Skip to main content
SpringerLink
Log in

Fear of the dark: substrate preference in Amazonian tadpoles

  • Original Paper
  • Published:
acta ethologica Aims and scope Submit manuscript

Abstract

Due to the importance of camouflage to avoid detection by predators, predation pressure can cause coupled evolution of skin colour and preference for substrate colour. Individuals can choose regions where the background makes their skin colour less noticeable (crypsis) or where it accentuates warning coloration (aposematism). In such scenario, individuals should optimally choose substrate according to their skin colour and mechanism of predation avoidance: toxic species are expected to choose highly lit places and non-toxic species should avoid such places. We studied substrate choice on five species of tadpoles that differ in body colour and toxicity. The results of the present study did not confirm our prediction that non-toxic and cryptically coloured species would prefer a lower contrast substrate that maximizes camouflage. We show that individuals preferred highly lit areas that accentuated their contrast with the substrate. The general preference for lighter substrate might be related to the tadpole’s limited vision on a dark substrate, which hampers their ability in detecting predators. This study demonstrates that tadpoles can distinguish the substrate colour and that their choice of habitat might be linked to both their defence mechanism in the case of aposematic species and recognition of habitat elements in the case of cryptically-coloured species.

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

Similar content being viewed by others

Data availability

The datasets generated and analysed during the current study are available from the corresponding author upon request.

References

  • Begon M, Townsend CR, Harper JL (2006) Ecology: from individuals to ecosystems, 4th edn. Blackwell Publishing

  • Bels V, Russell A (2019) Behavior of lizards: evolutionary and mechanistic perspectives. CRC Press

    Book  Google Scholar 

  • Bridges CDB (1973) Spectral sensitivity of the system controlling visual pigment composition in tadpole eyes. Vision Res 14:929–935

    Article  Google Scholar 

  • Briolat ES, Burdfield-Steel ER, Paul SC et al (2019) Diversity in warning coloration: selective paradox or the norm? Biol Rev 94:388–414

    Article  Google Scholar 

  • Buskirk J (2000) The costs of an inducible defense in anuran larvae. Ecology 81:2813–2821

    Article  Google Scholar 

  • Buxton VL, Ward MP, Sperry JH (2017) Frog breeding pond selection in response to predators and conspecific cues. Ethology 123:397–404

    Article  Google Scholar 

  • Cott HB (1940) Adaptive coloration in animals. Methuen, London

    Google Scholar 

  • Dong W, Lee RH, Xu H et al (2009) Visual avoidance in xenopus tadpoles is correlated with the maturation of visual responses in the optic tectum. J Neurophysiol 101:803–815

    Article  Google Scholar 

  • Donnelly WA, Dill LM (1984) Evidence for crypsis in coho salmon, Oncorhynchus kisutch (Walbaum), parr: substrate colour preference and achromatic reflectance. J Fish Biol 25:183–195

    Article  Google Scholar 

  • Edmunds M (1974) Defence in animals: a survey of anti-predator defences. Longman Publishing Group

  • Feltmate BW, Williams DD (1989) Influence of rainbow trout (Oncothynchus mykiss) on density and feeding behaviour of a perlid stonefly. Can J Fish Aquat Sci 56:1575–1580

    Article  Google Scholar 

  • Giaretta AA, da Silva WR, Facure KG (2019) Oviposition site selection in two basin-digging Leptodactylus Fitzinger, 1826 (Anura). Trop Zool 32:10–18

    Article  Google Scholar 

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

    Google Scholar 

  • Hödl W, Amézquita A (2001) Visual signalling in anuran amphibians. Anuran communication. Smithsonian Institution Press, Washington, pp 121–141

    Google Scholar 

  • Hughes A, Liggins E, Stevens M (2019) Imperfect camouflage: how to hide in a variable world? Proc R Soc B 286:20190646

    Article  Google Scholar 

  • Iwata N, Kikuchi K (1998) Effects os sandy substrate and light on hypermelanosis of the blind side in cultured Japanese flounder Paralichthys olivaceus. Environ Biol Fishes 52:291–297

    Article  Google Scholar 

  • Jamieson D, Roberts A (2000) Responses of young Xenopus laevis tadpoles to light dimming: possible roles for the pineal eye. J Exp Biol 203:1857–1867

    Article  CAS  Google Scholar 

  • Kang C, Kim YE, Jang Y (2016) Colour and pattern change against visually heterogeneous backgrounds in the tree frog Hyla japonica. Sci Rep 6:1–12

    Article  Google Scholar 

  • Kindermann C, Narayan EJ, Wild F et al (2013) The effect of stress and stress hormones on dynamic colour-change in a sexually dichromatic Australian frog. Comp Biochem Physiol Part A Mol Integr Physiol 165:223–227

    Article  CAS  Google Scholar 

  • Kopp K, Wachlevski M, Eterovick PC (2006) Environmental complexity reduces tadpole predation by water bugs. Can J Zool 84:136–140

    Article  Google Scholar 

  • McCollum SA, Leimberger JD (1997) Predator-induced morphological changes in an amphibian: predation by dragonflies affects tadpole shape and color. Oecologia 109:615–621

    Article  CAS  Google Scholar 

  • Moriya T, Kito K, Miyashita Y, Asami K (1996) Preference for background color of the Xenopus laevis tadpole. J Exp Zool 276:335–344

    Article  CAS  Google Scholar 

  • Nomura F, De Marco P, Carvalho AFA, Rossa-Feres DC (2013) Does background colouration affect the behaviour of tadpoles? An experimental approach with an odonate predator. Ethol Ecol Evol 25:185–198

    Article  Google Scholar 

  • Oliveira EF, Goulart E (2000) Distribuição espacial de peixes em ambientes lênticos : interação de fatores. Acta Sci 22:445–453

    Google Scholar 

  • Orton RW, McBrayer LD (2019) Resolving tradeoffs among crypsis, escape behavior, and microhabitat use in sexually dichromatic species. Oecologia 189:91–104

    Article  Google Scholar 

  • Prado CP, D’Heursel A (2006) The tadpole of Leptodactylus elenae (Anura: Leptodactylidae), with the description of the internal buccal anatomy. South Am J Herpetol 1:79–87

    Article  Google Scholar 

  • Prado CP, Uetanabaro M, Haddad CF (2002) Description of a new reproductive mode in Leptodactylus (Anura, Leptodactylidae), with a review of the reproductive specialization toward terrestriality in the genus. Copeia 2002:1128–1133

    Article  Google Scholar 

  • Price N, Green S, Troscianko J et al (2019) Background matching and disruptive coloration as habitat-specific strategies for camouflage. Sci Rep 9:7840

    Article  Google Scholar 

  • Richards SJ, Bull CM (1990) Non-visual detection of anuran tadpoles by odonate larvae. J Herpetol 24:311–313

    Article  Google Scholar 

  • Ruxton GD, Sherratt TN, Speed MP (2004) Avoiding attack: the evolutionary ecology of crypsis, warning signals e mimicry. Oxford University Press

    Book  Google Scholar 

  • Skelly DK (1997) Tadpole communities: pond permanence and predation are powerful forces shaping the structure of tadpole communities. Am Sci 85:36–45

    Google Scholar 

  • Smith GR, Harmon JJ (2019) Differential oviposition and offspring success of gray treefrogs in the presence of an invasive fish. Ecosphere 10:1–9

    Google Scholar 

  • Stamps J, Groothuis TGG (2010) The development of animal personality: relevance, concepts and perspectives. Biol Rev 85:301–325

    Article  Google Scholar 

  • Stevens M, Merilaita S (2009) Animal camouflage: current issues and new perspectives. Philos Trans R Soc B 364:423–424

    Article  Google Scholar 

  • Thibaudeau G, Altig R (2012) Coloration of Anuran tadpoles (Amphibia): development, dynamics, function, and hypotheses. ISRN Zool 2012:1–16

    Article  Google Scholar 

  • Troscianko J, Skelhorn J, Stevens M (2017) Quantifying camouflage: how to predict detectability from appearance. BMC Evol Biol 17:7

    Article  Google Scholar 

  • Van Buskirk J, Aschwanden J, Buckelmüller I et al (2004) Bold tail coloration protects tadpoles from dragonfly strikes. Copeia 2004:599–602

    Article  Google Scholar 

  • Voris HK, Bacon JP (1966) Differential predation on tadpoles. Copeia 1966:594

    Article  Google Scholar 

  • Wassersug R, Hessler CM (1971) Tadpole behaviour: aggregation in larval Xenopus laevis. Anim Behav 19:386–389

    Article  CAS  Google Scholar 

  • Wells KD (2007) The ecology and behavior of amphibians. The University of Chicago Press, London

    Book  Google Scholar 

  • Ximenez SS, Gonçalvez TP, Oliveira MCLM, Tozetti AM (2012) Substrate color selection by tadpoles of Physalaemus gracilis (Boulenger, 1883) (Anura, Leiuperidae). Panam J Aquat Sci 7:111–116

    Google Scholar 

  • Yuma M, Nakamura I, Fausch KD (1998) Fish biology in Japan: an anthology in honour of Hiroya Kawanabe

Download references

Acknowledgements

We thank Marcelo Menin (in memorium) for the identification of species and Fazenda Experimental da UFAM administration for allowing the collection of specimens. ISCG is grateful to João Kennedy Pereira Campos, Izabela Patrícia de Oliveira e Silva Campos and Rubia Neris Machado for helping in the construction of the experimental set-ups. We thank Mateus Darwin da Silva, Marcelo Andrade Maciel, and Italo Roberto Bastos da Silva for their help while collecting tadpoles.

Funding

This research was partially supported by JST/JICA, SATREPS, FIXAM/FAPEAM (#062.01500/2018). We also received financial support from Brazilian CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) and CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior).

Author information

Authors and Affiliations

  1. Programa de Pós-Graduação em Zoologia, Instituto de Ciências Biológicas, Universidade Federal do Amazonas, Av. General Rodrigo Otávio Jordão Ramos, Manaus, AM, 6200, 69077-000, Brazil

    Izabela Sabrina Campos Guimarães, Mahima Hemnani & Igor Luis Kaefer

  2. Laboratório de Ecologia Comportamental e Evolutiva (LECE), Instituto Nacional de Pesquisas da Amazônia (INPA), Av. André Araújo, 2936 - Petrópolis, Manaus, AM, Brazil

    Tiago Henrique da Silva Pires

Authors
  1. Izabela Sabrina Campos Guimarães
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mahima Hemnani
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Igor Luis Kaefer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tiago Henrique da Silva Pires
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the study conception and design. Material preparation and data collection were performed by Izabela Sabrina Campos Guimarães and Mahima Hemnani. The analyses were performed by Izabela Sabrina Campos Guimarães, Tiago Henrique da Silva Pires, and Igor Luis Kaefer. The first draft of the manuscript was written by Izabela Sabrina Campos Guimarães, and all authors contributed on subsequent versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Mahima Hemnani.

Ethics declarations

Ethics approval

All applicable international, national, and institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted. Ethics committee on animal experimentation (CEUA) protocol # 011/2017—CEUA/UFAM.

Consent to participate

All authors consented to participate.

Consent for publication

All authors consented for publication.

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Guimarães, I.S.C., Hemnani, M., Kaefer, I.L. et al. Fear of the dark: substrate preference in Amazonian tadpoles. acta ethol 24, 177–183 (2021). https://doi.org/10.1007/s10211-021-00374-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10211-021-00374-x

Keywords

Search

Navigation