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Trade-offs between visual and chemical behavioral responses

  • Emília P. MartinsEmail author
  • Alison G. Ossip-Drahos
  • Cuauhcihuatl Vital García
  • J. Jaime Zúñiga-Vega
  • Stephanie M. Campos
  • Diana K. Hews
Original Article

Abstract

Multiple and multimodal signals can evolve because they convey different information to different receivers or in different contexts. From the perspective of display receivers, however, multimodal signals may pose a challenge since evolutionary changes in any one aspect of the signal may require shifts in other aspects of receiver physiology and behavior. Here, we use field experiments with four species of Sceloporus lizards to test whether evolutionary loss of one element of a complex signal (a colorful belly patch) has led to a change in the behavioral response to a live conspecific. Instead, we found that males of three species (S. merriami, cozumelae, and siniferus) responded to the live conspecific with increased visual and decreased chemical behavior, supporting a Sensory Isolation hypothesis in which animals minimize interference by isolating a single sensory modality, for example, closing eyes to pay closer attention to a sound or smell. In an exception that offers additional support, males of the fourth species, S. parvus, also showed a trade-off in their response, but responded to the live stimulus with more chemical and less visual behavior. We found little evidence that lizards that have lost production of one signal element (belly color) have also altered their response behavior as a consequence. These results emphasize the potentially important role of receiver response in maintaining complex and multimodal signals.

Significance statement

Animals use all of their sensory systems to communicate with each other, but using more than one sense at a time can be a challenge. Here, we presented male lizards in the field to a tethered intruder to ask whether lizards that have lost one element of the signal (a color patch) over evolutionary time have also evolved their response to communicative signals. Instead, we found that males of three species responded primarily with visual behavior and decreased their use of chemical behavior, as if focusing their attention entirely on the visual sensory modality. Males of the fourth species responded primarily with chemical behavior, and decreased their use of visual behavior. These results suggest that there may be mechanical constraints limiting communication signals that make use of more than one sensory system.

Keywords

Multimodal communication Receiver Sceloporus lizards Sensory system Signal evolution 

Notes

Acknowledgments

We are indebted to Sharon Downes, Thomas Madsen, and four reviewers of the manuscript, all of whom offered numerous insightful comments. We thank Jesualdo Fuentes-G., Jay Goldberg, Delia Shelton, Cristina Romero-Diaz, Julio Rivera, Piyumika Suriyampola, and Delawrence Sykes for many helpful discussions, as well as Jake Pruett, José Oyola-Morales, and Patrick Cain for help in the field. We also thank the staff and volunteers at the Parque Nacional Huatulco for logistical support. We thank Big Bend Ranch State Park and El Parque Nacional Huatulco for granting access to public lands, and we thank Carolyn Ohl-Johnson for granting access to private land.

Funding information

This material is based upon work supported by the National Science Foundation under grant numbers IOS-1050274 to EPM and IOS-1052247 to DKH.

Compliance to ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

We followed all applicable international, national, and institutional guidelines for the care and use of animals. All procedures were in accordance with the ethical standards of the institutions at which we conducted the research. The work was approved as part of IACUC protocols 10-013 and 13-009. Permission to conduct this work was also granted by the Texas Parks and Wildlife Department (S. merriami: SPR-0511-129) and the Secretaría de Medio Ambiente y Recursos Naturales of México (SEMARNAT; S. siniferus: 09/O1-0557/12/13; S. cozumelae and S. parvus: 09/k50904/01/13).

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.School of Life SciencesArizona State UniversityTempeUSA
  2. 2.Department of Natural SciencesMiddle Georgia State UniversityMaconUSA
  3. 3.Departamento de Ciencias Veterinárias, Instituto de Ciencias BiomédicasUniversidad Autónoma de Ciudad JuárezCiudad JuárezMexico
  4. 4.Departamento de Ecología y Recursos Naturales, Facultad de CienciasUniversidad Nacional Autónoma de MéxicoMéxico D.F.Mexico
  5. 5.Department of BiologyIndiana UniversityBloomingtonUSA
  6. 6.Department of BiologyIndiana State UniversityTerre HauteUSA

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