Abstract
Predators can have dramatic effects on food web structure and ecosystem processes. However, the total effect of predators will be a combination of prey removal due to consumption and non-consumptive effects (NCEs) mediated through changes to prey behavioral, morphological, or life history traits induced to reduce predation risk. In this study, we examined how consumptive and NCEs alter community composition and ecosystem function using the aquatic ecosystem housed within tropical bromeliads. We allowed the recolonization of emptied bromeliads containing either no predators, caged predators (NCEs only), or uncaged predators (NCEs and consumptive effects) and recorded densities of all macro-invertebrates, microbial densities, and in situ CO2 concentrations after 30 days. We found that predators altered community composition and CO2 concentrations largely through NCEs. The magnitude of the effects of NCEs was substantial, contributing more than 50% of the total effects of predators on macro-invertebrate communities. The NCEs of predators were also strong enough to generate a trophic cascade, which significantly increased micro-organisms and ecosystem respiration, which led to increased in situ CO2 concentrations. The most likely mechanism behind the NCEs on macro-invertebrate density was detection of predator cues by ovipositing adult females, who actively choose to avoid bromeliads containing predators. Through this mechanism, predator NCEs modified community colonization, the structure of food webs, populations of lower trophic levels, and ecosystem processes performed by the community. We therefore propose that quantification of the relative strength of predator NCEs in natural ecosystems is critical for predicting the consequences of predator loss from the world’s ecosystems.




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Atwood T, Hammill E, Srivastava D, Richardson J. 2014. Competitive displacement alters top-down effects on carbon dioxide concentrations in a freshwater ecosystem. Oecologia 75:353–61.
Atwood TB, Hammill E, Grieg H, Kratina P, Shurin JB, Srivastava DS, Richardson JS. 2013. Predator-induced reduction of freshwater carbon dioxide emissions. Nat Geosci 6:191–4.
Berendonk TU, Bonsall MB. 2002. The phantom midge and a comparison of metapopulation structures. Ecology 83:116–28.
Borg I, Groenen P. 2005. Modern multidimensional scaling: theory and applications. New York: Springer.
Brodin T, Johansson F, Bergsten J. 2006. Predator related oviposition site selection of aquatic beetles (Hydroporus spp.) and effects on offspring life-history. Freshwater Biol 51:1277–85.
Cadotte MW, Carscadden K, Mirotchnick N. 2011. Beyond species: functional diversity and the maintenance of ecological processes and services. J Appl Ecol 48:1079–87.
Carpenter SR. 1996. Microcosm experiments have limited relevance for community and ecosystem ecology. Ecology 77:677–80.
Cole JJ, Prairie YT, Caraco NF, McDowell WH, Tranvik LJ, Striegl RG, Duarte CM, Kortelainen P, Downing JA, Middelburg JJ, Melack J. 2007. Plumbing the global carbon cycle: integrating inland waters into the terrestrial carbon budget. Ecosystems 10:171–84.
Del Giorgio PA, Cole JJ, Caraco NF, Peters RH. 1999. Linking planktonic biomass and metabolism to net gas fluxes in northern temperate lakes. Ecology 80:1422–31.
Eisenberg JNS, Washburn JO, Schreiber SJ. 2000. Generalist feeding behaviors of Aedes sierrensis larvae and their effects on protozoan populations. Ecology 81:921–35.
Forbes C, Hammill E. 2013. Fear in the dark? Community-level effects of non-lethal predators change with light regime. Oikos 122:1662–8.
Garpe KC, Yahya SAS, Lindahl U, Ohman MC. 2006. Long-term effects of the 1998 coral bleaching event on reef fish assemblages. Marine Ecol Progress Series 315:237–47.
Goffredi SK, Jang GE, Woodside WT, Ussler W. 2011. Bromeliad catchments as habitats for methanogenesis in tropical rainforest canopies. Front Microbiol 2:256.
Hammill E, Atwood TB, Corvalan P, Srivastava DS. 2015. Behavioural responses to predation may explain shifts in community structure. Freshwater Biol 60:125–35.
Hammill E, Beckerman AP. 2010. Reciprocity in predator-prey interactions: exposure to defended prey and predation risk affects intermediate predator life history and morphology. Oecologia 163:193–202.
Heard SB. 1994. Pitcher-plant midges and mosquitoes-a processing chain commensalism. Ecology 75:1647–60.
Hill JM, Weissburg MJ. 2013. Predator biomass determines the magnitude of non-consumptive effects (NCEs) in both laboratory and field environments. Oecologia 172:79–91.
Holm S. 1979. A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70.
Hooper DU, Adair EC, Cardinale BJ, Byrnes JEK, Hungate BA, Matulich KL, Gonzalez A, Duffy JE, Gamfeldt L, O’Connor MI. 2012. A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature 486:105–8.
Hope D, Dawson JJC, Cresser MS, Billett MF. 1995. A method for measuring free CO2 in upland streamwater using headspace analysis. J Hydrol 166:1–14.
Kneitel JM, Miller TE. 2002. Resource and top-predator regulation in the pitcher plant (Sarracenia purpurea) inquiline community. Ecology 83:680–8.
Kraus JM, Vonesh JR. 2010. Feedbacks between community assembly and habitat selection shape variation in local colonization. J Anim Ecol 79:795–802.
Martinson GO, Werner FA, Scherber C, Conrad R, Corre MD, Flessa H, Wolf K, Klose M, Gradstein SR, Veldkamp E. 2010. Methane emissions from tank bromeliads in neotropical forests. Nat Geosci 3:766–9.
Mowles SL, Rundle SD, Cotton PA. 2011. Susceptibility to predation affects trait-mediated indirect interactions by reversing interspecific competition. Plos One 6:e23068.
Ngai JT, Srivastava DS. 2006. Predators accelerate nutrient cycling in a bromeliad ecosystem. Science 314:963.
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Henry M, Stevens H, Wagner H. 2012. Vegan: Community Ecology Package. R package version 2.0-3.
Peacor SD, Pangle KL, Schiesari L, Werner EE. 2012. Scaling-up anti-predator phenotypic responses of prey: impacts over multiple generations in a complex aquatic community. Proc Royal Soc B 279:122–8.
Peacor SD, Werner EE. 2001. The contribution of trait-mediated indirect effects to the net effects of a predator. Proc Natl Acad Sci USA 98:3904–8.
Preisser EL, Orrock JL, Schmitz OJ. 2007. Predator hunting mode and habitat domain alter nonconsumptive effects in predator-prey interactions. Ecology 88:2744–51.
R Development Core Team. 2013. R: a language and environment for statistical computing. Computing RFfS editor. Vienna.
Resetarits WJ Jr, Binckley CA. 2009. Spatial contagion of predation risk affects colonization dynamics in experimental aquatic landscapes. Ecology 90:869–76.
Ribblett SG, Palmer MA, Coats DW. 2005. The importance of bacterivorous protists in the decomposition of stream leaf litter. Freshwater Biol 50:516–26.
Ripple WJ, Estes JA, Beschta RL, Wilmers CC, Ritchie EG, Hebblewhite M, Berger J, Elmhagen B, Letnic M, Nelson MP, Schmitz OJ, Smith DW, Wallach AD, Wirsing AJ. 2014. Status and ecological effects of the world’s largest carnivores. Science 343:151.
Schindler DE, Carpenter SR, Cole JJ, Kitchell JF, Pace ML. 1997. Influence of food web structure on carbon exchange between lakes and the atmosphere. Science 277:248–51.
Schmitz OJ, Beckerman AP, Obrien KM. 1997. Behaviorally mediated trophic cascades: effects of predation risk on food web interactions. Ecology 78:1388–99.
Schulze E-D, Mooney HA. 1994. Biodiversity and ecosystem function: with 22 tables. New York: Springer.
Srivastava DS. 2006. Habitat structure, trophic structure and ecosystem function: interactive effects in a bromeliad-insect community. Oecologia 149:493–504.
Srivastava DS, Bell T. 2009. Reducing horizontal and vertical diversity in a foodweb triggers extinctions and impacts functions. Ecol Lett 12:1016–28.
Srivastava DS, Kolasa J, Bengtsson J, Gonzalez A, Lawler SP, Miller TE, Munguia P, Romanuk T, Schneider DC, Trzcinski MK. 2004. Are natural microcosms useful model systems for ecology? Trends Ecol Evol 19:379–84.
Srivastava DS, Melnychuk MC, Ngai JT. 2005. Landscape variation in the larval density of a bromeliad-dwelling zygopteran, Mecistogaster modesta (Odonata: Pseudostigmatidae). Int J Odonatol 8:67–79.
Srivastava DS, Trzcinski MK, Richardson BA, Gilbert B. 2008. Why are predators more sensitive to habitat size than their prey? Insights from bromeliad insect food webs. Am Nat 172:761–71.
Strickland MS, Hawlena D, Reese A, Bradford MA, Schmitz OJ. 2013. Trophic cascade alters ecosystem carbon exchange. Proc Natl Acad Sci USA 110:11035–8.
Tollrian R, Harvell CD. 1999. The ecology and evolution of inducible defenses. Princeton: Princeton University Press.
Trussell GC, Ewanchuk PJ, Matassa CM. 2006a. The fear of being eaten reduces energy transfer in a simple food chain. Ecology 87:2979–84.
Trussell GC, Ewanchuk PJ, Matassa CM. 2006b. Habitat effects on the relative importance of trait- and density-mediated indirect interactions. Ecol Lett 9:1245–52.
Vonesh JR, Blaustein L. 2010. Predator-induced shifts in mosquito oviposition site selection: a meta-analysis and implications for vector control. Isr J Ecol Evol 56:263–79.
Vonesh JR, Kraus JM, Rosenberg JS, Chase JM. 2009. Predator effects on aquatic community assembly: disentangling the roles of habitat selection and post-colonization processes. Oikos 118:1219–29.
Werner EE, Anholt BR. 1996. Predator-induced behavioral indirect effects: Consequences to competitive interactions in anuran larvae. Ecology 77:157–69.
Young RG, Matthaei CD, Townsend CR. 2008. Organic matter breakdown and ecosystem metabolism: functional indicators for assessing river ecosystem health. J N Am Benthol Soc 27:605–25.
Acknowledgments
Permission to work in the Área de Conservación Guanacaste (ACG) was obtained from MINAE, the Costa Rican ministry for environment and energy. Particular thanks to Róger Blanco for assistance with administration and logistics. This work was funded through an NSERC E.W.R. Steacie Memorial Fellowship awarded to D.S.S. We thank Calixto Moraga and Petrona Rios for invaluable help in the field. We would like to also thank Oswald J. Schmitz, Wolf Mooij, and two anonymous reviewers for their insightful comments on earlier versions of this manuscript.
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E.H., T.B.A, and D.S.S. designed the study. The experiment was conducted in the field by E.H. and T.B.A. All authors contributed to the writing of the MS.
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Hammill, E., Atwood, T.B. & Srivastava, D.S. Predation Threat Alters Composition and Functioning of Bromeliad Ecosystems. Ecosystems 18, 857–866 (2015). https://doi.org/10.1007/s10021-015-9866-9
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DOI: https://doi.org/10.1007/s10021-015-9866-9


