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Drought alters the trophic role of an opportunistic generalist in an aquatic ecosystem

  • Sarah L. AmundrudEmail author
  • Sarina A. Clay-Smith
  • Bret L. Flynn
  • Kathleen E. Higgins
  • Megan S. Reich
  • Derek R. H. Wiens
  • Diane S. Srivastava
Community ecology – original research


Abiotic change can alter species interactions by modifying species’ trophic roles, but this has not been well studied. Until now, bromeliad-dwelling tipulid larvae were thought to positively affect other macroinvertebrates via a facilitative processing chain. However, under drought, we found the opposite. We performed two microcosm experiments in which we factorially manipulated water level and predation by tipulids, and measured the effects on mosquito and chironomid larvae. The experiments differed in whether high water was contrasted with low or no water, allowing us to distinguish between the effects of desiccation stress (no water) and increased encounter rates due to compression of habitat or reductions in prey mobility (low and no water). We also included a caged tipulid treatment to measure any non-consumptive effects. As well as directly reducing prey survival, reductions in water level indirectly decreased chironomid and mosquito survival by altering the trophic role of tipulids. Our results suggest that increased encounter rates with prey led to tipulids becoming predatory under simulated drought, as tipulids consumed prey under both low and no water. When water level was high, tipulids exerted negative non-consumptive effects on prey survival. Because opportunistic predators are common throughout aquatic ecosystems, the effects of drought on the trophic roles of species may be widespread. Such restructuring of food webs should be considered when attempting to predict the ecological effects of environmental change.


Insects Microcosm experiment Precipitation Tank bromeliad Trophic plasticity 



We thank the Monteverde Cloud Forest Reserve, the Children’s Eternal Rain Forest Reserve, and the University of Georgia (Costa Rica Campus) for providing us with collection sites and offering logistical support. Thank you to Nestor Guevara and Randall Zamora Castro for helping with field work, and to Bill Haber, Alan Pounds, Frank Joyce, and Mary and Elias Newswanger for advice and logistical support. Comments from Rachel Germain, Angie Nicolas, and Natalie Westwood improved this manuscript. Funding was provided by a Natural Sciences and Engineering Research Council of Canada (NSERC) CGS-D Grant and a NSERC MSFSS Grant to S. L. Amundrud, a NSERC Discovery Grant to D. S. Srivastava, and by the Agence Nationale de la Recherche (ANR) through the Rainwebs project to Régis Céréghino, Céline Leroy, Bruno Corbara, Jean-François Carrias and D. S. Srivastava. All work was performed under MINAE research permits (034-2015-INV-ACAT and 041-2016-INV-ACAT). This is a publication of the Bromeliad Working Group.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

All applicable institutional and/or national guidelines for the care and use of animals were followed.

Data availability

Data are available from the KNB Digital Repository:

Supplementary material

442_2019_4343_MOESM1_ESM.docx (85 kb)
Supplementary material 1 (DOCX 84 kb)


  1. Amundrud SL, Srivastava DS (2015) Drought sensitivity predicts habitat size sensitivity in an aquatic ecosystem. Ecology 96:1957–1965. CrossRefGoogle Scholar
  2. Amundrud SL, Srivastava DS (2016) Trophic interactions determine the effects of drought on an aquatic ecosystem. Ecology 97:1475–1483. CrossRefGoogle Scholar
  3. Amundrud SL, Srivastava DS (2019) Data from: drought alters the trophic role of an opportunistic generalist in an aquatic ecosystem, Oecologia. Knowl Netw Biocomplex 1:4. Google Scholar
  4. Ancona S, Calixto-Albarrán I, Drummond H (2012) Effect of El Niño on the diet of a specialist seabird, Sula nebouxii, in the warm eastern tropical Pacific. Mar Ecol Prog Ser 462:261–271. CrossRefGoogle Scholar
  5. Baker RL, Ball SL (1995) Microhabitat selection by larval Chironomus tentans (Diptera: Chironomidae): effects of predators, food, cover and light. Freshw Biol 34:101–106. CrossRefGoogle Scholar
  6. Blois JL, Zarnetske PL, Fitzpatrick MC, Finnegan S (2013) Climate change and the past, present, and future of biotic interactions. Science (80–) 341:499–504. CrossRefGoogle Scholar
  7. Boukal DS (2014) Trait- and size-based descriptions of trophic links in freshwater food webs: current status and perspectives. J Limnol 73:171–185. CrossRefGoogle Scholar
  8. Boyd PW, Cornwall CE, Davison A et al (2016) Biological responses to environmental heterogeneity under future ocean conditions. Glob Chang Biol 22:2633–2650. CrossRefGoogle Scholar
  9. Brackenbury J (2000) Locomotory modes in the larva and pupa of Chironomus plumosus (Diptera, Chironomidae). J Insect Physiol 46:1517–1527. CrossRefGoogle Scholar
  10. Brackenbury J (2001) Locomotion through use of the mouth brushes in the larva of Culex pipiens (Diptera: Culicidae). Proc R Soc B Biol Sci 268:101–106. CrossRefGoogle Scholar
  11. Cargill A, Cummins K, Hanson B, Lowry R (1985) The role of lipids as feeding stimulants for shreeding aquatic insects. Freshw Biol 15:455–464. CrossRefGoogle Scholar
  12. Carnicer J, Abrams PA, Jordano P (2008) Switching behavior, coexistence and diversification: comparing empirical community-wide evidence with theoretical predictions. Ecol Lett 11:802–808. CrossRefGoogle Scholar
  13. Chase JM, Knight TM (2003) Drought-induced mosquito outbreaks in wetlands. Ecol Lett 6:1017–1024. CrossRefGoogle Scholar
  14. Christophers R (1960) Aëdes aegypti (L.), the yellow fever mosquito: its life history, bionomics and structure. Cambridge University Press, New YorkGoogle Scholar
  15. Coll M, Hughes L (2008) Effects of elevated CO2 on an insect omnivore: a test for nutritional effects mediated by host plants and prey. Agric Ecosyst Environ 123:271–279. CrossRefGoogle Scholar
  16. de Barros FC, de Carvalho JE, Abe AS, Kohlsdorf T (2010) Fight versus flight: the interaction of temperature and body size determines antipredator behaviour in tegu lizards. Anim Behav 79:83–88. CrossRefGoogle Scholar
  17. Dell AI, Pawar S, Savage VM (2014) Temperature dependence of trophic interactions are driven by asymmetry of species responses and foraging strategy. J Anim Ecol 83:70–84. CrossRefGoogle Scholar
  18. Dudgeon D (1993) The effects of spate-induced disturbance, predation and environmental complexity on macroinvertebrates in a tropical stream. Freshw Biol 30:189–197. CrossRefGoogle Scholar
  19. Gestoso I, Arenas F, Olabarria C (2015) Feeding behaviour of an intertidal snail: does past environmental stress affect predator choices and prey vulnerability? J Sea Res 97:66–74. CrossRefGoogle Scholar
  20. Gormezano LJ, Rockwell RF (2013) What to eat now? Shifts in polar bear diet during the ice-free season in western Hudson Bay. Ecol Evol 3:3509–3523. Google Scholar
  21. Grémillet D, Fort J, Amélineau F et al (2015) Arctic warming: nonlinear impacts of sea-ice and glacier melt on seabird foraging. Glob Chang Biol 21:1116–1123. CrossRefGoogle Scholar
  22. 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. CrossRefGoogle Scholar
  23. Holt RD, Polis GA (1997) A theoretical framework for intraguild predation. Am Nat 149:745–764. CrossRefGoogle Scholar
  24. Humphries MM, Studd EK, Menzies AK, Boutin S (2017) To everything there is a season: summer-to-winter food webs and the functional traits of keystone species. Integr Comp Biol 57:961–976. CrossRefGoogle Scholar
  25. Karmalkar AV, Bradley RS, Diaz HF (2008) Climate change scenario for Costa Rican montane forests. Geophys Res Lett 35:L11702. CrossRefGoogle Scholar
  26. Kratina P, LeCraw RM, Ingram T, Anholt BR (2012) Stability and persistence of food webs with omnivory: is there a general pattern? Ecosphere 3:50. CrossRefGoogle Scholar
  27. Kruse PD, Toft S, Sunderland KD (2008) Temperature and prey capture: opposite relationships in two predator taxa. Ecol Entomol 33:305–312. CrossRefGoogle Scholar
  28. Ledger ME, Edwards FK, Brown LE et al (2011) Impact of simulated drought on ecosystem biomass production: an experimental test in stream mesocosms. Glob Chang Biol 17:2288–2297. CrossRefGoogle Scholar
  29. Ledger ME, Harris RML, Armitage PD, Milner AM (2012) Climate change impacts on community resilience: evidence from a drought disturbance experiment. Adv Ecol Res 46:211–258. CrossRefGoogle Scholar
  30. Ledger ME, Brown LE, Edwards FK et al (2013a) Extreme climatic events alter aquatic food webs. A synthesis of evidence from a mesocosm drought experiment. Adv Ecol Res 48:343–395. CrossRefGoogle Scholar
  31. Ledger ME, Brown LE, Edwards FK et al (2013b) Drought alters the structure and functioning of complex food webs. Nat Clim Chang 3:223–227. CrossRefGoogle Scholar
  32. Lemoine NP (2017) Predation risk reverses the potential effects of warming on plant–herbivore interactions by altering the relative strengths of trait- and density-mediated interactions. Am Nat 190:337–349. CrossRefGoogle Scholar
  33. MacAvoy SE, Braciszewski A, Tengi E, Fong DW (2016) Trophic plasticity among spring vs. cave populations of Gammarus minus: examining functional niches using stable isotopes and C/N ratios. Ecol Res 31:589–595. CrossRefGoogle Scholar
  34. Macchiusi F, Baker RL (1992) Effects of predators and food availability on activity and growth of Chironomus tentans (Chironomidae, Diptera). Freshw Biol 28:207–216CrossRefGoogle Scholar
  35. Magoulick DD, Kobza RM (2003) The role of refugia for fishes during drought: a review and synthesis. Fres 48:1186–1198. CrossRefGoogle Scholar
  36. Marino NAC, Srivastava DS, MacDonald AAM et al (2017) Rainfall and hydrological stability alter the impact of top predators on food web structure and function. Glob Chang Biol 23:673–685. CrossRefGoogle Scholar
  37. Martin MM, Martin JS, Kukor JJ, Merritt RW (1980) The digestion of protein and carbohydrate by the stream detritivore, Tipula abdominalis (Diptera, Tipulidae). Oecologia 46:360–364. CrossRefGoogle Scholar
  38. McCluney KE (2017) Implications of animal water balance for terrestrial food webs. Curr Opin Insect Sci 23:13–21. CrossRefGoogle Scholar
  39. McCluney KE, Sabo JL (2009) Water availability directly determines per capita consumption at two trophic levels. Ecology 90:1463–1469. CrossRefGoogle Scholar
  40. McGill BJ, Mittelbach GC (2006) An allometric vision and motion model to predict prey encounter rates. Evol Ecol Res 8:691–701Google Scholar
  41. McHugh PA, Thompson RM, Greig HS et al (2015) Habitat size influences food web structure in drying streams. Ecography (Cop) 38:700–712. CrossRefGoogle Scholar
  42. McMeans BC, McCann KS, Humphries M et al (2015) Food web structure in temporally-forced ecosystems. Trends Ecol Evol 30:662–672. CrossRefGoogle Scholar
  43. Merritt RW, Cummins KW (1995) Habitat, life history, and behavioral adaptations of aquatic insects. In: Merritt RW, Cummins KW (eds) An introduction to the aquatic insects of North America, 3rd edn. Kendall Hunt Pub Co, Dubuque, pp 41–73Google Scholar
  44. O’Connor MI (2009) Warming strengthens an herbivore–plant interaction. Ecology 90:388–398. CrossRefGoogle Scholar
  45. Petchey OL, Brose U, Rall BC (2010) Predicting the effects of temperature on food web connectance. Philos Trans R Soc B Biol Sci 365:2081–2091. CrossRefGoogle Scholar
  46. Pimm SL, Lawton JH (1978) On feeding on more than one trophic level. Nature 275:542–544CrossRefGoogle Scholar
  47. Pires APF, Marino NAC, Srivastava DS, Farjalla VF (2016) Predicted rainfall changes disrupt trophic interactions in a tropical aquatic ecosystem. Ecology 97:2750–2759. CrossRefGoogle Scholar
  48. Power ME (1992) Top-down and bottom-up forces in food webs: do plants have primacy. Ecology 73:733–746CrossRefGoogle Scholar
  49. Preisser EL, Bolnick DI, Benard MF (2005) Scared to death? The effects of intimidation and consumption in predator-pery interactions. Ecology 86:501–509. CrossRefGoogle Scholar
  50. Pritchard G (1985) On the locomotion of cranefly larvae (Tipulidae; Tipulinae). J Kansas Entomol Soc 58:152–156Google Scholar
  51. Prudhomme C, Giuntoli I, Robinson EL et al (2014) Hydrological droughts in the 21st century, hotspots and uncertainties from a global multimodel ensemble experiment. Proc Natl Acad Sci USA 111:3262–3267. CrossRefGoogle Scholar
  52. R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Retrieved from
  53. Rall BC, Vucic-Pestic O, Ehens RB et al (2010) Temperature, predator–prey interaction strength and population stability. Glob Chang Biol 16:2145–2157. CrossRefGoogle Scholar
  54. Schmitz OJ, Rosenblatt AE, Smylie M (2016) Temperature dependence of predation stress and the nutritional ecology of a generalist herbivore. Ecology 97:3119–3130. CrossRefGoogle Scholar
  55. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675. CrossRefGoogle Scholar
  56. Schoenfeld D (1980) Chi squared goodness-of-fit tests for the proportional hazards regression model. Biometrika 67:145–153CrossRefGoogle Scholar
  57. Sentis A, Hemptinne JL, Brodeur J (2014) Towards a mechanistic understanding of temperature and enrichment effects on species interaction strength, omnivory and food-web structure. Ecol Lett 17:785–793. CrossRefGoogle Scholar
  58. Srivastava DS, Bell T (2009) Reducing horizontal and vertical diversity in a foodweb triggers extinctions and impacts functions. Ecol Lett 12:1016–1028. CrossRefGoogle Scholar
  59. Start D, Kirk D, Shea D, Gilbert B (2017) Cannibalism by damselflies increases with rising temperature. Biol Lett 13:20170175. CrossRefGoogle Scholar
  60. Starzomski BM, Suen D, Srivastava DS (2010) Predation and facilitation determine chironomid emergence in a bromeliad-insect food web. Ecol Entomol 35:53–60. CrossRefGoogle Scholar
  61. Suttle AKB, Thomsen MA, Power ME (2007) Species interactions reverse grassland responses to changing climate. Science (80–) 315:640–642. CrossRefGoogle Scholar
  62. Terry MT (2015) coxme: mixed effects cox modelsGoogle Scholar
  63. Törnroos A, Nordström MC, Aarnio K, Bonsdorff E (2015) Environmental context and trophic trait plasticity in a key species, the tellinid clam Macoma balthica L. J Exp Mar Bio Ecol 472:32–40. CrossRefGoogle Scholar
  64. 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. CrossRefGoogle Scholar
  65. Tunney TD, McCann KS, Lester NP, Shuter BJ (2012) Food web expansion and contraction in response to changing environmental conditions. Nat Commun 3:1105–1109. CrossRefGoogle Scholar
  66. Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Global change and species interactions in terrestrial ecosystems. Ecol Lett 11:1351–1363. CrossRefGoogle Scholar
  67. van Uitregt VO, Hurst TP, Wilson RS (2013) Greater costs of inducible behavioural defences at cooler temperatures in larvae of the mosquito, Aedes notoscriptus. Evol Ecol 27:13–26. CrossRefGoogle Scholar
  68. Vázquez DP, Gianoli E, Morris WF, Bozinovic F (2017) Ecological and evolutionary impacts of changing climatic variability. Biol Rev 92:22–42. CrossRefGoogle Scholar
  69. Vucic-Pestic O, Ehnes RB, Rall BC, Brose U (2011) Warming up the system: higher predator feeding rates but lower energetic efficiencies. Glob Chang Biol 17:1301–1310. CrossRefGoogle Scholar
  70. Winder M, Schindler DE (2004) Climatic effects on the phenology of lake processes. Glob Chang Biol 10:1844–1856. CrossRefGoogle Scholar
  71. Wolkovich EM, Cook BI, Allen JM et al (2012) Warming experiments underpredict plant phenological responses to climate change. Nature 485:494–497. CrossRefGoogle Scholar
  72. Woodward G, Hildrew AG (2001) Invasion of a stream food web by a new top predator. J Anim Ecol 70:273–288. CrossRefGoogle Scholar
  73. Yanoviak SP (1999) Community ecology of water-filled tree holes in Panama. PhD Diss. Graduate College, University of OklahomaGoogle Scholar
  74. Zotz G, Thomas V (1999) How much water is in the tank? Model calculations for two epiphytic bromeliads. Ann Bot 83:183–192. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Zoology, Biodiversity Research CentreUniversity of British ColumbiaVancouverCanada

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