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Piperidine alkaloids from fire ants are not sequestered by the green and black poison frog (Dendrobates auratus)

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Abstract

Neotropical poison frogs possess alkaloid-based antipredator defenses which they sequester from a diet of arthropods such as oribatid mites and myrmicine ants. Alkaloid sequestration is still poorly understood and although several studies have examined its uptake, most experiments directly feed alkaloids to the frogs. Here, we examined the alkaloid uptake system in the poison frog species Dendrobates auratus by feeding it an alkaloid-containing prey item, the red imported fire ant Solenopsis invicta (Formicidae, Myrmicinae). Captive bred frogs were either fed live ants or fruit flies dusted with powdered ants for 4 months. Using GC–MS, we confirm that S. invicta contain previously described piperidine alkaloids known as solenopsins; however, none of these piperidine alkaloids was detected in the skin of D. auratus, suggesting the frogs are incapable of sequestering solenopsins from S. invicta. It is possible that D. auratus are unable to sequester fire ant piperidines due to their long hydrocarbon side chains, a feature that makes them structurally different than most known alkaloids in poison frogs.

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References

  • Andriamaharavo NR, Garraffo HM, Spande TF et al (2015) Individual and geographic variation of skin alkaloids in three swamp-forest species of Madagascan poison frogs (Mantella). J Chem Ecol 41:837–847

    Article  CAS  PubMed  Google Scholar 

  • Berenbaum MR (1995) The chemistry of defense: theory and practice. Proc Natl Acad Sci 92:2–8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bolton SK, Dickerson K, Saporito RA (2017) Variable alkaloid defenses in the Dendrobatid poison frog Oophaga pumilio are perceived as differences in palatability to arthropods. J Chem Ecol 43:273–289

    Article  CAS  PubMed  Google Scholar 

  • Born M, Bongers F, Poelman EH, Sterck FJ (2010) Dry-season retreat and dietary shift of the dart-poison frog Dendrobates tinctorius (Anura: Dendrobatidae). Phyllomendusa 9:37–52

    Article  Google Scholar 

  • Brand JM, Blum MS, Fales HM, MacConnell JG (1972) Fire ant venoms: comparative analyses of alkaloidal components. Toxicon 10:259–271

    Article  CAS  PubMed  Google Scholar 

  • Caldwell JP (1996) The evolution of myrmecophagy and its correlates in poison frogs (Family Dendrobatidae). J Zool 240:75–101

    Article  Google Scholar 

  • Caty SN, Alvarez-Buylla A, Byrd GD et al (2019) Molecular physiology of chemical defenses in a poison frog. J Exp Biol 222:jeb204149

    Article  PubMed  Google Scholar 

  • Chen L, Fadamiro HY (2009a) Re-investigation of venom chemistry of Solenopsis fire ants. II. Identification of novel alkaloids in S. invicta. Toxicon 53:479–486

    Article  CAS  PubMed  Google Scholar 

  • Chen L, Fadamiro HY (2009b) Re-investigation of venom chemistry of Solenopsis fire ants. I. Identification of novel alkaloids in S. richteri. Toxicon 53:469–478

    Article  CAS  PubMed  Google Scholar 

  • Chen L, Hu Q-B, Fadamiro HY (2010) Reduction of venom alkaloids in Solenopsis richteri × Solenopsis invicta hybrid: an attempt to identify new alkaloidal components. J Agric Food Chem 58:11534–11542

    Article  CAS  PubMed  Google Scholar 

  • Chen L, Lu Y, Hu Q, Fadamiro HY (2012) Similarity in venom alkaloid chemistry of alate queens of imported fire ants: Implication for hybridization between Solenopsis richteri and S. invicta in the southern United States. Chem Biodiv 9:702–713

    Article  CAS  Google Scholar 

  • Clark VC, Harinantenaina L, Zeller M et al (2012) An endogenous bile acid and dietary sucrose from skin secretions of alkaloid-sequestering poison frogs. J Nat Prod 75:473–478

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Daly JW, Secunda SI, Garraffo HM et al (1992) Variability in alkaloid profiles in neotropical poison frogs (Dendrobatidae): genetic versus environmental determinants. Toxicon 30:887–898

    Article  CAS  PubMed  Google Scholar 

  • Daly JW, Garraffo HM, Spande TF et al (1994a) Dietary source for skin alkaloids of poison frogs (Dendrobatidae)? J Chem Ecol 20:943–955

    Article  CAS  PubMed  Google Scholar 

  • Daly JW, Secunda SI, Garraffo HM et al (1994b) An uptake system for dietary alkaloids in poison frogs (Dendrobatidae). Toxicon 32:657–663

    Article  CAS  PubMed  Google Scholar 

  • Daly JW, Garraffo HM, Spande TF, Clark VC, Ma J, Ziffer H, Cover JF (2003) Evidence for an enantioselective pumiliotoxin 7-hydroxylase in dendrobatid poison frogs of the genus Dendrobates. Proc Natl Acad Sci U S A 100:11092–11097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Daly JW, Spande TF, Garraffo HM (2005) Alkaloids from amphibian skin: a tabulation of over eight-hundred compounds. J Nat Prod 68:1556–1575

    Article  CAS  PubMed  Google Scholar 

  • Donnelly MA (1991) Feeding patterns of the strawberry poison frog, Dendrobates pumilio (Anura: Dendrobatidae). Copeia 1991:723–730

    Article  Google Scholar 

  • Duffey SS (1980) Sequestration of plant natural products by insects. Annu Rev Entomol 25:447–477

    Article  CAS  Google Scholar 

  • Dumbacher JP, Menon GK, Daly JW (2009) Skin as a toxin storage organ in the endemic New Guinean genus Pitohui. Auk 126:520–530

    Article  Google Scholar 

  • Hovey KJ, Seiter EM, Johnson EE, Saporito RA (2018) Sequestered alkaloid defenses in the dendrobatid poison frog Oophaga pumilio provide variable protection from microbial pathogens. J Chem Ecol 44:312–325

    Article  CAS  PubMed  Google Scholar 

  • Jeckel AM, Matsumura K, Nishikawa K et al (2020) Use of whole-body cryosectioning and desorption electrospray ionization mass spectrometry imaging to visualize alkaloid distribution in poison frogs. J Mass Spectrom 55:e4520

    Article  CAS  PubMed  Google Scholar 

  • Jones TH, Adams RMM, Spande TF et al (2012) Histrionicotoxin alkaloids finally detected in an ant. J Nat Prod 75:1930–1936

    Article  CAS  PubMed  Google Scholar 

  • Lötters S, Jungfer K-H, Henkel F-W, Schmidt W (2007) Poison frogs: biology, species and captive Care. Chimaira, Frankfurt

  • MacConnell JG, Blum MS, Fales HM (1970) Alkaloid from fire ant venom: identification and synthesis. Science (80-) 168:840–841

    Article  CAS  Google Scholar 

  • McGugan JR, Byrd GD, Roland AB et al (2016) Ant and mite diversity drives toxin variation in the Little Devil Poison frog. J Chem Ecol 42:537–551

    Article  CAS  PubMed  Google Scholar 

  • McPhail KL, Davies-Coleman MT, Starmer J (2001) Sequestered chemistry of the Arminacean nudibranch Leminda millecra in Algoa Bay, South Africa. J Nat Prod 64:1183–1190

    Article  CAS  PubMed  Google Scholar 

  • Mebs D (2001) Toxicity in animals. Trends in evolution? Toxicon 39:87–96

    Article  CAS  PubMed  Google Scholar 

  • Mebs D, Alvarez JV, Pogoda W et al (2014) Poor alkaloid sequestration by arrow poison frogs of the genus Phyllobates from Costa Rica. Toxicon 80:73–77

    Article  CAS  PubMed  Google Scholar 

  • Morrison LW, Porter SD, Daniels E, Korzukhin MD (2004) Potential global range expansion of the invasive fire ant, Solenopsis invicta. Biol Invasions 6:183–191

    Article  Google Scholar 

  • Moskowitz NA, Dorritie B, Fay T et al (2020) Land use impacts poison frog chemical defenses through changes in leaf litter ant communities. Neotrop Biodiv 6:75–87

    Article  Google Scholar 

  • Nishida R (2002) Sequestration of defensive substances from plants by Lepidoptera. Annu Rev Entomol 47:57–92

    Article  CAS  PubMed  Google Scholar 

  • O’Connell LA, O’Connell JD, Paulo JA et al (2021) Rapid toxin sequestration modifies poison frog physiology. J Exp Biol 224:1–8

    Google Scholar 

  • Opitz SEW, Müller C (2009) Plant chemistry and insect sequestration. Chemoecology 19:117–154

    Article  CAS  Google Scholar 

  • Prates I, Paz A, Brown JL, Carnaval AC (2019) Links between prey assemblages and poison frog toxins: a landscape ecology approach to assess how biotic interactions affect species phenotypes. Ecol Evol 9:14317–14329

    Article  PubMed  PubMed Central  Google Scholar 

  • Sanchez E, Rodríguez A, Grau JH et al (2019) Transcriptomic signatures of experimental alkaloid consumption in a poison frog. Genes (Basel) 10:733

    Article  CAS  Google Scholar 

  • Santos JC, Tarvin RD, O’Connell LA (2016) A review of chemical defense in poison frogs (Dendrobatidae): ecology, pharmacokinetics, and autoresistance. In: Schulte BA, Goodwin TE, Ferkin MH (eds) Chemical signals in vertebrates 13. Springer, pp 305–337

    Chapter  Google Scholar 

  • Saporito RA, Donnelly MA, Hoffman RL et al (2003) A siphonotid millipede (Rhinotus) as the source of spiropyrrolizidine oximes of dendrobatid frogs. J Chem Ecol 29:2781–2786

    Article  CAS  PubMed  Google Scholar 

  • Saporito RA, Garraffo HM, Donnelly MA et al (2004) Formicine ants: an arthropod source for the pumiliotoxin alkaloids of dendrobatid poison frogs. Proc Natl Acad Sci 101:8045–8050

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saporito RA, Donnelly MA, Jain P et al (2007a) Spatial and temporal patterns of alkaloid variation in the poison frog Oophaga pumilio in Costa Rica and Panama over 30 years. Toxicon 50:757–778

    Article  CAS  PubMed  Google Scholar 

  • Saporito RA, Donnelly MA, Norton RA et al (2007b) Oribatid mites as a major dietary source for alkaloids in poison frogs. Proc Natl Acad Sci 104:8885–8890

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saporito RA, Donnelly MA, Madden AA et al (2010a) Sex-related differences in alkaloid chemical defenses of the dendrobatid frog Oophaga pumilio from Cayo Nancy, Bocas del Toro, Panama. J Nat Prod 73:317–321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saporito RA, Isola M, Maccachero VC et al (2010b) Ontogenetic scaling of poison glands in a dendrobatid poison frog. J Zool 282:238–245

    Article  Google Scholar 

  • Saporito RA, Norton RA, Andriamaharavo NR et al (2011) Alkaloids in the mite Scheloribates laevigatus: further alkaloids common to oribatid mites and poison frogs. J Chem Ecol 37:213–218

    Article  CAS  PubMed  Google Scholar 

  • Saporito RA, Donnelly MA, Spande TF, Garraffo HM (2012) A review of chemical ecology in poison frogs. Chemoecology 22:159–168

    Article  CAS  Google Scholar 

  • Saporito RA, Norton RA, Garraffo MH, Spande TF (2015) Taxonomic distribution of defensive alkaloids in Nearctic oribatid mites (Acari, Oribatida). Exp Appl Acarol 67:317–333

    Article  CAS  PubMed  Google Scholar 

  • Savitzky AH, Mori A, Hutchinson DA et al (2012) Sequestered defensive toxins in tetrapod vertebrates: principles, patterns, and prospects for future studies. Chemoecology 22:141–158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simon MP, Toft CA (1991) Diet specialization in small vertebrates: mite-eating in frogs. Oikos 61:263–278

    Article  Google Scholar 

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Acknowledgements

We are thankful to Allison M. Anthony, Adam M. M. Stuckert and Miho Yoshioka for their help taking care of the frogs, and M. A. Nichols for his assistance in maintaining the GC–MS.

Funding

Funding for this study was provided by an ECU THCAS Advancement Council Distinguished Professorship in the Natural Sciences and Mathematics to Kyle Summers, and a Kresge Challenge Grant awarded to JCU.

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Correspondence to Ralph A. Saporito.

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The protocol used was approved by East Carolina University’s Institutional Animal Care and Use Committee (AUP protocol #D288).

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Communicated by Günther Raspotnig.

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Davison, I., Saporito, R.A., Schulte, L.M. et al. Piperidine alkaloids from fire ants are not sequestered by the green and black poison frog (Dendrobates auratus). Chemoecology 31, 391–396 (2021). https://doi.org/10.1007/s00049-021-00357-1

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