Skip to main content

Advertisement

SpringerLink
Log in

Quantitative food web analysis supports the energy-limitation hypothesis in cave stream ecosystems

  • Ecosystem ecology - Original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Energy limitation has long been the primary assumption underlying conceptual models of evolutionary and ecological processes in cave ecosystems. However, the prediction that cave communities are actually energy-limited in the sense that constituent populations are consuming all or most of their resource supply is untested. We assessed the energy-limitation hypothesis in three cave streams in northeastern Alabama (USA) by combining measurements of animal production, demand, and resource supplies (detritus, primarily decomposing wood particles). Comparisons of animal consumption and detritus supply rates in each cave showed that all, or nearly all, available detritus was required to support macroinvertebrate production. Furthermore, only a small amount of macroinvertebrate prey production remained to support other predatory taxa (i.e., cave fish and salamanders) after accounting for crayfish consumption. Placing the energy demands of a cave community within the context of resource supply rates provided quantitative support for the energy-limitation hypothesis, confirming the mechanism (limited energy surpluses) that likely influences the evolutionary processes and population dynamics that shape cave communities. Detritus-based surface ecosystems often have large detrital surpluses. Thus, cave ecosystems, which show minimal surpluses, occupy the extreme oligotrophic end of the spectrum of detritus-based food webs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Benke A, Huryn A (2006) Secondary production of macroinvertebrates. In: Hauer FR, Lamberti GA (eds) Methods in stream ecology, 2nd edn. Academic, New York, pp 691–710

  • Benke AC, Wallace JB (1980) Trophic basis of production among net-spinning caddisflies in a southern Appalachian stream. Ecology 61:108–118

    Article  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 North Am Benthol Soc 18:308–343

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information-theoretic approach. Springer, New York

    Google Scholar 

  • Calow P (1975) Length–dry weight relationships in snails: some explanatory models. J Molluscan Stud 41:357–375

  • Caut S, Angulo E, Courchamp F (2009) Variation in discrimination factors (Δ15N and Δ13C): the effect of diet isotopic values and applications for diet reconstruction. J Appl Ecol 46:443–453

    Article  CAS  Google Scholar 

  • Chen B, Wise DH (1999) Bottom-up limitation of predaceous arthropods in a detritus-based terrestrial food web. Ecology 80:761–772

    Article  Google Scholar 

  • Cooney TJ, Simon KS (2009) Influence of dissolved organic matter and invertebrates on the function of microbial films in groundwater. Microb Ecol 58:599–610

    Article  PubMed  Google Scholar 

  • Cross WF, Wallace JB, Rosemond AD (2007) Nutrient enrichment reduces constraints on material flows in a detritus-based food web. Ecology 88:2563–2575

    Article  PubMed  Google Scholar 

  • Culver DC (1982) Cave life: evolution and ecology. Harvard University Press, Cambridge

    Book  Google Scholar 

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

    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 42:1380–1390

    Article  Google Scholar 

  • Culver DC, Kane TC, Fong DW (1995) Adaptation and natural selection in caves: the evolution of Gammarus minus. Harvard University Press, Cambridge

    Book  Google Scholar 

  • Datry T, Malard F, Gibert J (2005) Response of invertebrate assemblages to increased groundwater recharge rates in a phreatic aquifer. J N Am Benthol Soc 24:461–477

    Article  Google Scholar 

  • Dobson M, Hildrew AG (1992) A test of resource limitation among shredding detritivores in low order streams in southern England. J Anim Ecol 61:69–77

    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 44:446–455

    Article  Google Scholar 

  • Dyer LA, Letourneau D (2003) Top-down and bottom-up diversity cascades in detrital vs. living food webs. Ecol Lett 6:60–68

    Article  Google Scholar 

  • Efron B, Tibshirani RJ (1993) An introduction to the bootstrap. In: Hall C (ed) Monographs on statistics and applied probability, vol 57. Chapman and Hall, New York

    Google Scholar 

  • Engel AS (2007) Observations on the biodiversity of sulfidic karst habitats. J Cave Karst Stud 69:187–206

    CAS  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 

  • Fretwell SD (1977) The regulation of plant communities by food chains exploiting them. Perspect Biol Med 20:85

    Google Scholar 

  • Grimm NB (1988) Role of macroinvertebrates in nitrogen dynamics of a desert stream. Ecology 69:1884–1893

    Article  Google Scholar 

  • Gripenberg S, Roslin T (2007) Up or down in space? Uniting the bottom-up versus top-down paradigm and spatial ecology. Oikos 116:181–188

    Article  Google Scholar 

  • Gutiérrez-Yurrita PJ, Montes C (2001) Bioenergetics of juveniles of red swamp crayfish (Procambarus clarkii). Comp Biochem Physiol 130:29–38

    Article  Google Scholar 

  • Hairston NG, Smith FE, Slobodkin LB (1960) Community structure, population control, and competition. Am Nat 879:421–425

    Article  Google Scholar 

  • Hall RO Jr, Meyer JL (1998) The trophic significance of bacteria in a detritus-based stream food web. Ecology 79:1995–2012

    Article  Google Scholar 

  • Hall RO Jr, Wallace JB, Eggert SL (2000) Organic matter flow in stream food webs with reduced detrital resource base. Ecology 81:3445–3463

    Article  Google Scholar 

  • Hall RO Jr, Likens GE, Malcom HM (2001) Trophic basis of invertebrate production in 2 streams at the Hubbard Brook experimental forest. J N Am Benthol Soc 20:432–447

    Article  Google Scholar 

  • Hendricks S (1996) Bacterial biomass, activity, and production within the hyporheic zone of a north-temperate stream. Arch Hydrobiol 136:467–487

    Google Scholar 

  • Huntsman BM, Venarsky MP, Benstead JP, Huryn AD (2011a) 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 56:1746–1760

    Article  Google Scholar 

  • Huntsman BM, Venarsky MP, Benstead JP (2011b) Relating carrion breakdown rates to ambient resource level and community structure in four cave stream ecosystems. J N Am Benthol Soc 30:882–892

    Article  Google Scholar 

  • Hüppop K (2001) How do cave animals cope with the food scarcity in caves? In: Wilkens H, Culver DC, Humphreys WF (eds) Ecosystems of the world; subterranean ecosystems. Elsevier, New York, pp 159–188

    Google Scholar 

  • Huryn AD, Wallace JB (1987) Production and litter processing by crayfish in an Appalachian mountain stream. Freshw Biol 18:277–286

    Article  Google Scholar 

  • Leeper D, Taylor B (1998) Abundance, biomass and production of aquatic invertebrates in Rainbow Bay, a temporary wetland in South Carolina, USA. Arch Hydrobiol 143:335–362

    Google Scholar 

  • Lemke A, Benke AC (2009) Spatial and temporal patterns of microcrustacean assemblage structure and secondary production in a wetland ecosystem. Freshw Biol 54:1406–1426

    Article  Google Scholar 

  • Madsen EL, Sinclair JL, Ghiorse WC (1991) In situ biodegradation: microbiological patterns in a contaminated aquifer. Science 252:830–833

    Article  PubMed  CAS  Google Scholar 

  • Manly BFJ (1991) Randomization and Monte Carlo methods in biology. Chapman and Hall, London

    Book  Google Scholar 

  • Menge BA (2000) Top-down and bottom-up community regulation in marine rocky intertidal habitats. J Exp Mar Biol Ecol 250:257–289

    Article  PubMed  Google Scholar 

  • Momot WT (1995) Redefining the role of crayfish in aquatic ecosystems. Rev Fish Sci 3:33–63

    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 

  • Notenboom J, Plénet S, Turquin M (1994) Groundwater contamination and its impact on groundwater animals and ecosystems. In: Gibert J, Danielopol DL (eds) Groundwater ecology. Academic, San Diego, pp 477–504

  • Oksanen L, Fretwell SD, Arruda J, Niemela P (1981) Exploitation ecosystems in gradients of primary productivity. Am Nat 118:240–261

    Article  Google Scholar 

  • Parnell A, Jackson A (2011) SIAR: stable isotope analysis in R. R package version 4.1.3. http://CRAN.R-project.org/package=siar. Accessed Nov 2013

  • 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  Google Scholar 

  • Polis GA, Strong DR (1996) Food web complexity and community dynamics. Am Nat 147:813–846

    Article  Google Scholar 

  • Porter ML, Engel AS, Kane TC, Kinkle BK (2009) Productivity–diversity relationships from chemolithoautotrophically based sulfidic karst systems. Int J Speleol 38:27–40

  • Poulson TL, Lavoie KH (2001) The trophic basis of subsurface ecosystems. In: Wilkens H, Culver DC, Humphreys WF (eds) Ecosystems of the world: subterranean ecosystems. Elsevier, New York, pp 231–250

    Google Scholar 

  • Power ME (1992) Top-down and bottom-up forces in food webs: do plants have primacy. Ecology 73:733–746

    Article  Google Scholar 

  • R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0. http://www.R-project.org/. Accessed Nov 2013

  • Rathinam AMM, Kandasamy D, Kizhakudan JK, Leslie V, Gandhi A (2009) Effect of dietary protein on the growth of spiny lobster Panulirus homarus (Linnaeus). J Mar Biol Assoc India 51:114–117

    Google Scholar 

  • Roach KA, Tobler M, Winemiller KO (2011) Hydrogen sulfide, bacteria, and fish: a unique, subterranean food chain. Ecology 92:2056–2062

    Article  PubMed  Google Scholar 

  • Rosemond AD, Pringle CM, Ramírez A, Paul MJ (2001) A test of top-down and bottom-up control in a detritus-based food web. Ecology 82:2279–2293

    Article  Google Scholar 

  • Ross RM (1982a) Energetics of Euphausia pacifica. I. Effects of body carbon and nitrogen and temperature on measured and predicted production. Mar Biol 68:1–13

    Article  CAS  Google Scholar 

  • Ross RM (1982b) Energetics of Euphausia pacifica. II. Complete carbon and nitrogen budgets at 8 ° and 12 °C throughout the life span. Mar Biol 68:15–23

    Article  CAS  Google Scholar 

  • Rudnick D, Resh V (2005) Stable isotopes, mesocosms and gut content analysis demonstrate trophic differences in two invasive decapod crustacea. Freshw Biol 50:1323–1336

    Article  Google Scholar 

  • Sarbu SM (2001) Movile cave: a chemoautotrophically based groundwater ecosystem. In: Wilkens H, Culver DC, Humphreys WF (eds) Ecosystems of the world: subterranean ecosystems. Elsevier, New York, pp 319–344

  • Schneider K, Christman MC, Fagan WF (2011) The influence of resource subsidies on cave invertebrates: results from an ecosystem-level manipulation experiment. Ecology 93:765–776

    Article  Google Scholar 

  • Schwarz CJ, Arnason AN (1996) A general methodology for the analysis of capture–recapture experiments in open populations. Biometrics 52:860–873

    Article  Google Scholar 

  • Simon K, Benfield E (2001) Leaf and wood breakdown in cave streams. J N Am Benthol Soc 20:550–563

    Article  Google Scholar 

  • Simon KS, Buikema AL (1997) Effects of organic pollution on an Appalachian cave: changes in macroinvertebrate populations and food supplies. Am Midl Nat 138:387–401

    Article  Google Scholar 

  • Simon K, Benfield E, Macko S (2003) Food web structure and the role of epilithic biofilms in cave streams. Ecology 84:2395–2406

    Article  Google Scholar 

  • Simon KS, Pipan T, Culver DC (2007) A conceptual model of the flow and distribution of organic carbon in caves. J Cave Karst Stud 69:279–284

    CAS  Google Scholar 

  • Sinton LW (1984) The macroinvertebrates in a sewage-polluted aquifer. Hydrobiology 119:161–169

    Article  Google Scholar 

  • Sket B (1999) The nature of biodiversity in hypogean waters and how it is endangered. Biodivers Conserv 8:1319–1338

    Article  Google Scholar 

  • Sket B (2005) Dinaric karst, diversity. In: Culver DC, White WB (eds) Encyclopedia of caves. Elsevier/Academic, New York, pp 158–165

  • Smith GA, Nickels JS, Kerger BD, Davis JD, Collins SP, Wilson JT, Mcnabb JF, White DC (1986) Quantitative characterization of microbial biomass and community structure in subsurface material: a prokaryotic consortium responsive to organic contamination. Can J Microbiol 32:104–111

    Article  CAS  Google Scholar 

  • Smock LA, Roeding CE (1986) The trophic basis of production of the macroinvertebrate community of a southeastern USA blackwater stream. Ecography 9:165–174

    Article  Google Scholar 

  • Spänhoff B, Meyer EI (2004) Breakdown rates of wood in streams. J N Am Benthol Soc 23:189–197

    Article  Google Scholar 

  • Stagliano DM, Whiles MR (2002) Macroinvertebrate production and trophic structure in a tallgrass prairie headwater stream. J N Am Benthol Soc 21:97–113

    Article  Google Scholar 

  • Strayer D (1988) On the limits to secondary production. Limnol Oceanogr 33:1217–1220

    Article  Google Scholar 

  • Strayer DL (1994) Limits to biological distributions in groundwater. In: Gibert J, Danielopol DL, Stanford JA (eds) Groundwater ecology. Academic, San Diego, pp 287–313

  • Tobler M, Schlupp I, Heubel KU, Riesch R, De León FJG, Giere O, Plath M (2006) Life on the edge: hydrogen sulfide and the fish communities of a Mexican cave and surrounding waters. Extremophiles 10:577–585

    Article  PubMed  CAS  Google Scholar 

  • Vanderklift MA, Ponsard S (2003) Sources of variation in consumer-diet δ15N enrichment: a meta-analysis. Oecologia 136:169–182

    Article  PubMed  Google Scholar 

  • Veliscek Carolan V, Mazumder D, Dimovski C, Diocares R, Twining J (2012) Biokinetics and discrimination factors for δ13C and δ15N in the omnivorous freshwater crustacean, Cherax destructor. Mar Freshw Res 63:878–886

    Article  Google Scholar 

  • Venarsky MP, Huryn AD, Benstead JP (2012a) Re-examining extreme longevity of the cave crayfish Orconectes australis using new mark–recapture data: a lesson on the limitations of iterative size-at-age models. Freshw Biol 57:1471–1481

  • Venarsky MP, Benstead JP, Huryn AD (2012b) Effects of organic matter and season on leaf litter colonization and breakdown in cave streams. Freshw Biol 57:773–786

    Article  Google Scholar 

  • Villarreal H (1991) A partial energy budget for the Australian crayfish Cherax tenuimanus. J World Aquac Soc 22:252–259

    Article  Google Scholar 

  • Wallace JB, Eggert S, Meyer JL, Webster J (1999) Effects of resource limitation on a detrital-based ecosystem. Ecol Monogr 69:409–442

    Article  Google Scholar 

  • Ward GM, Cummins KW (1979) Effects of food quality on growth of a stream detritivore, Paratendipes albimanus (Meigen) (Diptera: Chironomidae). Ecology 60:57–64

    Article  Google Scholar 

  • Weingartner D (1977) Production and trophic ecology of two crayfish species cohabiting an Indiana cave. PhD dissertation. Michigan State University, East Lansing

  • Wood P, Gunn J, Perkins J (2002) The impact of pollution on aquatic invertebrates within a subterranean ecosystem: out of sight out of mind. Arch Hydrobiol 155:223–237

    Google Scholar 

Download references

Acknowledgments

Funding for this project was provided by the University of Alabama and two State Wildlife Grants entitled “Assessment of population dynamics of cave inhabiting crayfish in Alabama” to ADH and BRK (grant # T-03-02 and T-3-3-2). We are grateful to Horace Clemens and the Southeastern Cave Conservancy for cave access. Thanks to Chau Tran, Jim Godwin, Justin Cook, Tom Heatherly, Michael Kendrick, Randall Blackwood, Stuart W. McGregor, Lauren Showalter, Mica Junior, Dru Holla, Tim Wynn, Cameron Craig, Samantha Richter, Chase Moon, Jonathan Hopper, Jessica Rogers, James Ramsey, Mick Demi, Dan Nelson, Brook Fluker, Derrick Wells, and Michael Sandel for their assistance in the field and laboratory. We also thank Bob Hall, Kevin Simon, and two anonymous reviewers for comments that improved earlier versions of this manuscript.

Author information

Author notes

  1. Michael P. Venarsky

    Present address: United States Geological Survey, Fort Collins Science Center, 2150 Centre Ave, Building C, Fort Collins, CO, 80526, USA

Authors and Affiliations

  1. Department of Biological Sciences, University of Alabama, Box 870206, Tuscaloosa, AL, 35487, USA

    Michael P. Venarsky, Alexander D. Huryn & Jonathan P. Benstead

  2. Division of Forestry and Natural Resources, West Virginia University, Morgantown, WV, 26506, USA

    Brock M. Huntsman

  3. Tennessee Aquarium Conservation Institute, Chattanooga, TN, 37402, USA

    Bernard R. Kuhajda

Authors
  1. Michael P. Venarsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Brock M. Huntsman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alexander D. Huryn
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jonathan P. Benstead
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bernard R. Kuhajda
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michael P. Venarsky.

Additional information

Communicated by Robert O. Hall.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 74 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Venarsky, M.P., Huntsman, B.M., Huryn, A.D. et al. Quantitative food web analysis supports the energy-limitation hypothesis in cave stream ecosystems. Oecologia 176, 859–869 (2014). https://doi.org/10.1007/s00442-014-3042-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-014-3042-3

Keywords

Search

Navigation