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Arginine vasotocin modulates associative learning in a mutualistic cleaner fish

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Abstract

Social environmental complexity induces structural and biochemical changes in animals’ brains, which are linked to the improvement of animals’ learning abilities. The nonapeptides from the arginine vasopressin (AVP) family (arginine vasotocin, AVT, in non-mammals) play a significant role in the regulation of social behavior, particularly in the formation of social memories and individual recognition. Moreover, the role of AVT in the regulation of interspecific interactions has only recently started to be addressed in the context of cleaner fish mutualisms and learning. Variance in the distribution of AVP receptor expression, which is linked to distinct neural systems (related to the dorsolateral and the dorsomedial telencephalon), is known to be implicated in differences in individual learning processes. Here we asked if the associative learning performance of the Indo-Pacific bluestreak cleaner wrasse (Labroides dimidiatus) is regulated by AVT. We tested the influence of AVT upon the cleaners’ ability to solve two different problems (cue and place discrimination tasks) that in principle differ in ecological relevance and are associated with two different memory systems. We found that AVT affected the learning competence of cleaners differently between tasks, as individual performance showed distinct response selectivity to AVT dosage levels. However, only in the ecologically relevant task was their learning response improved by blocking AVT via treatment with the antagonist Manning compound. Our findings demonstrate that AVT pathways, which are implicated in the regulation of interspecific behavior (i.e., a cleaner’s willingness to seek interactions with clients), are also linked to individual learning ability in the context of mutualistic behavior, and in tune with socio-ecological demands.

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Acknowledgments

We thank the principal curator of Oceanário de Lisboa (Núria Baylina) and staff for logistical support. We also thank Liliana Lettieri and the three anonymous referees for relevant comments on earlier versions of this manuscript. This study was financed by Fundação para a Ciência e Tecnologia (FCT, grant PTDC/MAR/105276/2008 to MCS). SCC was supported by a FCT PhD fellowship. MCS is supported by the Project “Genomics and Evolutionary Biology,” co-financed by North Portugal Regional Operational Programme 2007/2013 (ON.2 – O Novo Norte), under the National Strategic Reference Framework (NSRF), through the European Regional Development Fund (ERDF), RFO by FCT strategic plan PEst-OE/MAR/UI0331/2011, RB by Swiss Science Foundation 31003AB grant and RM by the Brazilian National Council for Scientific and Technological Development (CNPQ; PhD Fellowship).

Author contributions

MCS and RB designed the study. SCC, JRP, and RM collected the data. SCC, MSC, RM, RFO, and RB analyzed the data and wrote the paper. All authors discussed results and commented on the manuscript.

Compliance with Ethical Standards

Animal procedures used in this study have been approved by the Portuguese Veterinary Office (Direcção Geral de Veterinária, license # 0420/000/000/2009).

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Authors and Affiliations

  1. Unidade de Investigação em Eco-Etologia, ISPA – Instituto Universitário, Lisboa, Portugal

    Sónia C. Cardoso, José R. Paitio & Rui F. Oliveira

  2. CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, Universidade do Porto, Campus Agrário de Vairão, 4485-661, Vairão, Portugal

    Sónia C. Cardoso, Renata Mazzei & Marta C. Soares

  3. Eco-Ethologie, Institut de Biologie, Université de Neuchâtel, Neuchâtel, Switzerland

    Redouan Bshary & Renata Mazzei

  4. Integrative Behavioural Biology Group, Instituto Gulbenkian de Ciência, Oeiras, Portugal

    Rui F. Oliveira

  5. Champalimaud Neuroscience Programme, Champalimaud Foundation, Lisboa, Portugal

    Rui F. Oliveira

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  1. Sónia C. Cardoso
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  2. Redouan Bshary
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  3. Renata Mazzei
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  4. José R. Paitio
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  5. Rui F. Oliveira
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  6. Marta C. Soares
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Corresponding author

Correspondence to Marta C. Soares.

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Communicated by C. R. Gabor

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Cardoso, S.C., Bshary, R., Mazzei, R. et al. Arginine vasotocin modulates associative learning in a mutualistic cleaner fish. Behav Ecol Sociobiol 69, 1173–1181 (2015). https://doi.org/10.1007/s00265-015-1931-z

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  • DOI: https://doi.org/10.1007/s00265-015-1931-z

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