Aquatic Sciences

, Volume 74, Issue 3, pp 397–404 | Cite as

Species loss in the brown world: are heterotrophic systems inherently stable?

  • Michael J. Rubbo
  • Lisa K. Belden
  • Sara I. Storrs-Mendez
  • Jonathan J. Cole
  • Joseph M. Kiesecker
Research Article


Determining the effects of species loss on ecosystems has received considerable attention given the current threats many ecosystems are facing. A significant body of research has yielded many insights to this question, but this work has been limited by a focus on ecosystems where primary production plays a significant role in energy transfer. As many ecosystems rely on energy sources that are not derived from in situ production, there is a need to better understand how species loss will affect ecosystems of varying trophic states. To examine the effects of species loss on an ecosystem that is not reliant on in situ primary production, we manipulated the larval amphibian community of temporary forest ponds. These ponds are heterotrophic systems that rely on allochthonous inputs of detritus as a basal energy source. The larvae of two amphibian species that are prone to local extinction, wood frogs (Lithobates sylvatica) and spotted salamanders (Ambystoma maculatum), were removed from ponds and net ecosystem production was monitored. We found no effects of the removal of these top consumers on ecosystem functioning or on lower trophic groups (i.e., zooplankton, algae, bacteria). While amphibians can influence food web dynamics in other systems, their influence on system processes in temporary forest ponds appears to be limited. We hypothesize that the lack of any effects is due to the microbial degradation of detritus “swamping” the system, providing more than enough energy to maintain the food web, and/or due to omnivory dampening species interactions. These data indicate that the functioning of heterotrophic systems may be inherently stable due to internal dynamics that minimize interaction strengths among trophic groups.


Heterotrophic Biodiversity Ecosystem function Detritus Amphibian 



We thank J. Chase for reviewing an earlier draft of this manuscript and J. Falkenbach and L. Grove for assistance with field work. Financial support was provided by the NIH/NSF Ecology of Infectious Disease Program (1R01ES11067-01 to JMK) and NSF (IBN) Grant #0131229 to JMK, and the Department of Biology, Pennsylvania State University.


  1. Balvanera P, Pfisterer AB, Buchmann N, He JS, Nakashizuka T, Raffaelli D, Schmid B (2006) Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecol Lett 9:1146–1156PubMedCrossRefGoogle Scholar
  2. Batzer DP, Palik BJ, Buech R (2004) Relationships between environmental characteristics and macroinvertebrate communities in seasonal woodland ponds in Minnesota. J North Am Benthol Soc 23:50–68CrossRefGoogle Scholar
  3. Bonner LA, Diehl WJ, Altig R (1997) Physical, chemical, and biological dynamics of five temporary dystrophic forest pools in central Mississippi. Hydrobiologia 353:77–89CrossRefGoogle Scholar
  4. Cardinale BJ, Srivastava DS, Duffy JE, Wright JP, Downing AL, Sankaran M, Jouseau C (2006) Effects of biodiversity on the functioning of trophic groups and ecosystems. Nature 443:989–992PubMedCrossRefGoogle Scholar
  5. Chase JM (2003) Strong and weak trophic cascades along a productivity gradient. Oikos 101:187–195CrossRefGoogle Scholar
  6. Cole JJ, Pace ML, Carpenter SR, Kitchell JF (2000) Persistence of net heterotrophy in lakes during nutrient addition and food web manipulation. Limnol Oceanogr 45:1718–1730CrossRefGoogle Scholar
  7. Colon-Gaud C, Whiles MR, Kilham SS, Lips KR, Pringle CM, Connelly S, Peterson SD (2009) Assessing ecological responses to catastrophic amphibian declines: patterns of macroinvertebrate production and food web structure in Panamanian streams. Limnol Oceanogr 54:331–343CrossRefGoogle Scholar
  8. de Ruiter PC, Neutel AM, Moore JC (1995) Energetics, patterns of interaction strengths, and stability in real ecosystems. Science 269:1257–1260PubMedCrossRefGoogle Scholar
  9. Dodds WK, Cole JJ (2007) Expanding the concept of trophic state in aquatic ecosystems: it’s not just the autotrophs. Aquat Sci 69:427–439CrossRefGoogle Scholar
  10. Downing AL (2005) Relative effects of species composition and richness on pond ecosystem properties in ponds. Ecology 86:701–715CrossRefGoogle Scholar
  11. Duarte CM, Prairie YT (2005) Prevalence of heterotrophy and atmospheric CO2 emissions from aquatic ecosystems. Ecosystems 8:862–870CrossRefGoogle Scholar
  12. Dudgeon D (2010) Prospects for sustaining freshwater biodiversity in the 21st century: linking ecosystem structure and function. Curr Opin Environ Sustain 2:422–430CrossRefGoogle Scholar
  13. Duffy JE (2003) Biodiversity loss, trophic skew and ecosystem functioning. Ecol Lett 6:680–687CrossRefGoogle Scholar
  14. Gessner MO, Swan CM, Dang CK, McKie BG, Bardgett RD, Wall DH, Hattenschwiler S (2010) Diversity meets decomposition. Trends Ecol Evol 25:372–380PubMedCrossRefGoogle Scholar
  15. Hairston NG Jr, Hairston NG Sr (1993) Cause-effect relationships in energy flow, trophic structure, and interspecific interactions. Am Nat 142:379–411CrossRefGoogle Scholar
  16. Hairston NG Sr, Smith FE, Slobodkin LB (1960) Community structure, population control, and competition. Am Nat 94:421–425CrossRefGoogle Scholar
  17. Hall RO Jr, Meyer JL (1998) The trophic significance of bacteria in a detritus-based stream food web. Ecology 79:1995–2012CrossRefGoogle Scholar
  18. Harper EB, Rittenhouse TA, Semlitsch RD (2008) Demographic consequences of terrestrial habitat loss for pool-breeding amphibians: predicting extinction risks associated with inadequate size of buffer zones. Conserv Biol 22:1205–1215PubMedCrossRefGoogle Scholar
  19. Harris PM (1995) Are autecologically similar species also functionally similar? A test in pond communities. Ecology 76:544–552CrossRefGoogle Scholar
  20. Holomuzki JR, Collins JP, Brunkow PE (1994) Trophic control of fishless ponds by tiger salamander larvae. Oikos 71:55–64CrossRefGoogle Scholar
  21. Jansson M, Persson L, De Roos AM, Jones RI, Tranvik. LJ (2007) Terrestrial carbon and intraspecific size-variation shape lake ecosystems. Trends Ecol Evol 22:316–322PubMedCrossRefGoogle Scholar
  22. Kupferberg S (1997) Facilitation of periphyton production by tadpole grazing: functional differences between species. Freshw Biol 37:427–439CrossRefGoogle Scholar
  23. Lecerf A, Richardson JS (2009) Biodiveristy–ecosystem function research: insight gained from streams. River Res Appl 26:45–54CrossRefGoogle Scholar
  24. Leeper DA, Taylor BE (1998) Abundance, biomass and production of aquatic invertebrates in Rainbow Bay, a temporary wetland in South Carolina USA. Arch Hydrobiol 143:335–362Google Scholar
  25. Lindeman RL (1942) The trophic-dynamic aspect of ecology. Ecology 23:399–418CrossRefGoogle Scholar
  26. Mikola J, Setala H (1998) No evidence of trophic cascades in an experimental microbial-based food web. Ecology 79:153–164CrossRefGoogle Scholar
  27. Moore JC, Berlow EL, Coleman DC, deRuiter PC, Dong Q, Hastings A, Collins Johnson N, McCann KS, Melville K, Morin PJ, Nadelhoffer K, Rosemond AD, Post DM, Sabo JL, Scow KM, Vanni MJ, Wall DH et al (2004) Detritus, trophic dynamics and biodiversity. Ecol Lett 7:584–600CrossRefGoogle Scholar
  28. Pace ML, Cole JJ (1994) Comparative and experimental approaches to top-down and bottom-up regulation of bacteria. Microb Ecol 28:181–193CrossRefGoogle Scholar
  29. Pace ML, Cole JJ, Carpenter SR, Kitchell JF (1999) Trophic cascades revealed in diverse ecosystems. Trends Ecol Evol 14:483–488PubMedCrossRefGoogle Scholar
  30. Pace ML, Cole JJ, Carpenter SR, Kitchell JF, Hodgson JR, Van de Bogert MC, Bade DL, Kritzberg ES, Bastviken D (2004) Whole-lake carbon-13 additions reveal terrestrial support of aquatic food webs. Nature 427:240–243PubMedCrossRefGoogle Scholar
  31. Petchey OL, Downing AL, Mittlebach GG, Persson L, Steiner CF, Warren PH, Woodward G (2004) Species loss and the structure and functioning of multitrophic aquatic systems. Oikos 104:467–478CrossRefGoogle Scholar
  32. Petranka JW (1998) Salamanders of the United States and Canada. Smithsonian Institution Press, Washington, D.C.Google Scholar
  33. Polis GA, Strong DR (1996) Food web complexity and community dynamics. Am Nat 147:813–846CrossRefGoogle Scholar
  34. 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 Syst 28:289–316CrossRefGoogle Scholar
  35. Regester KJ, Lips KR, Whiles MR (2006) Energy flow and subsidies associated with the complex life cycle of ambystomatid salamanders in ponds and adjacent forest in southern Illinois. Oecologia 147:303–314PubMedCrossRefGoogle Scholar
  36. Reiss J, Bridle JR, Montoya JM, Woodward G (2009) Emerging horizons in biodiversity and ecosystem functioning research. Trends Ecol Evol 24:505–514PubMedCrossRefGoogle Scholar
  37. Romanuk TN, Vogt RJ, Kolasa J (2009) Ecological realism and mechanisms by which diversity begets stability. Oikos 118:819–828CrossRefGoogle Scholar
  38. Rubbo MJ, Kiesecker JM (2004) Leaf litter composition and community structure: translating regional species changes into local dynamics. Ecology 85:2519–2525CrossRefGoogle Scholar
  39. Rubbo MJ, Kiesecker JM (2005) Amphibian breeding distribution in an urbanized landscape. Conserv Biol 19:504–511CrossRefGoogle Scholar
  40. Rubbo MJ, Cole JJ, Kiesecker JM (2006a) Terrestrial subsidies of organic carbon support net ecosystem production in temporary forest ponds: evidence from an ecosystem experiment. Ecosystems 9:1170–1176CrossRefGoogle Scholar
  41. Rubbo MJ, Shea K, Kiesecker JM (2006b) The influence of multi-stage predation on population growth and the distribution of the pond-breeding salamander (Ambystoma jeffersonianum). Can J Zool 84:449–458CrossRefGoogle Scholar
  42. Seale DB (1980) Influence of amphibian larvae on primary production, nutrient flux, and competition in a pond ecosystem. Ecology 61:1531–1550CrossRefGoogle Scholar
  43. Shurin JB, Gruner DS, Hillebrand H (2006) All wet or dried up? Real differences between aquatic and terrestrial food webs. Proc R Soc B 273:1–9PubMedCrossRefGoogle Scholar
  44. Skelly DK (2002) Experimental venue and estimation of interaction strength. Ecology 83:2097–2101CrossRefGoogle Scholar
  45. Skelly DK, Golon J (2003) Assimilation of natural benthic substrates by two species of tadpoles. Herpetolgica 59:37–42CrossRefGoogle Scholar
  46. Smith DC, Azam F (1992) A simple, economical method for measuring bacterial protein synthesis rates in sea water using 3H-leucine. Mar Microb Food Webs 6:107–114Google Scholar
  47. Thebault E, Loreau M (2003) Food-web constraints on biodiversity–ecosystem functioning relationships. Proc Nat Acad Sci 100:14949–14954PubMedCrossRefGoogle Scholar
  48. Tranvik K (1992) Allochthonous dissolved organic matter as an energy source for pelagic bacteria and the concept of the microbial loop. Hydrobiologia 229:107–114CrossRefGoogle Scholar
  49. Wallace JB, Eggert SL, Meyer JL, Webster JR (1997) Multiple trophic levels of a forest stream linked to terrestrial leaf litter inputs. Science 277:102–104CrossRefGoogle Scholar
  50. Wetzel RG (1995) Death, detritus, and energy flow in aquatic ecosystems. Freshw Biol 33:83–89CrossRefGoogle Scholar
  51. Whiles MR, Lips KR, Pringle CM, Kilham SS, Brenes R, Connelly S, Colon Gaud JC, Hunte-Brown M, Huryn AD, Montgomery C, Peterson S (2006) The consequences of amphibian population declines to the structure and function of neotropical stream ecosystems. Front Ecol Environ 4:27–34CrossRefGoogle Scholar
  52. Whiles MR, Gladyshev MI, Sushchik NN, Makhutova ON, Kalachova GS, Peterson SD, Regester KJ (2010) Fatty acid analyses reveal high degrees of omnivory and dietary plasticity in pond-dwelling tadpoles. Freshw Biol 55:1533–1547CrossRefGoogle Scholar
  53. Wilbur HM (1997) Experimental ecology of food webs: complex systems in temporary ponds. Ecology 78:2279–2302CrossRefGoogle Scholar

Copyright information

© Springer Basel AG 2011

Authors and Affiliations

  • Michael J. Rubbo
    • 1
  • Lisa K. Belden
    • 2
  • Sara I. Storrs-Mendez
    • 3
  • Jonathan J. Cole
    • 4
  • Joseph M. Kiesecker
    • 5
  1. 1.Teatown Lake ReservationOssiningUSA
  2. 2.Department of Biological SciencesVirginia Polytechnic Institute and State UniversityBlacksburgUSA
  3. 3.Division of Biological SciencesUniversity of MissouriColumbiaUSA
  4. 4.Cary Institute of Ecosystem StudiesMillbrookUSA
  5. 5.The Nature ConservancyFort CollinsUSA

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