment and that had reached Stage 2 on the Mason ( 19.'i8) scale could be conditioned during this period and at a water temperature of 13°C, DISCUSSION The in situ fluctuations in numbers of several species of eco- nomically important pectinids. e,g,. P. magellanicus (Dickie 1955), are well documented. Fluctuations in P. maximus numbers (Boucher 1985) were e-xamined as part of a National Program Determining Recruitment (PNDR). Observed fluctuations led Boucher et al. ( 1985) to suggest that there exists a hierarchy to the ciitical steps leading to recruitment steps, which include gamete production. A few years after the above study. Dorange (1989) carried out a meticulous cytochemical and cytological examination of P. maximus gametes obtained from hatcheries. She showed that there was great variability in the quality of gametes that produced viable larvae, and she listed three oocyte types that were relea.sed during in situ or hatchery spawns: immature, overly mature having a mature aspect, and mature oocytes. Of these three oocyte types, only the last will produce larvae. The study of reproductive cycles showed that signs of atresic oocytes (Dorange and Le Pennec 1989) are visible throughout gametogenesis. During spawns, which were never complete in P. maximus. these deteriorated oocytes were either released or re- mained within the gonad, where they degenerated. Results ob- tained for specimens sampled from the Bay of Saint-Brieuc re- vealed that the deterioration phenomenon increased with increas- ing gonadal maturation to reach a maximal level in late June (Dorange 1989) or. in other words. 15 days to 3 wk before the natural spawning period. Atresic oocytes can represent up to 409!^ of total oocyte numbers. Similar observations have been made in the Bay of Brest (Cochard and Gerard 1987) as well as for A. purpuratus (Avendafio 1993). Levels of lytic oocytes toward the end of gonadal maturation could be linked to depletion of glycogen reserves in muscle tissues. If this is true, then oocyte degeneration would represent a natural part of the reproductive cycle in several bivalve species, particular in pectinids. The importance of this information for hatcheries is that it is impossible to obtain oocytes that are 1007f fertilizable. regardless of the time of the year. Since 1986, the French have preferentially used conditioned spawners. with the exception of during the fall period. During fall, adults from the natural environment release relatively few oocytes. These oocytes, however, exhibit high fertilization rates, produce high-quality pediveligers. and generate an ongrowing survival level of approximately 40%. Previously conditioned adults used at the Tinduff hatchery all originated from the Bay of Brest. The annual pediveliger produc- tion in the hatchery is on the order of 65 x 10'^ (67.5 x 10'' in 1993 and 66.5 x 10'' in 1994). Larval production at this hatchery, how- ever, remains variable and problematic. Larval numbers are satis- factory from February to June, at which time they fluctuate be- tween 29 and 60%. but are very low from July through December (Carval and Muzellec 1995). For hatchery-conditioned P. maximus individuals originating from the Bay of Brest, analysis of the gametes released by each adult showed that the number of D larvae obtained remains similar, regardless of the number of oocytes initially released. This agrees with results obtained for conditioned adult Crassostrea gigas (Robinson 1992a). In contrast, the same analysis of P. maximus individuals sampled at gonadal maturity //; situ reveals that a nega- tive correlation exists between these two parameters. In other words, the more oocytes emitted, the lower the number of D larvae produced. In situ, the concept of quantity therefore seems incom- patible with that of gamete quality, which is in agreement with the conclusion on oocyte degeneration in this species (Le Pennec et al. 1 99 1 ). Mean fecundity of conditioned spawners is approximately 10.59 x 10* ± 1.36 (mean ± confidence interval), whereas values in the wild are on the order of 8.43 x 10'' ± 1.40 (mean ± confi- dence interval). Regardless of conditions, the variability of these values remains important, and as a result, no significant difference in fecundity is observed between wild and conditioned individuals. The same holds true v\hen the number of D larvae obtained was examined. Reasons for this high level of gamete variability in pectinids have been the object of a number of studies over the last 15 y. Several parameters can be pointed out as being responsible for these fluctuations: exogenous characteristics such as water quality and temporal fluctuations of intrinsic phytoplankton quality (Sa- main et al. 1992) or endogenous characteristics such as genetic variability (Cochard and Devauchelle 1993). On the basis of research by Lannan ( 1980) on C. g/ga.v, it would seem that a great portion of the variability experienced during bivalve rearing can be attributed to factors other than genetics. Among these other factors, food quality plays an important role and it has been shown that diet directly affects gamete composition 100 Le Pennec et al. and larval development (Whyte et al. 1987, Whyte et al. 1990, Salaun 1994, Soudant 1993). Although fragmentary, results in the literature indicate that variability in biochemical composition of the microalgal food source plays a determining role in the variable maturity of the gonad. Also, it is the levels of essential components such as fatty acids that are of paramount importance and not total levels of proteins, carbohydrates, and lipids (Delaunay 1992. Soudant 1995). Indeed, lipids play two fundamental roles in cellular me- tabolism — storage of energy in the form of triglycerides and the functioning of cellular membranes in the form of phospholipids and cholesterol (Holland 1978). The study by Delaunay (1992) confirms the limited ability of P. maxiimis when using precursors to synthesize polyunsaturated fatty acids necessary for metabolism and survival such as 20:4 (n-6), 20;5 (n-3), and 22:6 (n-3). Under hatchery conditions, a preferential accumulation of these three fatty acids in the oocytes will occur regardless of their concentration in the microalgae (Soudant et al. 1996). Similar results were recorded for P. imigel- laniciis taken from the natural environment (Napolito and Ackman 1993). It would seem that the 20:4 (n-6) fatty acid is important to the process of oogenesis, whereas in the male, the 20:1 (n-9) fatty acid is involved in gametogenesis. The 22:6 (n-3) molecule would be important during egg differentiation (Soudant et al. 1996). In the same way, bivalves have a very low or none.xistant capacity to synthesize or transform sterols ( Holden and Patterson 1991). Cholesterol, however, is used extensively by embryos to build cellular membranes (Delaunay 1992). Although it is generally accepted that lipids play an important role in the proper development of the bivalves" endolrophic phase, several authors believe that they are an essential factor in the exotrophic phase and, subsequently, determine the success of metamorphosis. This hypothesis seems to be validated in M. ediilis (Bayne et al. 1975), O. edulis (Helm et al. 1973), Ostrea chilensis (Wilson et al. 1986), and Argopecten iiradians (Kraeuter et al. 1982). However, it does not hold true for C. gigas (Gallager et al. 1986). The effect of dietary lipids on larval development in P. maximiis has only been evaluated for the endotrophic phase (Soudant et al. 1996). It would be of interest to determine its effect during the exotrophic phase because low metamorphosis levels are sometimes obtained in hatcheries despite a satisfactory larval de- velopment before this phase. DIRECTION OF FUTURE WORK It would appear that further studies should be carried out on dietary lipid, essential fatty acid, and sterol levels if we are to increase the reliability of pectinid and other bivalve hatcheries. Studies by Robinson (1992a and 1992b) on C. gigas demonstrate quite clearly the importance of this research. Indeed, she condi- tioned adults with either microalgae or simple lipid emulsions and observed identical oocyte maturation, fecundity, D larvae abun- dance, and spat production with the two dietary treatments. The addition of certain fatty acids, such as 20:4 (n-6). 20:5 (n-3). and 22:6 (n-3) either through use of new algal species or as a result of artificial feed additives, will mcrease the presence of these molecules within the oocytes, which should decrease oocyte deterioration, thereby increasing gametogenetic yield. It has been shown that use of a lipid emulsion brings about incorporation of fatty acids into triglycerides and polar lipids in O. edulis larvae and P. magellanicus juvenWef, (Coutteau et al. 1994. Coutteau et al. 1996), results that indicate that essential compounds present in the feed are transferred to the egg and. subsequently, play a role in later stages of development. In much the same manner, cholesterol should be administered at higher levels than are used at present during conditioning. This increase in cholesterol could be obtained through the use of new diatom or picoplankton strains, such as has been suggested by Patterson et al. ( 1994). ACKNOWLEDGMENTS Many thanks to M. Johnson for the English translation of the manuscript. This work was supported by an ECOS (action Chile n" C94B04) — CONICYT program of scientific cooperation between France and Chile. LITERATU Ansell, A. D.. J. C. Dao & J. Mason. IWI. Three European scallops: Pecten maximiis. Clilamys (Aeqiiipcclen) openiilciris and C (Clilamys) varia. pp. 715-751. In: S. E. Shumway (ed.). Scallops: Biology, Ecol- ogy and Aquaculture. Elsevier Publishers. Amsterdam. Avendano, M. 1993. Donnees sur la hiologie de Ari;opecU'ii piiipuriilus (Lamarck, 1819), MoUusques Bivalves du Chili. These d'Universite. Universite de Bretagne Occidentale, Brest. Bayne, B. L. 1976. Marme Mussels, Their Ecology and Physiology. Cam- bridge University Press, London. Bayne, B. L., P. A. Gabbott & J. Widdow. 1975. Some effects of stress in the adult on the eggs and larvae of Mvliliis t't Slu'lllish Kisiiiirh. Vol. 17. No. I, KM-lll. IWS. ZYGOCHLAMYS PATAGONICA IN THE ARGENTINE SEA: A NEW SCALLOP FISHERY MARIO L. LASTA' AND CLAUDIA S. BREMEC" 'insritiilo Nacional de Investigacion y Desarrollo Pesqucro (INIDEP). ami 'Consejo Nacional de Investigaciones CieiUiJlcas y Tccnicas (CONICETj c.c. 175, Paseo V. Ocainpo I 7600 Mar del Plata. Argentina ABSTRACT This paper gives informalion associaled with the development of a new fishery of patagonian scallop Uygochluniys palasonka King and Broderip 1832) in the Argentine Continental Shelf. A joint State-Industry research program was performed during 1995 with a 56 m scalloper F/V (Erin Bruce). A total of 7,134 trawl shots were performed over 246 days. Seven new beds with commercial potential were found between 38° 50' S and 42 30' S. largely along the 100 m isobath. Beds were discrete, ranging from 42.7 to 353.8 km". Proportions of scallops and invertebrate by-catch and population size structure varied between beds. CPUE varied from 291 to 4,927 (kg of commercial size scallops • towing h"' ) in different beds. Large differences were found between muscle yield estimated at laboratory (12.07% and 23.65'7r in Sea Bay and MdQ beds, respectively). On the basis of CPUE and muscle yield, the average landing per unit of effort ranged from 65.5 to 1,037.6 (kg of muscle • towing h"'), Dunng the study period a total of 1,315 I of muscle (160-240 pieces -kg"') was landed. Total scallop catch and commercial scallop catch were 13,580 and 10,592 t, respectively. We suggest that management of this new developing fishery should be based on the application of a rotation and reserves areas criteria. KEY WORDS: Scallop, Zygochlamys patagonica. fishery. Southwestern Atlantic Ocean INTRODUCTION The patagonian scallop, Zxgochlamxs patagonica (King and Broderip 1832). is distributed around the southern tip of South America from 42° S in the Pacific to 35" S in the Atlantic, between 40 and 200 m depth (Waloszek and Waloszek 1986. Lasta and Zampatti 1981. Defeo and Brazeiro 1994). Studies on reproduction indicate that se.xes are separate (Waloszek and Waloszek 1986). but Orensanz et al. (1991a) sug- gest sequential protandric hermaphroditism. Sexual maturity is reached at 45 mm shell height (=2 y old) with emission of gametes in two pulses during spring and late summer to early autumn (Waloszek and Waloszek 1986. Orensanz et al. 1991a). Annual growth rings are marked (in the shell and ligament) during the winter (Waloszek and Waloszek 1986). Scallops with a single growth ring were found to have bimodal size distribution (Waloszek and Waloszek 1986). related to the spawning period. Size at settlement (interred from the size of the prodissoconch) is =0.2 mm. Recorded maximum shell height and age are 79 mm and 8 y, respectively. Estimated parameters for the von Bertalanffy growth equation (size-at-age data) range between 53 and 79 min for asymptotic height and 0.35 and 0.67 y"' for k (Waloszek and Waloszek 1986. Orensanz et al. 1991a). Three general fishing surveys, "Prof. Siedlecki71973 (Oren- sanz et al. 1991a). 'Walther Herwig71978 to 1979 (Waloszek and Waloszek 1986) and "Walther Herwig"/1978 to 1979 and 'Shinkai Maru71978 (Lasta and Zampatti 1981) revealed largest concen- trations between 42° and 44" S and 46° and 48" S. and between 60 and 80 m depth (Fig. 1 ). These areas were explored during 1989 by the 67 m Norwegian scalloper FA' (Sea Bay Alpha) during 24 days. Catches taken in the Tres Puntas and Sea Bay beds were processed onboard and confirmed the economical value of the resource (Lasta 1992). Although the commercial potential of this species has been previously stressed (Waloszek 1991) and confirmed by the results of the short experimental fishing survey of the scalloper FA' 'Sea Bay Alpha' during 19X9 (Lasta 1992) the fishing industry did not express interest for a further 5 y. During 1995. a joint State- Industry research program was performed by the 56 m FA" 'Erin Bruce", scalloper equipped with bottom otter trawls (efficiency 21-31%. Lasta and Iribame 1997) and mechanical processing on- board (Lasta and Bremee 1995. Bremec et al.. in press). These investigations lead to the location of seven new beds of patagonian scallop and a novel fishing activity in the Argentine Sea. The research program produced a total of 1.315 t of inuscle from an estimated commercial scallops catch of 10.592 t (total weight). Muscles • kg'' were in a range of 160-240. Estimates of mean biomass in a dense patch in Valdes bed were in a range of 0.22- 0.23 kg of scallops • m"- (Lasta and Iribame 1997). Lack of baseline information on target and associated species is a limiting factor to elucidate changes from natural and/or anthro- pogenic causes. Following Brand and Prudden (1995). we are building complete databases as a tool for a long-term management- oriented research programme to assess the impact already pro- duced on the scallop stocks. The year-round experimental fishing survey represents an unusual possibility of collection of both fish- ery and ecological information before fishing disturbances. The objective of the present paper is to communicate the results of studies on spatial distribution and dimensions of beds, size frequency distributions, and scallop yield by beds during the study period. MATERIALS AND METHODS During 1995 a total of 15 trips were performed in the area from 38° to 48° south and between 50 and 130 m depth in the Argentine Sea using a 56 m scalloper (FA" 'Erin Bruce'). A total of 7,134 trawl shots (13.177 nets, 92% of paired of trawls) was performed in 246 days at sea, from January to December. Data on research sampling and fishing activity were obtained by observers onboard during all trips. A bottom otter trawl, similar to the gear used in the calico scallop fishery (Argopecten gihbiis Linnaeus. 1758). was used for this program. The estimated efficiency of this gear ranged between 21% and 31%' (Lasta and Iribarne 1997). Initial and final positions of each haul were registered by General Positioning Sys- tem equipment. Fishing distances were calculated on the basis of 103 104 Lasta and Bremec URUGUAY ARGENTINA RECLUTAS iAN BLAS MALVINAS ISLANDS Burdwood BahK 32° 34° 36° 38° 40° 42° Q 44° t 46° 48° 50° 52° .^f^ 54° 70° 65° 60° 55° LONGITUDE Figure 1. Spatial distribution of the pulagonian scallop (Z. palagonica. King & Broderip. 1832) on Ihc Argentine Continental Shelf (light gray). Largest concentrations (dark gray) and known beds ( , Sea Bay and Tres Puntas) before 1995. New beds discovered during the experimental fishing survey (•): MdQ, Redutas, San Bias, SAO, SWSAO. Valdes and Tango B. Line: trip L 1995. towing time (minutes) and speed (km • ii"'). Depth in meters was recorded using an echosounder. The mean trawling speed was 7.37 km ■ h~' (SD; 0.66, n: 7.134) and mean towing time was 1 1.23 min (SD: 2.23, n: 7,208). Unsorted catch (UC: scallops plus by-catch) per tow was cal- culated by visually estimating the extent to which the cod-end was filled, based on categories of 10% before it was opened on deck. The UC weight for different proportions of cod-end fullness (20%, 50%, 80%'. and 100%) piovided the following linear relationship: a: 22.98 (SE: 1.37). b: 4.28 (SE: 98.89), r": 0.9.S, n: 17 (Lasta and Iribarne 1997). A full net was estimated lo contain s 2.300 kg of UC. Scallop catch (SC) was estimated from the scallop yield (SY%i): samples ( 10 kg each) were taken randomly from the UC in 3.187 tows and scallop and bycatch fractions were weighted (ac- curacy 0.1 kg). On the basis of this proportion (SY%f). the SC in the UC was estimated. Commercial scallop catch (CSC) was es- timated by assessing that proportion of commercial scallop yield (CSY%i) of scallops s= 55 mm total height. This size was initially assumed as a minimum legal size from previous studies on repro- duction, growth, and muscles per kg (Waloszek and Waloszek 1986. Orensanz et al. 1991a. Lasta 1992). Catch per unit effort (CPUE) is expressed as commercial scallop kg • towing h"'. Muscle landing per unit effort (LPUE) is expressed as muscle kg • towing h~'. Estimates of average LPUE is the product of average commercial scallop CPUE and average muscle yield. SD of LPUE by bed were estimated by the variance of products (Goodman 1960 in Raj 1980) of commercial scallop CPLIE and muscle yield. ANOVA tests were performed to compare data from beds; arcsen (V x/lOO) transformation were applied to data in %■ (SY and CSY) and Ln transformation to CPUE data. Size frequency distributions were measured for all beds, with shell height (SH). being measured with a caliper to the nearest millimeter. Samples of standard specimens (60 mm SH) from different areas were taken and frozen (-20°C) for a range of measurements in the laboratory. Total weights without epibionts (TWWE) were measui'ed in grames (accuracy 0.1 g). Muscle weight (MW) was measui'ed (accuracy 0.01 g) and expressed as muscle yield (MY% ) in percentage of the TWWE. Samples sites and beds are shown in Figure 1 . The estimated dimension of beds was based on a fishing/ productive scope. Once a fishable area was found, the vessel was allowed to fish without technical intervention. Commercial fishing ceased and searching for another fishable bed whenever produc- tion dropped, according to some fishing/threshold of profitability criteria. Position of each tow and corresponding CPLIE were plot- ted. Then dimensions in latitude and longitude for the total tows were calculated in every profitable (fishing criteria) area. All CPUE values were included in the calculation of "average CPUE", only those "0" values caused by operational problems were not considered. RESULTS Location of Reds The prospection program conducted to the finding of seven new beds of patagonian scallop in the Argentine Sea (Fig. I). During the first trip the objective was to reconnoitre known pos- sible fishable areas and to find new ones. In this way, the track of the F/V indicates the wide area explored (Fig. 1), in which hauls were made both in places where previous information indicated the presence of scallops and at random in other areas. From this trip, 21 hauls indicated absence and 178 hauls indicated presence of scallops. Position, estimated dimension and depth of the known (Tres Puntas and Sea Bay) and the new beds (MdQ. Reclutas. San Bias, SAO, SWSAO. Valdes and Tango B) are presented in Table 1. TABLE 1. Location of '/.ygochlamys patagonica beds in the Argentine Continental ShelL Central position ( S; \V), dimension (km), area (knr), and depth (m). Central Position Dimensions Lat. Long. Depth Bed "S W km km km- m MdQ 38° 30' 55° 48' — — — 105 Reclutas W 24' 55° .56' — — — 104 San Bias 39° 47' 56° 15' 1 5.92 12.03 191.5 89 SAO 40° 45' 57° 02' 23.89 14.81 353.8 108 SWSAO 41° 50' 58° 10' 14.07 11.11 1 56.3 106 Valdes 42° 14' 58° 33' 7.22 5.92 42.7 98 Tango B 42° 30' 59° 15' 16.29 9.26 IsO.S 96 Sea Bay 43° 33' 63° OS' 9.63 6.4S 60.6 75 Tres Puntas 46° 47' 65° 24' — — ^ 67 Zygochlamys p.atagonica New Fishery 105 Valdes Bed was intensively fished once discovered (Trip 1, 7S hauls). During the following four trips (2. 3, 4, and 5: 3.097 hauls) this bed was the target. During trips 6, 7, and 8 (194 hauls) it was only partially fished. As a result of this fishing activity, average CPUE for trips 6. 7, and 8 dropped 55% of the average value for Xrips 1-4 (Fig. 2). This drop in the CPUE between virgin condi- tion and the leaving of the area is near to the maximum average CPUE - 2 SD (Fig. 2, Trip 3). CPUE values indicated that the finding of areas where CPUE was = average CPUE - 2 SD de- tennined the cease of fishing activity, points that were conse- quenth adopted as geographic limits of the bed. The procedures was repeated in every different bed and although "average CPUEs" were different, the indicated fishing behavior resulted in corre- spondence with the mentioned observation in each new profitable area. Commercial Scallop CPVE: Vnsorted Catch, Scallop Yield, and Commercial Scallop Yield ANOVA tests (p < 0.05) indicate differences in unsorted catch (UC. F: 100.5. F,.: 1.94. total n: 3,389). scallop yield (SY%. F; 105.44, F^,: 1.95, total n: 723). and commercial scallop yield (CSV/f. F: 153.55. F^.: 1.94. total n; 863) between beds. Relative compositions, expressed as CS CPUE were also statistically dif- ferent (ANOVA. p < 0.05. F: 186.54, F^,: 1.95, total n; 747) be- tween beds. Reclutas Bed was characterized by lower average values of CS CPUE (291 kg ■ h', SD: 199, n: 38) (Fig. 3a). Average UC was 6,415 kg • h"' (SD: 4,220, n: 32) and average SY: 27.02% (SD: 12.32. n: 29, so SC: 1.323 kg • h"') and CSV: 22.17% (SD: 5.87, n: 8) (Fig. 3, b, c, and d). Maximum average values of CS CPUE were observed at SWSAO Bed (4.927 kg • h"', SD: 1.440. n: 208) (Fig. 3a). Aver- age UC was 8.906 kg ■ h"' (SD: 2,646, n: 658), average SY: 83.21% (SD: 7.94, n: 207, so SC: 6.942 kg-h"') and CSY: 71.36% (SD: 7.85. n: 263) (Fig. 3, b. c. and d). Sice Frequency Composition by Bed Size frequency compositions were found during the experimen- tal fishing program in 1995. showing the recruitment pattern in an undisturbed condition (Fig. 4). With the exception of Reclutas Bed (Fig. 4b). aduhs (higher than 45 mm. 2 y old) dominated in num- ber. Absence of recruits at Valdes and Sea Bay Beds (Fig. 4. f. h) and low frequency of recruits and juveniles was observed at the other beds. 8000 7000 6000 Ul 5000 4000 8 3000 2000 1000 iiiiim 1 8 2 3 4 5 6 7 Trip Figure 2. Valdes Bed. Average commercial scallops catch per unit effort (CS CPUE. scallop kg • h ') by trip during 1995 (.January to June). Bars indicate 1 SD. Muscle Yield Differences in muscle yield (MY, %) were observed between beds (Fig. 5) during January 1995. Beds located along the 100 m isobath (MdQ. Reclutas and Valdes. Fig. 1) had higher MY than the previously known beds Sea Bay and Tres Puntas (67 and 75 m depth, respectively. Fig. 1 ). ANOVA analysis between beds indi- cates statistical differences (p < 0.01; F: 64.02, F,: 3.57, total n: 154). Tukey analysis indicates statistical differences between Sea Bay - Tres Puntas beds with MdQ - Reclutas - Valdes beds (p < 0.05). Yearly variations in the muscle weight (MW, g) and MY for specimens 60 mm SH (Fig. 6, a and b) were estimated from samples taken at Valdes and SWSAO beds. The trends for both variables suggest an increase in median values during summer to early autumn and a decrease during winter to early spring. Calch Per Unit Effort and Potential Muscle Landing Per Unit Effort Commercial scallop (CS) CPUE (Fig. 3a| varied between beds with UC, SY and CSY (Fig. 3, b. c, and d). Combining this in- formation with values of MY for different beds (Table 2), it is evident that there is a rank of potential muscle production or land- ing per unit effort (LPUE) by bed (Fig. 7). A maximum value of muscle LPUE was obtained at SWSAO. Higher values of UC and CSY were also observed there. A mini- mum of muscle LPUE was observed at Reclutas Bed, as expected for an area largely occupied by juveniles. Values of muscle LPUE could be used to rank the beds as follows: SWSAO > SAO > Tango B > San Bias > Valdes > Sea Bay > Tres Puntas > MdQ > Reclutas. DISCUSSION The patagonian scallop Z. patagonica forms discrete beds in the Argentine Sea. where commercial fishery could be conducted. Seven new beds have been found along the 100 m depth isobath between 38° 40' S and 42° 36' S. Those new beds demonstrated better commercial potential, because of the higher muscle yield. than those known from 60-70 m depth in southern areas (Sea Bay and Tres Puntas) (Figs. 1 and 5). Muscle production fluctuated between 160 and 240 pieces • kg"', which represents a relative low present market value. How- ever, increasing international scallops demand inferred from world landings (1985: 604.165 t: 1994: 1,634,32 t; FAO, 1996) and re- strictions in scallop fishing grounds (Naidu 1991. Bourne 1991) may lead to increased value of this species. Size composition show that recruitment conditions vary be- tween beds. Valdes and Sea Bay bed were composed largely of adults and characterized by unimodal size distributions (Fig. 4. f and h). On the basis of data in Waloszek and Waloszek (1986) and Waloszek ( 1991 ) size-at-age estimates, this suggests a recruitment failure during the past 4-5 y. The size frequency distribution dur- ing Sea Bay trip in July to August 1989 (Fig. 8) (Lasta 1992) shows a similar pattern. On the other hand, size composition in Reclutas Bed was consistent with intense recruitment during 1994, probably from the (early) spring spawning (average SH: 13.82 mm, SD: 3.61, n: 223) (Fig. 4b). Later, during October 1995 an- other cohort (average SH: 8.35 mm, SD: 1.78. n: 133) was ob- served in the same area, probably from the summer to autumn 1995 spawning (Fig. 4j). It occupied the same location as the previously mentioned cohort (average SH: 31.71 mm, SD: 4.23, n: 3.472). The observed size frequency distributions for all beds dur- 106 Lasta and Bremec 12000 11000 10000 9000 u eooo a. 7000 '^ 8000 sooo 4000 3000 2000 1000 8 ZC Min-M«» C3 26»-76» • MadlanvaltM I 3 100 SO 80 70 60 50 40 30 20 10 ni Mln-Max I I 25%-75% • Median vatue I ^ n I a I Bed CCPOE ZC Mln-Ma!i CD 26*.75% • VUdannJiM - - 1 n r p -, 1 " J ^ 10000 7500 5000 4 4 i t a E 1 [ ^ ? y 2S0O a: i ^ 1 1 ^ i _L "^ ' 1 I (0 I I BmI Figure 3. a. Commercial scallop (CS) CPUE (kg yield (CSyTr I in different beds during 1995. 100 90 80 70 60 50 40 30 20 10 Zn Min-Max IZZl 251t-75% * Median value Bed a h ' ). b, Unsorted catch (UC) CPUE (kg ■ h"'). c. Scallop yield (SY%). d. Commercial scallop ing 1995 suggest pulse recruitment. Assuming that there are two spawning periods (Waloszek and Waloszek 1986) it is unknown if the timing pattern is the same for the beds in different geographical locations and if all organisms spawn twice a year. The degree of synchronization of spawning varies among species and within populations of the same species both between locations and years. Known external environmental factors that synchronize the repro- ductive cycle of scallops include food and temperature (Barber and Blake 1991), and are also considered the main parameters that control growth in temperate regions (Griffiths and Griffiths 1987). Although the patagonian scallop is largely distributed in the Argentine Continental Shelf (Fig. I), the program confirmed the presence of dense discrete beds with significant differences in SY and CSV (Fig. 3, c and d). Noticeable differences among beds were found in 1995 in relation to MY estimated in laboratory (Table 2). Values ranged between 12.69Vr and 23.09% in Sea Bay and MdQ beds respectively, suggesting environmental differences between areas. A value of 12.03% MY (SD: 1 .42, n: 80) was found in Sea Bay Bed during 1989 (Lasta 1992), suggesting the persis- tence of environmental conditions when comparing MY values. However, similar size frequency distributions (Figs. 4h and S) in this bed in 1989 and 1995 were observed, indicating recruitment failures, commonly associated with variable environment. The observed pattern of muscle yield and spawning periodicity may be related to hydrographic processes that influence primary productivity. Two main hydrographic regimes can be observed in the Western South Atlantic. The spatial distribution and biological characteristics of scallops are probably related to them. One of those hydrographic regimes is the Malvinas Current, the other is the shelf regime (Fig. 9). The continental shelf is dominated by waters of subantarctic origin, mainly by the contribution of the upper layer of Malvinas Current, that flow through the west of Burdwood Bank (Thomsen 1962, Lusquinos and Valdes 1971. Piola and Gordon 1989, Guerrero et al. 1996). The continental shelf waters are also influenced by continental runoff that enters the shelf through the Magellan Strait (Krepper 1977, Bianchi et al. 1982) and the Tierra del Fuego Channels (Lusquinos and Valdes 1971). The Malvinas Current Hows towards the north along the continental slope, transporting subantarctic waters characterized by high salinity and low temperature (Piola and Gordon 1989). Between 35° and 40° S the Malvinas Current converges with the Brazil Cuirent flowing poleward, generating a strong frontal zone between Subantarctic and Subtropical waters (Reid et al. 1977, Legeckis and Gordon 1982, Gordon and Green Grove 1986). The differential heating between shelf and slope regiines during the warm seasons develops a shelflyreak front observed as a horizontal icmperature gradient over the 90-100 m isobath (Martos and Pic- colo 1988. Baldoni 1993). This front may be the factor that influ- ences the area of distribution of beds located at these depths (MdQ Bed in the north to Tango B Bed in the south. Figs. I and 9). The high productivity of the sheljlireak front is well documented on the basis of remote sensing (Podesta and Esai'as 1988) and in situ Zyguchluiys fatagonica Nkw Fishery 107 b : Reclutas 1-18-95 n : 233 10 20 30 40 50 60 70 80 90 Shell Height (mm) Figure 4. Size (shell height, mml frequency i'7c) distribution for beds during 1995. a. b, c, sampled. 10 20 30 40 50 60 70 80 90 Shell Height (mm) j: name of bed: date: n: number of individuals measurements (Brandhorst and Castello 1971. Carreto et al. 1981. Carreto et al. 1995). A seasonal study of primary productivity at 39°S (Negri 1993) indicated values ranging between 0.1 and 2.7 gC m"- day"', and a yearly regional production of about 350 gC m"". Satellite images collected from the Coastal Zone Color Scan- ning in summer and autumn, show an almost permanent lighter band along the edge of the shelf from 39°S to 47"S, contrasting markedly with the imagery corresponding to shelf waters and the adjacent offshore region (Podesta and Esaias 1988. Bertolotti et al. 1996). The two other beds (Sea Bay and Tres Puntas. Fig. I) are associated to a different hydrographic regime (Patagonian Current. Brandhorst and Castello 1971). Tres Puntas Bed and Sea Bay Bed are influenced by a low salinity coastal system. This water is of continental origin, mainly via Magellan Strait and Tierra del Fuego Channels runoff (Brandhorst and Castello 1971. Lusquifios and 108 Lasta and Bremec 30 26 22 >- 18 s 14 i Min-Max i I 26%-75% • Median value Bed Figure 5. Muscle yield in different beds durin;) IW5, in standard specimens (60 mm SH. n: 20). MV: muscle yield {9c. muscle weight TVVWE' I. Valdes 1971, Krepper and Rivas 1979. Guerrero and Piola, 1997). This system is coastal up to 47°S and separates from the coast to occupy the intermediate part of the shelf up to 38 'S (Brandhorst 3 ~r Mln-Max I I 255^75% * Median value 2 - Time ts o TABLE 2. Muscle yield (MY %) during 1995 for different beds. Average value, SD and number (n) of 60 mm SH specimens. Muscle Yield ( % ) Bed Average SD n Date MdQ 23.09 2.02 36 Jan. 18 Recliitas 22.49 2.15 28 Dec. 13 San Bkis 22.38 1.62 40 Set. 20 SAO 20.09 2.02 38 Jul. 29 SWSAO 19.58 2.16 38 Oct. 12 Valdes 21.03 2.09 34 Jan. 14 Tango B 22.67 1.76 32 Jun, 20 Sea Bay 12.69 2.39 28 Jan. 9 Tres Piinlas 18.13 2.00 28 Jan. 12 and Caslello 1471 ). The extent of this low salinity distribution is shown at the surface and bottom by Brunetti et al. (1996a. b). where the horizontal gradient occurs between 47""S (Tres Puntas Bed) and 44''S (Sea Bay Bed). Tres Puntas Bed is associated with the coastal regime, characterized by mi.xed water from tidal effect. Nutrients concentration is high throughout the year and high chlo- rophyll concentration is reported (Bertolotti et al. 1996). Sea Bay Bed is associated with the intermediate shelf regime, characterized by lower productivity (Carreto and Benavides 1990. Carreto et al. 1995) because of the strong seasonal variation in vertical structure of the water column, with an homogeneous layer in winter and two layered structure during warm months with a strong thermocline over the region (Bianchi et al. 1982, Krepper 1977). The high CS CPUE or LPUE (Figs. 3a and 7) in some beds suggest that the fishing activity can be economically viable even with the small size of muscle taken. Estimates of mean biomass density ranged between 0.23 and 0.22 kg of scallops ■ m"" (Leslie and DeLury methods respectively) in a dense patch in Valdes Bed (Lasta and Iribarne 1997), which was in an undisturbed condition. This biomass density corresponds to 14-6 scallops 55-70 mm SH (Total weight: 8 • 10^' ■ SH'"^"", r: 0.95, n: 100. M. L. Lasta un- publ.). As it was observed in Valdes Bed during a series of trips, the average CPUE dropped 55<7<: of the initial average value (Fig. 2), suggesting the nonprofitability of the fishing activity at this lower density of 6.3 to 2.7 scallops ■ m~". 32 30 28 26 £ 24 122 20 18 16 14 ~r Mln^Ulax I I 25%-75% • Median value a to m 11. s < < Time Figure 6U mm 6. a: Muscle weight (MW. g) and b: muscle yield (MY, %) for SH specimens at Valdes and SWSAO beds, 1995. 1100 1000 900 800 700 S 800 Q. 500 400 300 200 100 iJjJjllL o S5 o < Bed Figure 7. landing per unit effort (l.PliE, average muscle kg • h~') by bed during 1995, bars indicate SD. Zycochiamys patagonica Nf.w Fishery 109 16 14 12 m 10 I: O 6 a. 4 ■ 2 x = 58 92 mm 10 20 30 40 50 60 70 SO 90 Shall height (mm) Figure 8. Size (SH: shell helghl, iiinil (reqiienc> ( 9^ ) distribution of scallop catch during July to August ItH'). FA' "Sea Bay Alpha", Sea Bay Bed. Specimens »54 mm SH = 9'~i and sSS mm SH = <){%. On the basis ot nuiscle kiiidiiig per unit effort (LPUE) (Fig. 7). conditions of fishing and processing similar to those carried out by F/V "Erin Bruce", beds could be ranked from more profitable (SWSAO) to less profitable (Reclutas). The 1.315 metric tons (t) of muscle obtained during 1995 (mainly from the 100 m isobath beds) represent an average 12. 18% (SD: 2.23. n: 15) of the total CS catch. This value is lower than 19%-23% MY (Table 2). obtained -35° -40P -45° -70° -65° -60° -55° -50° -45° Figure 9. General water masses circulation in the SVV Atlantic Ocean (from Piola and Rivas 1997). in ihc kibiiiatiir\ . The dillcrcnce between the expected ( 19%-23%) and Ihc iihlamcd 12.18% is attributed to losses in the factory process. On an average fishing day. the FA' made 36 trawls (92% with paired trawls). With this intensity of fishing activity it was possible to obtain 7.54 t of muscle in the SWSAO bed. the more profitable area. However, less than 0.44 t could be obtained in Reclutas bed. Values of 12.81 t and 0.8 t. respectively, could be reached daily without factory losses. Differences in MY(%) between beds (Fig. 5) explain why Sea Bay and Tres Puntas beds did not demonstrate commercial interest. Regarding seasonality in MY(%). higher losses in muscle produc- tion were observed from June to November (M. L. Lasta, pers. obs.). because of the soft consistence of the muscles. According to the recruitment history, proportion of total and commercial scallops were significantly different in every bed. As those are dynamic in time and affected by the fishing activity as it was observed by the drop of CPUE in Valdes Bed (Fig. 2). the dimension of each fishable area would be dynamic (increase or decrease) in relation to biological-bioniass and/or economical- market variables. During the experimental program in 1995 the F/V left a bed when the CPUE dropped 55% of the initial values. In Valdes Bed (Fig. 2), the higher CPUE (Trip 3) is close to CPUE - 2 SD. This value was related to a threshold of profitability, inferred by the behavior of the FA' that left the fishing area when reaching this value. It made possible the mapping of the fishable areas, which could eventually change (increase by growth of re- maining populations or new recruitments and decrease by fishing activity). This speculation about the behavior of the FA', reflects the high vulnerability of sessile resources due to fishing effort in compact beds once detected and enhances the idea of a rotation areas strategy. According with average values of trawling speed, time, and mouth opening of the net (Lasta and Iribame 1997). Valdes Bed was swept 115% assuming a regular distribution of tows. With this fishing effort the observed drop was 55% of the initial value, suggesting a fishing effort of 100% as an experimen- tal limit management recommendation in a rotation area strategy. Management recommendations to develop the fishery during 1996 were made according to the present knowledge about the spatial pattern and size of beds. It is considered that proper advice would be dynamic in relation to the development of fishing ac- tivities and future research. In this sense, spatial patterns of fishing effort would be considered as the main key management in a rotation strategy between beds, on the basis of a predetermined degree of disturbance than to the biomass of the target species (Lasta et al. 1988. Orensanz et al. 1991b). A classic management and development program for the fish- ery could be based on studies about population dynamics in dif- ferent beds. Proper management not only depends on biomass evaluations, studies on age and growth, factors affecting recruit- ment and larval dispersal, natural mortality, etc. A more appropri- ate strategy to manage sessile resources will consider not only fishing effort (as disturbance effect) on a rotation area criteria but also the establishment of "no-take' reserves areas (Roberts 1997) within each bed as a way to maintain reproductive aggregations (Stokesbury and Himmelman 1993). Long-term research about community structure and bycalch in relation to trawling also conform aspects of relevant interest (Hutchings 1990. Alverson et al. 1994. Parsons 1996, Brand et al. 1997). Both natural and anthropogenic factors affecting scallop populations must be taken into account to develop an effective plan to manage the resource. no Lasta and Bremec ACKNOWLEDGMENTS We greatly appreciate the statistical assistance of D. Hernandez (INIDEP) and the useful suggestions of Dr. O. Iribarne (UNMDP) and Dr. H. Mianzan (CONICET-INIDEP). We also appreciate the suggestions of two anonymous reviewers. Alverson. D. L.. M. H. Freeberg. J. G. Pope & S. A. Murawski. 1994. A global assessment of fisheries bycatch and discards. FAO Fish. Tech. Paper. Roma. 3.^9, 233 pp. Baldoni, A. 1993. Frente del Talud. In: Semniarui Taller sobre la dinamica marina y su impacto en la productividad de las regiones frontales del Mar Argentine. INIDEP Tech. Rep. N" I.. Mar del Plata. Argentina. 8-10, Barber, B. J. & N. J. Blake. 1991. Reproductive Physiology, pp. 377-f28. In: S. E. Shumway (ed.). Scallops: Biology, Ecology and Aquaculture. Elsevier. Amsterdam. Holland. Bertolotti, M. I., N. E. Brunetti, J. 1. Carreto, L. B. Prenski & R. P. Sanchez. 1996. Influence of shelf-break fronts on shellfish and fish stocks off Argentina. ICES CM. I996/S:4\. 15 pp„ 9 figs. Bianchi. A., M. Massoneau & R. M. Olivera. 1982. Analisis estadi'stico de las caracteri'sticas T-S del sector austral de la plataforma continental argentina. Ada Oceanographica Argentina 3( I ):93-l 18. Bourne, N. 1991. West Coast of North America, pp. 925-942. In: S. E. Shumway (ed.). Scallops: Biology, Ecology and Aquaculture. Elsevier, Amsterdam, Holland. Brand, A. R. & K. L. Prudden. 1995. The Irish sea scallop database as a tool for fishery management. X International Pectinid Workshop. Cork. Ireland. April 27-May 2, 1995:7-8. Brand, A. R., A. S. Hill. L. O. Veale & S. .1. Hawkins. 1997. The environ- mental impact of scallop dredging. XI International Pectinid Work- shop, La Paz, Mexico, April 10-15, 1997:4(M1. Brandhorst, W. & J. P. Castello. 1975. Evaluaciiin de los recursos de anchoita (Engraulis anchoita) frente a la Argentina y Uruguay. I. Las condiciones oceanograficas, sinopsis del conocimiento actual sobre la anchoi'ta y el plan para su evaluacidn. Proy. Des. Pesq. FAO. Publica- cion 29, 63 pp. Bremec, C. S.. M. L. Lasta, L. Lucifora & J. Valero. In press. Analisis de la captura incidental asociada a la pesqueria de vieira patagonica (Zv- gochlamys pautgonica. King & Broderip. 1832). INIDEP Tech. Rep. Mar del Plata, Argentina, 22, 16 pp. Brunetti, N. E., G. Rossi, M. Ivanovic, B. Elena. R. Guerrero, H. Bena- vides. G. Blanco & C. Marchetti. 1996a. JAMARC-INIDEP Joint Re- search Cruise on Argentine Shortfin Squid (lUex argentimis). Argentine Final Report. INIDEP Tech. Rep. Mar del Plata, Argentina, 91. 32 pp. 19 tables. Brunetti, N. E.. G. Rossi, M. Ivanovic. B. Elena, R. Guerrero. H. Bena- vides. G. Blanco. C. Marchetti. N. Suekane, M. Kuroiwa & T. Murai. 1996b, Final Report of the JAMARC-INIDEP Joint Research Cruise on Argentine Short-finned Squid Ulle.\ argentinns) during January and February 1996. Jamarc Report 16, 42 pp. Carreto. J. I. & H. R. Benavides. 1990. Synopsis on the reproductive bi- ology and early life history of Engraulis anchoita. and related envi- ronmental conditions in Argentine waters. Phytoplankton. IOC Work- shop. Rep. N" 65. Annex V:2-5. Carreto. J. I,. R, M. Negri & H. R. Benavides. 1981. Fitophuicton, pigmen- tos y nutnentes. Resultados de las campaiias 111 y VI del B/I "Shinkai Maru", 1978. Campaiias de Investigacicin Pesqucra realizadas en el Mar Argentino por los B/I ■■Shinkai Maru" y "Walther Herwig" y el B/P "Marburg", afios 1978 y 1979. Resultados de la parte argentina, Inst. Nac. Inv. Des. Pesq., Contribuci6n 3X3:181-201, Carreto, J. I.. V. Lutz, M. O. Carignan, A. D. Cucchi Colleoni & S, G, De Marco. 1995. Hydrography and chlorophyll a in a transect from the coast to the shelf-break in the Argentinian Sea. Cont. Shelf Res. 15(2/ 3):3 15-336. Defeo, O. & A. Brazeiro. 1994. Distribucion. eslructuia poblacional y LITERATURE CITED relaciones biometricas de la vieira Zygochlamys patagonica en aguas Uruguayas. Com. Sac. Malac. Unig. VII(66-67):362-367. FAO. 1996. FAO Yearbook 1994. Vol 78. Fishery Statistics. Catches and Landings. Rome, Italy, 699 pp. Gordon, A, L. & C, L, Green Grove. 1986. Geostrophic circulation of the Brazil-Falkland Confluence. Deep-sea Res. 33:573-585, Griffiths, C. L. & R. J. Griffiths. 1987. Bivalvia. pp. 1-88. In: I. H. Pan- dian and F. J. Vernberg (eds). Animals Energetics. 2, Academy Press. New York. Guerrero. R. & A. R. Piola. 1997. Masas de agua en la Plataforma Conti- nental. In: E. Boschi (ed.): El Mar Argentino y sus Recursos Pesqueros. 1:107-118. Guerrero, R., A. Baldoni & H. Benavides. 1996. Oceanographic conditions at the southern end of the Argentine Continental Slope. In: Reproduc- tive habitat, biology and acoustic biomass estimates of the Southern blue whiting {Micromesistius anstralis) in the Sea off Southern Pat- agonia, 9 pp, 13 figs. (MS). Hatchings, P. 1990. Review of the effects of trawling on macrobenthic epifaunal communities. Austr. J. Mar. Freshwater Res. 41:111-120. Kinc. P. P. & W.J. Broderip. 1832. Description of the Cirripeda, Con- chifera and MoUusca, in a collection formed by the officers of H.M.S. Adventure and Beagle employed between the years 1826 and 1830 in surveying the southern coasts of South America, including the straits of Magellhaens and the Coast of Tierra del Fuego. Zoo/. /. 5:332-349. Krepper. C. M. 1977. Difusion del agua proveniente del Estrecho de Ma- gallanes en las aguas de la platatorma continental. Acta Oceano- graphica Argentina l(2):49-65. Krepper, C. M. & A. L. Rivas. 1979. Analisis de las caracteristicas oceano- graficas de la zona austral de la plataforma continental argentina y aguas adyacentes. Acta Oceanographica Argentina 2(2):55-82. Lasta. M. L. 1992. Chlamys patagonica: Resultados del Primer Crucero de Pesca Expenmental. IX Simp. Cient. Com. Tec. Mix. Frente Mari'timo Argentino-Uruguayo. Mar del Plata. Argentina. November 3(1- December 2. 1992: p. 13. Lasta. ML. & E. Zampatti, 1981. Distribution of commercial bivalve mollusks catches in the sea off Argentina. Results of the cruises of the R/V -Walther Herwig' and 'Shinkai Maru', 1978-1979. pp. 128-135. In: V. Angelescu (ed.). Campafias de Investigacion Pesquera realizadas en el Mar Argentino por los B/1 'Shinkai Maru' y 'Walther Herwig' y el B/P 'Marburg', anos 1978 y 1979. Resultados de la parte Argentina. INIDEP. Mar del Plata. Argentina. Lasta, M. L. & C. S. Bremec. 1995. Investigacion sobre vieira patagonica (Zvgi'clilann'S patagonica. King & Broderip. 1832). INIDEP Tech. Kcp N" 1026, Mar del Plata, Argentina, I 14 pp, Lasta, M. L. & CO. Iribarne. 1997. Southeastern Atlantic scallop {Zy- gochlamys patagonica) fishery: assessment of gear efficiency through a depletion experiment. J. Shellfi.yh Res. 16(l):59-62. Lasta. M. L., O. O. Iribarne, M. S. Pascual. E. A. Zampalti & H, Vacas, 1988. La pesqueria del Golfo San Mati'as: una aproximacion ul manejo experimental. UNESCO Cieiic. Mar. 47:168-175. Legeckis R. & A. L. Gordon. 1982. SateUite observation of the Brazil and Falkland Currents. 1975 to 1976 and 1978. Deep-sea Res. 29:375-402. Lusquihos A, & A. J. Valdes, 1971. Aportes al conocimiento de las masas de agua del Atlantico Sudoccidenlal. .Sen: Hidrogr. Naval. (Buenos Aires), H 659, 48 pp. Murtos. P, & M. C. Piccolo. 1988(a). Hydrography of the Argentine con- tinental shelf between 38° and 42° S. Cont. shelf Res. 8:1043-1056. Naidu. K. S. 1991. Sea scallop, Placopecten magellanicus. pp. 861-898. Zygochiamys rATAdONicA New Fishery 111 In: S. E. .Sliuiii«a\ (ed. ). Scallops: Builogy. Ecology and Aijiiaciiltuic. Elsevier. Amsterdam. Holland. Negri. R. M. 1993. Fitoplancton y produccidn primaria en el area de la platat'ornia bonaerense proxima al talud continental. In: Semniario Taller sobre la dinamica marina y su mipacto en la productividad de las regiones frontales del Mar .Argentmo. Tech. Rep. N" I. INIDEP. Mar del Plata. Argenlma. 7. Orensan/. J. M., M. S. Pascual & M. Fernandez. 1991a. Scallop resources from the Southwestern Atlantic (Argentina), pp. 981-1000. In: S. E. Shumway (ed.). Scallops: Biology. Ecology and Aquaculture. Elsevier. Amsterdam. Holland. Orensanz. J. M., A. M. Parma & O. O. Iribarne. 1991b. Population dynam- ics and management of natural stocks, pp. 625-713. In: S. E. Shumway (ed.). Scallops: Biology. Ecology and Aquaculture. Elsevier. Amster- dam. Holland. Parsons. T. R. 1996. Taking stock of fisheries management. Fish. Ocean- ogr. 5(3/4):224-226. Piola. A. R. & A. L. Gordon. 1989. Intermediate waters m the southwest South Atlantic. Deep-sea Res. 36:1-16. Piola. A. R. & A. Rivas. 1997. Corrientes en la Plataforma Continental. In: E. Boschi (ed.): El Mar Argentino y sus Recursos Pesqueros.. 1:1 19- 132. Podcsti. G. P. & W. E. Esaias. 1988. Satellite-derived phytoplankton pig- ment concentration along the shelf-break off Argentina, 1979-1980. £05 69:1144. Raj. U. 1980. Teoria del Muestreo. Fundacion dc Cultura Economica. Mexico (ed.), 305 pp. Reid, J. L., W. D. Nowlin & W. C. Patzert. 1977. On the characteristics and circulation of the southwestern Atlantic Ocean. J. Phys. Oceanogr. 7:62-91. Roberts, CM. 1997. Ecological advice for the global fisheries crisis. TREE 12(l):-35-38. Stokesbury, K. & J. H. Himmelman. 1993. Spatial distribution of the giant scallop Placopecten magellanicus in unharvested beds in the Bale des Chaleurs. Quebec. Mar. Ecol. Prog. Ser. 96:159-168. Thomsen. H. 1962. Masas de agua caracten'sticas del Oceano Atlantico. Sen: Hidrogr. Naval. (Buenos Aires), H 632, 31 pp. Waloszek. D. 1991. Chlamys patagonica (King & Broderip, 1832), a long 'neglected" species from the shelf off the Patagonian Coast, pp. 256- 263. In: S. E. Shumway and P. A. Sandifer (eds.). An International Compendium of Scallop Biology and Culture. Selected papers from the VII International Pectmid Workshop. National Shelt~isheries Associa- tion. The World Aquaculture Society. Parker Coliseum. Louisiana State Univ.. Baton Rouge. USA. Waloszek. D. & G. Waloszek. 1986. Ergebnmisse der Forschungsreisen des FFS 'Walther Herwig" nach Sudamerika. LXV. Vorkommen, Re- produktion. Wachstum und mogliche Nutzbarkeit von Chlamys patag- onica (King and Brodenp. 1832) (Bivalvia. Pectinidae) auf dem Schelf von Argentinien. Arch. Fish Wiss. 37:69-99. JiHirmil ol Shellfish Research. Vol 17, Nii. 1. 113-116. 1>WS. MOBILIZATION OF ENERGY FROM ADDUCTOR MUSCLE FOR GAMETOGENESIS OF THE SCALLOP, ARGOPECTEN PURPURATUS LAMARCK GLORIA MARTINEZ AND LIVIA METTIFOGO Faciiltcul de Ciencias del Mar Universidad Catolica del Norte Casilla 117 Coqiiiinho. Chile ABSTRACT Ganietogenesis is a high energy-demanding process, and in pectinids. adductor muscle has been suggested to be a storage tissue of energy substrate for this process. Carbohydrates have been suggested as the primary substrate mobilized. Analysis of the content of glycogen in adductor muscle of Argopecten purpurauis at different stages of gametogenesis showed an inverse relationship between the content of glycogen in muscular tissue and gonad index. The contents of dopamine, noradrenaline, and serotonin were measured in the muscle of scallops allowed to proceed with gametogenesis after spawning. These monoamines increased as the gonad attained its complete ripeness. Measurement of cyclic AMP (cAMP) content in the muscle showed a temporal course similar to that of the monoamines. Increases of cAMP levels when muscular tissue was incubated with dopamine were obtained onlv w hen gametes were nearly ripe. These results suggest an important role of muscle as a supplier of fuels for gametogenesis, mainly when the process is attaining its completion. It is hypothesized that a point of control of gametogenesis may be through the control of mobilization of substrates that supply energy for this process. This control could be through monoamines, which would increase the levels of cAMP. which in turn would induce the phosphorylation of glycolytic enzymes, increasing the catabolism of substrates. KEY WORDS: scallops, gametogenesis. Argopecten purpiiranis. reproduction, adductor muscle INTRODUCTION External factors that control the reproductive activity of scal- lops have been extensively investigated, but less research has been devoted to endogenous factors, Gametogenesis is an energy- demanding process (Sastry 1979) that depends on the catabolism of substrates for its occurrence. Adductor muscle weight decreases occur during gametogenesis in several species of scallops, such as Chlamys septemradiata (Ansell 1974). C, operculahs (Taylor and Venn 1979), Placopecten magellanicus (Robinson et al, 1981), Argopecten irradians concentricus (Barber and Blake, 1981 ), and Argopecten irradians irradians (Epp et al. 1988), suggesting that the adductor muscle is a storage tissue for energetic substrates for this process. More support for this hypothesis comes from studies of Tabarini (1984), who showed higher weight of adductor muscle of triploid Argopecten irradians than that of diploid controls. Not- withstanding, Paon and Kenchington (1995) have shown that in contrast to wild populations, adductor muscle weight did not de- cline when P. magellanicus broodstock were submitted to artificial conditioning, indicating that if enough exogenous food is pro- vided, endogenous stores are not depleted. In connection with the site of substrate storage for gametoge- nesis. biochemical analysis of adductor muscle of some scallops has shown decreases of glycogen accompanying gonadal matura- tion (Taylor and Venn 1979, Barber and Blake 1981, Robinson et al. 1981) suggesting this substrate to be the principal metabolic fuel used. A negative correlation between gonad index and carbo- hydrate content has been shown in tissues of Argopecten ptirpii- ratiis (Martinez 1991), supporting the metabolic use of this sub- strate during gametogenesis. Gametogenesis may be controlled endogenously through regu- lation of the catabolism of these substrates. It is known that some biogenic amines increase the catabolism of some substrates (gly- cogen and triacylglycerides) through cyclic AMP (cAMP)- dependent phosphorylation of glycolytic or lipolytic enzymes (Stryer 1988). Seasonal dynamics of some monoamines has been described for some pectinids and correlated with reproductive ac- tivity (Osada and Nomura 1989, Khotimchenko and Deridovich 1991, Paulet et al. 199.3), and Martinez and Rivera (1994) have related the gonadal levels of these monoamines with the reproduc- tive activity of /I. purpuratus. To obtain more knowledge about the possible role of adductor muscle tissue involved