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Scaredy-Oysters: In Situ Documentation of an Oyster Behavioral Response to Predators
John M. Carroll and Jeff C. Clements

Southeastern Naturalist, Volume 18, Issue 3 (2019): N21–N26

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N21 2019 Southeastern Naturalist Notes Vol. 18, No. 3 J.M. Carroll and J.C. Clements Scaredy-Oysters: In Situ Documentation of an Oyster Behavioral Response to Predators John M. Carroll1,* and Jeff C. Clements2,3 Abstract - Non-consumptive effects of predators on prey populations have received increased interest in recent years. For Crassostrea virginica (Eastern Oyster), much of the focus has been on induced morphological defenses (e.g., shell thickening). Here, we provide in situ documentation of a behavioral response of Eastern Oysters (valve closure) to the threat of predation on a natural reef. This behavioral response, while intuitive, has been largely ignored in the literature despite potential impacts on individual oyster health by affecting feeding and subsequently energy assimilation, reproductive condition, and growth. In situ photographs revealed that, under natural conditions, Eastern Oysters closed during the passive presence of a crab mate-guarding pair and took ~5 minutes to reopen to pre-predator gapes. Given that multiple oysters in our photos reacted similarly, this behavioral response may scale up to have effects on the population and the ecosystem services that Eastern Oysters provide. Ultimately, our observations open the door to a number of testable hypotheses regarding a predator’s non-consumptive effects on oyster reefs. Introduction. Predator–prey interactions play a major role in the structure and function of biological communities and in the overall ecology and evolution of animals, and predation has long been considered one of the most important factors affecting marine populations and communities (Connell 1961, Paine 1966). For prey, defending against and/or avoiding predation is key to surviving a predator’s attack. To combat predation, prey can employ a number of defenses against predators, including (but not limited to) morphological, chemical, and behavioral responses. For marine molluscs, induced morphological defenses such as shell thickening or enhanced attachment strength are often reported (Leonard et al. 1999, Trussel 1996), although induced behavioral defenses have also been observed (Duvall et al. 1994), including in some burrowing bivalves (Flynn and Smee 2010). Such defenses can be employed before or during a predation event, require energy investment, and can result in trade-offs with other biological processes, such as feeding, growth, and/or reproductive output (Clark and Harvell 1992). Thus, while a successful predator attack can result in lethal effects on prey species, the responses to the threat of predation can invoke numerous nonlethal effects for prey (Lima 1998). The effects of predation on Crassostrea virginica (Gmelin) (Eastern Oyster) have been particularly well-studied due to their economic and ecological importance (Coen et al. 2007). More recently, studies have focused on induced defenses in juvenile Eastern Oysters, which include changes in shell thickness and other shell properties (e.g., density, organic content; Scherer et al. 2018), which take time to accrue. Given the sessile nature of Eastern Oysters, however, studies to date have largely ignored their more immediate, behavioral responses that might help reduce predatory mortality. One behavior that is generally accepted to be important in predator avoidance, but has been largely ignored empirically, is valve closure. Although valve gaping/closing behavior has been investigated for other 1Department of Biology, Georgia Southern University, Statesboro, GA 30460. 2Department of Biology, Norwegian University of Science and Technology, 7491 Trondheim, Norway. 3Department of Biological and Environmental Sciences, University of Gothenburg, Sven Lovén Centre for Marine Sciences – Kristineberg, Fiskebäckskil 45178, Sweden. *Corresponding author - jcarroll@georgiasouthern.edu. Manuscript Editor: Eugene Turner Notes of the Southeastern Naturalist, Issue 18/3, 2019 2019 Southeastern Naturalist Notes Vol. 18, No. 3 N22 J.M. Carroll and J.C. Clements environmental stressors (e.g., water quality conditions [Porter and Breitburg 2016], harmful algae [Tran et al. 2010], oil spills [Redmond et al. 2017]), it likely plays a significant role in the relationships between sessile bivalves and their predators since inducible morphological defenses take time to accrue, but behavioral defenses are immediate. A handful of laboratory studies suggest that bivalve valve closure occurs almost immediately upon the threat of predation in freshwater mussels (Wilson et al. 2012) and marine mussels (Robson et al. 2007, 2010); however, these studies are restricted to laboratory observations. Data on valve closure responses to predators are lacking for Eastern Oysters, and such observations under natural conditions remain undocumented. During an oyster-predation study in October 2013 (Carroll et al. 2015), we deployed GoPro Hero3 cameras to identify potential Eastern Oyster predators at our study site in North Carolina. Here, we present interesting preliminary observations of in situ oyster behavior in response to the passive presence of a pair (a male mate-guarding a female) of Callinectes sapidus (Rathbun) (Blue Crab). Further, we discuss the potential implications of these observations. Methods. Opportunistically, we used photographic monitoring to observe intriguing evidence of previously undocumented in situ behavioral responses to predators in Eastern Oysters. This study was conducted on intertidal oyster reefs at the University of North Carolina Wilmington Research Lease, located at Hewletts Creek (34°35.29″N, 077°33.19″W) in Masonboro Sound, NC. This marine-dominated estuary, lined by marshes with intertidal sand flats and oyster reefs, has a tidal range of ~1.5 m. Oyster predators are present in the area, including Blue Crabs and Menippe mercenaria Say (Stone Crab), as well as Urosalpinx cinerea (Say) (Atlantic Oyster Drill; Harwell et al. 2011), although the dominant oyster predators in the system appear to be small xanthid crabs (Carroll et al. 2015). We deployed GoPro Hero3 cameras on intertidal oyster reefs before an incoming tide in the fall (October) 2013, which were set to take a photograph every minute, until the batteries died (~4 hours), during predator surveys at the field site (Carroll et al. 2015). Cameras were deployed so that the incoming tide was moving from behind to in front of the camera. During one deployment, the camera angle was, by chance, appropriate to document the valve gaping (i.e., degree of valve opening) behavior of 3 Eastern Oysters on a reef. Approximately 135 minutes after the oyster reef was submerged, the 3 oysters responded to the passive presence of a pair of Blue Crabs (a male mate-guarding a female; Fig. 1). Using the 3 oysters with visibly gaped valves, we measured the distance between the apertural edge of the shell and calculated a relative measure of gaping 10 minutes before, during, and 10 minutes after the Blue Crabs were present, using ImageJ (National Institutes of Health) image analysis software (Scheider et al. 2012), allowing for a quantitative assessment of oyster-gaping behavior. Results and Discussion. Before the presence of the crab mate-guarding pair, the gaping behavior of the 3 Eastern Oysters was consistently similar 10 minutes before crab arrival, with the Oysters being wide open (Figs. 1a, 2). When the crabs arrived, however, the valve-gaping behavior of the oysters was altered such that they were completely (or almost completely) closed (Figs. 1b, 2). Gaping was depressed during and 1 minute after the crabs’ presence (Figs. 1c–f, 2); however, the oysters gradually reopened, taking ~5 minutes after the crabs left for gaping to completely return to pre-crab levels (Fig. 2). While oysters closing their valves under threat of predation may be intuitive, as this would reduce risk of detection by chemosensory predators, this observation has neither been described previously in the literature as an Eastern Oyster response to predators, nor observed directly in situ. Valve closures may play a substantial role in predator avoidance in Eastern Oysters and other epibenthic, non-mobile bivalves, particularly in habitats where N23 2019 Southeastern Naturalist Notes Vol. 18, No. 3 J.M. Carroll and J.C. Clements actual or perceived predator threats are low. Although we could only clearly measure this behavior in 3 Eastern Oysters, similar effects have been observed under laboratory conditions in Mercenaria mercenaria L. (Quahog), whereby pumping rates were reduced in the presence of predators (valve gaping not measured; Smee and Weissberg 2006). Likewise, under laboratory conditions, mussels have been reported to restrict gaping in response to consumptive predator cues (conspecific homogenate; Robson et al. 2007, 2010). However, our observation provides the first direct evidence of a potential behavioral non-consumptive effect on Eastern Oysters in situ, as the sheer presence of non-feeding crabs evoked a behavioral response in the oysters. Valve-gaping behavior can be important for reasons other than predator avoidance. For example, valve opening is necessary for basic physiological functions such as feeding and Figure 1. Visual documentation of behavioral responses to the passive presence of a Callinectes sapidus (Blue Crab) pair. Eastern Oysters are highlighted with arrows. Images depict oyster behavior (a) 1 minute before, (b) during, and (c–f) 1– 4 minutes after the crab mating pair was present. The white lines in panel (a) indicate where the gape distance was measured for each image. 2019 Southeastern Naturalist Notes Vol. 18, No. 3 N24 J.M. Carroll and J.C. Clements respiration (Markicj et al. 2000). Consequently, predator-induced valve activity may invoke functional trade-offs for individual oysters such as reduced feeding (Porter and Breitburg 2009) that would restrict energy assimilation and affect fitness parameters (e.g., growth and reproduction), particularly given the delayed return (5 minutes) to “normal” gaping. Valve closure requires active contraction of adductor muscles, utilizing energy that might otherwise be allocated elsewhere (Ward and Langdon 1986), and rapid valve closures can be a dominant contributor to energy demands in bivalves (Hochachka et al. 1983). Therefore, it is possible that at some level of valve activity associated with predator presence, e.g., in reefs where predators are plentiful and active, the energetic costs associated with valve activity can have significant growth and condition ef fects (Ward and Langdon 1986). Many questions remain stemming from these induced behavioral defenses. First, and perhaps most importantly, is understanding the filtration and energy cost implications for this behavioral observation, particularly in regards to the functional trade-offs. Given that all 3 Eastern Oysters responded similarly to the crabs, such effects may not be restricted to individual oysters and may affect populations, although such inferences await a more robust documentation of the spatial and temporal ranges at which these non-consumptive effects operate in open systems. Further, the mechanism behind multi-oyster responses, and the spatial extent of such responses, remains unclear and should be explored. While our observations show that Eastern Oysters close their valves in the presence of non-feeding crabs, the images were only taken at 1-minute intervals. We observed the crabs directly on top of 1 Eastern Oyster and some distance away from the others. It is thus likely that the observed non-consumptive effect of non-feeding crabs in our oyster bed resulted from some combination of tactile and chemical cues, but more research is needed. In addition, given predator diversity in our system (Carroll et al. 2015, Harwell et al. 2011), how different predatory species and/or a greater frequentcy of predator encounters might alter this behavioral response should be explored. Despite our small sample, our results generally align with lab studies observing mussel gape (Robson et al. 2007) and clam pumping (Smee Figure 2. Eastern Oyster valve-gaping response 10 minutes before, during, and 10 minutes after the passive presence of a a Callinectes sapidus (Blue Crab) pair. Valve-gaping behavior was measured as a relative percentage of the gape distance for each oyster in the photo 1 minute before crab appearance (denoted with a diamond). Data are means (of the 3 individuals) ± standard error of the mean. N25 2019 Southeastern Naturalist Notes Vol. 18, No. 3 J.M. Carroll and J.C. Clements and Weissberg 2006). Similarities across these studies may suggest a common mechanistic post-threat response across bivalve species, but also raises intriguing questions regarding context-dependent responses to predator threats and, more broadly, the behavioral ecology of bivalves. Although we did not design an experiment to fully explore the effects of predator presence on Eastern Oyster behavior, our opportunistic in situ observation does indicate valve behavior as a potential non-consumptive effect of predators on Eastern Oysters in natural settings. The photographic evidence provided herein documents an understudied pathway for predators to impact Eastern Oyster behavior and oyster reefs as a whole. While we try not to make many broad conclusions due to the low sample size (n = 3 Eastern Oysters), our observations open up a multitude of testable hypotheses regarding the ecological relevancy of oyster valve-gaping responses to predators. Regardless, it is critical to understand the implications of this behavior for Eastern Oysters, both on their physiology and health, but also for their ecosystem services (e.g., filtration, nutrient se questration). New and emerging technologies for measuring bivalve gaping behavior can provide more tangible means to test related hypotheses, as well as to disentangle behavioral responses from induced morphological defenses. For example, electromagnetic and fibreoptic biosensors provide the capability of measuring bivalve gaping behavior on finer temporal scales (multiple measurements per second) and can be field deployed (Andrade et al. 2016; Clements and Comeau, in press). Given the potential population and ecological impacts of predator non-consumptive effects in oyster reefs and for other bivalve species, the observations reported here and the technologies currently available provide the basis to further explore how predators affect prey. Acknowledgments. We acknowledge Dr. Christopher Finelli and the University of North Carolina Wilmington, for access to their research lease and supplies that allowed these Oysters to be photographed. We also thank the editor and 2 anonymous reviewers for comments which helped improve this manuscript. Literature Cited Andrande, H., J.C. Massabau, S. Cochrane, P. Ciret, D. Tran, M. Sow, and L. Camus. 2016. 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