Skip to main content

Advertisement

Log in

Linking trophic interactions to plasticity in thermal sensitivity of geographically separated populations of a herbivore

  • Original Paper
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

The ability of species to tolerate a warming climate has important implications for ecological functioning. Theory and empirical synthesis suggest species adapted to more thermally variable climates are more capable of acclimating to rising temperatures, and are therefore characterized by greater phenotypic plasticity, than species adapted to less thermally variable environments. But this pattern has not been extensively evaluated for populations within a species that may inhabit different parts of a thermal gradient. In addition, it remains unclear whether different populations with different thermal sensitivities will maintain the same functional ecological roles as thermal regimes shift. To address this question, we conducted a reciprocal transplant experiment using Melanoplus femurrubrum grasshopper populations from Connecticut and Vermont, USA. During summer, the Vermont site was 3 °C cooler on average with 1.5-fold greater temperature variation than the Connecticut site. We measured thermal sensitivity (metabolic rate Q10) of individuals from each population reared in home field and transplanted sites and the nature and strength of trophic interactions with grasses and goldenrod (Solidago). Both grasshopper populations exhibited plasticity, but Q10 of both populations at Vermont was 1.5-fold broader than populations at the Connecticut site. All grasshoppers had similar survivorship but not similar effects on plants, exhibiting stronger effects on grasses in their home fields relative to their transplanted sites. Only Vermont grasshoppers transplanted to Connecticut significantly impacted Solidago. The study shows populations may physiologically acclimate quickly under new thermal conditions, suggesting stronger tolerance to change than often presumed. But, thermal acclimatization may not translate into the maintenance of a species’ functional role. The work underscores the need to link analyses of physiological performance with ecological function to obtain a complete picture of climate change effects on communities.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Angilletta MJ, Wilson RS, Navas CA, James R (2003) Trade-offs and the evolution of thermal reaction norms. Trends Ecol Evol 18:234–240

    Article  Google Scholar 

  • Barton BT (2010) Climate warming and predation risk during herbivore ontogeny. Ecology 91:2811–2818

    Article  PubMed  Google Scholar 

  • Barton BT (2011) Local adaption to temperature conserves top–down control in a grassland food web. Proc R Soc B 278:3102–3107

    Article  PubMed  PubMed Central  Google Scholar 

  • Barton BT, Beckerman AP, Schmitz OJ (2009) Climate warming strengthens indirect interactions in an old-field food web. Ecology 90:2346–2351

    Article  PubMed  Google Scholar 

  • Belovsky GE, Slade JB (1986) Time budgets of grassland herbivores—body size similarities. Oecologia 70:53–62

    Article  Google Scholar 

  • Bijlsma R, Loeschcke V (2005) Environmental stress, adaptation and evolution: an overview. J Evol Biol 18:744–749

    Article  CAS  PubMed  Google Scholar 

  • Bradshaw WE, Holzapfel CM (2006) Evolutionary response to rapid climate change. Science 312:1477–1478

    Article  CAS  PubMed  Google Scholar 

  • Buckley LB, Nufio CR, Kingsolver JG (2014) Phenotypic clines, energy balances and ecological responses to climate change. J Anim Ecol 83:41–50

    Article  PubMed  Google Scholar 

  • Capinera J, Scott RD, Walker TJ (2004) Field guide to grasshoppers, katydids, and crickets of the United States. Cornell University Press, Ithaca

    Google Scholar 

  • Chappell MA (1983) Metabolism and thermoregulation in desert and montane grasshoppers. Oecologia 56:126–131

    Article  Google Scholar 

  • Chown SL, Gaston KJ, Robinson D (2004) Macrophysiology: large-scale patterns in physiological traits and their ecological implications. Funct Ecol 18:159–167

    Article  Google Scholar 

  • Chown SL, Slabber S, McGeoch MA, Janion C, Leinaas HP (2007) Phenotypic plasticity mediates climate change responses among invasive and indigenous arthropods. Proc R Soc B 274:2531–2537

    Article  PubMed  PubMed Central  Google Scholar 

  • Compton TJ, Rijkenberg MJA, Drent J, Piersma T (2007) Thermal tolerance ranges and climate variability: a comparison between bivalves from differing climates. J Exp Mar Biol Ecol 352:200–211

    Article  Google Scholar 

  • De Block M, Pauwels K, van den Broeck M, de Meester L, Stoks R (2013) Local genetic adaptation generates latitude-specific effects of warming on predator-prey interactions. Glob Change Biol 19:689–696

    Article  Google Scholar 

  • Deutsch CA, Tewksbury JJ, Huey RB, Sheldon KS, Ghalambor CK, Haak DC, Martin PR (2008) Impacts of climate warming on terrestrial ectotherms across latitude. Proc Natl Acad Sci 105:6668–6672

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gilman SE, Urban MC, Tewksbury JJ, Gilchrist GW, Holt RD (2011) A framework for community interactions under climate change. Trends Ecol Evol 25:325–331

    Article  Google Scholar 

  • Harrison JF, Fewell JH (1995) Thermal effects on feeding behavior and net energy intake in a grasshopper experiencing large diurnal fluctuations in body temperature. Physiol Zool 68:453–473

    Article  Google Scholar 

  • Harrison JF, Phillips JE, Gleeson TT (1991) Activity physiology of the two striped grasshopper, Melanoplus bivittatus: gas exchange, hemolymph acid-base status, lactate production, and the effect of temperature. Physiol Zool 64:451–472

    Article  Google Scholar 

  • Hawlena D, Schmitz OJ (2010) Physiological stress as a fundamental mechanism linking predation to ecosystem functioning. Am Nat 176:537–556

    Article  PubMed  Google Scholar 

  • Hawlena D, Hughes KM, Schmitz OJ (2011) Trophic trait plasticity in response to changes in resource availability and predation risk. Funct Ecol 25:1223–1231

    Article  Google Scholar 

  • Hoffman AN, Chown SL, Clusella-Trullas S (2013) Upper thermal limits in terrestrial ectotherms: how constrained are they? Funct Ecol 27:934–949

    Article  Google Scholar 

  • Huey RB, Kearney MR, Krockenberger A, Holtum JAM, Jess M, Williams SE (2012) Predicting organismal vulnerability to climate warming: roles of behaviour, physiology and adaptation. Philos Trans R Soc B 367:1665–1679

    Article  Google Scholar 

  • Kareiva PM, Kingsolver JG, Huey RB (1993) Biotic interactions and global change. Sinauer Associates, Sunderland

    Google Scholar 

  • Kordas RL, Harley GDG, O’Connor MI (2011) Community ecology in a warming world: the influence of temperature on interspecific interactions in marine systems. J Exp Mar Biol Ecol 400:218–226

    Article  Google Scholar 

  • Lake S, MacMillan HA, Williams CM, Sinclair BJ (2013) Static and dynamic approaches yield similar estimates of the thermal sensitivity of insect metabolism. J Insect Physiol 59:761–766

    Article  CAS  PubMed  Google Scholar 

  • Logan JA, Regniere J, Powell JA (2003) Assessing the impacts of global warming on forest pest dynamics. Front Ecol Environ 1:130–137

    Article  Google Scholar 

  • Mattassa CM, Trussell GC (2015) Effects of predation risk across a latitudinal temperature gradient. Oecologia 177:775–784

    Article  Google Scholar 

  • Merilä J, Hendry AP (2014) Climate change, adaptation, and phenotypic plasticity: the problem and the evidence. Evol Appl 7:1–14

    Article  PubMed  PubMed Central  Google Scholar 

  • Nespolo R, Lardies MA, Bozinovic F (2003) Intrapopulational variation in the standard metabolic rate of insects: repeatability, thermal dependence and sensitivity (Q10) of oxygen consumption in a cricket. J Exp Biol 206:4309–4315

    Article  CAS  PubMed  Google Scholar 

  • New England Regional Assessment Group (2001) Preparing for a changing climate: the potential consequences of climate variability and change. University of New Hampshire Press, Durham

    Google Scholar 

  • O’Connor MI (2009) Warming strengthens an herbivore-plant interaction. Ecology 90:388–398

    Article  PubMed  Google Scholar 

  • Parsons S, Joern A (2014) Life history traits associated with body size covary along a latitudinal gradient in a generalist grasshopper. Oecologia 174:379–391

    Article  PubMed  Google Scholar 

  • Pörtner HO, Farrell AP (2008) Physiology of climate change. Science 322:690–692

    Article  PubMed  Google Scholar 

  • Post E (2013) Ecology of climate change: the importance of biotic interactions. Princeton University Press, Princeton

    Book  Google Scholar 

  • Przybylo R, Sheldon BC, Merilä J (2000) Climatic effects on breeding and morphology: evidence for phenotypic plasticity. J Anim Ecol 69:395–403

    Article  Google Scholar 

  • Reed TE, Schindler DE, Waples RS (2010) Interacting effects of phenotypic plasticity and evolution on population persistence in a changing climate. Conserv Biol 25:56–63

    Article  Google Scholar 

  • Ritchie ME (2000) Nitrogen limitation and trophic versus abiotic influences on insect herbivores in a temperate grassland. Ecology 81:1601–1612

    Article  Google Scholar 

  • Rogowitz GL, Chappell MA (2000) Energy metabolism of eucalyptus-boring beetles at rest and during locomotion: gender makes a difference. J Exp Biol 203:1131–1139

    CAS  PubMed  Google Scholar 

  • Schmitz OJ (2003) Top predator control of plant biodiversity and productivity in an old-field ecosystem. Ecol Lett 6:156–163

    Article  Google Scholar 

  • Schmitz OJ (2004) From mesocosms to the field: the role and value of cage experiments in understanding top–down effects in ecosystems. In: Weisser WW, Siemann E (eds) Insects and ecosystem function. Springer, Berlin, pp 277–302

    Chapter  Google Scholar 

  • Schmitz OJ (2013) Global climate change and the evolutionary ecology of ecosystem functioning. Ann NY Acad Sci 1297:61–72

    PubMed  Google Scholar 

  • Schmitz OJ, Post E, Burns CE, Johnston KM (2003) Ecosystem responses to global climate change: moving beyond color-mapping. Bioscience 53:1199–1205

    Article  Google Scholar 

  • Sheldon KS, Yang S, Tewksbury JJ (2011) Climate change and community disassembly: impacts of warming on tropical and temperate montane community structure. Ecol Lett 14:1191–1200

    Article  PubMed  Google Scholar 

  • Skelly DK, Joseph LN, Possingham HP, Freidenburg LK, Farrugia TJ, Kinnison MT, Hendry AP (2007) Evolutionary responses to climate change. Conserv Biol 21:1353–1355

    Article  PubMed  Google Scholar 

  • Somero GN (2010) The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine “winners” and “losers”. J Exp Biol 213:912–920

    Article  CAS  PubMed  Google Scholar 

  • Sunday JM, Bates AE, Dulvey NK (2011) Global analysis of thermal tolerance and latitude in ectotherms. Proc R Soc B 278:1823–1830

    Article  PubMed  Google Scholar 

  • Traill LW, Lim MLM, Sodhi NS, Bradshaw CJA (2010) Mechanisms driving change: altered species interactions and ecosystem function through global warming. J Anim Ecol 79:937–947

    Article  PubMed  Google Scholar 

  • Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Global change and species interactions in terrestrial ecosystems. Ecol Lett 11:1351–1363

    Article  PubMed  Google Scholar 

  • Van der Putten WH, Macel M, Visser ME (2010) Predicting species distribution and abundance responses to climate change: why it is essential to include biotic interactions across trophic levels. Philos Trans R Soc B 365:2025–2034

    Article  Google Scholar 

  • Watt A, Whittaker JB, Docherty M, Brooks G, Lindsay E, Salt DT (1995) The impact of elevated atmospheric CO2 on insect herbivores. In: Harrington R, Stork ME (eds) Insects in a changing environment. Academic Press, San Diego, pp 197–217

    Google Scholar 

  • Whitman DW (1988) Function and evolution of thermoregulation in the desert grasshopper Taeniopoda eques. J Anim Ecol 57:369–383

    Article  Google Scholar 

  • Williams CM, Chick WD, Sinclair BJ (2015) A cross-seasonal perspective on local adaptation: metabolic plasticity mediates responses to winter in a thermal-generalist moth. Funct Ecol 29:549–561

    Article  Google Scholar 

  • Zavaleta E, Pasari J, Moore J, Hernandez D, Suttle KB, Wilmers CC (2009) Ecosystem response to community disassembly. Ann NY Acad Sci 1162:311–333

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

The study was supported by a Yale Climate and Energy Institute Postdoctoral Fellowship to AER; by funds from the Yale Forestry and Environmental Studies Schiff Fund and Sussman Fund, the Yale Institute for Biospheric Studies, and the Norcross Wildlife Fund to BTC; and by Funds provided by NSF Grant DEB-1354762 to OJS. We thank Lauren Smith, Colin Donihue, Max Lambert, Robert Buchkowski, Brandon Barton, and three anonymous reviewers for comments on an earlier draft. We also thank Yale-Myers Forest and Kevin Johnston for allowing us to conduct the experiment on their property.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Adam E. Rosenblatt.

Additional information

Adam E. Rosenblatt and Bryan T. Crowley have contributed equally to the work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rosenblatt, A.E., Crowley, B.T. & Schmitz, O.J. Linking trophic interactions to plasticity in thermal sensitivity of geographically separated populations of a herbivore. Evol Ecol 30, 649–661 (2016). https://doi.org/10.1007/s10682-016-9827-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-016-9827-6

Keywords

Navigation