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Density mediates grasshopper performance in response to temperature manipulation and spider predation in tallgrass prairie

Published online by Cambridge University Press:  05 October 2016

A.N. Laws*
Affiliation:
Division of Biology, Kansas State University, Manhattan, KS 66506, USA
A. Joern
Affiliation:
Division of Biology, Kansas State University, Manhattan, KS 66506, USA
*
*Author for correspondence E-mail: [email protected]

Abstract

Species interactions are often context-dependent, where outcomes require an understanding of influences among multiple biotic and abiotic factors. However, it remains unclear how abiotic factors such as temperature combine with important biotic factors such as density-dependent food limitation and predation to influence species interactions. Using a native grassland – grasshopper – wolf spider model food chain in tallgrass prairie, we conducted a manipulative field experiment to examine how predator–prey interactions respond to manipulations of temperature, grasshopper density, and food chain length. We find that grasshopper performance responses to temperature and predator treatments were density dependent. At high densities, grasshopper survival decreased with increased temperature when no spiders were present. When spiders were present, grasshopper survival was reduced, and this effect was strongest in the cooled treatment. In contrast, grasshopper survival did not vary significantly with spider presence or among temperature treatments at low grasshopper densities. Our results indicate that context-dependent species interactions are common and highlight the importance of understanding how and when key biotic and abiotic factors combine to influence species interactions.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2016 

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Footnotes

† Current address: Department of Biology and Biochemistry, University of Houston, Houston, TX 77004, USA.

References

REFERENCES

Agrawal, A.A., Ackerly, D.D., Adler, F., Arnold, E.A., Caceres, C., Doak, D.F., Post, E., Hudson, P.J., Maron, J., Mooney, K.A., Power, M.E., Schemske, D., Stachowicz, J., Strauss, S., Turner, M.G. & Werner, E.E. (2007) Filling key gaps in population and community ecology. Frontiers in Ecology and the Environment 5, 145152.CrossRefGoogle Scholar
Bale, J.S., Masters, G.J., Hodkinson, I.D., Awmack, C., Bezemer, T.M., Brown, V.K., Butterfield, J., Buse, A., Coulson, J.C., Farrar, J., Good, J.E.G., Harrington, R., Hartley, S., Jones, T.H., Lindroth, R.L., Press, M.C., Symrnioudis, I., Watt, A.D. & Whittaker, J.B. (2002) Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Global Change Biology 8, 116.Google Scholar
Barton, B.T. (2010) Climate warming and predation risk during herbivore ontogeny. Ecology 91, 28112818.Google Scholar
Barton, B.T. (2011) Local adaptation to temperature conserves top-down control in a grassland food web. Proceedings of the Royal Society B-Biological Sciences 278, 31023107.Google Scholar
Barton, B.T. & Ives, A.R. (2014) Direct and indirect effects of warming on aphids, their predators, and ant mutualists. Ecology 95, 14791484.Google Scholar
Barton, B.T. & Schmitz, O.J. (2009) Experimental warming transforms multiple predator effects in a grassland food web. Ecology Letters 12, 13171325.Google Scholar
Barton, B.T., Beckerman, A.P. & Schmitz, O.J. (2009) Climate warming strengthens indirect interactions in an old-field food web. Ecology 90, 23462351.Google Scholar
Belovsky, G.E. & Joern, A. (1995) The dominance of different regulating factors for rangeland grasshoppers. In Cappuccino, N. & Price, P. (Eds) Population Dynamics, pp. 359386. San Diego, CA, Academic Press, Inc.Google Scholar
Belovsky, G.E. & Slade, J.B. (1993) The role of vertebrate and invertebrate predators in a grasshopper community. Oikos 68, 193201.Google Scholar
Belovsky, G.E. & Slade, J.B. (1995) Dynamics of two Montana grasshopper populations: relationships among weather, food abundance and intraspecific competition. Oecologia 101, 383396.Google Scholar
Blair, J.M., Johnson, L.C. & Knapp, A.K. (2007) Fire-induced changes in soil nitrogen and carbon dynamics in tallgrass prairie. pp. 60–60 in Masters, R.E. & Galley, K.E.M. (Eds) 23rd Tall Timbers Fire Ecology Conference: Fire in Grassland and Shrubland Ecosystems, Tallahassee, FL.Google Scholar
Borcard, D., Gillet, F. & Legendre, P. (2011) Numerical Ecology with R. New York, NY, Springer-Verlag.Google Scholar
Cammell, M. & Knight, J. (1992) Effects of climate change on the population dynamics of crop pests. Advances in Ecological Research 22, 117162.Google Scholar
Chase, J.M. (1996) Abiotic controls of trophic cascades in a simple grassland food chain. Oikos 77, 495506.Google Scholar
Chown, S.L. & Nicolson, S.W. (2004) Insect Physiological Ecology: Mechanisms and Patterns. New York City, Oxford University Press.Google Scholar
Costa, Z.J. & Kishida, O. (2015) Nonadditive impacts of temperature and basal resource availability on predator-prey interactions and phenotypes. Oecologia 178, 12151225.Google Scholar
Danner, B.J. & Joern, A. (2003) Stage-specific behavioral responses of Ageneotettix deorum (Orthoptera: Acrididae) in the presence of Lycosid spider predators. Journal of Insect Behavior 16, 453464.Google Scholar
Deutsch, C.A., Tewksbury, J.J., Huey, R.B., Sheldon, K.S., Ghalambor, C.K., Haak, D.C. & Martin, P.R. (2008) Impacts of climate warming on terrestrial ectotherms across latitude. Proceedings of the National Academy of Sciences of the United States of America 105, 66686672.CrossRefGoogle ScholarPubMed
Guo, K., Hao, S.G., Sun, O.J. & Kang, L. (2009) Differential responses to warming and increased precipitation among three contrasting grasshopper species. Global Change Biology 15, 25392548.Google Scholar
Hale, R., Calosi, P., McNeill, L., Mieszkowska, N. & Widdicombe, S. (2011) Predicted levels of future ocean acidification and temperature rise could alter community structure and biodiversity in marine benthic communities. Oikos 120, 661674.Google Scholar
Harrison, J.F., Woods, H.A. & Roberts, S.P. (2012) Ecological and Environmental Physiology of Insects. Oxford, UK, Oxford University Press.Google Scholar
Hewitt, G.B. & Onsager, J.A. (1983) Control of grasshoppers on rangeland in the United States – A perspective. Journal of Range Management 36, 202207.Google Scholar
Joern, A. (2005) Disturbance by fire frequency and bison grazing modulate grasshopper assemblages in tallgrass prairie. Ecology 86, 861873.Google Scholar
Joern, A., Danner, B.J., Logan, J.D. & Wolesensky, W. (2006) Natural history of mass-action in predator-prey models: a case study from wolf spiders and grasshoppers. American Midland Naturalist 156, 5264.Google Scholar
Jonas, J.L. & Joern, A. (2007) Grasshopper (Orthoptera : Acrididae) communities respond to fire, bison grazing and weather in North American tallgrass prairie: a long-term study. Oecologia 153, 699711.Google Scholar
Kajak, A., Breymeyer, A. & Petal, J. (1971) Productivity investigation of two types of meadows in the Vistula Valley. XI. Predatory arthropods. Ekologica Polska 19, 223233.Google Scholar
Kishi, D., Murakami, M., Nakano, S. & Maekawa, K. (2005) Water temperature determines strength of top-down control in a stream food web. Freshwater Biology 50, 13151322.CrossRefGoogle Scholar
Kistner, E. & Belovsky, G.E. (2014) Host dynamics determine responses to disease: additive versus compensatory mortality in a grasshopper-pathogen system. Ecology 95, 25792588.Google Scholar
Knapp, A.K., Briggs, J.M., Hartnett, D.C. & Collins, S.L. (Eds) (1998) Grassland Dynamics: Long-Term Ecological Research in Tallgrass Prairie. New York, NY, Oxford University Press, Inc.Google Scholar
Kohler, G., Perner, J. & Schumacher, J. (1999) Grasshopper population dynamics and meteorological parameters – lessons from a case study. Ecography 22, 205212.Google Scholar
Kruse, P.D., Toft, S. & Sunderland, K.D. (2008) Temperature and prey capture: opposite relationships in two predator taxa. Ecological Entomology 33, 305312.Google Scholar
Lathlean, J.A., Ayre, D.J. & Minchinton, T.E. (2013) Temperature variability at the larval scale affects early survival and growth of an intertidal barnacle. Marine Ecology Progress Series 475, 155166.Google Scholar
Laws, A.N. & Belovsky, G.E. (2010) How will species respond to climate change? Examining the combined effects of temperature and population density on an herbivorous insect. Environmental Entomology 39, 312319.Google Scholar
Laws, A.N. & Joern, A. (2013) Predator-prey interactions in a grassland food chain vary with temperature and food quality. Oikos 122, 977986.Google Scholar
Laws, A.N. & Joern, A. (2015) Predator-prey interactions are context dependent in a grassland plant-grasshopper-wolf spider food chain. Environmental Entomology 44, 519528.Google Scholar
Li, D.Q. & Jackson, R.R. (1996) How temperature affects development and reproduction in spiders: a review. Journal of Thermal Biology 21, 245274.Google Scholar
Logan, J.D., Joern, A. & Wolesensky, W. (2002) Location, time, and temperature dependence of digestion in simple animal tracts. Journal of Theoretical Biology 216, 518.Google Scholar
Logan, J.D., Wolesensky, W. & Joern, A. (2006) Temperature-dependent phenology and predation in arthropod systems. Ecological Modelling 196, 471482.CrossRefGoogle Scholar
Logan, J.D., Wolesensky, W. & Joern, A. (2007 a) Insect development under predation risk, variable temperature, and variable food quality. Mathematical Biosciences and Engineering 4, 4765.Google Scholar
Logan, J.D., Wolesensky, W. & Joern, A. (2007 b) Risk, development and foraging in a variable temperature environment. Mathematical Biosciences and Engineering 4, 4765.Google Scholar
Manca, M. & DeMott, W.R. (2009) Response of the invertebrate predator Bythotrephes to a climate-linked increase in the duration of a refuge from fish predation. Limnology and Oceanography 54, 25062512.Google Scholar
Oedekoven, M.A. & Joern, A. (1998) Stage-based mortality of grassland grasshoppers (Acrididae) from wandering spider (Lycosidae) predation. Acta Oecologica-International Journal of Ecology 19, 507515.Google Scholar
Onsager, J.A. (2000) Suppression of grasshoppers in the Great Plains through grazing management. Journal of Range Management 53, 592602.CrossRefGoogle Scholar
Ovadia, O. & Schmitz, O.J. (2004) Weather variation and trophic interaction strength: sorting the signal from the noise. Oecologia 140, 398406.Google Scholar
Petchey, O.L. (2000) Prey diversity, prey composition, and predator population dynamics in experimental microcosms. Journal of Animal Ecology 69, 874882.Google Scholar
Ritchie, M.E. (1996) Interaction of temperature and resources in population dynamics: an experimental test of theory. pp. 639 in Floyd, R., Sheppard, A. & De Barro, P. (Eds) Frontiers of Population Ecology. Collingwood, CSIRO Publishing.Google Scholar
Ritchie, M.E. (2000) Nitrogen limitation and trophic vs. abiotic influences on insect herbivores in a temperate grassland. Ecology 81, 16011612.Google Scholar
Rothley, K.D. & Dutton, G. (2006) Behavioral responses to environmental change alter direct and indirect trait-mediated interactions. Canadian Journal of Zoology-Revue Canadienne De Zoologie 84, 10531058.Google Scholar
Sanford, E. (2002) Water temperature, predation, and the neglected role of physiological rate effects in rocky intertidal communities. Integrative and Comparative Biology 42, 881891.Google Scholar
Saska, P., Martinkova, Z. & Honek, A. (2010) Temperature and rate of seed consumption by ground beetles (Carabidae). Biological Control 52, 9195.Google Scholar
Schmitz, O.J. (1993) Trophic exploitation in grassland food chains: simple models and a field experiment. Oecologia 93, 327335.Google Scholar
Schmitz, O.J. (1997) Press perturbations and the predictability of ecological interactions in a food web. Ecology 78, 5569.Google Scholar
Schmitz, O.J. (1998) Direct and indirect effects of predation and predation risk in old-field interaction webs. American Naturalist 151, 327342.Google Scholar
Schmitz, O.J. (2008) Herbivory from individuals to ecosystems. Annual Review of Ecology Evolution and Systematics 39, 133152.Google Scholar
Schmitz, O.J. & Suttle, K.B. (2001) Effects of top predator species on direct and indirect interactions in a food web. Ecology 82, 20722081.Google Scholar
Schmitz, O.J., Beckerman, A.P. & O'Brien, K.M. (1997) Behaviorally mediated trophic cascades: effects of predation risk on food web interactions. Ecology 78, 13881399.Google Scholar
Sentis, A., Morisson, J. & Boukal, D.S. (2015) Thermal acclimation modulates the impacts of temperature and enrichment on trophic interaction strengths and population dynamics. Global Change Biology 21, 32903298.CrossRefGoogle ScholarPubMed
Towne, E.G. (2002) Vascular plants of Konza Prairie Biological Station: an annotated checklist of species in a Kansas tallgrass prairie. SIDA, Contributions to Botany 20, 269294.Google Scholar
Van der Putten, W.H., Macel, M. & Visser, M.E. (2010) Predicting species distribution and abundance responses to climate change: why it is essential to include biotic interactions across trophic levels. Philosophical Transactions of the Royal Society B-Biological Sciences 365, 20252034.CrossRefGoogle ScholarPubMed
Vangansbeke, D., Nguyen, D.T., Audenaert, J., Verhoeven, R., Gobin, B., Tirry, L. & De Clercq, P. (2015) Prey consumption by phytoseiid spider mite predators as affected by diurnal temperature variations. Biocontrol 60, 595603.Google Scholar
Wagner, A., Hulsmann, S., Horn, W., Schiller, T., Schulze, T., Volkmann, S. & Benndorf, J. (2013) Food-web-mediated effects of climate warming: consequences for the seasonal Daphnia dynamics. Freshwater Biology 58, 573587.Google Scholar
Walther, G.R. (2010) Community and ecosystem responses to recent climate change. Philosophical Transactions of the Royal Society B-Biological Sciences 365, 20192024.Google Scholar
Werner, E.E. & Peacor, S.D. (2003) A review of trait-mediated indirect interactions in ecological communities. Ecology 84, 10831100.Google Scholar
Willott, S.J. (1997) Thermoregulation in four species of British grasshoppers (Orthoptera : Acrididae). Functional Ecology 11, 705713.Google Scholar
Yang, Y.L. & Joern, A. (1994) Influence of diet quality, developmental stage, and temperature on food residence time in the grasshopper Melanoplus differentialis . Physiological Zoology 67, 598616.Google Scholar
Zvereva, E.L. & Kozlov, M.V. (2006) Consequences of simultaneous elevation of carbon dioxide and temperature for plant-herbivore interactions: a metaanalysis. Global Change Biology 12, 2741.Google Scholar