Species interactions may mediate the ability of organisms and communities to provide valued services but are rarely considered in forecasting how service provisioning will change as restored communities mature and change in species composition. Bivalves are foundational species in many communities that contribute to services such as habitat provisioning, water filtration, and denitrification but that also may respond to predator presence by reducing activity. Filtering and biodeposition rates of ribbed mussels (Geukensia demissa) in the presence of predators (blue crabs (Callinectes sapidus), oyster drills (Urosalpinx cinerea)), injured conspecifics, or other local species (mud snails, Tritia obsoleta) were compared in laboratory experiments conducted in July–August 2019 in the Hudson River estuary (New York, USA). The effect of predator diet on ribbed mussel responses was also considered. Although mussels tended to be less active in the presence of predators and injured conspecifics, significant decreases were observed in few traits, and there was no evidence that predator diet influenced mussel responses. Variability in feeding rates and other factors such as water quality may play a larger role than predator presence in determining mussel activity. These results suggest that G. demissa will continue to provide positive impacts on water clarity and quality and increase denitrification rates via biodeposition even as restored communities attract predators.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Price excludes VAT (USA)
Tax calculation will be finalised during checkout.
Angelini, C., J.N. Griffin, J. van de Koppel, L.P.M. Lamers, A.J.P. Smolders, M. Derksen-Hooijberg, T. van der Heide, and B.R. Silliman. 2016. A keystone mutualism underpins resilience of a coastal ecosystem to drought. Nature Communications 7: 12473.
Arfken, A., B. Song, J.S. Bowman, and M. Piehler. 2017. Denitrification potential of the eastern oyster microbiome using a 16S rRNA gene based metabolic inference approach. PloS one 12: e0185071.
Auguie, B. 2019. egg: Extensions for 'ggplot2': Custom Geom, Custom Themes, Plot Alignment, Labelled Panels, Symmetric Scales, and Fixed Panel Size. R package version 0.4.5. https://CRAN.R-project.org/package=egg
Bates, D., M. Maechler, B. Bolker, and S. Walker. 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67: 1–48.
Benfield, E.F. 2006. Decomposition of leaf material. In Methods in stream ecology, ed. F.R. Hauer and G.A. Lamberti, 2nd ed., 711–720. San Diego: Academic Press.
Bilkovic, D.M., M.M. Mitchell, R.E. Isdell, M. Schliep, and A.R. Smyth. 2017. Mutualism between ribbed mussels and cordgrass enhances salt marsh nitrogen removal. Ecosphere 8: e01795.
Borrero, F.J., and T.J. Hilbish. 1988. Temporal variation in shell and soft tissue growth of the mussel Geukensia demissa. Marine Ecology Progress Series 42: 9–15.
Bourdeau, P.E., and D.K. Padilla. 2019. Cue specificity of predator-induced phenotype in a marine snail: is a crab just a crab? Marine Biology 166: 84.
Callier, M.D., M. Richard, C.W. McKindsey, P. Archambault, and G. Desrosiers. 2009. Responses of benthic macrofauna and biogeochemical fluxes to various levels of mussel biodeposition: an in situ “benthocosm” experiment. Marine Pollution Bulletin 58: 1544–1553.
Carroll, J.M., and J.C. Clements. 2019. Scaredy-oysters: in situ documentation of an oyster behavioral response to predators. Southeastern Naturalist 18.
Cheung, S.G., S. Lam, Q.F. Gao, K.K. Mak, and P.K.S. Shin. 2004a. Induced anti-predator responses of the green mussel, Perna viridis (L.), on exposure to the predatory gastropod, Thais clavigera Küster, and the swimming crab, Thalamita danae Stimpson. Marine Biology 144: 675–684.
Cheung, S.G., P.Y. Tong, K.M. Yip, and P.K.S. Shin. 2004b. Chemical cues from predators and damaged conspecifics affect byssus production in the green-lipped mussel Perna viridis. Marine and Freshwater Behaviour and Physiology 37: 127–135.
Derksen-Hooijberg, M., C. Angelini, L.P. Lamers, A. Borst, A. Smolders, J.R. Hoogveld, H. de Paoli, J. van de Koppel, B.R. Silliman, and T. van der Heide. 2018. Mutualistic interactions amplify saltmarsh restoration success. Journal of Applied Ecology 55: 405–414.
Dill, L.M., M.R. Heithaus, and C.J. Walters. 2003. Behaviorally mediated indirect interactions in marine communities and their conservation implications. Ecology 84: 1151–1157.
Dodd, L.F., J.C. Caracappa, S.R. Fegley, J.H. Grabowski, and M.F. Piehler. 2018. Threat of predation does not affect Crassostrea virginica filtration. Estuaries and Coasts 41: 293–298.
Fox, J., and S. Weisberg. 2019. An R Companion to Applied Regression. 3rd ed. Thousand Oaks CA: Sage https://socialsciences.mcmaster.ca/jfox/Books/Companion/.
Fraser, L.H., W.L. Harrower, H.W. Garris, S. Davidson, P.D. Hebert, R. Howie, A. Moody, D. Polster, O.J. Schmitz, A.R. Sinclair, and B.M. Starzomski. 2015. A call for applying trophic structure in ecological restoration. Restoration Ecology 23: 503–507.
Galimany, E., J.M. Rose, M.S. Dixon, and G.H. Wikfors. 2013. Quantifying feeding behavior of ribbed mussels Geukensia demissa in two urban sites (Long Island Sound, USA) with different seston characteristics. Estuaries and Coasts 36: 1265–1273.
Gosnell, J.S., K. Spurgin, and E.A. Levine. 2017. Caged oysters still get scared: predator presence and density influence growth in oysters, but only at very close ranges. Marine Ecology Progress Series 568: 111–122.
Henry, L., H. Wickham, and W. Chang. 2020. ggstance: Horizontal 'ggplot2' Components. R package version 0.3.4. https://CRAN.R-project.org/package=ggstance.
Hoellein, T.J., C.B. Zarnoch, and R.E. Grizzle. 2015. Eastern oyster (Crassostrea virginica) filtration, biodeposition, and sediment nitrogen cycling at two oyster reefs with contrasting water quality in Great Bay Estuary (New Hampshire, USA). Biogeochemistry 122: 113–129.
Hothorn, T., F. Bretz, and P. Westfall. 2008. Simultaneous inference in general parametric models. Biometrical Journal 50: 346–363.
Huang, S.C., and R.I.E. Newell. 2002. Seasonal variations in the rates of aquatic and aerial respiration and ammonium excretion of the ribbed mussel, Geukensia demissa (Dillwyn). Journal of Experimental Marine Biology and Ecology 270: 241–255.
Johnson, K.D., and D.L. Smee. 2012. Size matters for risk assessment and resource allocation in bivalves. Marine Ecology Progress Series 462: 103–110.
Johnston, B.R., M. Molis, and R.A. Scrosati. 2011. Predator chemical cues affect prey feeding activity differently in juveniles and adults. Canadian Journal of Zoology 90: 128–132.
Julien, A.R., A.W. Tweel, N. Hadley, and P.R. Kingsley-Smith. 2020. Demographics of the ribbed mussel Geukensia demissa (Dillwyn, 1817) and the effects of its simulated manual harvest on salt marsh health in South Carolina, USA. Journal of Shellfish Research 39: 67–76.
Kelaher, B.P., J.S. Levinton, and J.M. Hoch. 2003. Foraging by the mud snail, Ilyanassa obsoleta (Say), modulates spatial variation in benthic community structure. Journal of Experimental Marine Biology and Ecology 292: 139–157.
Kimbro, D.L., J.E. Byers, J.H. Grabowski, A.R. Hughes, and M.F. Piehler. 2014. The biogeography of trophic cascades on US oyster reefs. Ecology Letters 17: 845–854.
Kloskowski, J. 2018. Total non-consumptive effects of fish on Pelobates fuscus and Hyla orientalis tadpoles in pond enclosure experiments. Zoological Science 35: 528–534.
Lord, J.P., and R.B. Whitlatch. 2012. Inducible defenses in the eastern oyster Crassostrea virginica Gmelin in response to the presence of the predatory oyster drill Urosalpinx cinerea Say in Long Island Sound. Marine Biology 159: 1177–1182.
Moody, J., and D. Kreeger. 2020. Ribbed mussel (Geukensia demissa) filtration services are driven by seasonal temperature and site-specific seston variability. Journal of Experimental Marine Biology and Ecology 522: 151237.
Murphy, A.E., R. Kolkmeyer, B. Song, I.C. Anderson, and J. Bowen. 2019. Bioreactivity and microbiome of biodeposits from filter-feeding bivalves. Microbial Ecology 77: 343–357.
Naddafi, R., and L.G. Rudstam. 2013. Predator-induced behavioural defences in two competitive invasive species: the zebra mussel and the quagga mussel. Animal Behaviour 86: 1275–1284.
Peckarsky, B.L., P.A. Abrams, D.I. Bolnick, L.M. Dill, J.H. Grabowski, B. Luttbeg, J.L. Orrock, S.D. Peacor, E.L. Preisser, O.J. Schmitz, and G.C. Trussell. 2008. Revisiting the classics: considering nonconsumptive effects in textbook examples of predator-prey interactions. Ecology 89: 2416–2425.
Peers, M.J., Y.N. Majchrzak, E. Neilson, C.T. Lamb, A. Hämäläinen, J.A. Haines, L. Garland, D. Doran-Myers, K. Broadley, R. Boonstra, and S. Boutin. 2018. Quantifying fear effects on prey demography in nature. Ecology 99: 1716–1723.
Preisser, E.L., D.I. Bolnick, and M.F. Benard. 2005. Scared to death? The effects of intimidation and consumption in predator–prey interactions. Ecology 86: 501–509.
Preisser, E.L., J.L. Orrock, and O.J. Schmitz. 2007. Predator hunting mode and habitat domain alter nonconsumptive effects in predator-prey interactions. Ecology 88: 2744–2751.
Premo, K.M., and A.C. Tyler. 2013. Threat of predation alters the ability of benthic invertebrates to modify sediment biogeochemistry and benthic microalgal abundance. Marine Ecology Progress Series 494: 29–39.
R Core Team. 2017. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.https://www.R-project.org/.
Robson, A., R. Wilson, and C.G. de Leaniz. 2007. Mussels flexing their muscles: a new method for quantifying bivalve behaviour. Marine Biology 151: 1195–1204.
Scherer, A.E., and D.L. Smee. 2016. A review of predator diet effects on prey defensive responses. Chemoecology 26: 83–100.
Scherer, A.E., M.M. Garcia, and D.L. Smee. 2017. Predatory blue crabs induce stronger nonconsumptive effects in eastern oysters Crassostrea virginica than scavenging blue crabs. PeerJ 5: e3042.
Scherer, A.E., C.E. Bird, M.R. McCutcheon, X. Hu, and D.L. Smee. 2018. Two-tiered defense strategy may compensate for predator avoidance costs of an ecosystem engineer. Marine Biology 165: 131.
Seed, R. 1982. Predation of the ribbed mussel Geukensia demissa by the blue crab Callinectes sapidus. Netherlands Journal of Sea Research 16: 163–172.
Sheriff, M.J., S. Peacor, D. Hawlena, and M. Thaker. 2020. Non-consumptive predator effects on prey population size: a dearth of evidence. Journal of Animal Ecology.
Silliman, B.R., and M.D. Bertness. 2002. A trophic cascade regulates salt marsh primary production. Proceedings of the National Academy of Sciences 99: 10500–10505.
Silliman, B.R., and J.C. Zieman. 2001. Top-down control of Spartina alterniflora production by periwinkle grazing in a Virginia salt marsh. Ecology 82: 2830–2845.
Silliman, B.R., J. van de Koppel, M.D. Bertness, L.E. Stanton, and I.A. Mendelssohn. 2005. Drought, snails, and large-scale die-off of southern U.S. salt marshes. Science 310: 1803–1806.
Sitvarin, M.I., A.L. Rypstra, and J.D. Harwood. 2016. Linking the green and brown worlds through nonconsumptive predator effects. Oikos 125: 1057–1068.
Smee, D.L., and M.J. Weissburg. 2006. Hard clams (Mercenaria mercenaria) evaluate predation risk using chemical signals from predators and injured conspecifics. Journal of Chemical Ecology 32: 605–619.
Smith, L.D., and J.A. Jennings. 2000. Induced defensive responses by the bivalve Mytilus edulis to predators with different attack modes. Marine Biology 136: 461–469.
Tukey, J. 1949. Comparing individual means in the analysis of variance. Biometrics 5 (2): 99–114.
Weissburg, M., D.L. Smee, and M.C. Ferner. 2014. The sensory ecology of nonconsumptive predator effects. The American Naturalist 184: 141–157.
Wickham, H. 2007. Reshaping data with the reshape package. Journal of Statistical Software 21: 1–20.
Wickham, H. 2009. ggplot2: Elegant graphics for data analysis. Springer-Verlag New York.
Wilson, C.D., G. Arnott, and R.W. Elwood. 2012. Freshwater pearl mussels show plasticity of responses to different predation risks but also show consistent individual differences in responsiveness. Behavioural Processes 89: 299–303.
Winter, C., and K. Walters. 2019. Predation effects on mid-marsh ribbed mussel mortality, cluster size, and facilitation of cordgrass growth. Honors Theses, December. 361. https://digitalcommons.coastal.edu/honors-theses/361
Zhu, J., C. Zarnoch, J.S. Gosnell, M. Alldred, and T. Hoellein. 2019. Ribbed mussels Geukensia demissa enhance nitrogen-removal services but not plant growth in restored eutrophic salt marshes. Marine Ecology Progress Series 631: 67–80.
Zuur, A., E.N. Ieno, N. Walker, A.A. Saveliev, and G.M. Smith. 2009. Mixed effects models and extensions in ecology with R. New York: Springer.
Zuur, A.F., E.N. Ieno, and C.S. Elphick. 2010. A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution 1: 3–14.
We would like to thank the staff at The River Project Wetlab for sharing their laboratory space. We would also like to thank undergraduates from the Brooklyn Urban Ecology and Environment Program (Lorel Shaw and Valerie Kim), Baruch College undergraduates from the Gosnell Lab (Victor Siev, Brian Law, and Caroline Wojtowicz), and high school students (Liza Konopleva) from the Baruch College Now Program (Melissa Celik, Almedina Mulic, Brian Yeung, and Jun Qing Zhang) who helped with the data collection and sample processing.
This study was financially supported by the Science Resilience Institute at Jamaica Bay (Brooklyn, New York).
Communicated by Judy Grassle
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Zhu, J., Gosnell, J.S. Ribbed Mussels Continue to Feed and Biodeposit in the Presence of Injured Conspecifics and Predators. Estuaries and Coasts 44, 875–882 (2021). https://doi.org/10.1007/s12237-020-00794-1
- Geukensia demissa
- Non-consumptive effects
- Ribbed mussels
- Salt marsh