Animal size and sea water temperature, but not pH, influence a repeatable startle response behaviour in a wide-ranging marine mollusc

doi:10.1016/j.anbehav.2020.12.008

Animal Behaviour

Volume 173, March 2021, Pages 191-205

https://doi.org/10.1016/j.anbehav.2020.12.008 Get rights and content

Highlights

•
We measured startle response (time to open) in mussels following a predator cue.
•
We tested effects of temperature, pH and size and measured repeatability.
•
Larger mussels opened faster; repeatable startle response; evidence of habituation.
•
High temperature increased time to open; no effect of pH.
•
Blue mussels are sensitive to temperature and vulnerable to climate change.

Startle response behaviours are important in predator avoidance and escape for a wide array of animals. For many marine invertebrates, however, startle response behaviours are understudied, and the effects of global change stressors on these responses are unknown. We exposed two size classes of blue mussels (Mytilus edulis × trossulus) to different combinations of temperature (15 and 19 °C) and pH (8.2 and 7.5 pH_T) for 3 months and subsequently measured individual time to open following a tactile predator cue (i.e. startle response time) over a series of four consecutive trials. Time to open was highly repeatable in the short term and decreased linearly across the four trials. Individuals from the larger size class had a shorter time to open than their smaller-sized counterparts. High temperature increased time to open compared to low temperature, while pH had no effect. These results suggest that bivalve time to open is repeatable, related to relative vulnerability to predation and affected by temperature. Given that increased closure times impact feeding and respiration, the effect of temperature on closure duration may play a role in the sensitivity to ocean warming in this species and contribute to ecosystem level effects.

Section snippets

Animal Collection and Husbandry

Adult mussels (Fig. A1a) were hand-collected from the Gullmar Fjord (located in Skagerrak in the North Sea on the southwest coast of Sweden) in late May 2018. The animals were collected from the side of a nearshore pier at a depth of 0–1 m adjacent to the Kristineberg Marine Research and Innovation Centre (KMRIC; 58°15′N, 11°26′49″E). During collection, sea water temperature was ≈14 °C, salinity was ≈22 and pH_T was ≈8.1 (Fig. A2). The mussels were transported to a temperature-controlled wet

Shell Length and Wet Weight

Following exposure, mean shell lengths were 67.5 ± 5.1 mm and 50.9 ± 4.1 mm and mean wet weights were 40.8 ± 8.9 g and 17.6 ± 4.2 g in large and small size classes, respectively (Fig. A3b and c). For growth rates (i.e. changes in shell length and wet weight), initial size had a significant independent effect on growth rate, with smaller animals showing larger increases in both shell length and wet weight than larger individuals (Fig. 1a and b). There were no significant effects of temperature or pH_T, or

Discussion

This study provides novel insights into the behavioural ecology of a bivalve startle response (time to open) and how this behaviour might be impacted under global changes. Results suggest that startle responses in bivalves are repeatable in short-term contexts, are a function of animal size and are negatively affected by elevated temperatures but not by reduced pH_T. Given the important role of valve closures in avoiding and escaping predation (Carroll & Clements, 2019; Clements, Poirier et al.,

Data Availability

All statistical results, raw data, R code and original data files uploaded to R are available as supplementary material. Annotated analysis code (in R) is in Supplementary material 1, raw data are in Supplementary material 2, and the source data files for analysis are contained in Supplementary material 3–7.

Author Contributions

J.C.C. conceptualized the idea. J.C.C., F.J. and K.R. designed the experiment. J.C.C. and K.R. tended to the animals and collected abiotic sea water parameters. J.C.C. and J.N. carried out the behavioural experiments. J.C.C. analysed data and wrote the manuscript. S.D. and F.J. provided in-kind support and technical guidance. All authors revised and approved the manuscript.

Funding

This work was supported by a Marie Skłodowska-Curie Individual Fellowship funded through the European Union Horizon 2020 program (project number 752813 to J.C.C.); a KVA Fund through the University of Gothenburg (to J.C.C.); an Assemble Plus Grant from the European Marine Biological Resource Centre (EMBRC) (to J.C.C); the Research Council of Norway (262942 to F.J.); and by a Carl Tryggers Fellowship (to K.R.).

Competing Interests

We declare we have no competing interests.

Acknowledgments

We thank the support staff at the Kristineberg Marine Research and Innovation Centre (KMRIC) for outstanding support throughout the experiment. We also thank Alice D'Hurlaborde and Maria Asplund for assistance in collecting and cleaning mussels. Thanks Dr Joacim Näslund for statistical advice regarding Cox proportional hazards models. J.C.C. and K.R. also thank our many friends at the KMRIC for taking care of logistical aspects on short notice throughout the experiment: Roland Pfeiffer, Prema

References (90)

S.D. Bamber et al.
Behavioral responses of Arctica islandica (Bivalvia: Arcticidae) to simulated leakages of carbon dioxide from sub-sea geological storage
Aquatic Toxicology
(2016)
M.A. Barbeau et al.
Behavioral mechanisms of prey size selection by sea stars (Asterias vulgaris Verrill) and crabs (Cancer irroratus Say) preying on juvenile sea scallops (Placopecten magellanicus (Gmelin))
Journal of Experimental Marine Biology and Ecology
(1994)
A.M. Bell et al.
The repeatability of behaviour: A meta-analysis
Animal Behaviour
(2009)
M. Briffa et al.
How does temperature affect behaviour? Multilevel analysis of plasticity, personality and predictability in hermit crabs
Animal Behaviour
(2013)
M. Briffa et al.
High CO₂ and marine animal behaviour: Potential mechanisms and ecological consequences
Marine Pollution Bulletin
(2012)
K. Brokordt et al.
Heritability and genetic correlations of escape behaviours in juvenile scallop Argopecten purpuratus
Animal Behaviour
(2012)
M.M. Casey et al.
Clumping behavior as a strategy against drilling predation: Implications for the fossil record
Journal of Experimental Marine Biology and Ecology
(2008)
J.C. Clements et al.
Nitrogen removal potential of shellfish aquaculture harvests in eastern Canada: A comparison of culture methods
Aquaculture Reports
(2019)
J.C. Clements et al.
Short-term exposure to elevated pCO₂ does not affect the valve gaping response of adult eastern oysters, Crassostrea virginica, to acute heat shock under an ad libitum feeding regime
Journal of Experimental Marine Biology and Ecology
(2018)
J.C. Clements et al.
Behavioural responses to predators in Mediterranean mussels (Mytilus galloprovincialis) are unaffected by elevated pCO₂
Marine Environmental Research
(2020)

I.M. Côté et al.

Predator-induced clumping behaviour in mussels (Mytilus edulis Linnaeus)

Journal of Experimental Marine Biology and Ecology

(1999)

A.G. Dickson et al.

A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media

Deep-Sea Research Part I Oceanographic Research Papers

(1987)

A.M. Flynn et al.

Behavioral plasticity of the soft-shell clam, Mya arenaria (L.), in the presence of predators increases survival in the field

Journal of Experimental Marine Biology and Ecology

(2010)

A.A. Klompmaker et al.

Predation in the marine fossil record: Studies, data, recognition, environmental factors, and behavior

Earth-Science Reviews

(2019)

J. Kobak et al.

Environmental factors affecting behavioural responses of an invasive bivalve to conspecific alarm cues

Animal Behaviour

(2014)

H. Kong et al.

Seawater acidification and temperature modulate anti-predator defenses in two co-existing Mytilus species

Marine Pollution Bulletin

(2019)

J.M. Koolhaas et al.

Coping styles in animals: Current status in behavior and stress-physiology

Neuroscience & Biobehavioral Reviews

(1999)

A. Sih et al.

Behavioral syndromes: An ecological and evolutionary overview

Trends in Ecology & Evolution

(2004)

D.L. Sinn et al.

Development of shy/bold behaviour in squid: Context-specific phenotypes associated with developmental plasticity

Animal Behaviour

(2008)

U. Sommer et al.

An experimental analysis of the importance of body-size in the seastar–mussel predator–prey relationship

Acta Oecologica

(1999)

C.D. Wilson et al.

Freshwater pearl mussels show plasticity of responses to different predation risks but also show consistent individual differences in responsiveness

Behavioural Processes

(2012)

F. Wu et al.

Effects of seawater pH and temperature on foraging behavior of the Japanese stone crab Charybdis japonica

Marine Pollution Bulletin

(2017)

B.J.M. Allan et al.

Warming has a greater effect than elevated CO₂ on predator–prey interactions in coral reef fish

Proceedings of the Royal Society B: Biological Sciences

(2017)

A. Anestis et al.

Behavioral, metabolic, and molecular stress responses of marine bivalve Mytilus galloprovincialis during long-term acclimation at increasing ambient temperature

American Journal of Physiology - Regulatory, Integrative and Comparative Physiology

(2007)

A. Antoł et al.

Sedentary prey facing an acute predation risk: Testing the hypothesis of inducible metabolite emission suppression in zebra mussels, Dreissena polymorpha

Hydrobiologia

(2018)

M.M. Ashur et al.

Impacts of ocean acidification on sensory function in marine organisms

Integrative and Comparative Biology

(2017)

R. Bibby et al.

Ocean acidification disrupts induced defences in the intertidal gastropod Littorina littorea

Biology Letters

(2007)

V. Bretagnolle et al.

Predator–prey interactions and climate change

M. Briffa et al.

High in situ repeatability of behaviour indicates animal personality in the beadlet anemone Actinia equina (Cnidaria)

PLoS One

(2011)

J.M. Carroll et al.

Scaredy-oysters: In situ documentation of an oyster behavioral response to predators

Southeastern Naturalist

(2019)

M.C.N. Castorani et al.

Native predator chemical cues induce anti-predation behaviors in an invasive marine bivalve

Biological Invasions

(2016)

H.T. Christensen et al.

Comparative study of predatory responses in blue mussels (Mytilus edulis L.) produced in suspended long line cultures or collected from natural bottom mussel beds

Helgoland Marine Research

(2012)

T.D. Clark et al.

Ocean acidification does not impair the behaviour of coral reef fishes

Nature

(2020)

J.C. Clements et al.

Behavioral defenses of shellfish prey under ocean acidification

Journal of Shellfish Research

(2019)

J.C. Clements et al.

Marine animal behaviour in a high CO₂ ocean

Marine Ecology Progress Series

(2015)

J.C. Clements et al.

An extreme decline effect in ocean acidification fish ecology

EcoEvoRxiv

(2020)

J.H. Connell

The influence of interspecific competition and other factors on the distribution of the barnacle Chthamalus stellatus

Ecology

(1961)

R. Dawkins et al.

Arms races between and within species

Proceedings of the Roal Society of London, Series B: Biological Science

(1979)

N.J. Dingemanse et al.

Quantifying individual variation in behaviour: Mixed-effect modelling approaches

Journal of Animal Ecology

(2013)

N. Dorey et al.

Assessing physiological tipping point of sea urchin larvae exposed to a broad range of pH

Global Change Biology

(2013)

A.M. Draper et al.

Impacts of global warming and elevated CO₂ on sensory behavior in predator–prey interactions: A review and synthesis

Frontiers in Ecology and Evolution

(2019)

A. Dzierżyńska-Białończyk et al.

What scares a mussel? Changes in valve movement pattern as an immediate response of a byssate bivalve to biotic factors

Hydrobiologia

(2019)

J. Fox et al.

An R companion to applied regression

(2019)

S. Galler et al.

The highly efficient holding function of the mollusc ‘catch’ muscle is not based on decelerated myosin head cross-bridge cycles

Proceedings of the Royal Society B: Biological Sciences

(2010)

S.D. Gosling

From mice to men: What can we learn about personality from animal research?

Psychological Bulletin

(2001)

Cited by (16)

The effects of plastic additives on swimming activity and startle response in marine amphipod Echinogammarus marinus
2024, Science of the Total Environment
Plastic additives are widely used in plastic production and are found in the environment owing to their widespread applications. Among these additives, N-butyl benzenesulfonamide (NBBS) and triphenyl phosphate (TPHP) are under international watchlist for evaluation, with limited studies on amphipods. Di-ethylhexyl phthalate (DEHP) and dibutyl phthalate (DBP) are banned in some countries and categorised as substances of very high concern. This study aimed to investigate the effects of NBBS, TPHP, DEHP and DBP on the swimming activity of a coastal intertidal marine amphipod, Echinogammarus marinus. Furthermore, this study is the first to quantify startle response in E. marinus in response to light stimuli. Amphipods were exposed to 0, 0.5, 5, 50 and 500 μg/l concentrations of all test compounds. Swimming activity and startle responses were assessed by video tracking and analysis using an 8-min alternating dark and light protocol after exposure on days 7 and 14. We observed an overall compound and light effect on the swimming activity of E. marinus. A significant decrease in swimming distance was found in 500 μg/l NBBS and TPHP. We observed that the startle response in E. marinus had a latency period of >2 s and animals were assessed at 1 s and the sum of the first 5 s. There was a clear startle response in E. marinus during dark to light transition, evident with increased swimming distance. NBBS exposure significantly increased startle response at environmental concentrations, while significant effects were only seen in 500 μg/l TPHP at 5 s. We found no significant effects of DEHP and DBP on swimming behaviour at the concentrations assessed. The findings of this study affirm the necessity for a continuous review of plastic additives to combat adverse behavioural effects that may be transferable to the population levels.
Body traits variation of a reef building polychaete across a latitudinal gradient
2024, Marine Environmental Research
Body size is considered the most important trait in ecology, and as such, helps to understand the species-environment interactions. We explored the relationship between body traits and environmental variables along a gradient range using the polychaete Phragmatopoma caudata, with well-defined and diversified morphological structures. Measurements of five traits (body length, opercular crown, branchiae, tentacles and building organ sizes) were taken at nine sites along the Southwestern Atlantic coast and their relationships to temperature, salinity, tidal range, waves height, and dissolved oxygen were assessed. Our results demonstrate that traits were influenced by the environmental gradient and temperature was the main factor that drives this variation in body traits, while the other variables showed a minor influence on this. The approach showed patterns of variation of body traits in a macroscale context, increasing the understanding of its relationships with environmental variables and eventual shifts in the distribution in the future climate scenarios.
Hermit crabs as model species for investigating the behavioural responses to pollution
2024, Science of the Total Environment
Human impacts on the environment affect organisms at all levels of biological organisation and ultimately can change their phenotype. Over time, phenotypic change may arise due to selection but individual phenotypes are also subject to change via genotype × environment interactions. In animals, behaviour is the most flexible aspect of phenotype, and hence the most liable to change across environmental gradients including exposure to pollution. Here we review current knowledge on the impacts of pollution, broadly defined to include the release of substances, energy, and the effects of carbon emissions, on the behaviour of a highly studied group, the globally distributed hermit crabs. We first show how their obligate association with empty gastropod shells underpins their use as model organisms for the study of resource-assessment, contest, and risk-coping behaviours. Intense study of hermit crabs has advanced our understanding of how animals use information, and we discuss the ways in which pollutants can disrupt the cognitive processes involved. We then highlight current studies of hermit crabs, which paint a clear picture of behavioural changes due to multiple pollutants. Impacts on behaviour vary across pollutants and entire suites of behaviours can be influenced by a single pollutant, with the potential for interactive and cascade effects. Hermit crabs offer the opportunity for detailed behavioural analysis, including application of the repeated measures animal-personality framework, and they are highly amenable to experimental manipulations. As such, we show how they now provide a model system for studying the impacts of pollution on behaviour, yielding insights broadly applicable across animal diversity.
Impacts of ocean warming and acidification on predator-prey interactions in the intertidal zone: A research weaving approach
2023, Journal of Experimental Marine Biology and Ecology
The effect of ocean warming and acidification on predator-prey interactions in the intertidal zone is a topic of growing concern for the scientific community. In this review, we aim to describe how scientists have explored the topic via research weaving, a combination of a systematic review, and a bibliometric approach. We assess articles published in the last decade exploring the impact of both stressors on predation in the intertidal zone, via experimental or observational techniques. Several methods were used to delve into how climate change-induced stress affected intertidal predation, as the study design leaned toward single-based driver trials to the detriment of a multi-driver approach. Mollusks, echinoderms, and crustaceans have been extensively used as model organisms, with little published data on other invertebrates, vertebrates, and algae taxa. Moreover, there is a strong web of co-authoring across institutions and countries from the Northern Hemisphere, that can skew our understanding towards temperate environments. Therefore, institutions and countries should increase participation in the southern hemisphere networking, assessing the problems under a global outlook. Our review also addresses the various impacts of ocean acidification, warming, or their interaction with predation-related variables, affecting organisms from the genetic to a broader ecological scope, such as animal behaviour or interspecific interactions. Finally, we argue that the numerous synonyms used in keywording articles in the field, possibly hurting future reviews in the area, as we provide different keyword standardizations. Our findings can help guide upcoming approaches to the topic by assessing what has been already done and revealing gaps in emerging themes, like a strong skew towards single-driver (specially acidification) lab experiments of northern hemisphere organisms and a lack of field multi-stressor experiments.
Valve gaping behaviour in the European oyster (Ostrea edulis) in response to changes in light intensity when combined with variations in salinity and seawater temperature
2023, Journal of Experimental Marine Biology and Ecology
Valve gaping behaviour in bivalve molluscs controls the flow of water across gills that provides both food, and oxygen for respiration. Closure of the valves also provides protection from predators and poor-quality water conditions. Research presented here used a flow through seawater system with controlled changes in salinity and temperature, combined with continuous measurement of valve gape using Hall effect sensors, to study how changes in these variables affect the valve movements of the European oyster (Ostrea edulis) held under controlled long day-length conditions. A clear relationship between periods of reduced light intensity and maximum valve gape was recognised in preliminary studies and provided a benchmark against which to compare how changes in environmental conditions linked to climate change may alter the behaviour of these coastal marine bivalves. Oysters collected from the southwest coast of Norway in August 2022 were held for 72 h at full seawater salinity of 33.6 and a temperature of 15.8 ± 0.5 °C prior to exposure to a reduction in salinity down to 18.2 over a 3 h period. Oysters showed an initial reduction in valve gape width as salinity reached 31.4, with valve gape decreasing further as salinity fell to 28.8. All valves were fully closed at salinity 20.5. Oysters remained in this condition throughout the subsequent 21 h exposure period with salinity at 18.2. Thereafter salinity was increased in 3 steps. In the first step, salinity reached 24.2 over 2 h, and was held there over the following 22 h. All oysters commenced re-opening valves between salinity 22.8 and 24.2. When salinity was further increased to 27.3 over the subsequent 24 h, oysters returned to approximately their pre-exposure valve gape widths. When salinity 33.8 was delivered to the tanks there were 2 d during which maximum valve gape was significantly reduced, after which valve gape width returned to a pre-exposure condition. The predicted pattern of valve opening during reduced light intensity periods was maintained when seawater temperature was raised from 15.8 °C up to 20.1 °C in approximately 1 °C steps every 24 h. However, reduction of temperature from 20.1 °C in similar sized increments altered the expected patterns of behaviour. The results indicate that increasing occurrences of fluxes in salinity and temperature due to climate change have the potential to disrupt normal valve gaping behaviour in European oysters, creating an additional challenge to those they already face from invasive species and disease.
Burrowing behaviour of soft-shell clams (Mya arenaria) following human disturbance
2023, Journal of Experimental Marine Biology and Ecology
The soft-shell clam, Mya arenaria, is an endobenthic marine bivalve species that is abundant in the intertidal and shallow-subtidal zones of eastern Canadian and New England shores. In these coastal environments, clams are subjected to both natural and anthropogenic disturbances that can result in dislodgement from the sediment. This is especially relevant for harvested clam species that are managed by a legal size limit. Herein, live clams that are too small to be retained by harvesters are discarded back onto the sediment surface. These clams must reburrow in order to survive; however, the reburrowing behaviour of these clams after being disturbed is not well known. To fill this knowledge gap, a series of five field trials were conducted in Kouchibouguac National Park, New Brunswick, Canada, during the summer and fall of 2021 to measure reburrowing rates of discarded sub-legal sized (<50 mm) soft-shell clams. Three size groups (20–30, 31–40, and 41–50 mm) of soft-shell clams were excavated and returned to the sediment surface at three different tidal levels inside protective enclosures during low tide for each trial. Time to initiate and complete reburrowing was subsequently observed over a 24 h (h) period. Results showed that reburrowing time was not affected by size class; however, reburrowing time was affected by tidal level, site, and trial. Results suggest that disturbed clams discarded onto submerged sediment surfaces (tidal levels 2 and 3) reburrow quicker than those discarded onto air-exposed sediment (tidal level 1). Reburrowing rates of subtidally-discarded clams were faster during the first three months of the study (June–August) compared to rates observed in the September trials. Comparing reburrowing rates to environmental conditions during the trials suggested that decreasing salinity in September likely drove the slower reburrowing rates compared to rates observed earlier in the season; decreasing temperatures may also have had some influence. These findings suggest that discarding sub-legal sized clams onto submerged sediment will increase the probability of clam survival via faster reburrowing, and that environmental conditions at the time of discard can affect reburrowing rates.

View all citing articles on Scopus

View full text

Animal size and sea water temperature, but not pH, influence a repeatable startle response behaviour in a wide-ranging marine mollusc

Highlights

Section snippets

Animal Collection and Husbandry

Shell Length and Wet Weight

Discussion

Data Availability

Author Contributions

Funding

Competing Interests

Acknowledgments

Aquatic Toxicology

Journal of Experimental Marine Biology and Ecology

Animal Behaviour

Animal Behaviour

Marine Pollution Bulletin

Animal Behaviour

Journal of Experimental Marine Biology and Ecology

Aquaculture Reports

Journal of Experimental Marine Biology and Ecology

Marine Environmental Research

Journal of Experimental Marine Biology and Ecology

Deep-Sea Research Part I Oceanographic Research Papers

Journal of Experimental Marine Biology and Ecology

Earth-Science Reviews

Animal Behaviour

Marine Pollution Bulletin

Neuroscience & Biobehavioral Reviews

Trends in Ecology & Evolution

Animal Behaviour

Acta Oecologica

Behavioural Processes

Marine Pollution Bulletin

Warming has a greater effect than elevated CO2 on predator–prey interactions in coral reef fish

Proceedings of the Royal Society B: Biological Sciences

Behavioral, metabolic, and molecular stress responses of marine bivalve Mytilus galloprovincialis during long-term acclimation at increasing ambient temperature

American Journal of Physiology - Regulatory, Integrative and Comparative Physiology

Sedentary prey facing an acute predation risk: Testing the hypothesis of inducible metabolite emission suppression in zebra mussels, Dreissena polymorpha

Hydrobiologia

Impacts of ocean acidification on sensory function in marine organisms

Integrative and Comparative Biology

Ocean acidification disrupts induced defences in the intertidal gastropod Littorina littorea

Biology Letters

Predator–prey interactions and climate change

High in situ repeatability of behaviour indicates animal personality in the beadlet anemone Actinia equina (Cnidaria)

PLoS One

Scaredy-oysters: In situ documentation of an oyster behavioral response to predators

Southeastern Naturalist

Native predator chemical cues induce anti-predation behaviors in an invasive marine bivalve

Biological Invasions

Comparative study of predatory responses in blue mussels (Mytilus edulis L.) produced in suspended long line cultures or collected from natural bottom mussel beds

Helgoland Marine Research

Ocean acidification does not impair the behaviour of coral reef fishes

Nature

Behavioral defenses of shellfish prey under ocean acidification

Journal of Shellfish Research

Marine animal behaviour in a high CO2 ocean

Marine Ecology Progress Series

An extreme decline effect in ocean acidification fish ecology

EcoEvoRxiv

The influence of interspecific competition and other factors on the distribution of the barnacle Chthamalus stellatus

Ecology

Arms races between and within species

Proceedings of the Roal Society of London, Series B: Biological Science

Quantifying individual variation in behaviour: Mixed-effect modelling approaches

Journal of Animal Ecology

Assessing physiological tipping point of sea urchin larvae exposed to a broad range of pH

Global Change Biology

Impacts of global warming and elevated CO2 on sensory behavior in predator–prey interactions: A review and synthesis

Frontiers in Ecology and Evolution

What scares a mussel? Changes in valve movement pattern as an immediate response of a byssate bivalve to biotic factors

Hydrobiologia

An R companion to applied regression

The highly efficient holding function of the mollusc ‘catch’ muscle is not based on decelerated myosin head cross-bridge cycles

Proceedings of the Royal Society B: Biological Sciences

From mice to men: What can we learn about personality from animal research?

Psychological Bulletin

Warming has a greater effect than elevated CO₂ on predator–prey interactions in coral reef fish

Marine animal behaviour in a high CO₂ ocean

Impacts of global warming and elevated CO₂ on sensory behavior in predator–prey interactions: A review and synthesis