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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
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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
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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.
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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.
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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.
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