Oecologia

, Volume 178, Issue 1, pp 239–248

Trophic dynamics in an aquatic community: interactions among primary producers, grazers, and a pathogenic fungus

  • Julia C. Buck
  • Katharina I. Scholz
  • Jason R. Rohr
  • Andrew R. Blaustein
Community ecology - Original research

Abstract

Free-living stages of parasites are consumed by a variety of predators, which might have important consequences for predators, parasites, and hosts. For example, zooplankton prey on the infectious stage of the amphibian chytrid fungus, Batrachochytrium dendrobatidis (Bd), a pathogen responsible for amphibian population declines and extinctions worldwide. Predation on parasites is predicted to influence community structure and function, and affect disease risk, but relatively few studies have explored its consequences empirically. We investigated interactions among Rana cascadae tadpoles, zooplankton, and Bd in a fully factorial experiment in outdoor mesocosms. We measured growth, development, survival, and infection of amphibians and took weekly measurements of the abundance of zooplankton, phytoplankton (suspended algae), and periphyton (attached algae). We hypothesized that zooplankton might have positive indirect effects on tadpoles by consuming Bd zoospores and by consuming phytoplankton, thus reducing the shading of a major tadpole resource, periphyton. We also hypothesized that zooplankton would have negative effects on tadpoles, mediated by competition for algal resources. Mixed-effects models, repeated-measures ANOVAs, and a structural equation model revealed that zooplankton significantly reduced phytoplankton but had no detectable effects on Bd or periphyton. Hence, the indirect positive effects of zooplankton on tadpoles were negligible when compared to the indirect negative effect mediated by competition for phytoplankton. We conclude that examination of host-pathogen dynamics within a community context may be necessary to elucidate complex community dynamics.

Keywords

Batrachochytrium dendrobatidis Food web Pathogen Structural equation modeling Trophic cascade 

References

  1. Altig R, Whiles MR, Taylor CL (2007) What do tadpoles really eat? Assessing the trophic status of an understudied and imperiled group of consumers in freshwater habitats. Freshwater Biol 52:386–395CrossRefGoogle Scholar
  2. Altwegg R, Reyer HU (2003) Patterns of natural selection on size at metamorphosis in water frogs. Evolution 57:872–882CrossRefPubMedGoogle Scholar
  3. Blaustein AR, Romansic JM, Scheessele EA, Han BA, Pessier AP, Longcore JE (2005) Interspecific variation in susceptibility of frog tadpoles to the pathogenic fungus Batrachochytrium dendrobatidis. Conserv Biol 19:1460–1468CrossRefGoogle Scholar
  4. Boone MD, Semlitsch RD (2001) Interactions of an insecticide with larval density and predation in experimental amphibian communities. Conserv Biol 15:228–238CrossRefGoogle Scholar
  5. Boone MD, Semlitsch RD (2002) Interactions of an insecticide with competition and pond drying in amphibian communities. Ecol Appl 12:307–316CrossRefGoogle Scholar
  6. Boone MD, Semlitsch RD (2003) Interaction of bullfrog tadpole predators and an insecticide: Predation release and facilitation. Oecologia 137:610–616CrossRefPubMedGoogle Scholar
  7. Boyle DG, Boyle DB, Olsen V, Morgan JAT, Hyatt AD (2004) Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Dis Aquat Org 60:141–148CrossRefPubMedGoogle Scholar
  8. Briggs CJ, Knapp RA, Vredenburg VT (2010) Enzootic and epizootic dynamics of the chytrid fungal pathogen of amphibians. PNAS 107:9695–9700CrossRefPubMedCentralPubMedGoogle Scholar
  9. Brown JH, Davidson DW (1977) Competition between seed-eating rodents and ants in desert ecosystems. Science 196:880–882CrossRefPubMedGoogle Scholar
  10. Buck JC, Truong L, Blaustein AR (2011) Predation by zooplankton on Batrachochytrium dendrobatidis: biological control of the deadly amphibian chytrid fungus? Biodivers Conserv 20:3549–3553CrossRefGoogle Scholar
  11. Buck JC, Scheessele EA, Relyea RA, Blaustein AR (2012) The effects of multiple stressors on wetland communities: pesticides, pathogens, and competing amphibians. Freshwater Biol 57:61–73CrossRefGoogle Scholar
  12. Fisher MC, Garner TWJ, Walker SF (2009) Global emergence of Batrachochytrium dendrobatidis and amphibian chytridiomycosis in space, time, and host. Annu Rev Microbiol 63:291–310CrossRefPubMedGoogle Scholar
  13. Gleason FH, Kagami M, Lefevre E, Sime-Ngando T (2008) The ecology of chytrids in aquatic ecosystems: roles in food web dynamics. Fungal Biol Rev 2:17–25CrossRefGoogle Scholar
  14. Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190Google Scholar
  15. Grace JB (2006) Structural equation modeling and natural systems. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  16. Hamilton PT, Richardson JML, Anholt BR (2012) Daphnia in tadpole mesocosms: trophic links and interactions with Batrachochytrium dendrobatidis. Freshwater Biol 57:676–683CrossRefGoogle Scholar
  17. Han BA, Bradley PW, Blaustein AR (2008) Ancient behaviors of larval amphibians in response to an emerging fungal pathogen, Batrachochytrium dendrobatidis. Behav Ecol Sociobiol 63:241–250CrossRefGoogle Scholar
  18. Jennings DE, Krupa JJ, Raffel TR, Rohr JR (2010) Evidence for competition between carnivorous plants and spiders. Proc R Soc B—Biol Sci 277:3001–3008Google Scholar
  19. Johnson PTJ, Dobson A, Lafferty KD, Marcogliese DJ, Memmott J, Orlofske SA, Poulin R, Thietges DW (2010) When parasites become prey: ecological and epidemiological significance of eating parasites. Trends Ecol Evol 25:362–371CrossRefPubMedGoogle Scholar
  20. Kagami M, Van Donk E, de Bruin A, Rijkeboer M, Ibelings BW (2004) Daphnia can protect diatoms from fungal parasitism. Limnol Oceanogr 49:680–685CrossRefGoogle Scholar
  21. Kagami M, von Elert E, Ibelings BW, de Bruin A, Van Donk E (2007) The parasitic chytrid, Zygorhizidium, facilitates the growth of the cladoceran zooplankter, Daphnia, in cultures of the inedible alga, Asterionella. Proc R Soc B 274:1561–1566CrossRefPubMedCentralPubMedGoogle Scholar
  22. Keesing F, Belden LK, Daszak P, Dobson A, Harvell CD, Holt RD, Hudson P, Jolles A, Jones KE, Mitchell CE, Myers SS, Bogich T, Ostfeld RS (2010) Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468:647–652CrossRefPubMedGoogle Scholar
  23. Knisely K, Geller W (1986) Selective feeding of 4 zooplankton species on natural lake phytoplankton. Oecologia 69:86–94CrossRefGoogle Scholar
  24. Lafferty KD, Dobson AP, Kuris AM (2006) Parasites dominate food web links. PNAS 103:11211–11216CrossRefPubMedCentralPubMedGoogle Scholar
  25. Larson GL, McIntire CD, Buktenica MW, Girdner SF, Truitt RE (2007) Distribution and abundance of zooplankton populations in Crater Lake, Oregon. Hydrobiologia 574:217–233CrossRefGoogle Scholar
  26. Leibold MA, Wilbur HM (1992) Interactions between food-web structure and nutrients on pond organisms. Nature 360:341–343CrossRefGoogle Scholar
  27. Longcore JE, Pessier AP, Nichols DK (1999) Batrachochytrium dendrobatidis gen. et sp.nov., a chytrid pathogenic to amphibians. Mycologia 91:219–227CrossRefGoogle Scholar
  28. McIntire CD, Larson GL, Truitt RE, Debacon MK (1996) Taxonomic structure and productivity of phytoplankton assmblages in Crater Lake, Oregon. J Lake Reservior Manage 12:259–280CrossRefGoogle Scholar
  29. Mendelson JR, Lips KR, Gagliardo RW, Rabb GB, Collins JP, Diffendorfer JE, Daszak P, Ibanez R, Zippel KC, Lawson DP, Wright KM, Stuart SN, Gascon C, da Silva HR, Burrowes PA, Joglar RL, La Marca E, Lotters S, du Preez LH, Weldon C, Hyatt A, Rodriguez-Mahecha JV, Hunt S, Robertson H, Lock B, Raxworthy CJ, Frost DR, Lacy RC, Alford RA, Campbell JA, Parra-Olea G, Bolanos F, Domingo JJC, Halliday T, Murphy JB, Wake MH, Coloma LA, Kuzmin SL, Price MS, Howell KM, Lau M, Pethiyagoda R, Boone M, Lannoo MJ, Blaustein AR, Dobson A, Griffiths RA, Crump ML, Wake DB, Brodie ED (2006) Biodiversity. Confronting amphibian declines and extinctions. Science 313:48CrossRefPubMedGoogle Scholar
  30. Metcalfe NB, Monaghan P (2001) Compensation for a bad start: grow now, pay later? Trends Ecol Evol 16:254–260CrossRefPubMedGoogle Scholar
  31. Mokany A, Shine R (2003) Competition between tadpoles and mosquito larvae. Oecologia 135:615–620CrossRefPubMedGoogle Scholar
  32. Morin PJ, Lawler SP, Johnson EA (1988) Competition between aquatic insects and vertebrates: interaction strength and higher-order interactions. Ecology 69:1401–1409CrossRefGoogle Scholar
  33. Oregon Department of Environmental Quality (1998) Columbia Slough total maximum daily loads (TMDLs) for: chlorophyll a, dissolved oxygen, pH, phosphorus, bacteria, DDE/DDT, PCBs, Pb, dieldrin, and 2,3,7,8 TCDD. www.deq.state.or.us/wq/tmdls/docs/willamettebasin/columbiaslough/tmdl.pdf
  34. Pace ML, Funke E (1991) Regulation of planktonic microbial communities by nutrients and herbivores. Ecology 72:904–914CrossRefGoogle Scholar
  35. Parris MJ, Beaudoin JG (2004) Chytridiomycosis impacts predator-prey interactions in larval amphibian communities. Oecologia 140:626–632CrossRefPubMedGoogle Scholar
  36. Parris MJ, Cornelius TO (2004) Fungal pathogen causes competitive and developmental stress in larval amphibian communities. Ecology 85:3385–3395CrossRefGoogle Scholar
  37. Parris MJ, Reese E, Storfer A (2006) Antipredator behavior of chytridiomycosis infected northern leopard frog (Rana pipiens) tadpoles. Can J Zool 84:58–65CrossRefGoogle Scholar
  38. Piotrowski JS, Annis SL, Longcore JE (2004) Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. Mycologia 96:9–15CrossRefPubMedGoogle Scholar
  39. Relyea RA (2005) The impact of insecticides and herbicides on the biodiversity and productivity of aquatic communities. Ecol Appl 15:618–627CrossRefGoogle Scholar
  40. Relyea RA, Diecks N (2008) An unforeseen chain of events: lethal effects of pesticides on frogs at sublethal concentrations. Ecol Appl 18:1728–1742CrossRefPubMedGoogle Scholar
  41. Retallick RWR, Miera V, Richards KL, Field KJ, Collins JP (2006) A non-lethal technique for detecting the chytrid fungus Batrachochytrium dendrobatidis on tadpoles. Dis Aquat Org 72:77–85CrossRefPubMedGoogle Scholar
  42. Rohr JR, Crumrine PW (2005) Effects of an herbicide and an insecticide on pond community structure and processes. Ecol Appl 15:1135–1147CrossRefGoogle Scholar
  43. Rohr JR, Palmer BD (2013) Climate change, multiple stressors, and the decline of ectotherms. Conserv Biol 27:741–751CrossRefPubMedGoogle Scholar
  44. Rohr JR, Sager T, Sesterhenn TM, Palmer BD (2006) Exposure, postexposure, and density-mediated effects of atrazine on amphibians: breaking down net effects into their parts. Environ Health Perspect 114:46–50CrossRefPubMedCentralPubMedGoogle Scholar
  45. Rohr JR, Raffel TR, Romansic JM, McCallum H, Hudson PJ (2008a) Evaluating the links between climate, disease spread, and amphibian declines. PNAS 105:17436–17441CrossRefPubMedCentralPubMedGoogle Scholar
  46. Rohr JR, Schotthoefer AM, Raffel TR, Carrick HJ, Halstead N, Hoverman JT, Johnson CM, Johnson LB, Lieske C, Piwoni MD, Schoff PK, Beasley VR (2008b) Agrochemicals increase trematode infection in a declining amphibian species. Nature 455:1235–1240CrossRefPubMedGoogle Scholar
  47. Sanders RW, Porter KG (1990) Bacterivorous flagellates as food resources for the freshwater crustacean zooplankter Daphnia ambigua. Limnol Oceanogr 35:188–191CrossRefGoogle Scholar
  48. Schoener TW, Spiller DA (1987) Effects of lizards on spider populations: manipulative reconstruction of a natural experiment. Science 236:949–952CrossRefPubMedGoogle Scholar
  49. Seale DB (1980) Influence of amphibian larvae on primary production, nutrient flux, and competition on a pond ecosystem. Ecology 61:1531–1550CrossRefGoogle Scholar
  50. Seale DB (1982) Obligate and facultative suspension feeding in anuran larvae—feeding regulation in Xenopus and Rana. Biol Bull 162:214–231CrossRefGoogle Scholar
  51. Searle CL, Gervasi SS, Hua J, Hammond JI, Relyea RA, Olson DH, Blaustein AR (2011) Differential host susceptibility to Batrachochytrium dendrobatidis, an emerging amphibian pathogen. Conserv Biol 25:965–974CrossRefPubMedGoogle Scholar
  52. Searle CL, Mendelson JR III, Green LE, Duffy MA (2013) Daphnia predation on the amphibian chytrid fungus and its impacts on disease risk in tadpoles. Ecol Evol 3:4129–4138CrossRefPubMedCentralPubMedGoogle Scholar
  53. Skerratt LF, Berger L, Speare R, Cashins S, McDonald KR, Phillott AD, Hines HB, Kenyon N (2007) Spread of chytridiomycosis has cause the rapid global decline and extinction of frogs. EcoHealth 4:125–134CrossRefGoogle Scholar
  54. Thieltges DW, Amundsen PA, Hechinger RF, Johnson PTJ, Lafferty KD, Mouritsen KN, Preston DL, Reise K, Zander CD, Poulin R (2013) Parasites as prey in aquatic food webs: implications for predator infection and parasite transmission. Oikos 122:1473–1482Google Scholar
  55. Venesky MD, Parris MJ, Storfer A (2009) Impacts of Batrachochytrium dendrobatidis infection of tadpole foraging performance. EcoHealth 6:565–575CrossRefPubMedGoogle Scholar
  56. Venesky MD, Liu X, Sauer EL, Rohr JR (2014) Linking manipulative experiments to field data to test the dilution effect. J Anim Ecol 83:557–565. doi:10.1111/1365-2656.12159 Google Scholar
  57. Vredenburg VT, Knapp RA, Tunstall TS, Briggs CJ (2010) Dynamics of an emerging disease drive large-scale amphibian population extinctions. PNAS 107:9689–9694CrossRefPubMedCentralPubMedGoogle Scholar
  58. Wake DB, Vredenburg VT (2008) Are we in the midst of the sixth mass extinction? A view from the world of amphibians. PNAS 105:11466–11473CrossRefPubMedCentralPubMedGoogle Scholar
  59. Welschmeyer NA (1994) Fluorometric analysis of chlorophyll-a in the presence of chlorophyll-b and pheopigments. Limnol Oceanogr 39:1985–1992CrossRefGoogle Scholar
  60. Whiles M, Gladyshev MI, Sushchik NN, Makhutova ON, Kalachova GS, Peterson SD (2010) Fatty acid analyses reveal high degrees of omnivory and dietary plasticity in pond-dwelling tadpoles. Freshwater Biol 55:1533–1547CrossRefGoogle Scholar
  61. Woodhams DC, Bosch J, Briggs CJ, Cashins S, Davis LR, Lauer A, Muths E, Puschendorf R, Schmidt BR, Sheafor B, Voyles J (2011) Mitigating amphibian disease: strategies to maintain wild populations and control chytridiomycosis. Front Zool 8:8CrossRefPubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Julia C. Buck
    • 1
    • 4
  • Katharina I. Scholz
    • 2
  • Jason R. Rohr
    • 3
  • Andrew R. Blaustein
    • 1
  1. 1.Department of Integrative BiologyOregon State UniversityCorvallisUSA
  2. 2.Agricultural SciencesUniversity of HohenheimStuttgartGermany
  3. 3.Department of Integrative BiologyUniversity of South FloridaTampaUSA
  4. 4.Texas Research Institute for Environmental StudiesSam Houston State UniversityHuntsvilleUSA

Personalised recommendations