Bivalve Response to Estuarine Eutrophication: The Balance between Enhanced Food Supply and Habitat Alterations Author(s) :Ruth H. Carmichael, A. C. Shriver and I. Valiela Source: Journal of Shellfish Research, 31(1):1-11. 2012. Published By: National Shellfisheries Association DOI: http://dx.doi.org/10.2983/035.031.0101 URL: http://www.bioone.org/doi/full/10.2983/035.031.0101 BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. Journal of Shellfish Research, Vol. 31, No. 1, 1–11, 2012. BIVALVE RESPONSE TO ESTUARINE EUTROPHICATION: THE BALANCE BETWEEN ENHANCED FOOD SUPPLY AND HABITAT ALTERATIONS RUTH H. CARMICHAEL,1,2* A. C. SHRIVER3 AND I. VALIELA3 1Dauphin Island Sea Lab, 101 Bienville Boulevard, Dauphin Island, AL 36528; 2University of South Alabama, Mobile, AL 36688; 3The Ecosystems Center, Marine Biology Laboratory, Woods Hole, MA 02343 ABSTRACT As a result of insufficient sampling, differences in estuarine attributes, species variation, and poor links to anthropogenic sources, responses of bivalve mollucs to anthropogenic nutrient enrichment of coastal waters remains poorly defined for most systems worldwide. To establish the net effect of nutrient enrichment on bivalves, we compared changes in growth and survival of different bivalve species reported in 5 studies conducted in a representative estuarine system (on Cape Cod, MA) in which effects of eutrophication on food supply and habitat were quantified and related directly to land-derived nitrogen (N) sources. N-stable isotope ratios in suspended particulates and bivalve tissues demonstrated that N derived from anthropogenic wastewater was assimilated into bivalve tissues as N loads increased. Bivalve shell and soft-tissue growth also increased in response to increased chlorophyll a concentrations driven by land-derived N loads. Growth was accompanied by increased percent N content of tissues in some species, suggesting a change in tissue composition with N enrichment. In contrast, bivalve survival was lower in years of higher microalgal production, suggesting eutrophic-driven habitat degradation may have contributed to mortality. The net effect of eutrophication on bivalves, therefore, depended on the balance between enhanced food supply and habitat alterations that are mediated by attributes of the receiving estuary, and differences among species, particularly feeding habits, feeding physiology, and tolerance to hypoxia. KEY WORDS: nitrogen, stable isotope, chlorophyll, growth, survival INTRODUCTION lochs more than 60 y ago (Orr 1947, Raymont 1947), and to a lesser degree from more recent studies in the Baltic and North Increased nutrient enrichment to coastal waters worldwide Seas, the Kattegat, and Cape Cod estuaries (Tober et al. 2000, (National Research Council 2000, Paerl 2006) has increased Nixon & Buckley 2002). These studies show increases in abun- algal productivity, stimulated accumulation of organic matter dance or biomass of finfish through time or across locations as from detritus of algae, and increased nitrogen (N) content of N and/or phosphorus (P) inputs to water bodies increased. If particles in the water and sediment (Zeitzschel 1980, Grane´ li & enrichment-driven secondary production can be detected in some Sundba¨ ck 1985, Cloern 2001). The resulting eutrophication of finfish, which tend to be migratory and herbivorous, then pro- coastal waters ultimately may cause loss of seagrasses, anoxia duction in other primary consumers, particularly sedentary in near-bottom waters, and lower sediment redox (Paerl et al. bivalves, should be at least equally coupled to nutrient enrich- 1998, Gray et al. 2002, Hauxwell et al. 2003). Although the ment and quantifiable (Tober et al. 2000, Carmichael 2004). susceptibility of a coastal system to these effects depends on physical–chemical attributes of the water body, such as salinity, temperature, mixing, discharge, and flushing rates (Cloern 2001, BIVALVE RESPONSES TO NUTRIENT ENRICHMENT Paerl 2006), eutrophic-driven changes in water quality have Previous studies suggest the effects of nutrient enrichment resulted in widespread species loss in many estuaries (Baden on bivalves may be positive or negative, depending on whether et al. 1990, Cloern 2001, Gray et al. 2002). enrichment affected primarily food resources or habitat (Table 1). Because increased primary production often translates to in- Positive effects of nutrient enrichment on bivalves have in- creased food quantity and quality for primary consumers such cluded increased abundance, biomass, and assimilation effi- as bivalves (e.g., Bayne & Widdows 1978, Newell et al. 1982, ciency, largely attributed to increased food supply, whereas Smaal & Van Stralen 1990, Fegley et al. 1992, Carmichael et al. negative effects included increased mortality, reduced biomass, 2004), there may be corresponding increases in growth and and lower recruitment, resulting from habitat loss or degrada- abundance of consumers in nutrient-enriched estuaries (Nixon & tion (Table 1, Fig. 1). Some studies reported a combination of Buckley 2002, Kirby & Miller 2005). The extent to which these enrichment-related effects (Feinstein et al. 1996, Josefson & potentially positive effects of enrichment are detectable in coastal Rasmussen 2000, Kirby & Miller 2005, Verdelhos et al. 2005), food webs, however, is not well established (Micheli 1999). The suggesting that the response of bivalves to nutrient enrichment notion that nutrient enrichment may stimulate production of may be more complex than a simple positive or negative response. consumers has been largely overlooked in favor of efforts to Until recently, however, most studies regarding the effects of identify, diagnose, and remediate the negative effects of eutro- eutrophication on bivalves relied on circumstantial evidence. phication (Micheli 1999, Fluharty 2000, Nixon & Buckley 2002, For example, the Scottish loch studies reported increased Verdelhos et al. 2005). abundance among bivalves as they did for finfish, but did The bulk of evidence supporting eutrophic-driven secondary not similarly detail the effects on bivalves (Orr 1947, Raymont production comes from fertilization experiments in Scottish sea 1947). Until 2001, no studies provided direct links between bivalve responses and a specific source of nutrient enrichment *Corresponding author. E-mail: [email protected] across sites, and only 25% of the reported bivalve responses DOI: 10.2983/035.031.0101 were substantiated by measuring a potential mechanism of 1 TABLE 1. 2 Historically reported bivalve responses to nutrient enrichment, and mechanisms of effect (eutrophic-driven changes in food supply or habitat) across different species, locations, and enrichment types. Bivalve Response Mechanism of Effect Species Location Enrichment Type to Enrichment (food supply or habitat metric) Source Mytilus edulis Loch Craiglin, Scotland P and N fertilization Increased abundance Increased food supply Marshall (1947) Mya arenaria (phytoplankton abundance) Raymont (1947) Macoma balthica Cardium edule Paphia pullastra Scrobicularia plana Modiolus spp. Mytilus edulis Baltic Sea Urbanization: increased Increased abundance and tissue Presumed increased food supply Cederwal and Mya arenaria P and N (not measured) weight (Mya, Macoma only) (not measured) Elmgren (1980) Macoma balthica Cardium spp. Mytilus edulis Rı´ as Bajas, Spain Upwelling Increased tissue weight Presumed increased food supply Blanton et al. (1987) (not measured) C ARMICHAEL ET AL Mya arenaria Kettegat, Sweden Urbanization: N and P Mortality among most species Habitat change: hypoxia (measured Baden et al. (1990) Cardium edule oxygen concentrations) Abra alba Arctica islandica Corbula gibba Corbula gibba Adriatic Sea Urbanization: increased Increased abundance Presumed habitat change: anoxic Crema et al. (1991) . nutrients stress (not measured) Argopecten irradians Waquoit Bay, USA Urbanization: increased N Reduced catch Habitat change: eelgrass loss Valiela et al. (1992) (measured) and presumed anoxia (not measured) Ruditapes decussatus Ria Formosa, Urbanization (not measured) Increased respiration, reduced Increased organic content Costa et al. (1993) South Portugal absorption efficiency (not directly measured) Mya arenaria Waquoit Bay, USA Urbanization: increased N Increased shell growth Increased food supply Chalfoun et al. (1994) Mercenaria mercenaria (Mya only) (not directly measured) Nucula annulata Narragansett Bay, USA Increased organic matter; Increased mortality and Presumed habitat change: hypoxia, Craig (1994) N, P, and silica fertilization recruitment failure settlement interference (not measured) Katelysia spp. Princess Royal Harbor,