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Individual and Geographic Variation of Skin Alkaloids in Three Species of Madagascan Poison Frogs (Mantella)

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Abstract

Alkaloid profiles for 81 individual mantellid frogs, Mantella baroni (Boulenger 1988) (N = 19), M. bernhardi (N = 51), and M. madagascariensis (Grandidier 1877) (N = 11), from six different populations from Madagascar were examined. Marked individual differences in alkaloid composition (number, type, and amount) were observed between different species and between populations of the same species. Disjunct populations of each of the three species differed significantly in alkaloid composition. Sympatric populations of M. baroni and M. madagascariensis also differed significantly in alkaloid composition. In M. bernhardi, differences in alkaloid composition were marginally associated with different sexes. A total of 111 alkaloids, including isomers, were detected in analysis of the individuals from the three species. The majority (47%) appear likely to be obtained from dietary mites, whereas many of the others (18%) are presumed to be from ants, and a few (4%) are from millipedes. Putative dietary sources for the remaining alkaloids are generally unknown, but beetles are probably the source of at least some of the tricyclic alkaloids (6%). In addition, alkaloid compositions from extracts of groups of individuals from five additional populations of M. baroni and from one population of M. bernhardi (Vences et al. 1994) and one population of M. cowanii (Boulenger 1882) were examined. An additional 50 alkaloids, including isomers, were detected in the combined samples, bringing the total number of alkaloids identified from these four species of mantellid frogs to 161. Alkaloid compositions in mantellid poison frogs are diverse and highly dependent on geographic location that appear to be largely determined by the nature and availability of alkaloid-containing prey items.

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Abbreviations

ANOSIM:

analysis of similarity

FAME:

fatty acid methyl ester

GC–MS:

gas chromatography–mass spectrometry

3,5-I; 5,8-I:

disubstituted indolizidine

5,6,8-I:

trisubstituted indolizidine

nMDS:

nonmetric multidimensional scaling

PTX:

pumiliotoxin

aPTX:

allopumiliotoxin

hPTX:

homopumiliotoxin

3,5-P:

3,5-disubstituted pyrrolizidine

1,4-Q:

1,4-disubstituted quinolizidine

SVL:

snout-to-vent length

Spiro:

spiropyrrolizidine

Tri:

tricyclic alkaloid

ZCMV:

zoological collection Miguel Vences

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Acknowledgments

We are grateful to numerous students, guides, and colleagues for their assistance during fieldwork, in particular to Parfait Bora, Euan Edwards, Falitiana Rabemananjara, Emile Rajeriarison, Theo Rajaofiarison, Edouard Randriamitso, Tokihery Razafindrabe, and Cindy Woodhead. Olga Ramilijaona and Noromalala Raminosoa provided valuable assistance. We are indebted to MICET/ICTE for logistical support. The Tsinjoarivo samples were kindly provided by Franco Andreone in January of 2003. The work was carried out in the framework of collaboration accords of the authors’ institutions with the Département de Biologie Animale, Université d’Antananarivo and the Association Nationale pour la Gestion des Aires Protegées, ANGAP. We are grateful to the Malagasy authorities, in particular the Ministère de l’Environnement, des Eaux et Forêts and the ANGAP, for research and export permits. Fieldwork was supported by the Volkswagen Foundation and the BIOPAT foundation. One of the authors (R.A.S.) was the recipient of an NIH Courtesy Associates appointment. The support of the NIH undergraduate Scholarship Program for author L.-A.G. is gratefully acknowledged. D.R.V. was supported by the NSF AmphibiaTree Grant EF-0334939. The research at NIH was supported by intramural funds of the National Institute of Diabetes and Digestive and Kidney Diseases.

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Authors and Affiliations

  1. Laboratory of Bioorganic Chemistry, NIDDK, NIH, HHS, Bethesda, MD, 20892, USA

    John W. Daly, H. Martin Garraffo, Thomas F. Spande & Lesley-Ann Giddings

  2. Department of Biological Sciences, Florida International University, Miami, FL, 33199, USA

    Ralph A. Saporito

  3. Museum of Vertebrate Zoology and Department of Integrative Biology, University of California, Berkeley, CA, 94720-3160, USA

    David R. Vieites

  4. Division of Evolutionary Biology, Zoological Institute, Technical University of Braunschweig, Spielmannstrasse 8, 38106, Braunschweig, Germany

    Miguel Vences

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  1. John W. Daly
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  2. H. Martin Garraffo
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  3. Thomas F. Spande
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  4. Lesley-Ann Giddings
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  5. Ralph A. Saporito
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  6. David R. Vieites
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  7. Miguel Vences
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Correspondence to John W. Daly or Miguel Vences.

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Daly, J.W., Garraffo, H.M., Spande, T.F. et al. Individual and Geographic Variation of Skin Alkaloids in Three Species of Madagascan Poison Frogs (Mantella). J Chem Ecol 34, 252–279 (2008). https://doi.org/10.1007/s10886-007-9396-9

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