Abstract
Most animal signals across sensory modalities are multicomponent traits that can be broken down into discrete elements. If different elements are perceived as unique, independent units (elemental perception), instead of as integrated percepts (configural perception), single changes in the presence/absence or the abundance of specific elements of a multicomponent signal may be enough to impact communication. Here, we found that male Yarrow’s spiny lizards (Sceloporus jarrovii) can discriminate single compounds of a multicomponent chemical signal (femoral gland secretions), different concentrations of a signaling compound, and a single compound from a mixture of compounds. In addition, one chemical compound elicited a response similar to that evoked by the complete natural scent. We conclude that perception of chemical signals in S. jarrovii lizards is elemental but also configural. The elemental perception of signaling compounds seems to occur with high sensitivity and narrow resolution, so that minor changes in single key elements may affect chemical communication. Given the multicomponent nature of most animal signals, hypotheses regarding signal function and evolution would be enhanced if researchers could determine whether these results apply to signals in other sensory modalities and identify the key elements of complex signals, from a receiver’s perspective.
Significance statement
Most signals in animal communication are quite complex. For example, odors are mixtures of multiple volatile chemical compounds, and the way in which receivers perceive and process these mixtures to extract relevant information influences the structure and evolution of chemical signals. In a series of behavioral trials, we investigated how male Sceloporus jarrovii lizards may perceive conspecific odors by testing their response to individual and combined mixtures of two compounds present in femoral gland secretions at two different concentrations. We demonstrate that lizards can discriminate structurally similar compounds and that the response to a compound changes when said compound is part of a larger mixture. Compound concentration affected the perception of individual compounds but not complex mixtures. Deciphering what elements and/or configurations are perceived in an odor mixture is the only way to understand the role of mixture composition and its impact on communication.
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Data availability
The data generated and analyzed during the current study are available from the manuscript and supplementary material.
References
Abell AJ (1997) Estimating paternity with spatial behaviour and DNA fingerprinting in the striped plateau lizard, Sceloporus virgatus (Phrynosomatidae). Behav Ecol Sociobiol 41:217–226
Apfelbach R, Parsons M, Soini HA, Novotny MV (2015) Are single odorous components of a predator sufficient to elicit defensive behaviors in prey species? Front Neurosci 9:263
Apps PJ (2013) Are mammal olfactory signals hiding right under our noses? Naturwissenschaften 100:487–506
Apps PJ, Weldon PJ, Kramer M (2015) Chemical signals in terrestrial vertebrates: search for design features. Nat Prod Rep 32:1131–1153
Baeckens S, Van Damme R, Cooper WE (2017) How phylogeny and foraging ecology drive the level of chemosensory exploration in lizards and snakes. J Evol Biol 30:627–640
Baugh AT, Akre KL, Ryan MJ (2008) Categorical perception of a natural, multivariate signal: mating call recognition in túngara frogs. Proc Natl Acad Sci U S A 105:8985–8988
Berglund B, Berglund U, Lindvall T (1976) Psychological processing of odor mixtures. Psychol Rev 83:432–441
Bondoc KGV, Lembke C, Vyverman W, Pohnert G (2016) Searching for a mate: pheromone-directed movement of the benthic diatom Seminavis robusta. Microb Ecol 72:287–294
Bro-Jørgensen J (2010) Dynamics of multiple signalling systems: animal communication in a world in flux. Trends Ecol Evol 25:292–300
Campos SM, Strauss C, Martins EP (2017) In space and time: territorial animals are attracted to conspecific chemical cues. Ethology 123:136–144
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 Sceloporus lizards. Behav Ecol 31:978–991
Candolin U (2003) The use of multiple cues in mate choice. Biol Rev 78:575–595
Catchpole CK, Slater PJB (2008) Bird song: biological themes and variations, 2nd edn. Cambridge University Press, New York
Caves EM, Green PA, Zipple MN, Peters S, Johnsen S, Nowicki S (2018) Categorical perception of colour signals in a songbird. Nature 560:365–367
Coleman SW (2009) Taxonomic and sensory biases in the mate-choice literature: there are far too few studies of chemical and multimodal communication. Acta Ethol 12:45–48
Cooper WE Jr (1998) Evaluation of swab and related tests as a bioassay for assessing responses by squamate reptiles to chemical stimuli. J Chem Ecol 24:841–866
Cooper WE Jr, Burghardt GM (1990) A comparative analysis of scoring methods for chemical discrimination of prey by squamate reptiles. J Chem Ecol 16:45–65
Coureaud G, Langlois D, Sicard G, Schaal B (2004) Newborn rabbit responsiveness to the mammary pheromone is concentration-dependent. Chem Senses 29:341–350
Coureaud G, Hamdani Y, Schaal B, Thomas-Danguin T (2009) Elemental and configural processing of odour mixtures in the newborn rabbit. J Exp Biol 212:2525–2531
Coureaud G, Gibaud D, Le Berre E, Schaal B, Thomas-Danguin T (2011) Proportion of odorants impacts the configural versus elemental perception of a binary blending mixture in newborn rabbits. Chem Senses 36:693–700
Cruz D, Eizaguirre M (2015) Response to conspecific and heterospecific semiochemicals by Sesamia nonagrioides (L.) (Lepidoptera: Noctuidae) gravid females. Bull Entomol Res 105:347–354
Duvall D (1979) Western fence lizard (Sceloporus occidentalis) chemical signals. I. Conspecific discriminations and release of a species-typical visual display. J Exp Zool 210:321–325
Endler JA (1992) Signals, signal conditions, and the direction of evolution. Am Nat 139:S125–S153
Furtado NAJC, Pupo MT, Carvalho I, Campo VL, Duarte MCT, Bastos JK (2005) Diketopiperazines produced by an Aspergillus fumigatus Brazilian strain. J Braz Chem Soc 16:1448–1453
Grether GF, Kolluru GR, Nersissian K (2004) Individual colour patches as multicomponent signals. Biol Rev 79:583–610
Halekoh U, Højsgaard S, Yan J (2006) The R package geepack for generalized estimating equations. J Stat Softw 15:1–11
Halfwerk W, Varkevisser J, Simon R, Mendoza E, Scharff C, Riebel K (2019) Toward testing for multimodal perception of mating signals. Front Ecol Evol 7:124
Hebets EA, Papaj DR (2005) Complex signal function: developing a framework of testable hypotheses. Behav Ecol Sociobiol 57:197–214
Hebets EA, Uetz GW (2000) Leg ornamentation and the efficacy of courtship display in four species of wolf spider (Araneae: Lycosidae). Behav Ecol Sociobiol 47:280–286
Herrmann MA, Campos SM, Martins EP, Romero-Diaz C (2020) Eye-bulging behavior in lizards of the genus Sceloporus: a role in chemical communication? Copeia 108:309–315
Hews DK, Martins EP (2013) Visual and chemical signals of social communication: providing the link to habitat and environment. In: Lutterschmidt W (ed) Reptiles in research: investigations of ecology, physiology and behavior from desert to sea. Nova Publishers, Hauppauge, pp 111–141
Hews DK, Date P, Hara E, Castellano M (2011) Field presentation of male secretions alters social display in Sceloporus virgatus but not S. undulatus lizards. Behav Ecol Sociobiol 65:1403–1410
Holveck MJ, Riebel K (2007) Preferred songs predict preferred males: consistency and repeatability of zebra finch females across three test contexts. Anim Behav 74:297–309
Huberman L, Gollop N, Mumcuoglu KY, Breuer E, Bhusare SR, Shai Y, Galun R (2007) Antibacterial substances of low molecular weight isolated from the blowfly, Lucilia sericata. Med Vet Entomol 21:127–131
Jacot A, Romero-Diaz C, Tschirren B, Richner H, Fitze PS (2010) Dissecting carotenoid from structural components of carotenoid-based coloration: a field experiment with great tits (Parus major). Am Nat 176:55–62
Jemiolo B, Novotny M (1994) Inhibition of sexual maturation in juvenile female and male mice by a chemosignal of female origin. Physiol Behav 55:519–522
Johnston RE (2005) Communication by mosaic signals: individual recognition and underlying neural mechanisms. In: Mason RT, LeMaster MP, Müller-Schwarze D (eds) Chemical signals in vertebrates 10. Springer, Boston, pp 269–282
Kelso EC, Martins EP (2008) Effects of two courtship display components on female reproductive behaviour and physiology in the sagebrush lizard. Anim Behav 75:639–646
Lei H, Vickers N (2008) Central processing of natural odor mixtures in insects. J Chem Ecol 34:915–927
LeMaster MP, Mason RT (2003) Pheromonally mediated sexual isolation among denning populations of red-sided garter snakes, Thamnophis sirtalis parietalis. J Chem Ecol 29:1027–1043
Livermore A, Hutson M, Ngo V, Hadjisimos R, Derby CD (1997) Elemental and configural learning and the perception of odorant mixtures by the spiny lobster Panulirus argus. Physiol Behav 62:169–174
López P, Martín J (2012) Chemosensory exploration of male scent by female rock lizards result from multiple chemical signals of males. Chem Senses 37:47–54
López P, Amo L, Martín J (2006) Reliable signaling by chemical cues of male traits and health state in male lizards, Lacerta monticola. J Chem Ecol 32:473–488
Martín J, López P (2014) Pheromones and chemical communication in lizards. In: Rheubert JL, Siegel DS, Trauth SE (eds) The reproductive biology and phylogeny of lizards and tuatara. CRC Press, Boca Raton, pp 43–77
Martín J, Moreira PL, López P (2007) Status-signalling chemical badges in male Iberian rock lizards. Funct Ecol 21:568–576
Martín J, Ortega J, López P (2015) Interpopulational variations in sexual chemical signals of Iberian wall lizards may allow maximizing signal efficiency under different climatic conditions. PLoS ONE 10:e0131492
Martins EP (1993) A comparative study of the evolution of Sceloporus push-up displays. Am Nat 142:994–1018
Martins EP, Ord TJ, Davenport SW (2005) Combining motions into complex displays: playbacks with a robotic lizard. Behav Ecol Sociobiol 58:351–360
Martins EP, Ord TJ, Slaven J, Wright JL, Housworth EA (2006) Individual, sexual, seasonal, and temporal variation in the amount of sagebrush lizard scent marks. J Chem Ecol 32:881–893
Mason RT, Parker MR (2010) Social behavior and pheromonal communication in reptiles. J Comp Physiol A 196:729–749
Micheletta J, Engelhardt A, Matthews L, Agil M, Waller BM (2013) Multicomponent and multimodal lipsmacking in crested macaques (Macaca nigra). Am J Primatol 75:763–773
Novotny MV, Jemiolo B, Harvey S, Wiesler D, Marchlewska-Koj A (1986) Adrenal-mediated endogenous metabolites inhibit puberty in female mice. Science 231:722–725
Ord TJ, Martins EP (2006) Tracing the origins of signal diversity in anole lizards: phylogenetic approaches to inferring the evolution of complex behaviour. Anim Behav 71:1411–1429
Ossip-Drahos AG, Oyola Morales JR, Vital-García C, Zúñiga-Vega JJ, Hews DK, Martins EP (2016) Shaping communicative colour signals over evolutionary time. R Soc Open Sci 3:160728
Ossip-Klein AG, Fuentes-González JA, Hews DK, Martins EP (2013) Information content is more important than sensory system or physical distance in guiding the long-term evolutionary relationships between signaling modalities in Sceloporus lizards. Behav Ecol Sociobiol 67:1513–1522
Pinheiro J, Bates D, DebRoy S, Sarkar D, Development Core Team R (2018) nlme: linear and nonlinear mixed effects models. R Package Version 3:1–137. http://CRAN.R-project.org/package=nlme
Price AC, Weadick CJ, Shim J, Rodd FH (2008) Pigments, patterns, and fish behavior. Zebrafish 5:297–307
Pruett JA, Zuniga-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
Quinn VS, Hews DK (2010) The evolutionary decoupling of behavioral and color cues in a multicomponent signal in two Sceloporus lizards. Ethology 116:509–516
R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org
Rand AS, Ryan MJ (1981) The adaptive significance of a complex vocal repertoire in a neotropical frog. Z Tierpsychol 57:209–214
Reinhard J, Sinclair M, Srinivasan MV, Claudianos C (2010) Honeybees learn odour mixtures via a selection of key odorants. PLoS ONE 5:e9110
Renou M (2014) Pheromones and general odor perception in insects. In: Mucignat-Caretta C (ed) Neurobiology of chemical communication. CRC Press/Taylor & Francis, Boca Raton, pp 23–56
Rhee KH (2004) Cyclic dipeptides exhibit synergistic, broad spectrum antimicrobial effects and have anti-mutagenic properties. Int J Antimicrob Agents 24:423–427
Riebel K (2009) Song and female mate choice in zebra finches: a review. Adv Study Behav 40:197–238
Riffell JA, Lei H, Christensen TA, Hildebrand JG (2009) Characterization and coding of behaviorally significant odor mixtures. Curr Biol 19:335–340
Romero-Diaz C, Richner H, Granado-Lorencio F, Tschirren B, Fitze PS (2013) Independent sources of condition dependency and multiple pathways determine a composite trait: lessons from carotenoid-based plumage colouration. J Evol Biol 26:635–646
Romero-Diaz C, Rivera JA, Ossip-Drahos AG, Zúñiga-Vega JJ, Vital-García C, Hews DK, Martins EP (2019) Losing the trait without losing the signal: evolutionary shifts in communicative colour signalling. J Evol Biol 32:320–330
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. Sci Rep 10:4303
Rowe C (1999) Receiver psychology and the evolution of multicomponent signals. Anim Behav 58:921–931
Ruby DE (1981) Phenotypic correlates of male reproductive success in the lizard, Sceloporus jarrovi. In: Alexander RD, Tinkle DW (eds) Natural selection and social behavior: recent research and new theory. Chiron Press, New York, pp 96–107
Ryan MJ (1991) Sexual selection and communication in frogs. Trends Ecol Evol 6:351–355
Ryan MJ, Rand AS (2003) Mate recognition in túngara frogs: a review of some studies of brain, behavior, and evolution. Acta Zool Sin 49:713–726
Schaal B, Coureaud G, Langlois D, Giniès C, Sémon E, Perrier G (2003) Chemical and behavioural characterization of the rabbit mammary pheromone. Nature 424:68–72
Schneider NY, Datiche F, Wilson DA, Gigot V, Thomas-Danguin T, Ferreira G, Coureaud G (2016) Brain processing of a configural vs elemental odor mixture in the newborn rabbit. Brain Struct Funct 221:2527–2539
Smith CL, Evans CS (2013) A new heuristic for capturing the complexity of multimodal signals. Behav Ecol Sociobiol 67:1389–1398
Taylor RC, Klein B, Stein J, Ryan M (2008) Faux frogs: multimodal signalling and the value of robotics in the study of animal behaviour. Anim Behav 76:1089–1097
Thomas-Danguin T, Sinding C, Romagny S, El Mountassir F, Atanasova B, Le Berre E, Le Bon A-M, Coureaud G (2014) The perception of odor objects in everyday life: a review on the processing of odor mixtures. Front Psychol 5:504
Thompson JT, Bissell AN, Martins EP (2008) Inhibitory interactions between multimodal behavioural responses may influence the evolution of complex signals. Anim Behav 76:113–121
Tumlinson JH, Brennan MM, Doolittle RE, Mitchell ER, Brabham A, Mazomenos BE, Baumhover AH, Jackson DM (1989) Identification of a pheromone blend attractive to Manduca sexta (L.) males in a wind tunnel. Arch Insect Biochem Physiol 10:255–271
Uetz GW, Clark DL, Roberts JA (2016) Multimodal communication in wolf spiders (Lycosidae) — an emerging model for study. Adv Study Behav 48:117–159
Weldon PJ, Flachsbarth B, Schulz S (2008) Natural products from the integument of nonavian reptiles. Nat Prod Rep 25:738–756
Wyatt TD (2014) Introduction to chemical signaling in vertebrates and invertebrates. In: Mucignat-Caretta C (ed) Neurobiology of chemical communication. Taylor & Francis Group LLC, Boca Raton, pp 1–22
Yew JY, Chung H (2015) Insect pheromones: an overview of function, form, and discovery. Prog Lipid Res 59:88–105
Yorzinski JL, Patricelli GL, Babcock JS, Pearson JM, Platt ML (2013) Through their eyes: selective attention in peahens during courtship. J Exp Biol 216:3035–3046
Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R, 1st edn. Springer, New York
Acknowledgements
We are thankful to Cindy Xu and Kenro Kusumi for sharing laboratory equipment, to Julio Rivera, Jesualdo Fuentes-G, Ciara Sypherd and Anna Hu for the help in the field, and to two anonymous reviewers for their helpful comments. The Department of Animal Care & Technologies at ASU and the Southwestern Research Station provided logistical support.
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This work was supported by the National Science Foundation under grant numbers IOS-1050274 to EPM and IOS-1052247 to DKH.
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Lizard capture was approved by the Arizona Game and Fish Department (LIC #SP597303) and the US Forest Service. All procedures and animal care were conducted according to protocols approved by Arizona State University Animal Care and Use Committee (protocol No. 17-1597R to EPM) and adhered to ASAB/ABS Guidelines for the Use of Animals in Research. Lizards were monitored daily for welfare and were allowed to live in the laboratory after the behavior experiments.
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Romero-Diaz, C., Campos, S.M., Herrmann, M.A. et al. Composition and compound proportions affect the response to complex chemical signals in a spiny lizard. Behav Ecol Sociobiol 75, 42 (2021). https://doi.org/10.1007/s00265-021-02987-5
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DOI: https://doi.org/10.1007/s00265-021-02987-5