Advertisement

Oecologia

, Volume 173, Issue 1, pp 95–105 | Cite as

Plastic changes in tadpole trophic ecology revealed by stable isotope analysis

  • Stéphane CautEmail author
  • Elena Angulo
  • Carmen Díaz-Paniagua
  • Ivan Gomez-Mestre
Population ecology - Original research

Abstract

Amphibian larvae constitute a large fraction of the biomass of wetlands and play important roles in their energy flux and nutrient cycling. Interactions with predators and competitors affect their abundance but also their foraging behaviour, potentially leading to non-consumptive cascading effects on the whole trophic web. We experimentally tested for plastic changes in larval trophic ecology of two anuran species in response to competitors and the non-lethal presence of native and non-native predators, using stable isotope analysis. We hypothesized that tadpoles would alter their diet in the presence of competitors and native predators, and to a lesser extent or not at all in the presence of non-native predators. First, we conducted a controlled diet experiment to estimate tadpole turnover rates and discrimination factors using Pelobates cultripes and Bufo calamita. Turnover rates yielded a half-life of 15–20 days (attaining a quasi-isotopic equilibrium after 2 months), whereas discrimination factors for natural controlled diets resulted in different isotopic values essential for calibration. Second, we did an experiment with P. cultripes and Rana perezi (=Pelophylax perezi) where we manipulated the presence/absence of predators and heterospecific tadpoles using microcosms in the laboratory. We detected a significant shift in trophic status of both amphibian species in the presence of non-native crayfish: the δ15N values and macrophyte consumption of tadpoles increased, whereas their detritus consumption decreased. This suggests that tadpoles could have perceived crayfish as a predatory risk or that crayfish acted as competitors for algae and zooplankton. No dietary changes were observed in the presence of native dragonflies or when both tadpole species co-occurred. Stable isotopic analysis is an efficient way to assess variation in tadpoles’ tropic status and hence understand their role in freshwater ecosystems. Here we provide baseline isotopic information for future trophic studies and show evidence for plastic changes in tadpoles’ use of food resources under different ecological scenarios.

Keywords

Discrimination factor Turnover Isotopic incorporation Invasive species Diet shift 

Notes

Acknowledgments

P. Burraco, D. Cabrera and C. Pérez helped with animal husbandry. E. Costas provided advice and logistical support for algae production and identification, and M. C. Lozano helped with zooplankton identification. The authorities of Doñana National Park gave the authorization for the fieldwork. Other fieldwork facilities were provided by ICTS-RBD. This work was supported by grant CGL-11123 from the Spanish Ministry of Science and Innovation, Junta Andalucía PAI group RNM 128 and co-funded by the FEDER Program CGL2009-11123. The personnel were supported by a Ramon y Cajal contract to I. G. M. (MICINN), a Juan de la Cierva contract to E. A. (MICINN) and a JAE postdoctoral contract to S. C. (CSIC).

Supplementary material

442_2012_2428_MOESM1_ESM.doc (790 kb)
Supplementary material 1 (DOC 793 kb)

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. Anholt BR, Werner EE (1995) Interaction between food availability and predation mortality mediated by adaptive behavior. Ecology 76:2230–2234CrossRefGoogle Scholar
  3. Ben-David M, Schell DM (2001) Mixing models in analyses of diet using multiple stable isotopes: a response. Oecologia 127:180–184CrossRefGoogle Scholar
  4. Caut S, Angulo E, Courchamp F (2008a) Caution on isotopic model use for analyses of consumer diet. Can J Zool 86:438–445CrossRefGoogle Scholar
  5. Caut S, Angulo E, Courchamp F (2008b) Dietary shift of an invasive predator: rats, seabirds and sea turtles. J Appl Ecol 45:428–437PubMedCrossRefGoogle Scholar
  6. Caut S, Angulo E, Courchamp F (2008c) Discrimination factors (∆N and ∆C) in a omnivorous consumer: the effect of diet isotopic ratio. Funct Ecol 22:255–263CrossRefGoogle Scholar
  7. Caut S, Angulo E, Courchamp F (2009) Variation in discrimination factors (∆15N and ∆13C): the effect of diet isotopic values and applications for diet reconstruction. J Appl Ecol 46:443–453CrossRefGoogle Scholar
  8. Caut S, Angulo E, Courchamp F, Figuerola J (2010) Trophic experiments to estimate isotope discrimination factors. J Appl Ecol 47:948–954CrossRefGoogle Scholar
  9. Coll M, Guershon M (2002) Omnivory in terrestrial arthropods: mixing plant and prey diets. Annu Rev Entomol 47:267–297PubMedCrossRefGoogle Scholar
  10. Cox JG, Lima SL (2006) Naïveté and an aquatic-terrestrial dichotomy in the effects of introduced predators. Trends Ecol Evol 21:674–680PubMedCrossRefGoogle Scholar
  11. Cruz MJ, Rebelo R, Crespo EG (2006) Effects of an introduced crayfish, Procambarus clarkii, on the distribution of south-western Iberian amphibians in their breeding habitats. Ecography 29:329–338CrossRefGoogle Scholar
  12. Cruz MJ, Segurado P, Sousa M, Rebelo R (2008) Collapse of the amphibian community of the Paul do Boquilobo Natural Reserve (central Portugal) after the arrival of the exotic American crayfish Procambarus clarkii. Herpetol J 18:197–204Google Scholar
  13. Díaz-Paniagua C (1985) Larval diets related to morphological characters of five anuran species in the Biological Reserve of Doñana (Huelva, Spain). Amphib Reptil 6:307–322CrossRefGoogle Scholar
  14. Ficetola FG, Siesa ME, Manenti R, Bottoni L, De Bernardi F, Padoa-Schioppa E (2011) Early assessment of the impact of alien species: differential consequences of an invasive crayfish on adult and larval amphibians. Divers Distrib 17:1141–1151CrossRefGoogle Scholar
  15. Folch J, Lees M, Stanley GHS (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509PubMedGoogle Scholar
  16. Frankino WA, Pfennig DW (2001) Condition-dependent expression of trophic polyphenism: effects of individual size and competitive ability. Evol Ecol Research 3:939–951Google Scholar
  17. Freeman AS, Byers JE (2006) Divergent induced responses to an invasive predator in marine mussel populations. Science 313:831–833PubMedCrossRefGoogle Scholar
  18. Gannes LZ, Obrien DM, Martínez del Rio C (1997) Stable isotopes in animal ecology: assumptions, caveats, and a call for more laboratory experiments. Ecology 78:1271–1276CrossRefGoogle Scholar
  19. García Murillo P, Fernández Zamudio R, Cirujano S, Sousa A (2006) Aquatic macrophytes in Doñana protected area (SW Spain): an overview. Limnetica 25:71–80Google Scholar
  20. Geiger W, Alcorlo P, Baltanás A, Montes C (2005) Impact of an introduced Cristacean on the trophic webs of Mediterranean wetlands. Biol Invasion 7:49–73CrossRefGoogle Scholar
  21. Gherardi F (2007) Understanding the impact of invasive crayfish. In: Gherardi F (ed) Biological invaders in inland waters: profiles, distribution, and threats. Springer, Dordrecht, pp 507–542CrossRefGoogle Scholar
  22. Gomez-Mestre I, Díaz-Paniagua C (2011) Invasive predatory crayfish do not trigger inducible defences in tadpoles. Proc R Soc Lond B Biol Sci 278:3364–3370CrossRefGoogle Scholar
  23. Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190Google Scholar
  24. Gutiérrez-Yurrita PJ, Sancho G, Bravo MA, Baltanás A, Montes C (1998) Diet of the red swamp crayfish Procambarus clarkii in natural ecosystems of the Doñana National Park temporary fresh-water marsh (Spain). J Crustacean Biol 18:120–127CrossRefGoogle Scholar
  25. Jefferson DM, Russell W (2008) Ontogenetic and fertilizer effects on stable isotopes in the green frog (Rana clamitas). Appl Herpetol 5:189–196CrossRefGoogle Scholar
  26. Kupfer A, Langel R, Scheu S, Himstedt W, Maraun M (2006) Trophic ecology of a tropical aquatic and terrestrial food web: insights from stable isotopes (15 N). J Trop Ecol 22:469–476CrossRefGoogle Scholar
  27. Hoff KV, Blaustein AR, McDiarmid RW, Altig R (1999) Behavior: interactions and their consequences. In: McDiarmid RW, Altig R (eds) Tadpoles: the biology of anuran larvae. University of Chicago Press, Chicago, pp 215–239Google Scholar
  28. López T, Toja J, Gabellone NA (1991) Limnological comparison of two peridunar ponds in the Doñana National Park (Spain). Arch Hydrobiol 120:357–378Google Scholar
  29. Martin RA, Pfennig DW (2010) Field and experimental evidence that competition and ecological opportunity promote resource polymorphism. Biol J Linn Soc 100:73–88CrossRefGoogle Scholar
  30. Martínez del Rio C, Wolf N, Carleton SA, Gannes LZ (2009) Isotopic ecology ten years after a call for more laboratory experiments. Biol Rev 84:91–111CrossRefGoogle Scholar
  31. Miner BG, Sultan SE, Morgan SG, Padilla DK, Relyea RA (2005) Ecological consequences of phenotypic plasticity. Trends Ecol Evol 20:685–692PubMedCrossRefGoogle Scholar
  32. Parnell AC, Inger R, Bearhop S, Jackson AL (2010) Source partitioning using stable isotopes: coping with too much variation. PLoS ONE 5(3):e9672. doi: 10.1371/journal.pone.0009672 PubMedCrossRefGoogle Scholar
  33. Peacor SD, Werner EE (1997) Trait-mediated indirect interactions in a simple aquatic food web. Ecology 78:1146–1156CrossRefGoogle Scholar
  34. Peacor SD, Werner EE (2000) Predator effects on an assemblage of consumers through induced changes in consumer foraging behavior. Ecology 81:1998–2010CrossRefGoogle Scholar
  35. Pfennig DW, Rice AM, Martin RA (2006) Ecological opportunity and phenotypic plasticity interact to promote character displacement and species coexistence. Ecology 87:769–779PubMedCrossRefGoogle Scholar
  36. Phillips DL, Gregg JW (2001) Uncertainty in source partitioning using stable isotopes. Oecologia 127:171–179CrossRefGoogle Scholar
  37. Post DM, Layman CA, Arrington DA, Takimoto G, Quattrochi J, Montana CG (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152:179–189PubMedCrossRefGoogle Scholar
  38. Relyea RA (2002) Local population differences in phenotypic plasticity: predator-induced changes in wood frog tadpoles. Ecol Monogr 72:77–93CrossRefGoogle Scholar
  39. Relyea RA, Auld JR (2004) Having the guts to compete: how intestinal plastivity explains costs of inducible defenses. Ecol Lett 7:869–875CrossRefGoogle Scholar
  40. Relyea RA, Auld JR (2005) Predator- and competitor-induced plasticity: how changes in foraging morphology affect phenotypic trade-offs. Ecology 86:1723–1729CrossRefGoogle Scholar
  41. Richardson JML (2001) A comparative study of activity levels in larval anurans and response to the presence of different predators. Behav Ecol 12:51–58CrossRefGoogle Scholar
  42. Ruehl CB, DeWitt TJ (2007) Trophic plasticity and foraging performance in red drum, Sciaenops ocellatus (Linnaeus). J Exp Mar Biol Ecol 349:284–294CrossRefGoogle Scholar
  43. Schiesari L, Werner EE, Kling GW (2009) Carnivory and resource-based niche differentiation in anuran larvae: implications for food web and experimental ecology. Freshwater Biol 54:572–586CrossRefGoogle Scholar
  44. StatSoft (2007) STATISTICA (data analysis software system), version 8.0. http://www.statsoft.com
  45. Sweeting CJ, Polunin NVC, Jennings S (2006) Effects of chemical lipid extraction and arithmetic lipid correction on stable isotope ratios of fish tissues. Rapid Commun Mass Spectrom 20:595–601PubMedCrossRefGoogle Scholar
  46. Van Buskirk J (2001) Specific induced responses to different predator species in anuran larvae. J Evol Biol 14:482–489CrossRefGoogle Scholar
  47. Verburg P, Kilham SS, Pringle CM, Lips KR, Drake DL (2007) A stable isotope study of a Neotropical stream food web prior to the extirpation of its large amphibian community. J Trop Ecol 23:643–651CrossRefGoogle Scholar
  48. Wells KD (2007) The ecology and behavior of amphibians. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  49. Werner EE, Anholt BR (1993) Ecological consequences of the trade-off between growth and mortality rates mediated by foraging activity. Am Nat 142:242–272PubMedCrossRefGoogle Scholar
  50. Whiles MR, Gladyshev MI, Sushchik NN, Makhutova ON, Kalachova GS, Peterson SD, Regester KL (2010) Fatty acid analyses reveal high degrees of omnivory and dietary plasticity in pond-dwelling tadpoles. Freshwater Biol 55:1533–1547CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Stéphane Caut
    • 1
    Email author
  • Elena Angulo
    • 1
  • Carmen Díaz-Paniagua
    • 1
  • Ivan Gomez-Mestre
    • 1
    • 2
  1. 1.Estación Biológica de DoñanaCSICSevillaSpain
  2. 2.Research Group of Biodiversity (UO, CSIC, PA)OviedoSpain

Personalised recommendations