The relationship between poison frog chemical defenses and age, body size, and sex

Frontiers in Zoology

Taran Grant²  Ralph A. Saporito¹  Adriana M. Jeckel² 

[1] Department of Biology, John Carroll University, University Heights 44118, OH, USA;Department of Zoology, Institute of Biosciences, University of São Paulo, São Paulo, 05508-090, São Paulo, Brazil

关键词: Skeletochronology;    Sequestration;    Melanophryniscus;    Bufotenine;    Bufonidae;    Anura;    Amphibia;    Alkaloids;   

Others  :  1231129
DOI  :  10.1186/s12983-015-0120-2

 received in 2015-07-31, accepted in 2015-09-21,  发布年份 2015

【 摘 要 】

Introduction

Amphibians secrete a wide diversity of chemicals from skin glands as defense against predators, parasites, and pathogens. Most defensive chemicals are produced endogenously through biosynthesis, but poison frogs sequester lipophilic alkaloids from dietary arthropods. Alkaloid composition varies greatly, even among conspecific individuals collected at the same time and place, with some individuals having only a few micrograms of one or a few alkaloids and others possessing >1 mg of >30 alkaloids. The paucity of alkaloids in juveniles and their abundance in adults suggests that alkaloids accumulate over time; however, alkaloid diversity is highly variable among adult poison frogs and has never been studied in relation to individual age. Using skeletochronology to infer individual ages and gas chromatography–mass spectrometry and vapor phase Fourier-transform infrared spectral analysis to identify the defensive chemicals of 63 individuals, we tested the relationship between defensive chemicals and age, size, and sex in the Brazilian red-belly toad, Melanophryniscus moreirae, a poison frog that possesses both sequestered alkaloids and the biosynthesized indolealkylamine bufotenine.

Results

Adult females were, on average, older and larger than adult males. Juveniles were smaller but not necessarily younger than adults and possessed bufotenine and 18 of the 37 alkaloids found in adults. Alkaloid richness was positively related to age, but not size, whereas the quantities of sequestered alkaloids and bufotenine were positively related to size, but not age. Defensive chemicals were unrelated to sex, independent of size.

Conclusions

The relationship between alkaloid richness and age appears to result from the gradual accumulation of alkaloids over a frog’s lifetime, whereas the relationship between the quantity of defensive chemicals and size appears to be due to the greater storage capacity of larger individuals. The decoupling of age and size effects increases the amount of individual variation that can occur within a population, thereby possibly enhancing anti-predator efficacy. Further, given that both richness and quantity contribute to the overall chemical defense of individual frogs, our results suggest that older, larger individuals are better defended than younger, smaller ones. These considerations underscore the importance of including age in studies of the causes and consequences of variation in poison frog chemical defenses.

【 授权许可】

   
2015 Jeckel et al.

【 图 表 】

Fig. 1.

【 参考文献 】

• [1]Opitz SEW, Müller C. Plant chemistry and insect sequestration. Chemoecology. 2009; 19:117-54.
• [2]Hay ME. Marine chemical ecology: what’s known and what’s next? J Exp Mar Bio Ecol. 1996; 200:103-34.
• [3]Paul VJ, Arthur KE, Ritson-Williams R, Ross C, Sharp K. Chemical defenses: from compounds to communities. Biol Bull. 2007; 213:226-51.
• [4]Savitzky AH, Mori A, Hutchinson DA, Saporito RA, Burghardt GM, Lillywhite HB et al.. Sequestered defensive toxins in tetrapod vertebrates: principles, patterns, and prospects for future studies. Chemoecology. 2012; 22:141-58.
• [5]Speed MP, Ruxton GD, Mappes J, Sherratt TN. Why are defensive toxins so variable? An evolutionary perspective. Biol Rev. 2012; 87:874-84.
• [6]Fritz G, Rand AS, Claude W. The aposematically colored frog, Dendrobates pumilio, is distasteful to the large, predatory ant, Paraponera clavata. Biotropica. 1981; 13:158-9.
• [7]Macfoy C, Danosus D, Sandit R, Jones TH, Garraffo HM, Spande TF et al.. Alkaloids of anuran skin: antimicrobial function? Z Naturforsch C. 2005; 60:932-7.
• [8]Rivas L, Luque-Ortega JR, Andreu D. Amphibian antimicrobial peptides and Protozoa: lessons from parasites. Biochem Biophys Acta. 1788;2009:1570–81.
• [9]Conlon JM. The contribution of skin antimicrobial peptides to the system of innate immunity in anurans. Cell Tissue Res. 2011; 343:201-12.
• [10]Stynoski JL, Shelton G, Stynoski P. Maternally derived chemical defences are an effective deterrent against some predators of poison frog tadpoles (Oophaga pumilio). Biol Lett. 2014; 10:20140187.
• [11]Saporito RA, Spande TF, Garraffo HM, Donnelly MA. Arthropod alkaloids in poison frogs: a review of the “dietary hypothesis.”. Heterocycles. 2009; 79:277-97.
• [12]Saporito RA, Donnelly MA, Spande TF, Garraffo HM. A review of chemical ecology in poison frogs. Chemoecology. 2012; 22:159-68.
• [13]Hantak MM, Grant T, Reinsch S, McGinnity D, Loring M, Toyooka N et al.. Dietary alkaloid sequestration in a poison frog: an experimental test of alkaloid uptake in Melanophryniscus stelzneri (Bufonidae). J Chem Ecol. 2013; 39:1400-6.
• [14]Jeckel AM, Grant T, Saporito RA. Sequestered and synthesized chemical defenses in the poison frog Melanophryniscus moreirae. J Chem Ecol. 2015; 41:505-12.
• [15]Daly JW, Secunda SI, Garraffo HM, Spande TF, Wisnieski A, Nishihira C et al.. Variability in alkaloid profiles in neotropical poison frogs (Dendrobatidae): genetic versus environmental determinants. Toxicon. 1992; 30:887-98.
• [16]Myers CW, Daly JW, Garraffo HM, Wisnieski A, Cover JF. Discovery of the Costa Rican poison frog Dendrobates granuliferus in sympatry with Dendrobates pumilio, and comments on taxonomic use of skin alkaloids. Am Museum Novit. 1995; 3144:1-21.
• [17]Mebs D, Pogoda W, Maneyro R, Kwet A. Studies on the poisonous skin secretion of individual red bellied toads, Melanophryniscus montevidensis (Anura, Bufonidae), from Uruguay. Toxicon. 2005; 46:641-50.
• [18]Saporito RA, Donnelly MA, Jain P, Garraffo HM, Spande TF, Daly JW. Spatial and temporal patterns of alkaloid variation in the poison frog Oophaga pumilio in Costa Rica and Panama over 30 years. Toxicon. 2007; 50:757-78.
• [19]Saporito RA, Donnelly MA, Garraffo HM, Spande TF, Daly JW. Geographic and seasonal variation in alkaloid-based chemical defenses of Dendrobates pumilio from Bocas del Toro, Panama. J Chem Ecol. 2006; 32:795-814.
• [20]Saporito RA, Donnelly MA, Madden AA, Garraffo HM, Spande TF. Sex-related differences in alkaloid chemical defenses of the dendrobatid frog Oophaga pumilio from Cayo Nancy, Bocas del Toro, Panama. J Nat Prod. 2010; 73:317-21.
• [21]Daly JW, Wilham JM, Spande TF, Garraffo HM, Gil R, Silva G et al.. Alkaloids in bufonid toads (Melanophryniscus): temporal and geographic determinants for two Argentinian species. J Chem Ecol. 2007; 33:871-87.
• [22]Daly JW, Garraffo HM, Spande TF, Yeh HJC, Peltzer PM, Cacivio PM et al.. Indolizidine 239Q and quinolizidine 275I. Major alkaloids in two Argentinian bufonid toads (Melanophryniscus). Toxicon. 2008; 52:858-70.
• [23]Garraffo HM, Andriamaharavo NR, Vaira M, Quiroga MF, Heit C, Spande TF. Alkaloids from single skins of the Argentinian toad Melanophryniscus rubriventris (Anura, Bufonidae): an unexpected variability in alkaloid profiles and a profusion of new structures. Springerplus. 2012; 1:51. BioMed Central Full Text
• [24]Grant T, Colombo P, Verrastro L, Saporito RA. The occurrence of defensive alkaloids in non-integumentary tissues of the Brazilian red-belly toad Melanophryniscus simplex (Bufonidae). Chemoecology. 2012; 22:169-78.
• [25]Shine R. Sexual selection and sexual dimorphism in the Amphibia. Copeia. 1979; 1979:297-306.
• [26]Monnet JM, Cherry MI. Sexual size dimorphism in anurans. Proc R Soc London Ser B Biol Sci. 2002; 269:2301-7.
• [27]Myers CW, Daly JW, Malkin B. A dangerously toxic new frog (Phyllobates) used by Emberá indians of western Colombia, with discussion of blowgun fabrication and dart poisoning. Bull Am Museum Nat Hist. 1978; 161:307-66.
• [28]Daly JW, Kaneko T, Wilham JM, Garraffo HM, Spande TF, Espinosa A et al.. Bioactive alkaloids of frog skin: combinatorial bioprospecting reveals that pumiliotoxins have an arthropod source. Proc Natl Acad Sci U S A. 2002; 99:13996-4001.
• [29]Stynoski JL, Torres-Mendoza Y, Sasa-Marin M, Saporito RA. Evidence of maternal provisioning of alkaloid-based chemical defenses in the strawberry poison frog Oophaga pumilio. Ecology. 2014; 95:587-93.
• [30]Santos RR, Grant T. Diel pattern of migration in a poisonous toad from Brazil and the evolution of chemical defenses in diurnal amphibians. Evol Ecol. 2011; 25:249-58.
• [31]Santos RR, Leonardi SB, Caorsi VZ, Grant T. Directional orientation of migration in an aseasonal explosive-breeding toad from Brazil. J Trop Ecol. 2010; 26:415-21.
• [32]Caorsi VZ, Colombo P, Freire MD, Amaral IB, Zank C, Borges-Martins M et al.. Natural history, coloration pattern and conservation status of the threatened south Brazilian red bellied toad, Melanophryniscus macrogranulosus Braun. Herpetol Notes. 1973; 2014:585-98.
• [33]Nishida R. Sequestration of defensive substances from plants by Lepidoptera. Annu Rev Entomol. 2002; 47:57-92.
• [34]Donnelly MA. Feeding patterns of the strawberry poison frog, Dendrobates pumilio (Anura: Dendrobatidae). Copeia. 1991; 1991:723-30.
• [35]Daly JW, Myers CW, Warnick JE, Albuquerque EX. Levels of batrachotoxin and lack of sensitivity to its action in poison-dart frogs (Phyllobates). Science. 1980; 208:1383-5.
• [36]Daly JW, Garraffo HM, Spande TF, Jaramillo CA, Rand AS. Dietary source for skin alkaloids of poison frogs (Dendrobatidae)? J Chem Ecol. 1994; 20:943-55.
• [37]Saporito RA, Isola M, Maccachero VC, Condon K, Donnelly MA. Ontogenetic scaling of poison glands in a dendrobatid poison frog. J Zool. 2010; 282:238-45.
• [38]Barnett CA, Bateson M, Rowe C, Barnett CA. Better the devil you know: avian predators find variation in prey toxicity aversive. Biol Lett. 2014; 10:20140553.
• [39]Mina AE, Ponti AK, Woodcraft NL, Johnson EE, Saporito RA. Variation in alkaloid-based microbial defenses of the dendrobatid poison frog Oophaga pumilio. Chemoecology. 2015; 25:169-78.
• [40]Halliday TR, Verrell PA. Body size and age in amphibians and reptiles. J Herpetol. 1988; 22:253-65.
• [41]Wake DB, Castanet J. A skeletochronological study of growth and age in relation to adult size in Batrachoseps attenuatus. J Herpetol. 1995; 29:60-5.
• [42]Ento K, Matsui M. Estimation of age structure by skeletochronology of a population of Hynobius nebulosus in a breeding season (Amphibia, Urodela). Zoolog Sci. 2002; 19:241-7.
• [43]Morrison C, Hero JM, Browning J. Altitudinal variation in the age at maturity, longevity, and reproductive lifespan of anurans in subtropical Queensland. Herpetologica. 2004; 60:34-44.
• [44]Yamamoto T, Ota H, Chiba S. The age structure of a breeding population of Hynobius lichenatus (Amphibia, Caudata). Curr Herpetol. 2011; 30:7-14.
• [45]Sinsch U. Review: skeletochronological assessment of demographic life-history traits in amphibians. Herpetol J. 2015; 25:5-13.
• [46]Rozenblut B, Ogielska M. Development and growth of long bones in European water frogs (Amphibia: Anura: Ranidae), with remarks on age determination. J Morphol. 2005; 265:304-17.
• [47]Bokermann WCA. Observações sobre Melanophryniscus moreirae (Mir. Rib.) (Amphibia—Brachycephalidae). An Acad Bras Cienc. 1967; 39:301-6.
• [48]Marques RM, Colas-Rosas PF, Toledo LF, Haddad CFB. Amphibia, Anura, Bufonidae, Melanophryniscus moreirae: distribution extension. Check List. 2006; 2:68-9.
• [49]Weber LN, Procaci LDS, Salles R, Silva SP, Corrêa AL, Carvalho-e-Silva SP. Amphibia, Anura, Bufonidae, Melanophryniscus moreirae: distribution extension. Check List. 2007; 3:346-7.
• [50]Carvajalino-Fernández JM, Jeckel AM, Indicatti RP. Melanophryniscus moreirae (Amphibia, Anura, Bufonidae): dormancy and hibernacula use during cold season. Herpetol Bras. 2013; 2:61-2.
• [51]Kusrini MD, Alford RA. The application of skelectochronology to estimate ages of three species of frogs in West Java, Indonesia. Herpetol Rev. 2006; 37:423-5.
• [52]Rasband WS. ImageJ, version 1.48. 2014. http://imagej. nih.gov/ij
• [53]Hemelaar A. An improved method to estimate the number of year rings resorbed in phalanges of Bufo bufo (L.) and its application to populations from different latitudes and altitudes. Amphibia-Reptilia. 1985; 6:323-41.
• [54]Castanet J, Smirina EM. Introduction to the skeletochronological method in amphibians and reptiles. Ann Sci Nat Zool. 1990; 11:191-6.
• [55]Sagor ES, Ouellet M, Barten E, Green DM. Skeletochronology and geographic variation in age structure in the wood frog, Rana sylvatica. J Herpetol. 1998; 32:469-74.
• [56]Guarino FM, Lunardi S, Carlomagno M, Mazzotti S. A skeletochronological study of growth, longevity, and age at sexual maturity in a population of Rana latastei (Amphibia, Anura). J Biosci. 2003; 28:775-82.
• [57]Piantoni C, Ibargüengoytía N, Cussac V. Age and growth of the Patagonian lizard Phymaturus patagonicus. Amphibia-Reptilia. 2006; 27:385-92.
• [58]Daly JW, Spande TF, Garraffo HM. Alkaloids from amphibian skin: a tabulation of over eight-hundred compounds. J Nat Prod. 2005; 68:1556-75.
• [59]Rice WR. Analyzing tables of statistical tests. Evolution. 1989; 43:223-5.
• [60]Paradis E, Claude J, Strimmer K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics. 2004; 20:289-90.
• [61]R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria; 2015. http://www. R-project.org/