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Disease-Driven Amphibian Declines Alter Ecosystem Processes in a Tropical Stream

Abstract

Predicting the ecological consequences of declining biodiversity is an urgent challenge, particularly in freshwater habitats where species declines and losses are among the highest. Small-scale experiments suggest potential ecosystem responses to losses of species, but definitive conclusions require verification at larger scales. We measured ecosystem metabolism and used whole-ecosystem stable isotope tracer additions to quantify nitrogen cycling in a tropical headwater stream before and after the sudden loss of amphibians to the fungal pathogen Batrachochytrium dendrobatidis. Tadpoles are normally dominant grazers in such streams, where greater than 18 species may co-occur and densities often exceed 50 individuals m−2. Loss of 98% of tadpole biomass corresponded with greater than 2× increases in algae and fine detritus biomass in the stream and a greater than 50% reduction in nitrogen uptake rate. Nitrogen turnover rates in suspended and deposited organic sediments were also significantly lower after the decline. As a consequence, the stream cycled nitrogen less rapidly, and downstream exports of particulate N were reduced. Whole stream respiration was significantly lower following the decline, indicating less biological activity in the stream sediments. Contrary to our predictions, biomass of grazing invertebrates, or any invertebrate functional groups, did not increase over 2 years following loss of tadpoles. Thus, reductions in ecosystem processes linked to the amphibian decline were not compensated for by other, functionally redundant consumers. Declining animal biodiversity has ecosystem-level consequences that may not be offset by ecological redundancy, even in biologically diverse regions such as the Neotropics.

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Acknowledgments

This research was supported by National Science Foundation Grants DEB #0717741 and DEB #0645875. The Smithsonian Tropical Research Institute and Autoridad Nacional del Ambiente (ANAM) provided logistical support in Panamá. E. Rosi-Marshall, J. Tank, and J. E. Garvey provided constructive comments on the manuscript. E. Griffiths and H. Ross assisted with field sampling and provided taxonomic expertise. L. Barrow, D. Govoni, T. Frauendorf, and J. Uzzardo assisted with sample processing. All the research detailed in this manuscript complies with the current laws of the Republic of Panamá. Animal handling and sacrifices followed SIU animal care protocols (Protocol 06-008).

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Correspondence to M. R. Whiles.

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Author contributions

MRW, ROH, and WKD led development of the study design and manuscript and participated in field work. PV, ATR, SC, and ADH performed much of the field work. CC-G, SC, PV, and SP analyzed data. KRL, PV, CMP, SSK, and ADH designed components of the study and wrote portions of the manuscript.

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Whiles, M.R., Hall, R.O., Dodds, W.K. et al. Disease-Driven Amphibian Declines Alter Ecosystem Processes in a Tropical Stream. Ecosystems 16, 146–157 (2013). https://doi.org/10.1007/s10021-012-9602-7

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Keywords:

  • biodiversity-ecosystem function
  • extinction
  • ecological redundancy
  • nitrogen cycling
  • emerging infectious disease
  • isotope tracer
  • ecosystem metabolism
  • primary production