Skip to main content
SpringerLink
Log in

Meta-analysis of tadpole taste tests: consumption of anuran prey across development and predator strategies

  • Behavioral ecology – original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

The risk of predation and the costs and benefits of diverse anti-predator strategies can shift across the life stages of an organism. Yet, empirical examples of ontogenetic switches in defense mechanisms are scarce. Anurans represent an alleged exception; previous meta-analytic work suggests that unpalatability of developing anurans is “rare”, whereas adult anurans in many lineages are well defended by toxic and/or unpalatable skin secretions. Here, we revisit the question of the unpalatability of anuran young in a meta-analysis of the relative proportion of prey consumed within 922 predation tests, including 135 anuran species. We tested the hypotheses that a predator’s propensity to consume anuran young depends on (1) prey family, (2) predator manipulation strategy, and (3) prey ontogenetic stage. We used a binomial mixed model approach with considerations for multiple effect sizes within studies to evaluate the log odds ratio of the proportion of prey consumed by individual predators. Prey consumption was highly variable, but toads (Bufonidae) were consumed in lower proportions. Chewing invertebrates consumed more anuran prey than biting vertebrates. Late stage tadpoles were more vulnerable to predation than other stages of anuran ontogeny. However, more studies are needed to unravel the roles of development and evolutionary history in the chemical ecology of anuran young. This synthesis provides clear meta-analytic evidence that relative unpalatability is an important component in the anti-predator defenses of young in some anuran families, calling into question the degree to which chemically defended anuran families undergo ontogenetic switches in anti-predator strategies.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Availability of data and material

The datasets generated during the study are included in this published article and its supplementary information files.

Code availability

Custom R script of data analyses and visualizations are included in this published article and its supplementary information files.

References

  • Adams CK, Saenz D, Conner R (2011) Palatability of twelve species of anuran larvae in eastern Texas. Am Midl Nat 166:211–223. https://doi.org/10.1674/0003-0031-166.1.211

    Article  Google Scholar 

  • Arbuckle K, Speed MP (2015) Antipredator defenses predict diversification rates. Proc Natl Acad Sci USA 112:13597–13602

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arbuckle K, Rodríguez de la Vega RC, Casewell NR (2017) Coevolution takes the sting out of it: Evolutionary biology and mechanisms of toxin resistance in animals. Toxicon 140:118–131

    Article  CAS  PubMed  Google Scholar 

  • Arnold SJ, Wassersug RJ (1978) Differential predation on metamorphic anurans by garter snakes (Thamnophis): social behavior as a possible defense. Ecology 59:1014–1022

    Article  Google Scholar 

  • Berger A, Petschenka G, Degenkolb T, Geisthardt M, Vilcinskas A (2021) Insect collections as an untapped source of bioactive compounds-fireflies (Coleoptera: Lampyridae) and cardiotonic steroids as a proof of concept. Insects 12:689

    Article  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 

  • Booth CL (1990) Evolutionary significance of ontogenetic colour change in animals. Biol J Linn Soc 40:125–163

    Article  Google Scholar 

  • Brodie ED, Formanowicz DR (1987) Antipredator mechanisms of larval anurans: Protection of palatable individuals. Herpetologica 43:369–373

    Google Scholar 

  • Brodie ED, Formanowicz DR, Mezzocannone V (1978) The development of noxiousness of Bufo americanus tadpoles to aquatic insect predators. Herpetologica 34:302–306

    Google Scholar 

  • Cabrera-Guzmán E, Crossland MR, Shine R (2012) Predation on the eggs and larvae of invasive cane toads (Rhinella marina) by native aquatic invertebrates in tropical Australia. Biol Cons 153:1–9. https://doi.org/10.1016/j.biocon.2012.04.012

    Article  Google Scholar 

  • Caro T, Sherratt TN, Stevens M (2016) The ecology of multiple colour defences. Evol Ecol 30:797–809

    Article  Google Scholar 

  • Chamberlain S (2020) rphylopic: get 'Silhouettes' of 'Organisms' from 'Phylopic'. R package version 0.3.0. https://CRAN.R-project.org/package=rphylopic

  • Chamberlain S, Szocs E (2013) taxize—taxonomic search and retrieval in R. F1000Research. https://f1000research.com/articles/2-191/v2.

  • Chang B, Hoaglin DC (2017) Meta-analysis of odds ratios: current good practices. Med Care 55:328–335

    Article  PubMed  PubMed Central  Google Scholar 

  • Crossland MR (1998) Ontogenetic variation in toxicity of tadpoles of the introduced toad Bufo marinus to native australian aquatic invertebrate predators. Herpetologica 54:364–369

    Google Scholar 

  • Darst CR, Cummings ME, Cannatella DC (2006) A mechanism for diversity in warning signals: conspicuousness versus toxicity in poison frogs. Proc Natl Acad Sci USA 103:5852–5857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferreira RB, Lourenço-de-Moraes R, Zocca C, Duca C, Beard KH, Brodie ED (2019) Antipredator mechanisms of post-metamorphic anurans: a global database and classification system. Behav Ecol Sociobiol 73:69

    Article  Google Scholar 

  • Fischer EK, Roland AB, Moskowitz NA, Vidoudez C, Ranaivorazo N, Tapia EE, Trauger SA, Vences M, Coloma LA, O’Connell LA (2019) Mechanisms of convergent egg provisioning in poison frogs. Curr Biol 29:4145–4151

    Article  CAS  PubMed  Google Scholar 

  • Formanowicz DR, Brodie ED (1982) Relative palatabilities of members of a larval amphibian community. Copeia 91–97

  • Garton JD, Mushinsky HR (1979) Integumentary toxicity and unpalatability as an antipredator mechanism in the narrow mouthed toad, Gastrophryne carolinensis. Can J Zool 57:1965–1973

    Article  Google Scholar 

  • Gonzalez M, Palacios-Rodriguez P, Hernandez-Restrepo J, González-Santoro M, Amézquita A, Brunetti AE, Carazzone C (2021) First characterization of toxic alkaloids and volatile organic compounds (VOCs) in the cryptic dendrobatid Silverstoneia punctiventris. Front Zool 18:1–15

    Article  CAS  Google Scholar 

  • Gosavi SM, Gaikwad PS, Gramapurohit NP, Kumar AR (2014) Occurrence of parotoid glands in tadpoles of the tropical frog, Clinotarsus curtipes and their role in predator deterrence. Comp Biochem Physiol A Mol Integr Physiol 170:31–37

    Article  CAS  PubMed  Google Scholar 

  • Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190

    Google Scholar 

  • Grant JB (2007) Ontogenetic colour change and the evolution of aposematism: a case study in panic moth caterpillars. J Anim Ecol 76:439–447

    Article  PubMed  Google Scholar 

  • Gunzburger MS, Travis J (2005) Critical literature review of the evidence for unpalatability of amphibian eggs and larvae. J Herpetol 39:547–571. https://doi.org/10.1670/1-05A.1

    Article  Google Scholar 

  • Halliday DC, Venables D, Moore D, Shanmuganathan T, Pallister J, Robinson AJ, Hyatt A (2009) Cane toad toxicity: an assessment of extracts from early developmental stages and adult tissues using MDCK cell culture. Toxicon 53:385–391. https://doi.org/10.1016/j.toxicon.2008.10.012

    Article  CAS  PubMed  Google Scholar 

  • Hanlon SM, Parris MJ (2013) Previous exposure of predatory fish to a pesticide alters palatability of larval amphibian prey. Environ Toxicol Chem 32:2861–2865. https://doi.org/10.1002/etc.2380

    Article  CAS  PubMed  Google Scholar 

  • Hawlena D, Boochnik R, Abramsky Z, Bouskila A (2006) Blue tail and striped body: Why do lizards change their infant costume when growing up? Behav Ecol 17:889–896

    Article  Google Scholar 

  • Hayes RA, Barrett A, Alewood PF, Grigg GC, Capon RJ (2007) Use of chemical ecology for control of the cane toad? Chem Signals Vertebr 11:409–417. https://doi.org/10.1007/978-0-387-73945-8_39

    Article  Google Scholar 

  • Hayes RA, Crossland MR, Hagman M, Capon RJ, Shine R (2009) Ontogenetic variation in the chemical defenses of cane toads (Bufo marinus): toxin profiles and effects on predators. J Chem Ecol 35:391–399

    Article  CAS  PubMed  Google Scholar 

  • Heyer WR, McDiarmid RW, Weigmann DL (1975) Tadpoles, predation and pond habitats in the tropics. Biotropica 7:100. https://doi.org/10.2307/2989753

    Article  Google Scholar 

  • Higginson AD, Ruxton GD (2010) Adaptive changes in size and age at metamorphosis can qualitatively vary with predator type and available defenses. Ecology 91:2756–2768

    Article  CAS  PubMed  Google Scholar 

  • Ho LST, Ane C (2014) A linear-time algorithm for Gaussian and non-Gaussian trait evolution models. Syst Biol 63:397–408

    Article  PubMed  Google Scholar 

  • Hoffman EA, Blouin MS (2000) A review of colour and pattern polymorphisms in anurans. Biol J Linn Soc 70:633–665

    Article  Google Scholar 

  • Hoso M (2012) Cost of autotomy drives ontogenetic switching of anti-predator mechanisms under developmental constraints in a land snail. Proc R Soc B Biol Sci 279:411–4816

    Google Scholar 

  • Hossie T, Landolt K, Murray DL (2017) Determinants and co-expression of anti-predator responses in amphibian tadpoles: a meta-analysis. Oikos 126:173–184

    Article  Google Scholar 

  • Hossie T, Chan K, Murray D (2021) Increasing availability of palatable prey induces predator-dependence and increases predation on unpalatable prey. Sci Rep 11:1–12

    Article  CAS  Google Scholar 

  • Ives A, Dinnage R, Nell LA, Helmus M, Li D (2019) phyr: model based phylogenetic analysis. R package version 1.0.2. https://CRAN.R-project.org/package=phyr

  • Jackson D, Law M, Stijnen T, Viechtbauer W, White IR (2018) A comparison of seven random-effects models for meta-analyses that estimate the summary odds ratio. Stat Med 37:1059–1085. https://doi.org/10.1002/sim.7588

    Article  PubMed  PubMed Central  Google Scholar 

  • Jara FG, Perotti MG (2009) Toad tadpole responses to predator risk: ontogenetic change between constitutive and inducible defenses. J Herpetol 43:82–88. https://doi.org/10.1670/07-229R2.1

    Article  Google Scholar 

  • Jetz W, Pyron RA (2018) The interplay of past diversification and evolutionary isolation with present imperilment across the amphibian tree of life. Nat Ecol Evol 2:850–858. https://doi.org/10.1038/s41559-018-0515-5

    Article  PubMed  Google Scholar 

  • Karraker NE (2011) Are toad tadpoles unpalatable: evidence from the behaviour of a predatory dragonfly in South China. Amphib Reptil 32:413–418. https://doi.org/10.1163/017353711X571892

    Article  Google Scholar 

  • Kats LB, Petranka JW, Sih A (1988) Antipredator defenses and the persistence of amphibian larvae with fishes. Ecology 69:1865–1870

    Article  Google Scholar 

  • König E, Bininda-Emonds OR, Shaw C (2015) The diversity and evolution of anuran skin peptides. Peptides 63:96–117

    Article  PubMed  CAS  Google Scholar 

  • Kruse KC, Francis MG (1977) A predation deterrent in larvae of the bullfrog, Rana catesbeiana. Trans Am Fish Soc 106:248–252. https://doi.org/10.1577/1548-8659(1977)106%3c248:apdilo%3e2.0.co;2

    Article  Google Scholar 

  • Kruse B, Stone B (1984) Largemouth bass (Micropterus salmoides) learn to avoid feeding on toad (Bufo) tadpoles. Anim Behav 32:1035–1039

    Article  Google Scholar 

  • Lajeunesse MJ (2011) PhyloMeta: a program for phylogenetic comparative analyses with meta-analysis. Bioinformatics 27:2603–2604

    CAS  PubMed  Google Scholar 

  • Lawler KL, Hero JM (1997) Palatability of Bufo marinus tadpoles to a predatory fish decreases with development. Wildl Res 24:327–334. https://doi.org/10.1071/WR96089

    Article  Google Scholar 

  • Licht L (1968) Unpalatability and toxicity of toad eggs. Herpetologica 24:93–98

    Google Scholar 

  • Llewelyn J, Bell K, Schwarzkopf L, Alford RA, Shine R (2012) Ontogenetic shifts in a prey’s chemical defences influence feeding responses of a snake predator. Oecologia 169:965–973

    Article  PubMed  Google Scholar 

  • Medina I, Vega-Trejo R, Wallenius T, Symonds MRE, Stuart-Fox D (2020) From cryptic to colorful: evolutionary decoupling of larval and adult color in butterflies. Evol Lett 4:34–43

    Article  PubMed  Google Scholar 

  • Mohammadi S, Gompert Z, Gonzalez J, Takeuchi H, Mori A, Savitzky AH (2016) Toxin-resistant isoforms of Na+/K+-ATPase in snakes do not closely track dietary specialization on toads. Proc Biol Sci 283:20162111

    PubMed  PubMed Central  Google Scholar 

  • Moran NA (1994) Adaptation and constraint in the complex life cycles of animals. Annu Rev Ecol Syst 25:573–600

    Article  Google Scholar 

  • Okamura H, Yasuhara JC, Fambrough DM, Takeyasu K (2003) P-type ATPases in Caenorhabditis and Drosophila: implications for evolution of the P-type ATPase subunit families with special reference to the Na, K-ATPase and H, K-ATPase subgroup. J Membr Biol 191:13–24. https://doi.org/10.1007/s00232-002-1041-5

    Article  CAS  PubMed  Google Scholar 

  • Paradis E, Schliep K (2019) ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35:526–528

    Article  CAS  PubMed  Google Scholar 

  • Park S, Beretvas SN (2019) Synthesizing effects for multiple outcomes per study using robust variance estimation versus the three-level model. Behav Res Methods 51:152–171. https://doi.org/10.3758/s13428-018-1156-y

    Article  PubMed  Google Scholar 

  • Peterson J, Blaustein AR (1992) Relative palatabilities of anuran larvae to natural aquatic insect predators. Copeia 577–584

  • Portheault A, Díaz-Paniagua C, Gómez-Rodríguez C (2007) Predation on amphibian eggs and larvae in temporary ponds: the case of Bufo calamita in southwestern Spain. Revue D’ecologie (la Terre Et La Vie) 62:315–322

    Google Scholar 

  • Protti-Sánchez F, Quirós-Guerrero L, Vásquez V, Willink B, Pacheco M, León E, Pröhl H, Bolaños F (2019) Toxicity and alkaloid profiling of the skin of the golfo dulcean poison frog Phyllobates vittatus (Dendrobatidae). J Chem Ecol 45:914–925

    Article  PubMed  CAS  Google Scholar 

  • Putman BJ, Coss RG, Clark RW (2015) The ontogeny of antipredator behavior: Age differences in California ground squirrels (Otospermophilus beecheyi) at multiple stages of rattlesnake encounters. Behav Ecol Sociobiol 69:1447–1457

    Article  Google Scholar 

  • Regueira E, Dávila C, Hermida GN (2016) Morphological changes in skin glands during development in Rhinella arenarum (Anura: Bufonidae). Anat Rec 299:141–156. https://doi.org/10.1002/ar.23284

    Article  CAS  Google Scholar 

  • Rodríguez C, Rollins-Smith L, Ibáñez R, Durant-Archibold AA, Gutiérrez M (2017) Toxins and pharmacologically active compounds from species of the family Bufonidae (Amphibia, Anura). J Ethnopharmacol 198:235–254

    Article  PubMed  CAS  Google Scholar 

  • Rojas B, Burdfield-Steel E, Pakkanen H, Suisto K, Maczka M, Schulz S, Mappes J (2017) How to fight multiple enemies: target-specific chemical defences in an aposematic moth. Proc R Soc B Biol Sci 284:1863. https://doi.org/10.1098/rspb.2017.1424

    Article  Google Scholar 

  • Ruxton GD, Sherratt TN, Speed MP (2019) Avoiding attack: the evolutionary ecology of crypsis, aposematism, and mimicry. Oxford University Press, Oxford

    Google Scholar 

  • Saporito RA, Russell MW, Richards-Zawacki CL, Dugas MB (2019) Experimental evidence for maternal provisioning of alkaloid defenses in a dendrobatid frog. Toxicon 161:40–43

    Article  CAS  PubMed  Google Scholar 

  • Schulte LM, Saporito RA, Davison I, Summers K (2017) The palatability of Neotropical poison frogs in predator-prey systems: do alkaloids make the difference? Biotropica 49:23–26. https://doi.org/10.1111/btp.12404

    Article  Google Scholar 

  • Shine R (2010) The ecological impact of invasive cane toads (Bufo marinus) in Australia. Q Rev Biol 85:253–291

    Article  PubMed  Google Scholar 

  • Sievers M, Hale R, Parris KM, Melvin SD, Lanctôt CM, Swearer SE (2019) Contaminant-induced behavioural changes in amphibians: a meta-analysis. Sci Total Environ 693:133570

    Article  CAS  PubMed  Google Scholar 

  • Skelhorn J, Rowe C (2006) Avian predators taste-reject aposematic prey on the basis of their chemical defence. Biol Lett 2:348–350. https://doi.org/10.1098/rsbl.2006.0483

    Article  PubMed  PubMed Central  Google Scholar 

  • Skelhorn J, Halpin CG, Rowe C (2016) Learning about aposematic prey. Behav Ecol 27:955–964. https://doi.org/10.1093/beheco/arw009

    Article  Google Scholar 

  • Stynoski JL, O’Connell LA (2017) Developmental morphology of granular skin glands in pre-metamorphic egg-eating poison frogs. Zoomorphology 136:219–224. https://doi.org/10.1007/s00435-017-0344-0

    Article  Google Scholar 

  • Stynoski JL, Torres-Mendoza Y, Sasa-Marin M, Saporito RA (2014) Evidence of maternal provisioning of alkaloid-based chemical defenses in the strawberry poison frog Oophaga pumilio. Ecology 95:587–593

    Article  PubMed  Google Scholar 

  • Szuroczki D, Richardson JML (2011) Palatability of the larvae of three species of Lithobates. Herpetologica 67:213–221. https://doi.org/10.1655/HERPETOLOGICA-D-10-00059.1

    Article  Google Scholar 

  • Valkonen JK, Nokelainen O, JokimãKi M, Kuusinen E, Paloranta M, Peura M, Mappes J (2014) From deception to frankness: benefits of ontogenetic shift in the anti-predator strategy of alder moth Acronicta alni larvae. Curr Zool 60:114–122

    Article  Google Scholar 

  • Viechtbauer W (2010) Conducting meta-analyses in R with the metafor package. J Stat Soft 36:1–48

    Article  Google Scholar 

  • Wassersug RJ (1971) On the comparative palatability of some dry-season tadpoles from Costa Rica. Am Midl Nat 86:101–109

    Article  Google Scholar 

  • Wassersug RJ (1973) Aspects of social behavior in anuran larvae. In: Vial JL (ed) Evolutionary biology of the anurans: contemporary research on major problems. Univ. Missouri Press, Columbia, pp 273–297

  • Wassersug RJ, Sperry DG (1977) The relationships of locomotion to differential predation on Pseudacris triseriata (Anura: Hylidae). Ecology 58:830–839

    Article  Google Scholar 

  • Weldon PJ (2017) Poison frogs, defensive alkaloids, and sleepless mice: critique of a toxicity bioassay. Chemoecology 27:123–126

    Article  CAS  Google Scholar 

  • Wilbur HM (1997) Experimental ecology of food webs: complex systems in temporary ponds. Ecology 78:2279–2302. https://doi.org/10.1890/0012-9658(1997)078[2279:EEOFWC]2.0.CO;2

    Article  Google Scholar 

  • Wilson NJ, Williams CR (2014) A critical review of freshwater crayfish as amphibian predators: capable consumers of toxic prey? Toxicon 82:9–17

    Article  CAS  PubMed  Google Scholar 

  • Yu G (2020) Using ggtree to visualize data on tree-like structures. Curr Protoc Bioinform 69:e96. https://doi.org/10.1002/cpbi.96

    Article  Google Scholar 

Download references

Funding

Financial support was provided by an International Centre for Genetic Engineering and Biotechnology (IGCEB) Early Career Grant (CRI19-04_EC) and a Seed Grant from the Office of Research at the University of Costa Rica (741-C0-470) to JLS.

Author information

Authors and Affiliations

  1. Clodomiro Picado Institute, University of Costa Rica, San José, Costa Rica

    Jennifer L. Stynoski

  2. School of Biological Sciences, National University of Costa Rica, Heredia, Costa Rica

    Katherine Porras-Brenes

Authors
  1. Jennifer L. Stynoski
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Katherine Porras-Brenes
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

JLS and KPB conceived and designed the study, performed the literature review and indexing, and edited the manuscript. JLS analyzed the data and wrote the manuscript.

Corresponding author

Correspondence to Jennifer L. Stynoski.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article was based on an analysis of data that are available in previously published research articles and does not contain any studies with human participants or animals performed by any of the authors.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Additional information

Communicated by Osamu Kishida.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (XLSX 230 KB)

Supplementary file2 (R 14 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Stynoski, J.L., Porras-Brenes, K. Meta-analysis of tadpole taste tests: consumption of anuran prey across development and predator strategies. Oecologia 199, 845–857 (2022). https://doi.org/10.1007/s00442-022-05221-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-022-05221-9

Keywords

Search

Navigation