Consumptive effects and mismatch in predator–prey turnover rates cause inversion of biomass pyramids
- 122 Downloads
The mismatch between the turnover rates of predators and prey is one of the oldest explanations for the existence of inverted trophic pyramids. To date, the hypotheses regarding trophic pyramids have all been based on consumptive trophic links between predators and prey, and the relative contribution of non-consumptive effects is still unknown. In this study, we investigated if the inversion of pyramids in bromeliad ecosystems is driven by (i) a rapid colonization of organisms having short cohort interval production (CPI), and (ii) the prevalence of consumptive or non-consumptive effects of top predators. We used a manipulative experiment to investigate the patterns of prey colonization and to partition the net effects of the dominant predator (damselfly larvae) on biomass pyramids into consumptive (uncaged damselfly larvae) and non-consumptive effects (caged damselfly larvae). Consumptive effects of damselflies strengthened the inversion of trophic pyramids. Non-consumptive effects, however, did not affect the shape of biomass pyramids. Instead, the rapid colonization of organisms with predominantly short CPI sustained the large biomass of top predators found in natural bromeliad ecosystems. Prey colonized bromeliads rapidly, but this high production was never visible as standing stock because damselflies reduce prey densities by more than a magnitude through direct consumption. Our study adds to the growing evidence that there are a variety of possible ways that biomass can be trophically structured. Moreover, we suggest that the strength of biomass pyramids inversion may change with the time of ecological succession as prey communities become more equitable.
KeywordsApex predator Predator–prey ratio Macroinvertebrate Top-heavy pyramid Top–down control
The authors thank T. N. Bernabé, M. R. Braga, A. Degressi, C. Vieira, G. C. O. Piccoli, G. H. Migliorini, N. A. C. Marino for field assistance; the staff of the “Parque Estadual da Ilha do Cardoso” for the logistic support. P. M. de Omena received fellowship from São Paulo Research Foundation (FAPESP: 2009/51702-0), “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior” and Department of Foreign Affairs, Trade and Development Canada (CAPES-DFAIT: BEX 8377/12-0), and “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior” (PNPD-CAPES; 2014/04603-4). G. Q. Romero was supported by the “Conselho Nacional de Desenvolvimento Científico e Tecnológico” (CNPq) research grant, and D.S. Srivastava by Natural Science and Engineering Research Council (Canada) Discovery and Accelerator Grants. This study was also supported by CESAB-FRB as part of the activities of the FunctionalWebs Working Group.
Author contribution statement
PMO, DSS, GQR conceived the study. PMO performed the field experiment, insect identification and biomass estimations. PMO, DSS and GQR interpreted the data. PMO wrote the paper with the assistance of DSS and GQR.
All data analysed during this study are available as electronic supplementary material.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
All applicable institutional and/or national guidelines for care and use of animals were followed.
- Benke AC, Huryn AD (2007) Secondary production of macroinvertebrates. In: Hauer FR, Lamberti G (eds) Methods in stream ecology. Academic Press, Elsevier, pp 691–710Google Scholar
- Buskirk JV (2000) The costs of an inducible defense in anuran larvae. Ecology 10:2813–2821. https://doi.org/10.1890/0012-9658(2000)081%5b2813:tcoaid%5d2.0.co;2 CrossRefGoogle Scholar
- Del Giorgio PA, Cole JJ, Caraco NF, Peters RH (1999) Linking planktonic biomass and metabolism to net gas fluxes in northern temperate lakes. Ecology 80:1422–1424. https://doi.org/10.1890/0012-9658(1999)080%5b1422:lpbamt%5d2.0.co;2 CrossRefGoogle Scholar
- Downes S (2001) Trading heat and food for safety: costs of predator avoidance in a lizard. Ecology 82:2870–2881. https://doi.org/10.1890/0012-9658(2001)082%5b2870:thaffs%5d2.0.co;2 CrossRefGoogle Scholar
- Drake EF, Bishop BP (1971) Life cycle and laboratory diet for Atrichopogon jacobsoni (de Meijere) (Diptera: Ceratopogonidae). Proc Hawaii Entomol Soc 21:63–66Google Scholar
- Elton C (1927) Animal ecology. Macmillan, New YorkGoogle Scholar
- Farjalla VF, González AL, Céréghino R, Dézeral O, Marino NAC, Piccoli GCO, Richardson BA, Richardsion MJ, Romero GQ, Srivastava DS (2016) Terrestrial support of aquatic food webs depends on light inputs: a geographically-replicated test using tank bromeliads. Ecology 97:2147–2156. https://doi.org/10.1002/ecy.1432 CrossRefGoogle Scholar
- Gilbert B, Tunney TD, McCann KS, DeLong JP, Vasseur DA, Savage V, Shurin JB, Dell AI, Barton BT, Harley CDG, Kharouba HM, Kratina P, Blanchard JL, Clements C, Winder M, Greig HS, O’Connor MI (2014) A bioenergetics framework for the temperature dependence of trophic interactions. Ecol Lett 17:902–914. https://doi.org/10.1111/ele.12307 CrossRefGoogle Scholar
- Hedström I, Sahlén G (2001) A key to the adult Costa Rican “helicopter” damselflies (Odonata: Pseudostigmatidae) with notes on their phenology and life zone preferences. Rev Biol Trop 49:1037–1056Google Scholar
- Kitching RL (2004) Food webs and container habitats: the natural history and ecology of phytotelmata. Cambridge University Press, CambridgeGoogle Scholar
- Merritt RW, Cummings KW (1996) An introduction to the aquatic insects of North America, 3rd edn. Kendall/Hunt Publishing Company, DubuqueGoogle Scholar
- Odum EP (1971) Fundamentals of Ecology, 3rd edn. WB Saunders Co, PhiladelphiaGoogle Scholar
- Petermann JS, Farjalla VF, Jocque M, Kratina P, MacDonald AAM, Marino NAC, de Omena PM, Piccoli GC, Richardson BA, Richardson MJ, Romero GQ, Videla M, Srivastava DS (2015) Dominant predators mediate the impact of habitat size on trophic structure in bromeliad invertebrate communities. Ecology 96:428–439. https://doi.org/10.1890/14-0304.1 CrossRefGoogle Scholar
- Sandin SA, Smith JE, DeMartini EE, Dinsdale EA, Donner SD, Friedlander AM, Konotchick T, Malay M, Maragos JE, Obura D, Pantos O, Paulay G, Richie M, Rohwer F, Schroeder RE, Walsh S, Jackson JBC, Knowlton N, Sala E (2008) Baselines and degradation of coral reefs in the Northern Line Islands. PLoS One 3:e1548. https://doi.org/10.1371/journal.pone.0001548 CrossRefGoogle Scholar
- Werner EE, Peacor SD (2003) A review of trait-mediated indirect interactions in ecological communities. Ecology 84:1083–1100. https://doi.org/10.1890/0012-9658(2003)084%5b1083:AROTII%5d2.0.CO;2 CrossRefGoogle Scholar