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Experimental Detritus Manipulations Unite Surface and Cave Stream Ecosystems Along a Common Energy Gradient

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Abstract

Subsidies of detritus from donor habitats are important energy sources for many ecosystems, but understanding their role in structuring recipient food webs requires comparative experimental studies along the full spectrum of detrital fluxes. Here we report results from an experimental addition of maize (Zea mays L.) litter to a detritus-poor cave stream ecosystem, which we then compare with analogous, past experiments using detritus-rich surface stream ecosystems that similarly have detritus-based food webs and extremely low in situ primary production. Bulk-tissue and compound-specific stable isotope analyses showed that maize litter carbon (C) was rapidly assimilated by microbes and transferred via successive trophic levels to the top of the cave stream food web (omnivorous crayfishes and predatory salamanders). All trophic levels increased in abundance and biomass, but only facultative cave taxa, that is those also found in surface streams, contributed to this numerical response. The lack of response by obligate cave species presumably occurred because evolutionary trade-offs associated with adaptations to low-C environments constrained their population-level responses during the one-year period of the litter addition. Comparison of the responses of the cave community with the analogous litter manipulation experiments in surface streams showed strong convergence in the functional relationship between invertebrate and detritus biomass (R 2 = 0.72, P < 0.0001). Our results suggest that these seemingly disparate stream food webs lie along a single, common gradient of detritus supply, occupied at its extreme minimum by communities of obligate cave taxa adapted to low-energy environments.

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References

  • Aden E. 2005. Adaptation to darkness. In: Culver DC, White WB, Eds. Encyclopedia of caves. Burlington (MA): Elsevier Academic Press.

    Google Scholar 

  • Andersen T, Baranov V, Hagenlund LK, Ivković M, Kvifte GM, Pavlek M. 2016. Blind flight? A new troglobiotic orthoclad (Diptera, Chironomidae) from the Lukina Jama-Trojama Cave in Croatia. PLoS ONE 11:e0152884.

    Article  PubMed  PubMed Central  Google Scholar 

  • Benke AC, Huryn AD, Smock LA, Wallace JB. 1999. Length-mass relationships for freshwater macroinvertebrates in North America with particular reference to the southeastern United States. J N Am Benthol Soc 18:308–43.

    Article  Google Scholar 

  • Benstead JP, Rosemond AD, Cross WF, Wallace JB, Eggert AL, Suberkropp K, Tant CJ. 2009. Nutrient enrichment alters storage and fluxes of detritus in a headwater stream ecosystem. Ecology 90:2556–66.

    Article  PubMed  Google Scholar 

  • Calow P. 1975. Length-dry weight relationships in snails: some explanatory models. J Molluscan Stud 41:357–75.

    Article  Google Scholar 

  • Cebrian J. 1999. Patterns in the fate of production in plant communities. Am Nat 154:449–68.

    Article  PubMed  Google Scholar 

  • Chambers CP, Whiles MR, Rosi-Marshall EJ, Tank JL, Royer TV, Griffiths NA, Evans-White MA, Stojak AR. 2010. Responses of stream macroinvertebrates to Bt maize leaf detritus. Ecol Appl 20:1949–60.

    Article  PubMed  Google Scholar 

  • Chen B, Wise DH. 1999. Bottom-up limitation of predaceous arthropods in a detritus-based terrestrial food web. Ecology 80:761–72.

    Article  Google Scholar 

  • Cole JJ, Carpenter SR, Pace ML, Van de Bogert MC, Kitchell JL, Hodgson JR. 2006. Differential support of lake food webs by three types of terrestrial organic carbon. Ecol Lett 9:558–68.

    Article  PubMed  Google Scholar 

  • Culver DC, Pipan T. 2014. Shallow subterranean habitats. New York: Oxford University Press.

    Book  Google Scholar 

  • Culver DC, Pipan T. 2009. The biology of caves and other subterranean habitats. New York: Oxford University Press.

    Google Scholar 

  • Culver DA, Boucherle MM, Bean DJ, Fletcher JW. 1985. Biomass of freshwater crustacean zooplankton from length-weight regressions. Can J Fish Aquat Sci 42:1380–90.

    Article  Google Scholar 

  • Doroszuk A, Te Brake E, Crespo-Gonzalez D, Kammenga JE. 2007. Response of secondary production and its components to multiple stressors in nematode field populations. J Appl Ecol 44:446–55.

    Article  Google Scholar 

  • Engel AS, Porter ML, Stern LA, Quinlan S, Bennett PC. 2004. Bacterial diversity and ecosystem function of filamentous microbial mats from aphotic (cave) sulfidic springs dominated by chemolithoautotrophic “Epsilonproteobacteria”. FEMS Microbiol Ecol 51:31–53.

    Article  PubMed  CAS  Google Scholar 

  • Fernandes CS, Batalha MA, Bichuette ME. 2016. Does the cave environment reduce functional diversity? PLoS ONE 11(3):e0151958.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Figueroa JMT, López-Rodríguez MJ. 2010. Protonemura gevi sp. n., a cavernicolous new species of stonefly (Insecta: Plecoptera). Zootaxa 2365:48–54.

    Google Scholar 

  • García L, Richardson JS, Pardo I. 2012. Leaf quality influences invertebrate colonization and drift in a temperate rainforest stream. Can J Fish Aquat Sci 69:1663–73.

    Article  Google Scholar 

  • Gibert J, DeHarveng L. 2002. Subterranean ecosystems: a truncated functional biodiversity. Bioscience 52:473–81.

    Article  Google Scholar 

  • Griffiths NA, Tank JL, Royer TV, Rosi-Marshall EJ, Whiles MR, Chambers CP, Frauendorf TC, Evans-White MA. 2009. Rapid decomposition of maize detritus in agricultural headwater streams. Ecol Appl 19:133–42.

    Article  PubMed  Google Scholar 

  • Hagen EM, McCluney KE, Wyant KA, Soykan CU, Keller AC, Luttermoser KC, Holmes EJ, Moore JC, Sabo JL. 2012. A meta-analysis of the effects of detritus on primary producers and consumers in marine, freshwater, and terrestrial ecosystems. Oikos 121:1507–15.

    Article  Google Scholar 

  • Hains JJ 1981. The response of stream flora to watershed perturbation. Thesis. Clemson University, Clemson, South Carolina, USA.

  • Hershey AE, Fortino K, Peterson BJ, Ulseth AJ. 2006. Stream food webs. In: Hauer FR, Lamberti GA, Eds. Methods in stream ecology. 2nd edn. Burlington (MA): Elsevier Academic Press.

    Google Scholar 

  • Huntsman BM, Venarsky MP, Benstead JP. 2011a. Relating carrion breakdown rates to ambient resource level and community structure in four cave stream ecosystems. J N Am Benthol Soc 30:882–92.

    Article  Google Scholar 

  • Huntsman BM, Venarsky MP, Benstead JP, Huryn AD. 2011b. Effects of organic matter availability on the life history and production of a top vertebrate predator (Plethodontidae: Gyrinophilus palleucus) in two cave streams. Freshw Biol 56:1746–60.

    Article  Google Scholar 

  • Hüppop K. 2000. How do cave animals cope with the food scarcity in caves? In: Goodall DW, Wilkens H, Culver DC, Humphreys WF, Eds. Ecosystems of the world: subterranean ecosystems. Amsterdam: Elsevier Science.

    Google Scholar 

  • Hüppop K. 2005. Adaptation to low food. In: Culver DC, White WB, Eds. Encyclopedia of caves. Burlington: Elsevier Academic Press.

    Google Scholar 

  • Huxel GR, McCann K. 1998. Food web stability: the influence of trophic flows across habitats. Am Nat 152:460–9.

    Article  PubMed  CAS  Google Scholar 

  • Juberthie C. 2000. The diversity of the karstic and pseudokarstic hypogean habitats in the world. In: Goodall DW, Wilkens H, Culver DC, Humphreys WF, Eds. Ecosystems of the world: subterranean ecosystems. Amsterdam: Elsevier Science.

    Google Scholar 

  • Leeper DA, Taylor BE. 1998. Abundance, biomass, and production of aquatic invertebrates in Rainbow Bay, a temporary wetland in South Carolina, USA. Arch Hydrobiol 143:335–62.

    Article  Google Scholar 

  • Lemke A, Benke AC. 2009. Spatial and temporal patterns of microcrustacean assemblage structure and secondary production in a wetland ecosystem. Freshw Biol 54:1406–26.

    Article  Google Scholar 

  • Marcarelli AM, Baxter CV, Mineau MM, Hall RO Jr. 2011. Quantity and quality: unifying food web and ecosystem perspectives on the role of resource subsidies in freshwaters. Ecology 92:1215–25.

    Article  PubMed  Google Scholar 

  • Marczak LB, Thompson RM, Richardson JS. 2007. Meta-analysis: trophic level, habitat, and productivity shape the food web effects of resource subsidies. Ecology 88:140–8.

    Article  PubMed  Google Scholar 

  • McGrath CC, Matthews RA. 2000. Cellulase activity in the freshwater amphipod Gammarus lacustris. J N Am Benthol Soc 19:298–307.

    Article  Google Scholar 

  • Moore JC, Berlow EL, Coleman DC, Ruiter PC, Dong Q, Hastings A, Johnson NC, McCann KS, Melville K, Morin PJ, Nadelhoffer K, Rosemond AD, Post DM, Sabo JL, Scow KM, Vanni MJ, Wall DH. 2004. Detritus, trophic dynamics and biodiversity. Ecol Lett 7:584–600.

    Article  Google Scholar 

  • Ostrofsky ML. 1997. Relationship between chemical characteristics of autumn-shed leaves and aquatic processing rates. J N Am Benthol Soc 16:750–9.

    Article  Google Scholar 

  • Parnell AC, Jackson AL. 2011. SIAR: stable isotope analysis in R. R Package Version 4.1. 3.

  • Parnell AC, Inger R, Bearhop S, Jackson AL. 2010. Source partitioning using stable isotopes: coping with too much variation. PLoS ONE 5:e9672.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Polis GA, Strong DR. 1996. Food web complexity and community dynamics. Am Nat 147:813–46.

    Article  Google Scholar 

  • Polis GA, Anderson WB, Holt RD. 1997. Toward an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annu Rev Ecol Evol Syst 28:289–316.

    Article  Google Scholar 

  • Polis GA, Sears ALW, Huxel GR, Strong DR, Maron J. 2000. When is a trophic cascade a trophic cascade? Trends Ecol Evol 15:473–5.

    Article  PubMed  CAS  Google Scholar 

  • Poulson TL, Lavoie KH. 2000. The trophic basis of subsurface ecosystems. In: Goodall DW, Wilkens H, Culver DC, Humphreys WF, Eds. Ecosystems of the world: subterranean ecosystems. Amsterdam: Elsevier Science.

    Google Scholar 

  • R Core Team. 2013. R: a language and environment for statistical computing. R 4.1.3. R Foundation for Statistical Computing, Vienna. http://CRAN.R-project.org/package=siar.

  • Ray JA. 2005. Sinking streams and losing systems. In: Culver DC, White WB, Eds. Encyclopedia of caves. Burlington, MA: Elsevier Academic Press.

    Google Scholar 

  • Richardson JS. 1991. Seasonal food limitation of detritivores in a montane stream: an experimental test. Ecology 72:873–87.

    Article  Google Scholar 

  • Rosi-Marshall E, Tank J, Royer T, Whiles MR, Evans-White M, Chambers C, Griffiths N, Pokelsek J, Stephen M. 2007. Toxins in transgenic crop byproducts may affect headwater stream ecosystems. Proc Natl Acad Sci 104:16204–8.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sarbu SM, Kane TC, Kinkle BK. 1996. A chemoautotrophically based cave ecosystem. Science 272:1953–5.

    Article  PubMed  CAS  Google Scholar 

  • Scharnweber K, Syvaranta J, Hilt S, Brauns M, Vanni MJ, Brothers S, Kohler J, Knezevic-Jaric J, Mehner T. 2014. Whole-lake experiments reveal the fate of terrestrial particulate organic carbon in benthic food webs of shallow lakes. Ecology 95:1496–505.

    Article  PubMed  CAS  Google Scholar 

  • Schroeter SC, Dixon JD, Kastendiek J, Smith RO. 1993. Detecting the ecological effects of environmental impacts—a case-study of kelp forest invertebrates. Ecol Appl 3:331–50.

    Article  PubMed  Google Scholar 

  • Simon K, Benfield E. 2001. Leaf and wood breakdown in cave streams. J N Am Benthol Soc 20:550–63.

    Article  Google Scholar 

  • Sket B. 1973. Gegenseitige beeinflussung der wasserpollution und des höhlenmilieus. In: Proceedings of the 6th international congress on speleology. Olomuc, Czechoslovakia.

  • Sket B. 1986. Ecology of the mixohaline hypogean fauna along the Yugoslav coasts. Stygologia 2:317–38.

    Google Scholar 

  • Stewart-Oaten A, Murdoch WW, Park KR. 1986. Environmental-impact assessment—pseudoreplication in time. Ecology 67:929–40.

    Article  Google Scholar 

  • Tank JL, Rosi-Marshall EJ, Griffiths NA, Entrekin SA, Stephen ML. 2010. A review of allochthonous organic matter dynamics and metabolism in streams. J N Am Benthol Soc 29:118–46.

    Article  Google Scholar 

  • Townsend CR. 1989. The patch dynamics concept of stream community ecology. J N Am Benthol Soc 8:36–50.

    Article  Google Scholar 

  • Venarsky MP, Benstead JP, Huryn AD. 2012. Effects of organic matter and season on leaf litter colonization and breakdown in cave streams. Freshw Biol 57:773–86.

    Article  Google Scholar 

  • Venarsky MP, Huntsman BM, Huryn AD, Benstead JP, Kuhajda BR. 2014. Quantitative food web analysis supports the energy-limitation hypothesis in cave stream ecosystems. Oecologia 176:859–69.

    Article  PubMed  Google Scholar 

  • Wallace JB, Eggert SL, Meyer JL, Webster JR. 1997. Multiple trophic levels of a forest stream linked to terrestrial litter inputs. Science 277:102–4.

    Article  CAS  Google Scholar 

  • Wallace JB, Eggert SL, Meyer JL, Webster JR. 1999. Effects of resource limitation on a detrital-based ecosystem. Ecol Monogr 69:409–42.

    Article  Google Scholar 

  • 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 96:1213–28.

    Article  PubMed  Google Scholar 

  • Webster JR, Benfield EF. 1986. Vascular plant breakdown in freshwater ecosystems. Annu Rev Ecol Syst 17:567–94.

    Article  Google Scholar 

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Acknowledgements

This study was supported by Alabama State Wildlife Grants (T-03-02, T-3-3-2), a National Science Foundation Doctoral Dissertation Improvement Grant DDIG (DEB-1011403), and a National Science Foundation Major Research Instrumentation Grant (DEB-521018). This project was approved by the University of Alabama Institutional Animal Care and Use Committee (protocols 08-313-1 and 09-321-1) and conducted under State of Alabama Department of Conservation Permit 2010000029568680. Additional funds were provided by the University of Alabama, the Birmingham Audubon Society, and the National Speleological Society. Members of the Sewanee and Birmingham grottos (P. Michaud, M. Attaway, J. Attaway, J. Hardy, C.D. “Hazard” Bryant, A. Bullen, D. Hahn, J. Harrod, B. Skelton, D. Wood) provided housing, cave locations, and field assistance. We thank J. Wilson for cave access and B. Fluker, M. Sandel, C. Craig, N. Whelan, M. Kendrick, J. Ramsey, D. Hall, C. Tran (T-RFLP analysis), D. Nelson, J. Brown (PLFA-SIP analyses), and M. Demi for assistance with laboratory and field work. Kevin Simon and three anonymous reviewers provided helpful criticism of earlier versions of this paper. Finally, we thank M.H. Huryn for translating German literature.

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Author notes

  1. Michael P. Venarsky

    Present address: Australian Rivers Institute, Griffith University, Nathan Campus, Sir Samuel, Griffith Building N78, 4.11, 170 Kessels Road, Nathan, Queensland, 4111, Australia

  2. Brock M. Huntsman

    Present address: Department of Fish, Wildlife and Conservation Ecology, New Mexico State University, Las Cruces, New Mexico, 88003, USA

Authors and Affiliations

  1. Department of Biological Sciences, University of Alabama, Tuscaloosa, Alabama, 35487, USA

    Michael P. Venarsky, Jonathan P. Benstead, Alexander D. Huryn, Brock M. Huntsman & Robert H. Findlay

  2. Nevada State College, Physical and Life Sciences, Henderson, Nevada, 89002, USA

    Jennifer W. Edmonds

  3. Department of Entomology, University of Georgia, Athens, Georgia, 30602, USA

    J. Bruce Wallace

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  1. Michael P. Venarsky
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Correspondence to Michael P. Venarsky.

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Authors’ contributions

MPV, JPB, and ADH conceived study; MPV and BMH performed research; MPV, JPB, ADH, JWE, and RHF analyzed data; JBW contributed data; MPV, JPB, ADH, BMH, JWE, RHF, and JBW wrote paper.

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Venarsky, M.P., Benstead, J.P., Huryn, A.D. et al. Experimental Detritus Manipulations Unite Surface and Cave Stream Ecosystems Along a Common Energy Gradient. Ecosystems 21, 629–642 (2018). https://doi.org/10.1007/s10021-017-0174-4

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