Robot Lizard

We study the mechanisms underlying the evolution of complex and multimodal communicative signals. Why are there so many kinds of lizard displays? Why use both visual and chemical signals? Does using multiple sensory modalities enhance communication, fitness, or resilience to environmental change?

Most recently, in a collaboration with Diana Hews and Jaime Zúñiga-Vega (and many others. Our work has been supported, in part, by the National Science Foundation under Grant Nos. 1050274 and 0236049), we found evidence for a negative relationship between visual and chemical signals. For example:  

Currently, we are using laboratory and field playback experiments to study the behavioral interactions between motion, color and chemical signals, how these impact space use & interspecific communication, and how they change with climate and other forms of rapid environmental change. We're collaborating with geologists & phylogeographers to map the history of Sceloporus displays through time and space, with artists & engineers to create robotic lizards, with chemists to analyse the composition of pheromones, and with evolutionary genomics researchers to study the mechanisms underlying evolutionary change.  

Some relevant publications:
  • Romero-Diaz C, Pruett JA, Campos SM, Ossip-Drahos AG, Zúñiga-Vega JJ, Vital-García C, Hews, DK, Martins EP. 2021. Evolutionary loss of a signalling colour is linked to increased response to conspecific chemicals. Proceedings of the Royal Society B 288(1947):20210256. (https://doi.org/10.1098/rspb.2021.0256)
  • Romero-Diaz C, Campos SM, Herrmann MA, Soini HA, Novotny MV, Hews, DK, Martins EP. 2021. Composition and compound proportions affect the response to complex chemical signals in a spiny lizard. Behavioral Ecology & Sociobiology, in press. (https://doi.org/10.1007/s00265-021-02987-5; https://rdcu.be/ceALC)
  • Campos SM, Pruett JA, Soini HA, Zúñiga-Vega JJ, Goldberg JK, Vital García C, Hews DK, Novotny MV, Martins EP. 2020. Volatile fatty acid and aldehyde abundances evolve with behavior and habitat temperature in lizards. Behav Ecol 31: 978-991.(https://doi.org/10.1093/beheco/araa044)
  • Romero-Diaz C, Campos SM, Herrmann MA, Lewis KN, Williams DR, Soini HA, Novotny MV, Hews DK, Martins EP. 2020. Structural identification, synthesis and biological activity of two volatile cyclic dipeptides in a terrestrial vertebrate. Scientific Reports 10:4303 (doi:10.1038/s41598-020-61312-8).
  • Herrmann MA, Campos SM, Martins EP, Romero-Diaz C. 2020. Eye-bulging behavior in Sceloporus lizards: A role in chemical communication? Copeia 108:309-315. (doi: https://doi.org/10.1643/CE-19-249)
  • Goldberg JK, Pintel G, Weiss SL, Martins EP. 2019. Predatory lizards perceive plant-derived volatile odorants. Ecology & Evolution 9:4733-4738 (doi:10.1002/ece3.5076).
  • Romero-Díaz C, Rivera JA, Ossip-Drahos AG, Zúñiga-Vega JJ, Vital Garcia C, Hews DK, Martins EP. 2019. Losing the trait without losing the signal: Evolutionary shifts in communicative colour signaling of Sceloporus lizards. Journal of Evolutionary Biology (doi: 10.1111/jeb.13416).
  • Martins EP, Ossip-Klein AG, Vital Garcia C, Zúñiga-Vega JJ, Campos SM, Hews DK. 2018. Trade-offs between visual and chemical behavioral responses. Behavioral Ecology & Sociobiology 72:189 (doi: 10.1007/s00265-018-2617-0).
  • Ossip-Drahos AG, Berry NH, King CM, Martins EP. 2018. Information-gathering as a response to manipulated signals in the Eastern Fence Lizard, Sceloporus undulatus. Ethology 124: 684-690. (doi: 10.1111/eth.12801)
  • Campos SM, Straus C, Martins EP. 2017. In space and time: Territorial animals are attracted to conspecific chemical cues. Ethology 123: 136-144. (doi:10.1111/eth.12582)
  • Ossip-Drahos AG, Oyola Morales JR, Vital Garcia C, Zúñiga-Vega JJ, Hews DK, Martins EP. 2016. Shaping communicative color signals over evolutionary time. Royal Society Open Science 3:160728. (doi:10.1098/rsos.160728)
  • Pruett JA, Zúñiga-Vega JJ, Campos SM, Soini HA, Novotny MV, Vital Garcia C, Martins EP, Hews DK. 2016. Evolutionary interactions between visual and chemical signals: Chemosignals compensate for the loss of a visual signal in male Sceloporus lizards. J Chem Ecol 42:1164-1174. (doi: 10.1007/s10886-016-0778-8)
  • Lawing AM, Polly PD, Hews DK, Martins EP. 2016. Including fossils in phylogenetic climate reconstructions: A deep time perspective on the climatic niche evolution and diversification of Spiny Lizards (Sceloporus). Am Nat, 188:133-148. (doi:10.1086/687202)
  • Martins EP, Ossip-Klein AG, Zúñiga-Vega JJ, Vital Garcia C, Campos SM, Hews DK. 2015. Evolving from static to dynamic signals: evolutionary compensation between two communicative signals. Animal Behaviour 102:223-229. (doi:10.1016/j.anbehav.2015.01.028)
  • Hews DK, Martins EP. 2013. Visual and chemical signals of social communication: Providing the link to habitat and environment. In: Reptiles in Research: Investigations of Ecology, Physiology and Behavior from Desert to Sea. WL Lutterschmidt, ed. Nova Publishers, Hauppauge NY. (pdf and book)
  • Ossip-Klein AG, Fuentes JA, Hews DK, Martins EP. 2013. Information content is more important than sensory system in guiding the long-term evolutionary relationships between signaling modalities in Sceloporus lizards. Behavioral Ecology and Sociobiology 67:1513-1522. doi:10.1007/s00265-013-1535-4
  • Nava S, Morena L, Wang D. 2012. Receiver sex differences in visual response to dynamic motion signals in lizards. Behavioral Ecology and Sociobiology 66:1357-1362. doi:10.1007/s00265-012-1392-6
  • Ruiz, M, Wang D, Reinke EA, Demas GE, Martins EP. 2011. Trade-offs between reproductive coloration and innate immunity in a natural population of female Sagebrush lizards. Herpetological Journal 21:131-134. 
  • Ruiz M, French SS, Demas GE, Martins EP. 2010. Food supplementation and testosterone interact to influence reproductive behavior and immune function in Sceloporus graciosus. Hormones and Behavior 57:134-139. doi:10.1016/j.yhbeh.2009.09.019
  • Ruiz M, Beals ZM, Martins EP. 2010. Male sagebrush lizards (Sceloporus graciosus) increase exploratory behavior towards females with more courtship experience. Herpetologica 66:142-147. doi:10.1655/09-022R2.1
  • Nava S, Conway M, Martins EP. 2009. Sex-specific visual performance: female lizards outperform males motion detection. Biology Letters 5: 732-734. doi:10.1098/rsbl.2009.0348
  • Nava, S.S., M. Conway and E.P. Martins. 2009. Divergence of visual motion detection in diurnal geckos that inhabit bright and dark habitats. Functional Ecology 23: 794-799. doi:10.1111/j.1365-2435.2009.01565.x
  • Ruiz, M., E. Davis and E.P. Martins. 2008. Courtship attention in Sagebrush lizards varies with male identity and female reproductive state. Behavioral Ecology 19: 1326-1332. doi:10.1093/beheco/arn072
  • Thompson, J.T., Bissell, A.N. and E.P. Martins. 2008. Inhibitory interactions between multimodal behavioral responses may influence the evolution of complex signals. Animal Behaviour, 76: 113-121.doi.10.1016/j.anbehav.2007.12.015).
  • Kelso, E.C. and E.P. Martins. 2008. The effects of two courtship display components on female reproductive behaviour and physiology in the sagebrush lizard. Animal Behaviour 75: 639-646. (doi:10.1016/j.anbehav.2007.07.017)
  • Smith, C.B. and E.P. Martins. 2006. Display plasticity in response to a robotic lizard: Signal matching or song-sharing in lizards? Ethology 112: 955-962 (doi:10.1111/j.1439-0310.2006.01253.x)
  • Bissell, A.N. and E.P. Martins. 2006. Male choice and female avoidance as mechanisms of population discrimination in Sagebrush lizards. Behavioral Ecology and Sociobiology 60: 655-662 (doi:10.1007/s00265-006-0209-x.)
  • Ord, T.J. and E.P. Martins. 2006. Tracing the origins of signal diversity in anole lizards: phylogenetic approaches to inferring the evolution of complex behaviour. Animal Behaviour, 71:1411-1429 (doi:10.1016/j.anbehav.2005.12.003.)
  • Martins, E.P., T.J. Ord, J. Slaven, J.L. Wright, and E.A. Housworth. 2006. Individual, sex, seasonal and temporal variation in the amount of Sagebrush lizard scent-marks. Journal of Chemical Ecology, 32: 881-893. (doi:10.1007/s10886-006-9029-8.)
  • Martins, E.P., T. J. Ord, and S.W. Davenport. 2005. Combining motions into complex displays: playbacks with a robotic lizard. Behavioral Ecology and Sociobiology, 58: 351-360. (doi:10.1007/s00265-005-0954-2.)
  • Martins, E.P., A. Labra, M.P. Halloy and J.T. Thompson. 2004. Large-scale patterns of signal evolution: An interspecific study of Liolaemus lizard headbob displays. Animal Behaviour, 68: 453-463. (doi:10.1016/j.anbehav.2003.08.026.)
  • Bissell, A. N. and E.P. Martins. 2004. Complex behavior and ecology of rock iguanas. II. Population differences, behavior and conservation. In "Iguanas: Biology and conservation" edited by Allison Alberts, Ron Carter, William Hayes, & Emilia Martins. University of California Press. PP.109-118. (pdf)
  • Martins, E.P. and K.E. Lacy. 2004. Complex behavior and ecology of rock iguanas. I. Evidence for an appeasement display. IN: "Iguanas: Biology and conservation" edited by Allison Alberts, Ron Carter, William Hayes, & Emilia Martins. University of California Press. PP. 101-108. (pdf)
  • Martins, E.P. 2004. Behavior and Ecology. Introduction. IN: "Iguanas: Biology and conservation" edited by Allison Alberts, Ron Carter, William Hayes, & Emilia Martins. University of California Press. PP. 97-100. (pdf)
  • Alberts, A., R. Carter, W. Hayes and E. Martins, eds. 2004. Iguanas: Biology and conservation. University of California Press.
  • Lacy, K.E. and E. P. Martins. 2003. The effects of anthropogenic habitat usage on the social behaviour of a vulnerable species, Cyclura nubila. Animal Conservation, 6: 3-9. (pdf)
  • Zani, P.A. 2001. Clinging performance of the Western fence lizard, Sceloporus occidentalis.Herpetologica 57:423-432.
  • Sheldahl, L.A. and E.P. Martins. 2000. Territorial behavior in the western fence lizard. Herpetologica, 56: 469-479. (pdf)
  • Zani, P.A. 1999. The comparative evolution of lizard claw and toe morphology, clinging performance, and microhabitat use. Journal of Evolutionary Biology, 13: 316-325. (pdf)
  • Martins, E. P., A. N. Bissell, and K.K. Morgan. 1998. Population differences in a lizard communicative display: evidence for rapid change in structure and function. Animal Behaviour 56: 1113-1119. (doi:10.1016/anbe.1998.0872.)
  • Martins, E. P. and J. Lamont. 1998. Estimating ancestral states of a communicative display: a comparative study of Cyclura rock iguanas. Animal Behaviour, 55:1685-1706. (doi:10.1016/anbe.1997.0722.)
  • Martins, E. P. 1994. Structural complexity in a lizard communication system: the Sceloporus graciosus"push-up" display. Copeia, 1994: 944-955. (pdf)
  • Martins, E. P. 1994. Phylogenetic perspectives on the evolution of lizard territoriality. IN: Lizard Ecology: Historical and Experimental Perspectives (L. Vitt and E. R. Pianka, eds.). pp. 117-144. Princeton University Press. (pdf)
  • Martins, E. P. 1993. A comparative study of the evolution of Sceloporus push-up displays. American Naturalist 142: 994-1018. (Read on-line through JSTOR.)
  • Martins, E. P. 1993. Contextual use of the push-up display by the Sagebrush Lizard, Sceloporus graciosus. Animal Behaviour, 45: 25-36. (doi:10.1016/anbe.1993.1003.)
  • Martins, E. P. 1991. A field study of individual and sex differences in the push-up display of the Sagebrush Lizard, Sceloporus graciosus. Animal Behaviour, 41: 403-416. (pdf)
  • Romero-Diaz, Rivera et al. 2019