FISHERIES OCEANOGRAPHY Fish. Oceanogr. 22:3, 220–233, 2013 Underestimation of primary productivity on continental shelves: evidence from maximum size of extant surfclam (Spisula solidissima) populations D.M. MUNROE,1,* E.N. POWELL,1 R. MANN,2 change on benthic secondary production and fishery J.M. KLINCK3 AND E.E. HOFMANN3 yield on the continental shelf. 1 Haskin Shellfish Research Laboratory, Rutgers University, 6959 Key words: benthic production, chlorophyll, clam Miller Ave, Port Norris, NJ, 08349, U.S.A feeding, filter feeder, individual-based model, spisula 2Virginia Institute of Marine Sciences, The College of William and Mary, Rt. 1208 Greate Road, Gloucester Point, VA, 23062-1346, U.S.A 3Department of Ocean, Earth and Atmospheric Sciences, Center INTRODUCTION for Coastal Physical Oceanography, Old Dominion University, 4111 Monarch Way, 3rd Floor, Norfolk, VA, 23529, U.S.A Atlantic surfclams (Spisula solidissima) are among the largest extant non-symbiotic clam species in the world and the largest mactrid bivalves living on continental ABSTRACT shelves. They are long-lived (maximum age >30 yr) and form dense aggregations along the extensive con- Atlantic surfclams (Spisula solidissima), among the larg- tinental shelf in the northwestern Atlantic Ocean in est extant non-symbiotic clam species in the world, sandy bottoms from southern Virginia to Georges live in dense aggregations along the Middle Atlantic Bank (Jacobson and Weinberg, 2006; NEFSC North- Bight (MAB) continental shelf. The food resources east Fisheries Science Center, 2010). With a biomass that support these populations are poorly understood. in this region greater than 850 9 103 metric tons, this An individual-based model that simulates the growth species is the basis of a major commercial fishery in the of post-settlement surfclams was used to investigate western North Atlantic Ocean (NEFSC Northeast the quantity of food needed to maintain existing surf- Fisheries Science Center, 2010). Maintenance of bio- clam populations along the MAB continental shelf. mass on this scale requires substantial food resources. Food inputs to the model were based on measured Distinct and rapid changes in climate are leading to near-bottom water-column chlorophyll concentra- shifts in primary production that have community- tions. Simulations showed that these water-column level effects (Keller et al., 2001; Prasad et al., 2010), food sources supported only 65% of the observed body making an understanding of food resources on the con- mass of a standard large surfclam (160-mm shell tinental shelf critical to management of fishery length). Additional simulations using benthic food resources and stability of large-scale ecosystems. sources to supplement water-column food sources by Since 1997, populations from southern inshore 20% generated surfclams that grew to observed size regions of the surfclam range have experienced signifi- and biomass and exhibited spawn timing consistent cant mortality events coincident with warm bottom with the known surfclam spawning season. The simu- water temperatures, reaching 21–24°C in September lation results suggest that measured water-column (Kim and Powell, 2004; Weinberg, 2005). Hence, surf- chlorophyll concentrations may underestimate the clams are potentially indicative of the influence of glo- food available to the continental shelf benthos. Large bal warming on secondary production and benthic continental shelf bivalves are an essential resource for community dynamics in this region. The resulting con- fisheries and higher trophic level consumers. Under- traction in population distribution has major implica- standing available and utilized food resources is impor- tions for the clam fishery. An effort is currently tant for predicting long-term impacts of climate underway that uses biological models in a cohesive framework with oceanographic and socio-economic *Correspondence. e-mail: [email protected] models to understand causes of declines in surfclam Received 2 March 2012 populations over the southern part of their range and Revised version accepted 14 November 2012 to make predictive management decisions regarding 220 doi:10.1111/fog.12016 © 2013 Blackwell Publishing Ltd. Gaps in understanding food resources of surfclams 221 biological and sociological goals of the fishery as both Figure 1. Individual surfclam model schematic. Schematic the clam and the fishery respond to climate change of processes included in the individual surfclam model, (McCay et al., 2011). A critical component to manag- adapted from Hofmann et al. (2006). Net production ing these biological responses is understanding food depends on temperature, clam weight and clam condition. resources and growth of individual clams in this region. Positive net production produces reproductive and somatic tissue, whereas negative net production causes resorption of A mathematical model is a useful tool for investi- reproductive tissue. gating the quantity of food needed to maintain existing surfclam populations along the Mid-Atlantic Bight (MAB) continental shelf. In this study, an individual-based model that simulates the growth of post-settlement surfclams was used to perform a series of simulations to compare growth of clams under vari- ous filtration, assimilation, and respiration rates, using three probable food sources. These simulations demon- strate that either the clam biological and energetic relationships used in the model are misunderstood, or the species is sustained by more abundant food than is documented by measurements of water-column plank- tonic food resources. Supplementation of pelagic food with benthic sources has been documented previously for many shallow water and intertidal filter-feeding macrobenthic bivalves (Coe, 1948; Sasaki, 1989; Emerson, 1990; De Jonge and Van Beuselom, 1992; Kamermans, 1994; Page and Lastra, 2003 Kang et al., oceanographic model, the Regional Ocean Modeling 2006; Yokoyama et al., 2009) and epibenthic bivalves System (ROMS; Shchepetkin and McWilliams, 2005; (Rhoads, 1973; Kiørboe et al., 1981; Winter, 1978; Haidvogel et al., 2008). Direct measurements of respi- Pernet et al., 2012). Fewer studies have shown evi- ration and filtration rates are not available for surfcl- dence for the inclusion of benthic food sources in diets ams. Consequently, we used a range of general of suspension-feeding benthos from deeper continental relationships covering the physiological capabilities of shelf habitats (Fry, 1988; Hobson et al., 1995). In the most bivalves: 10°C and 20°C respiration curves of following, we describe the simulation results and Powell and Stanton (1985) with a Q10 temperature discuss food sources that could potentially sustain response of 2 (Rueda and Smaal, 2004), and the high-gear surfclams, a high-biomass suspension-feeder, on the and low-gear filtration rate curves (we use high-gear scale of biomass that is currently observed on the and low-gear in reference to the pace of functioning of continental shelf of the Mid-Atlantic Bight. the two filtration rate curves described by Powell et al, 1992; the high-gear curve predicts filtration rates approximately three times that of the low-gear curve METHODS for a given shell length), with a modal temperature A series of simulations was performed using an individ- relationship well described for bivalves (Hofmann ual-based model, adapted from the model for hard et al., 2006; Flye-Sainte-Marie et al., 2007; Fulford clams, Mercenaria mercenaria, described by Hofmann et al., 2010) that has a temperature optimum at 18°C et al. (2006) to simulate growth of a surfclam (Spisula and cessation near 0°C and 24°C, consistent with solidissima). A schematic of the processes included in observed physiological responses (Marzec et al., 2010). the model is provided in Figure 1, the equations used Biological processes such as reproduction, growth rate are provided in Table 1, and a summary of simulation and maximum size integrate all physiological functions inputs is listed in Table 2. Simulations used a maximal specified in the model. Thus, in the absence of direct bivalve assimilation efficiency of 0.77 (Møhlenberg measurements for respiration and filtration, simulated and Kiørboe, 1981; Laing et al., 1987; Powell and Stan- reproductive behaviour, growth rates, and maximum ton, 1985; Reid et al., 2010; Ren et al., 2006) and an shell lengths, when verified against field-based observa- annual time series of bottom water temperatures from tions, offer strong support that the process rates, weight an area supporting growth of large (>160 mm) surfcl- dependencies, and temperature dependencies are ams (20–40 m depth off New Jersey in 2007). The tem- properly parameterized. In our study, spawning and perature time series was provided by a physical reproduction were verified against Ropes (1968) and © 2013 Blackwell Publishing Ltd., Fish. Oceanogr., 22:3, 220–233. 222 Table 1. Summary of governing equations for calculation of changes in weight, condition and length and parameterizations used to represent the physiological processes determining growth and reproduction used in the individual model. Equation Name Equation Definitions Reference D.M. Munroe dW ¼ ðÞÀ ð ; Þ = = Weight dt A R W T WWweight (mg dry wt.) A Assimilation Hofmann et al. (2006) R(W,T) = Respiration À ðÞ Condition CLðÞ¼; W WðÞt W0 L C(L,W) = condition index Hofmann et al. (2006) WmðÞÀL W0ðÞL index W(t) = current weight defined by weight et al. equation W0(L) = standard weight at length L Wm(L) = maximum weight at length L b Standard W0ðÞ¼L