, Volume 175, Issue 1, pp 353–361 | Cite as

Competitive displacement alters top-down effects on carbon dioxide concentrations in a freshwater ecosystem

  • Trisha B. Atwood
  • Edd Hammill
  • Diane S. Srivastava
  • John S. Richardson
Ecosystem ecology - Original research


Climate change and invasive species have the potential to alter species diversity, creating novel species interactions. Interspecific competition and facilitation between predators may either enhance or dampen trophic cascades, ultimately influencing total predator effects on communities and biogeochemical cycling of ecosystems. However, previous studies have only investigated the effects of a single predator species on CO2 flux of aquatic ecosystems. In this study, we measured and compared the individual and joint effects of predatory damselfly larvae and diving beetles on total prey biomass, leaf litter processing, and dissolved CO2 concentrations of experimental bromeliad ecosystems. Damselfly larvae created strong trophic cascades that reduced CO2 concentrations by ~46 % relative to no-predator treatments. Conversely, the effects of diving beetles on prey biomass, leaf litter processing, and dissolved CO2 were not statistically different to no-predator treatments. Relative to multiplicative null models, the presence of damselfly larvae and diving beetles together resulted in antagonistic relations that eliminated trophic cascades and top-down influences on CO2 concentrations. Furthermore, we showed that the antagonistic interactions between predators occurred due to a tactile response that culminated in competitive displacement of damselfly larvae. Our results demonstrate that predator identity and predator–predator interactions can influence CO2 concentrations of an aquatic ecosystem. We suggest that predator effects on CO2 fluxes may depend on the particular predator species removed or added to the ecosystem and their interactions with other predators.


Bromeliads Carbon dioxide saturation Multiple-predator effects Interference competition Trophic cascades 



We would like to thank J. C. R. Conner, P. Corvalan, B. Gilbert, K. R. Kirby, J. T. Ngai, A. J. D. Pelletier, and J. Peterman for data on diving beetle densities. This research was funded by Natural Sciences and Engineering Research Council (Canada) grants to D. S. S. and J. S. R.

Conflict of interest

The authors declare that they have no competing financial interests. All experiments performed conformed to the laws and regulations of both Canada and Costa Rica.


  1. Altshuler DL (2006) Flight performance and competitive displacement of hummingbirds across elevational gradients. Am Nat 167:216–229. doi: 10.1086/498622 PubMedCrossRefGoogle Scholar
  2. Atwood TB, Hammill E, Greig HS et al (2013) Predator-induced reduction of freshwater carbon dioxide emissions. Nat Geosci 6:191–194. doi: 10.1038/ngeo1734 CrossRefGoogle Scholar
  3. Baker RL (1983) Spacing behaviour by larval Ischnura cervula Selys: effects of hunger, previous interactions, and familiarity with an area (Zygoptera: Coenagrionidae). Odonatologica 12:201–207Google Scholar
  4. Bhola N, Ogutu JO, Said MY et al (2012) The distribution of large herbivore hotspots in relation to environmental and anthropogenic correlates in the Mara region of Kenya. J Anim Ecol 81:1268–1287. doi: 10.1111/j.1365-2656.2012.02000.x PubMedCrossRefGoogle Scholar
  5. Cardinale BJ, Srivastava DS, Duffy JE et al (2006) Effects of biodiversity on the functioning of trophic groups and ecosystems. Nature 443:989–992. doi: 10.1038/nature05202 PubMedCrossRefGoogle Scholar
  6. Cardinale BJ, Duffy JE, Gonzalez A et al (2012) Biodiversity loss and its impact on humanity. Nature 486:59–67. doi: 10.1038/nature11148 PubMedCrossRefGoogle Scholar
  7. Casula P, Wilby A, Thomas MB (2006) Understanding biodiversity effects on prey in multi-enemy systems. Ecol Lett 9:995–1004. doi: 10.1111/j.1461-0248.2006.00945.x PubMedCrossRefGoogle Scholar
  8. Duffy JE (2002) Biodiversity and ecosystem function: the consumer connection. Oikos 99:201–219. doi: 10.1034/j.1600-0706.2002.990201.x CrossRefGoogle Scholar
  9. Estes JA, Terborgh J, Brashares JS et al (2011) Trophic downgrading of planet Earth. Science 333:301–306. doi: 10.1126/science.1205106 PubMedCrossRefGoogle Scholar
  10. Fargione J, Brown CS, Tilman D (2004) Community assembly and invasion: an experimental test of neutral versus niche processes. Proc Natl Acad Sci USA 101:8916–8920Google Scholar
  11. Finke DL, Denno RF (2004) Predator diversity dampens trophic cascades. Nature 429:407–410. doi: 10.1038/nature02526.1 PubMedCrossRefGoogle Scholar
  12. Finke DL, Denno RF (2005) Predator diversity and the functioning of ecosystems: the role of intraguild predation in dampening trophic cascades. Ecol Lett 8:1299–1306. doi: 10.1111/j.1461-0248.2005.00832.x CrossRefGoogle Scholar
  13. Finke DL, Denno RF (2006) Spatial refuge from intraguild predation: implications for prey suppression and trophic cascades. Oecologia 149:265–275. doi: 10.1007/s00442-006-0443-y PubMedCrossRefGoogle Scholar
  14. Flanagan KM, McCauley E, Wrona F (2006) Freshwater food webs control carbon dioxide saturation through sedimentation. Glob Change Biol 12:644–651. doi: 10.1111/j.1365-2486.2006.01127.x CrossRefGoogle Scholar
  15. Frank JH, Lounibous LP (2010) Insects and allies associated with bromeliads: a review. Terr Arthropod Rev 1:1–23. doi: 10.1163/187498308X414742.Insects Google Scholar
  16. Greig HS, Kratina P, Thompson PL et al (2012) Warming, eutrophication, and predator loss amplify subsidies between aquatic and terrestrial ecosystems. Glob Change Biol 18:504–514. doi: 10.1111/j.1365-2486.2011.02540.x CrossRefGoogle Scholar
  17. Hart DR (2002) Intraguild predation, invertebrate predators, and trophic cascades in lake food webs. J Theor Biol 218:111–128. doi: 10.1006/yjtbi.3053 PubMedCrossRefGoogle Scholar
  18. Hobbs RJ, Higgs E, Harris JA (2009) Novel ecosystems: implications for conservation and restoration. Trends Ecol Evol 24:599–605. doi: 10.1016/j.tree.2009.05.012 PubMedCrossRefGoogle Scholar
  19. Honek A (1993) Intraspecific variation in body size and fecundity in insects: a general relationship. Oikos 66:483–492CrossRefGoogle Scholar
  20. Hudson F (2004) Sample preparation and calculations for dissolved gas analysis in water samples using a GC headspace equilibration technique. Method RSKSOP-175, US Environmental Protection Agency (EPA) Region 1: Ground Water and Ecosystems Restoration Division.
  21. Ives AR, Cardinale BJ, Snyder WE (2005) A synthesis of subdisciplines: predator–prey interactions, and biodiversity and ecosystem functioning. Ecol Lett 8:102–116. doi: 10.1111/j.1461-0248.2004.00698.x CrossRefGoogle Scholar
  22. Lavorel S, Garnier E (2002) Predicting changes in community composition and ecosystem functioning from plant traits : revisiting the Holy Grail. Funct Ecol 16:545–556CrossRefGoogle Scholar
  23. Leroux SJ, Hawlena D, Schmitz OJ (2012) Predation risk, stoichiometric plasticity and ecosystem elemental cycling. Proc R Soc B Biol Sci 279:4183–4191. doi: 10.1098/rspb.2012.1315 CrossRefGoogle Scholar
  24. Loreau M, Naeem S, Inchausti P et al (2001) Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294:804–808. doi: 10.1126/science.1064088 PubMedCrossRefGoogle Scholar
  25. Lurgi M, López BC, Montoya JM (2012) Novel communities from climate change. Philos Trans R Soc Ser B Biol Sci 367:2913–2922. doi: 10.1098/rstb.2012.0238 CrossRefGoogle Scholar
  26. Martinson GO, Werner FA, Scherber C et al (2010) Methane emissions from tank bromeliads in Neotropical forests. Nat Geosci 3:766–769. doi: 10.1038/ngeo980 CrossRefGoogle Scholar
  27. Mascaro J, Hughes RF, Schnitzer SA (2012) Novel forests maintain ecosystem processes after the decline of native tree species. Ecol Monogr 82:221–228CrossRefGoogle Scholar
  28. McPeek MA, Crowley PH (1987) The effects of density and relative size on the aggressive behaviour, movement and feeding of damselfly larvae (Odonata: Coenagrionidae). Anim Behav 35:1051–1061CrossRefGoogle Scholar
  29. Milazzo M, Mirto S, Domenici P, Gristina M (2013) Climate change exacerbates interspecific interactions in sympatric coastal fishes. J Anim Ecol 82:468–477. doi: 10.1111/j.1365-2656.2012.02034.x PubMedCrossRefGoogle Scholar
  30. Ngai JT, Srivastava DS (2006) Predators accelerate nutrient cycling in a bromeliad ecosystem. Science 314:963. doi: 10.1126/science.1132598 PubMedCrossRefGoogle Scholar
  31. Osakabe M, Hongo K, Funayama K, Osumi S (2006) Amensalism via webs causes unidirectional shifts of dominance in spider mite communities. Oecologia 150:496–505. doi: 10.1007/s00442-006-0560-7 PubMedCrossRefGoogle Scholar
  32. Otto SB, Berlow EL, Rank NE et al (2008) Predator diversity and identity drive interaction strength and trophic cascades in a food web. Ecology 89:134–144PubMedCrossRefGoogle Scholar
  33. Reitz SR, Trumble JT (2002) Competitive displacement among insects and arachnids. Annu Rev Entomol 47:435–465PubMedCrossRefGoogle Scholar
  34. Reznick DN, Ghalambor CK (2001) The population ecology of contemporary adaptations: what empirical studies reveal about the conditions that promote adaptive evolution. Genetica 112–113:183–198PubMedCrossRefGoogle Scholar
  35. Romero GQ, Srivastava DS (2010) Food-web composition affects cross-ecosystem interactions and subsidies. J Anim Ecol 79:1122–1131. doi: 10.1111/j.1365-2656.2010.01716.x PubMedCrossRefGoogle Scholar
  36. Runquist RB, Stanton ML (2013) Asymmetric and frequency-dependent pollinator-mediated interactions may influence competitive displacement in two vernal pool plants. Ecol Lett 16:183–190. doi: 10.1111/ele.12026 PubMedCrossRefGoogle Scholar
  37. Schindler DE, Carpenter SR, Cole JJ et al (1997) Influence of food web structure on carbon exchange between lakes and the atmosphere. Science 277:248–251CrossRefGoogle Scholar
  38. Schmitz OJ (2007) Predator diversity and trophic interactions. Ecology 88:2415–2426PubMedCrossRefGoogle Scholar
  39. Schmitz OJ (2008) Effects of predator hunting mode on grassland ecosystem function. Science 319:952–954. doi: 10.1126/science.1152355 PubMedCrossRefGoogle Scholar
  40. Schmitz OJ, Hambäck PA, Beckerman AP (2000) Trophic cascades in terrestrial systems: a review of the effects of carnivore removals on plants. Am Nat 155:141–153. doi: 10.1086/303311 PubMedCrossRefGoogle Scholar
  41. Shaffer LR, Robinson JV (1996) Do damselfly larvae recognize and differentially respond to distinct categories of macroinvertebrates? J Insect Behav 9:407–419. doi: 10.1007/BF02214019 CrossRefGoogle Scholar
  42. Shurin JB, Borer T, Seabloom EW et al (2002) A cross-ecosystem comparison of the strength of trophic cascades. Ecol Lett 5:785–791CrossRefGoogle Scholar
  43. Sih A, Englund G, Wooster D (1998) Emergent impacts of multiple predators on prey. Trends Ecol Evol 13:350–355PubMedCrossRefGoogle Scholar
  44. Sokolovska N, Rowe L, Johansson F (2000) Fitness and body size in mature odonates. Ecol Entomol 25:239–248CrossRefGoogle Scholar
  45. Soluk DA (1993) Multiple predator effects: predicting combined functional response of stream fish and invertebrates predators. Ecology 74:219–225CrossRefGoogle Scholar
  46. Soluk DA, Collins NC (1988) Synergistic interactions between fish and stoneflies: facilitation and interference among stream predators. Oikos 52:94–100CrossRefGoogle Scholar
  47. Soluk DA, Richardson JS (1997) The role of stoneflies in enhancing growth of trout: a test of the importance of predator–predator facilitation within a stream community. Oikos 80:214–219CrossRefGoogle Scholar
  48. Srivastava DS (2006) Habitat structure, trophic structure and ecosystem function: interactive effects in a bromeliad-insect community. Oecologia 149:493–504. doi: 10.1007/s00442-006-0467-3 PubMedCrossRefGoogle Scholar
  49. Starzomski BM, Suen D, Srivastava DS (2010) Predation and facilitation determine chironomid emergence in a bromeliad-insect food web. Ecol Entomol 35:53–60. doi: 10.1111/j.1365-2311.2009.01155.x CrossRefGoogle Scholar
  50. Steffan SA, Snyder WE (2010) Cascading diversity effects transmitted exclusively by behavioral interactions. Ecology 91:2242–2252PubMedCrossRefGoogle Scholar
  51. Vermeij GJ (1994) The evolutionary interaction among species: selection, escalation, and coevolution. Annu Rev Ecol Syst 25:219–236CrossRefGoogle Scholar
  52. Vonesh JR, Osenberg CW (2003) Multi-predator effects across life-history stages: non-additivity of egg- and larval-stage predation in an African treefrog. Ecol Lett 6:503–508. doi: 10.1046/j.1461-0248.2003.00470.x CrossRefGoogle Scholar
  53. Wilmers CC, Estes JA, Edwards M et al (2012) Do trophic cascades affect the storage and flux of atmospheric carbon? An analysis of sea otters and kelp forests. Front Ecol Environ 10:409–415. doi: 10.1890/110176 CrossRefGoogle Scholar
  54. Woodcock BA, Heard MS (2011) Disentangling the effects of predator hunting mode and habitat domain on the top-down control of insect herbivores. J Anim Ecol 80:495–503. doi: 10.1111/j.1365-2656.2010.01790.x PubMedCrossRefGoogle Scholar
  55. Yang D, González-Bernal E, Greenlees M, Shine R (2012) Interactions between native and invasive gecko lizards in tropical Australia. Aust Ecol 37:592–599. doi: 10.1111/j.1442-9993.2011.02319.x CrossRefGoogle Scholar
  56. Zotz G, Thomas V (1999) How much water is in the tank? Model calculations for two epiphytic bromeliads. Ann Bot 83:183–192CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Trisha B. Atwood
    • 1
    • 2
  • Edd Hammill
    • 3
    • 4
  • Diane S. Srivastava
    • 3
  • John S. Richardson
    • 1
  1. 1.Department of Forest and Conservation SciencesUniversity of British ColumbiaVancouverCanada
  2. 2.Global Change InstituteUniversity of QueenslandSt LuciaAustralia
  3. 3.Department of Zoology and Biodiversity Research CentreUniversity of British ColumbiaVancouverCanada
  4. 4.School of the EnvironmentUniversity of Technology SydneyUltimoAustralia

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