Aquatic Sciences

, 80:14 | Cite as

Tank bromeliads sustain high secondary production in neotropical forests

  • Olivier Dézerald
  • Céline Leroy
  • Bruno Corbara
  • Alain Dejean
  • Stanislas Talaga
  • Régis Céréghino
Research Article


In neotropical landscapes, a substantial fraction of the still waters available is found within tank bromeliads, plants which hold a few milliliters to several litres of rainwater within their leaf axils. The bromeliad ecosystem is integrated into the functioning of rainforest environments, but no study has ever estimated the secondary production, nor the biomass turnover rates of bromeliad macroinvertebrates in relation to other functional traits. We estimated secondary production at invertebrate population to metacommunity level in bromeliads of French Guiana. Coleoptera, Diptera and Crustacea with traits that confer resistance to drought had lower biomass turnover, longer generation times, and slower individual growth than species without particular resistance traits, suggesting convergent life history strategies in phylogenetically distant species. Detritivores and predators accounted for 87% and 13% of the overall annual production, respectively, but had similar production to biomass ratios. An average bromeliad sustained a production of 23.93 g dry mass m−2 year−1, a value which exceeds the medians of 5.0–14.8 g DM m−2 year−1 for lakes and rivers worldwide. Extrapolations to the total water volumes held by bromeliads at our field site yielded secondary production estimates of 226.8 ± 32.5 g DM ha−1 year−1. We conclude that the ecological role of tank bromeliads in neotropical rainforests may be as important as that of other freshwater ecosystems.


Biomass turnover Epiphytes Functional traits Food webs Invertebrates Rainforests 



We thank Frédéric Petitclerc, Clément Andrzejewski, Arthur Compin for field support, the Laboratoire Environnement Hydreco (Petit-Saut) for providing logistical support, Andrea Yockey-Dejean for proofreading the English text, and Andrew MacDonald for his comments on an advanced version of the manuscript. Two anonymous reviewers provided helpful comments on an earlier version of this paper.

Author contributions

Wrote the paper: OD, RC, CL; designed and conceived the study: OD, RC, CL, BC, AD, ST; analyzed the data: OD, RC. All authors contributed to the interpretation of the results and conclusions. All co-authors have read the submitted version of the manuscript and approve its submission, and we confirm that all persons entitled to authorship have been so included.


Financial support was provided by the Agence Nationale de la Recherche throught the Rainwebs project (grant ANR-12-BSV7-0022-01) and an “Investissement d’Avenir” grant (Labex CEBA, ref. ANR-10-LABX-25-01). OD and ST were funded by a PhD scholarship (CNRS and the FSE for OD; Université de Guyane for ST).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

27_2018_566_MOESM1_ESM.pdf (284 kb)
Appendix S1 Efficiency of sampling method. Appendix S2 Linear regressions used to correct for the density of each size class, based on measurements of non-deformable body parts. Appendix S3 Production values for lakes and streams synthesized from the literature. (PDF 283 KB)


  1. Amundrud SL, Srivastava DS (2015) Drought sensitivity predicts habitat size sensitivity in an aquatic ecosystem. Ecology 96:1957–1965. CrossRefPubMedGoogle Scholar
  2. Armbruster P, Hutchinson RA, Cotgreave P (2002) Factors influencing community structure in a South American tank bromeliad fauna. Oikos 96:225–234. CrossRefGoogle Scholar
  3. Babler AL, Solomon CT, Schilke PR (2008) Depth-specific patterns of benthic secondary production in an oligotrophic lake. J N Am Benthol Soc 27:108–119. CrossRefGoogle Scholar
  4. Baxter CV, Fausch KD, Saunders WC (2005) Tangled webs: reciprocal flows of invertebrate prey link streams and riparian zones. Freshwat Biol 50:201–220CrossRefGoogle Scholar
  5. Benbow ME, Burky AJ, Way CM (2003) Life cycle of a torrenticolous Hawaiian chironomid (Telmatogeton torrenticola): stream flow and microhabitat effects. Annales de Limnologie—Int J Limnol 39:103–114. CrossRefGoogle Scholar
  6. Benke AC, Huryn AD (2010) Benthic invertebrate production-facilitating answers to ecological riddles in freshwater ecosystems. J N Am Benthol Soc 29:264–285. CrossRefGoogle Scholar
  7. Benke AC, Wallace BJ (2014) High secondary production in a Coastal Plain river is dominated by snag invertebrates and fuelled mainly by amorphous detritus. Freshwat Biol 60:236–255. CrossRefGoogle Scholar
  8. Benke AC, Van Arsdall TC, Gillespie DM, Parrish FK (1984) Invertebrate productivity in a subtropical blackwater river: the importance of habitat and life history. Ecol Monogr 54:25–63. CrossRefGoogle Scholar
  9. Benzing DH (2000) Bromeliaceae: profile of an adaptive radiation. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  10. Brett MT et al (2017) How important are terrestrial organic carbon inputs for secondary production in freshwater ecosystems? Freshwat Biol 62:833–853. CrossRefGoogle Scholar
  11. Brouard O, Céréghino R, Corbara B, Leroy C, Pélozuelo L, Dejean A, Carrias J-F (2012) Understorey environments influence functional diversity in tank-bromeliad ecosystems. Freshwat Biol 57:815–823. CrossRefGoogle Scholar
  12. Céréghino R et al (2011) Ant-plant mutualisms promote functional diversity in phytotelm communities. Funct Ecol 25:954–963. CrossRefGoogle Scholar
  13. Chessel D, Dufour AB, Thioulouse J (2004) The ade4 package—I: one-table methods. R News 4:5–10Google Scholar
  14. Coq S, Souquet J-M, Meudec E, Cheynier V, Hattenschwiler S (2010) Interspecific variation in leaf litter tannins drives decomposition in a tropical rain forest of French Guiana. Ecology 91:2080–2091. CrossRefPubMedGoogle Scholar
  15. Dézerald O, Leroy C, Corbara B, Carrias J-F, Pélozuelo L, Dejean A, Céréghino R (2013) Food-web structure in relation to environmental gradients and predator-prey ratios in tank-bromeliad ecosystems. Plos One 8:e71735. CrossRefPubMedPubMedCentralGoogle Scholar
  16. Dézerald O, Talaga S, Leroy C, Carrias J-F, Corbara B, Dejean A, Céréghino R (2014) Environmental determinants of macroinvertebrate diversity in small water bodies: insights from tank-bromeliads. Hydrobiologia 723:77–86. CrossRefGoogle Scholar
  17. Dézerald O, Céréghino R, Corbara B, Dejean A, Leroy C (2015) Functional trait responses of aquatic macroinvertebrates to simulated drought in a Neotropical bromeliad ecosystem. Freshwat Biol 60:1917–1929. CrossRefGoogle Scholar
  18. Dézerald O, Leroy C, Corbara B, Dejean A, Talaga S, Céréghino R (2017) Environmental drivers of invertebrate population dynamics in Neotropical tank bromeliads. Freshwat Biol 62:229–242. CrossRefGoogle Scholar
  19. Farjalla VF et al (2016) Terrestrial support of aquatic food webs depends on light inputs: a geographically-replicated test using tank bromeliads. Ecology 97:2147–2156. CrossRefPubMedGoogle Scholar
  20. Frank JH, Lounibos LP (2009) Insects and allies associated with bromeliads: a review. Terrestrial Arthropod Rev 1:125–153. CrossRefGoogle Scholar
  21. Gamez-Virues S et al. (2015) Landscape simplification filters species traits and drives biotic homogenization. Nature Commun. Google Scholar
  22. Givnish TJ et al (2011) Phylogeny, adaptive radiation, and historical biogeography in Bromeliaceae: insights from an eight-locus plastid phylogeny. Am J Bot 98:872–895. CrossRefPubMedGoogle Scholar
  23. Gonçalves-Souza T, Brescovit AD, Rossa-Feres DD, Romero GQ (2010) Bromeliads as biodiversity amplifiers and habitat segregation of spider communities in a Neotropical rainforest. J Arachnol 38:270–279CrossRefGoogle Scholar
  24. Gratton C, Vander Zanden MJ (2009) Flux of aquatic insect productivity to land: comparison of lentic and lotic ecosystems. Ecology 90:2689–2699. CrossRefPubMedGoogle Scholar
  25. Haubrich CS, Pires APF, Esteves FA, Farjalla VF (2009) Bottom-up regulation of bacterial growth in tropical phytotelm bromeliads. Hydrobiologia 632:347–353. CrossRefGoogle Scholar
  26. Huryn AD (1990) Growth and voltinism of lotic midge larvae - patterns across an Appalachian mountain basin. Limnol Oceanogr 35:339–351CrossRefGoogle Scholar
  27. Hynes HBN, Coleman MJ (1968) A simple method of assessing the annual production of stream benthos. Limnol Oceanogr 13:569–573. CrossRefGoogle Scholar
  28. Lau DCP, Sundh I, Vrede T, Pickova J, Goedkoop W (2014) Autochthonous resources are the main driver of consumer production in dystrophic boreal lakes. Ecology 95:1506–1519CrossRefPubMedGoogle Scholar
  29. Lecraw RM, Romero GQ, Srivastava DS (2017) Geographic shifts in the effects of habitat size on trophic structure and decomposition. Ecography 1–10.
  30. Leroy C, Carrias J-F, Céréghino R, Corbara B (2016) The contribution of microorganisms and metazoans to mineral nutrition in bromeliads. J Plant Ecol 9:241–255. CrossRefGoogle Scholar
  31. Leroy C, Corbara B, Dézerald O, Trzcinski MK, Carrias J-F, Dejean A, Céréghino R (2017) What drives detrital decomposition in neotropical tank bromeliads? Hydrobiologia.
  32. Marino NAC, Guariento RD, Dib V, Azevedo FD, Farjalla VF (2011) Habitat size determine algae biomass in tank-bromeliads. Hydrobiologia 678:191–199. CrossRefGoogle Scholar
  33. Marino NAC, Srivastava DS, Farjalla VF (2016) Predator kairomones change food web structure and function, regardless of cues from consumed prey. Oikos 125:1017–1026. CrossRefGoogle Scholar
  34. Marino NAC 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. CrossRefPubMedGoogle Scholar
  35. Merritt RW, Cummins KW, Berg MB (2008) An introduction to aquatic insects of North America, 4th edn. Kendall/Hunt Publishing Company, DubuqueGoogle Scholar
  36. Morin A, Mousseau TA, Roff DA (1987) Accuracy and precision of secondary production estimates. Limnol Oceanogr 32:1342–1352. CrossRefGoogle Scholar
  37. Ngai JT, Srivastava DS (2006) Predators accelerate nutrient cycling in a bromeliad ecosystem. Science 314:963. CrossRefPubMedGoogle Scholar
  38. Perán A, Velasco J, Millán A (1999) Life cycle and secondary production of Caenis luctuosa (Ephemeroptera) in a semiarid stream (Southeast Spain). Hydrobiologia 400:187–194. CrossRefGoogle Scholar
  39. Petermann JS et al (2015) Dominant predators mediate the impact of habitat size on trophic structure in bromeliad invertebrate communities. Ecology 96:428–439. CrossRefPubMedGoogle Scholar
  40. Pianka ER (1970) On r- and K-selection. Am Nat 105:592–597CrossRefGoogle Scholar
  41. Plante C, Downing JA (1989) Production of freshwater invertebrate populations in lakes. Can J Fish Aquat Sci 46:1489–1498CrossRefGoogle Scholar
  42. Poelman EH, van Wijngaarden RPA, Raaijmakers CE (2013) Amazon poison frogs (Ranitomeya amazonica) use different phytotelm characteristics to determine their suitability for egg and tadpole deposition. Evol Ecol 27:661–674. CrossRefGoogle Scholar
  43. R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  44. Richardson BA (1999) The bromeliad microcosm and the assessment of faunal diversity in a neotropical forest. Biotropica 31:321–336. CrossRefGoogle Scholar
  45. Richardson BA, Richardson MJ, Scatena FN, McDowell WH (2000a) Effects of nutrient availability and other elevational changes on bromeliad populations and their invertebrate communities in a humid tropical forest in Puerto Rico. J Trop Ecol 16:167–188. CrossRefGoogle Scholar
  46. Richardson BA, Rogers C, Richardson MJ (2000b) Nutrients, diversity, and community structure of two phytotelm systems in a lower montane forest, Puerto Rico. Ecol Entomol 25:348–356. CrossRefGoogle Scholar
  47. Richardson BA, Richardson MJ, Soto-Adames FN (2005) Separating the effects of forest type and elevation on the diversity of litter invertebrate communities in a humid tropical forest in Puerto Rico. J Anim Ecol 74:926–936. CrossRefGoogle Scholar
  48. Romero GQ, Srivastava DS (2010) Food-web composition affects cross-ecosystem interactions and subsidies. J Anim Ecol 79:1122–1131. CrossRefPubMedGoogle Scholar
  49. Sabagh LT, Rocha CFD (2014) Bromeliad treefrogs as phoretic hosts of ostracods. Naturwissenschaften 101:493–497CrossRefPubMedGoogle Scholar
  50. 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
  51. Stead TK, Schmid-Araya JM, Hildrew AG (2005) Secondary production of a stream metazoan community: does the meiofauna make a difference? Limnol Oceanogr 50:398–403CrossRefGoogle Scholar
  52. Stork NE, Eggleton P (1992) Invertebrates as determinants and indicators of soil quality. Am J Alternative Agric 7:38–47. doiCrossRefGoogle Scholar
  53. Wallace JB, Eggert SL, Meyer JL, Webster JR (2015) Stream invertebrate productivity linked to forest subsidies: 37 stream-years of reference and experimental data. Ecology 96:1213–1228. CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.CNRS, UMR Ecologie des Forêts de Guyane (AgroParisTech, CIRAD, INRA, Université des Antilles, Université de Guyane)Kourou cedexFrance
  2. 2.Université de Lorraine, UMR Laboratoire Interdisciplinaire des Environnements Continentaux (CNRS)MetzFrance
  3. 3.AMAP, IRD, CNRS, INRA, Université MontpellierMontpellierFrance
  4. 4.Université Clermont Auvergne, CNRS, LMGEClermont-FerrandFrance
  5. 5.Ecolab, Laboratoire Ecologie Fonctionnelle et EnvironnementUniversité de Toulouse, CNRS-UPS-INPTToulouseFrance
  6. 6.Université de Guyane, UMR Écologie des Forêts de Guyane (AgroParisTech, CIRAD, CNRS, INRA, Université des Antilles)Kourou cedexFrance

Personalised recommendations