Skip to main content
Log in

Individual Variation in Alkaloid Content of Poison Frogs of Madagascar (Mantella; Mantellidae)

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Brightly colored Malagasy poison frogs, Mantella spp., sequester lipophilic, basic alkaloids from arthropod prey for their own chemical defense. Consequently, microsympatric prey diversity is expected to influence alkaloid diversity observed in poison frogs. Twenty-two specimens of three Mantella species from four localities in moist forests of southeastern Madagascar were analyzed individually via gas chromatography-mass spectrometry, revealing that they contain over 80 known alkaloids. Frogs within a locality possessed significantly similar alkaloid content and diversity, while frogs from areas that varied in disturbance, elevation, and/or species showed greater differences. Based on dietary data, the larger frog species Mantella baroni consumed more and larger prey, and showed greater diversity in skin alkaloids than significantly smaller Mantella bernhardi. Additionally, frogs from the most pristine locality had the greatest number of alkaloids, whereas individuals from the most disturbed localities had the least. In a comparison of frog alkaloid profiles over a 10- to 14-yr period, alkaloid turnover, and thus presumably alkaloid-source arthropod turnover, was high in a disturbed locality and low in the pristine primary forest locality. We demonstrate that the nonlethal transcutaneous amphibian stimulator (TAS) is effective for harvesting alkaloids from poison frogs; future studies using this device could obtain larger sample sizes without harming local frog populations.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

TAS:

transcutaneous amphibian stimulator

Ampa:

Ampasimpotsy

Vato:

Vatoharanana

Saha:

Sahavondrona

Vohi:

Vohiparara

AMNH:

American Museum of Natural History

UADAB:

University of Antananarivo Department of Animal Biology

RA:

relative abundance in EI mode

SVL:

snout–vent length

References

  • Bradt, H. 1999. Madagascar, the Bradt Travel Guide. Globe Pequot Press, USA.

    Google Scholar 

  • Clark, V. C., Raxworthy, C. J., Rakotomalala, V., Sierwald, P., and Fisher, B. L. 2005. Convergent evolution of chemical defense in poison frogs and arthropod prey between Madagascar and the Neotropics. Proc. Natl. Acad. Sci. USA 102:11617–11622.

    Article  PubMed  CAS  Google Scholar 

  • Daly, J. W. 1982. Alkaloids of Neotropical poison frogs (Dendrobatidae). Fortschr. Chem. Org. Naturst. (Prog. Chem. Org. Natl. Prod.) 41:205–340.

    CAS  Google Scholar 

  • Daly, J. W. 2005. Nicotinic agonists, antagonists, and modulators from natural sources. Cell. Mol. Neurobiol. 25:513–552.

    Article  PubMed  CAS  Google Scholar 

  • Daly, J. W., Garraffo, H. M., Pannell, L. K., Spande, T. F., Severini, C., and Erspamer, V. 1990. Alkaloids from Australian frogs (Myobatrachidae): pseudophyrnamines and pumiliotoxins. J. Nat. Prod. 53:401–21.

    Article  Google Scholar 

  • Daly, J. W., Secunda, S. I., Garraffo, H. M., Spande, T. F., Wisneiski, A., Nishihira, C., and Cover, J. F. Jr. 1992. Variability in alkaloid profiles in Neotropical poison frogs (Dendrobatidae): Genetic versus environmental determinants. Toxicon 30:887–98.

    Article  PubMed  CAS  Google Scholar 

  • Daly, J. W., Garraffo, H. M., Spande, T. F., Jaramillo, C., and Rand, A. S. 1994a. Dietary source for skin alkaloids of poison frogs (Dendrobatidae)? J. Chem. Ecol. 20:943–55.

    Article  CAS  Google Scholar 

  • Daly, J. W., Secunda, S. I., Garraffo, H. M., Spande, T. F., Wisnieski, A., and Cover, J. F. Jr. 1994b. An uptake system for dietary alkaloids in poison frogs (Dendrobatidae). Toxicon 32:657–63.

    Article  PubMed  CAS  Google Scholar 

  • Daly, J. W., Andriamaharavo, N. R., Andriantsiferana, M., and Myers, C. W. 1996. Madagascan poison frogs (Mantella) and their skin alkaloids. Am. Mus. Novit. 3177:1–34.

    Google Scholar 

  • Daly, J. W., Garraffo, H. M., Hall, G. S., and Cover, J. F. Jr. 1997. Absence of skin alkaloids in captive-raised Madagascan mantelline frogs (Mantella) and sequestration of dietary alkaloids. Toxicon 35:1131–5.

    Article  PubMed  CAS  Google Scholar 

  • Daly, J. W., Garraffo, H. M., and Spande, T. F. 1999. Alkaloids from amphibian skins, pp. 1–161, in S. W. Pelletier (ed.). Alkaloids: Chemical and Biological Perspectives, vol. 13. Pergamon, New York.

    Google Scholar 

  • Daly, J. W., Kaneko, T. Wilham, J. Garraffo, H. M. Spande, T. F. Espinosa A., and Donnelly, M. A. 2002. Bioactive alkaloids of frog skin: combinatorial bioprospecting reveals that pumiliotoxins have an arthropod source. Proc. Natl. Acad. Sci. USA. 99:13996–14001.

    Article  PubMed  CAS  Google Scholar 

  • Daly, J. W., Garraffo, H. M., Spande, T. F., Clark, V. C., Ma, J., Ziffer, H., and Cover, J. F. Jr. 2003. Evidence for an enantioselective pumiliotoxin 7-hydroxylase in dendrobatid poison frogs of the genus Dendrobates. Proc. Natl. Acad. Sci. USA 100:11092–7.

    Article  PubMed  CAS  Google Scholar 

  • Daly, J. W., Noimai, N., Kongkathip, B., Kongkathip, N., Wilham, J., Garraffo, H. M., Kaneko, T., Spande, T. F., Nimit, Y., Nabhitabhata, J., and Chan-Ard, T. 2004. Biologically active substances from amphibians: preliminary studies on anurans from twenty-one genera of Thailand. Toxicon 44:805–15.

    Article  PubMed  CAS  Google Scholar 

  • Daly, J. W., Spande, T. F., and Garraffo, H. M. 2005. Alkaloids from amphibian skin: a tabulation of over eight-hundred compounds. J. Nat. Prod. 68:1556–1575.

    Article  PubMed  CAS  Google Scholar 

  • Eisner, T., Alsop, D., Hicks, K., and Meinwald, J. 1978. Defensive secretions of millipeds. In S. Bettini (ed.). Handbook of Experimental Pharmacology, vol. 48, Arthropod Venoms. Springer-Verlag, New York.

    Google Scholar 

  • Fisher, B. 1998. Ant diversity patterns along an elevational gradient in the Reserve Speciale d’Anjanaharibe-Sud and on the Western Masoala Peninsula, Madagascar. Fieldiana, Zool. 90:39–67.

    Google Scholar 

  • Fisher, B. L., Ratsirarson, H., and Razafimandimby, S. 1998. Les Fourmis (Hymenoptera: Formicidae) pp. 107–131. In: Inventaire biologique de la Forêt Littorale de Tampolo (Fenoarivo Atsinaanana). J. Ratsirarson and S.M. Goodman (eds.). Recherches pour le Développement, Série Sciences Biologiques. No. 14. Centre d’Information et de Documentation Scientifique et Technique, Antananarivo, Madagascar.

  • Fisher, B. L. 2005. A new species of Discothyrea Roger from Mauritius and a new species of Proceratium from Madagascar (Hymenoptera: Formicidae). Proc. Calif. Acad. Sci. 56:657–667.

    Google Scholar 

  • Grant, J. B. and Land, B. 2002. Transcutaneous Amphibian Stimulator (TAS): a device for the collection of amphibian skin secretions. Herpetol. Rev. 33:38–41.

    Google Scholar 

  • Jones, T. H., Gorman, J. S., Snelling, R. R., Delabie, J. H., Blum, M. S., Garraffo, H. M., Jain, P., Daly, J. W., and Spande, T. F. 1999. Further alkaloids common to ants and frogs: decahydroquinolines and a quinolizidine. J. Chem. Ecol. 25:1179–93.

    Article  CAS  Google Scholar 

  • King, A. G. and Meinwald, J. 1996. Review of the defensive chemistry of Coccinellids. Chem. Rev. 96:1105–22.

    Article  CAS  Google Scholar 

  • Laurent, P., Braekman, J. C., and Daloze, D. 2005. Insect chemical defense. Top. Curr. Chem. 240:167–229.

    CAS  Google Scholar 

  • Leclercq, S., Braekman, J. C., Daloze, D., and Pasteels, J. M. 2000. The defensive chemistry of ants. Prog. Chem. Org. Nat. Prod. 79:115–229.

    CAS  Google Scholar 

  • Mebs, D., Pogoda, W., Maneyro, R., and Kwet, A. 2005. Studies on the poisonous skin secretion of individual red bellied toads, Melanophyrniscus montevidensis (Anura, Bufonidae), from Uruguay. Toxicon 46:641–650.

    Article  PubMed  CAS  Google Scholar 

  • Myers, C. W. and Daly, J. W. 1980. Taxonomy and ecology of Dendrobates bombetes, a new Andean poison frog with new skin toxins. Am. Mus. Novit. 2692:1–23.

    Google Scholar 

  • Myers, C. W., Daly, J. W., Garraffo, H. M., Wisnieski, A., and Cover, J. F. Jr. 1995. Discovery of the Costa Rican poison frog Dendrobates granuliferus in sympatry with Dendrobates pumilio, and comments on taxonomic use of skin alkaloids. Am. Mus. Novit. 3144:1–21.

    Google Scholar 

  • Rabemananjara, F., Bora, P., Cadle, J. E., Anderone, F., Rajeriarison, E., Talata, P., Glaw, F., Vences, M., and Vietes, D. R. 2005. New records, distribution and conservation of Mantella bernhardi, an endangered frog species from south-eastern Madagascar. Oryx 39:339–342.

    Article  Google Scholar 

  • Saporito, R. A., Garraffo, H. M., Donnelly, M. A., Edwards, A. L., Longino, J. T., and Daly, J. W. 2004. Formicine ants: an arthropod source for the pumiliotoxin alkaloids of dendrobatid poison frogs. Proc. Natl. Acad. Sci. USA 101:8045–50.

    Article  PubMed  CAS  Google Scholar 

  • Saporito, R. A., Donnelly, M. A., Garraffo, H. M., Spande, T. F. and Daly, J. W. 2006. Geographic and seasonal variation in alkaloid-based chemical defenses of Dendrobates pumilio from Bocas del Toro, Panama. J. Chem. Ecol. DOI http://dx.doi.org/10.1007/s10886-006-9034.

  • Smith, B. P., Tyler, M. J., Kaneko, T., Garraffo, H. M., Spande, T. F., and Daly, J. W. 2002. Evidence for biosynthesis of pseudophrynamine alklaloids by an Australian Myobatrachid frog (Pseudophryne) and for the sequestration of dietary pumiliotoxins. J. Nat. Prod. 65:439–47.

    Article  PubMed  CAS  Google Scholar 

  • Takada, W., Sakata, T., Shimano, S., Enami, Y., Mori, N., Nishida, R., and Kuwahara, Y. 2005. Scheloribatid mites as the source of pumiliotoxins in dendrobatid frogs. J. Chem. Ecol. 31:2403–2415.

    Article  PubMed  CAS  Google Scholar 

  • Vences, M., Glaw, F., and Bohme, W. 1999. A review of the genus Mantella (Anura, Ranidae, Mantellinae): taxonomy, distribution and conservation of Malagasy poison frogs. Alytes 17:3–72.

    Google Scholar 

Download references

Acknowledgments

We thank Elizabeth E., Sandra P., and William S. Clark, John W. Daly, Jerrold Meinwald, Helian Ratsirarson, Aimee Razafiarimalala, and Justin Solo for their help, anonymous reviewers for critical readings of this manuscript, Christopher J. Raxworthy for discussions, Julián Faivovich for frog dissection training, and Florio Arguillas and Françoise Vermeylen for statistical consulting at Cornell. This work was supported by National Science Foundation Grants DEB-9984496 (to C.J. Raxworthy) for VC Clark’s 2003 fieldwork, DEB-0344731 (to B.L.F. and P.S. Ward) for arthropod processing, and CHE-0216226 to Prof. Koji Nakanishi for GC-TOF-MS acquisition and partial support of L.A. The UADAB, Association Nationale pour la Gestion des Aires Protégées, Direction Generale des Eaux et Forêts, Madagascar Institute pour la Conservation des Ecosystèmes Tropicaux, and California Academy of Sciences team in Antananarivo facilitated activities in Madagascar, and Columbia University (including Edward Bass for Biosphere 2) and the American Museum of Natural History provided research support in the United States.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Valerie C. Clark.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplement 1

Supplementary information for journal of chemical ecology (PDF 494 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Clark, V.C., Rakotomalala, V., Ramilijaona, O. et al. Individual Variation in Alkaloid Content of Poison Frogs of Madagascar (Mantella; Mantellidae). J Chem Ecol 32, 2219–2233 (2006). https://doi.org/10.1007/s10886-006-9144-6

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-006-9144-6

Keywords

Navigation