Blind date: female fossorial amphisbaenians prefer scent marks of large and healthy males

José MARTÍN , Gonzalo RODRÍGUEZ-RUIZ , Álvaro NAVARRO-CASTILLA , Isabel BARJA , Pilar LÓPEZ

Integrative Zoology ›› 2024, Vol. 19 ›› Issue (6) : 1018 -1033.

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Integrative Zoology ›› 2024, Vol. 19 ›› Issue (6) : 1018 -1033. DOI: 10.1111/1749-4877.12802
ORIGINAL ARTICLE

Blind date: female fossorial amphisbaenians prefer scent marks of large and healthy males

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Abstract

Selecting a good mate is a decision with important fitness consequences. For this reason, mate choice has promoted the evolution of sexual ornaments signaling the quality of an individual. In fossorial animals, inhabiting visually restricted underground environments, chemical senses should be very important for mate choice. We examined whether sexual chemical signals (substrate scent marks) produced by males of the Iberian worm lizard,Blanus cinereus, a strictly fossorial blind amphisbaenian, provide information to females on morphological traits and health state. We administered corticosterone (CORT) to males simulating a continuous stressor affecting their health. Females preferred settling at sites scent-marked by males in comparison with similar sites with female scent or unmarked sites, but the attractiveness of males’ scent differed between individuals. Females preferred scent marks of larger/older males and with a higher immune response, while their body condition and CORT treatment were unrelated to female preferences. Chemical analyses showed that proportions of some compounds in precloacal secretions of males (used to produce scent marks) were correlated with the morphological (body size) and health state (immune response and body condition, but not CORT treatment) of these males. These results suggest that females may make site-selection decisions based on assessing the chemical characteristics of males’ scent marks, which were reliably related to some of the traits of the male that produced the scent. Therefore, females might use chemical senses to increase the opportunities to find and mate with males of high quality, coping with the restrictions of the subterranean environment.

Keywords

amphisbaenian / Blanus cinereus / chemical signals / glucocorticoids / health state / mate choice

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José MARTÍN, Gonzalo RODRÍGUEZ-RUIZ, Álvaro NAVARRO-CASTILLA, Isabel BARJA, Pilar LÓPEZ. Blind date: female fossorial amphisbaenians prefer scent marks of large and healthy males. Integrative Zoology, 2024, 19(6): 1018-1033 DOI:10.1111/1749-4877.12802

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References

[1]

AdamoSA (2004). How should behavioural ecologists interpret measurements of immunity? Animal Behaviour 68,1443–1449.

[2]

AebischerNJ,Robertson PA,KenwardRE (1993). Compositional analysis of habitat use from animal radio-tracking data. Ecology 74,1313–1325.

[3]

AlataloRV,Gustafsson L,LundbergA (1986). Do females prefer older males in polygynous bird species? American Naturalist 127,241–245.

[4]

AlbertsAC (1992). Pheromonal self-recognition in desert iguanas. Copeia 1992,229–232.

[5]

AndersonMJ (2001). A new method for non-parametric multivariate analysis of variance. Austral Ecology 26,32–46.

[6]

AndersonMJ,GorleyRN,ClarkeKR (2008). PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods. PRIMER-E Ltd.,Plymouth, UK.

[7]

AnderssonM,SimmonsLW (2006). Sexual selection and mate choice. Trends in Ecology and Evolution 21,296–302.

[8]

AnderssonMB (1994). Sexual Selection. Princeton University Press,Princeton, NJ.

[9]

AngelierF,Wingfield JC (2013). Importance of the glucocorticoid stress response in a changing world: Theory, hypotheses and perspectives. General and Comparative Endocrinology 190,118–128.

[10]

AragónP,MassotM, GaspariniJ,Clobert J (2006). Socially acquired information from chemical cues in the common lizard,Lacerta vivipara. Animal Behaviour 72,965–974.

[11]

BaeckensS,HuygheK, PalmeR,Van Damme R (2017). Chemical communication in the lacertid lizard Podarcis muralis: The functional significance of testosterone. Acta Zoologica 98,94–103.

[12]

Bairos-NovakKR,RyanCP, FreemanAR,Anderson WG,HareJF,LemaS (2018). Like mother, like daughter: Heritability of female Richardson’s ground squirrel Urocitellus richardsonii cortisol stress responses. Current Zoology 64,153–163.

[13]

BarjaI,Silván G,RoselliniS et al. (2007). Stress physiological responses to tourist pressure in a wild population of European pine marten. The Journal of Steroid Biochemistry and Molecular Biology 104,136–142.

[14]

BatesonP (1983). Mate Choice. Cambridge University Press,Cambridge, UK.

[15]

BelliureJ,ClobertJ (2004). Behavioral sensitivity to corticosterone in juveniles of the wall lizard,Podarcis muralis. Physiology & Behavior 81,121–127.

[16]

BonnetX,Naulleau G (1994). Utilisation d’un indice de condition corporelle (BCI) pour l’étude de la reproduction chez les serpents. Comptes Rendus de l’Académie des Sciences -Series III -Sciences de la Vie 317,34–41.

[17]

BortolottiGR,MougeotF, Martinez-PadillaJ,WebsterLMI,Piertney SB (2009). Physiological stress mediates the honesty of social signals. PLoS ONE 4,e4983.

[18]

BradburyJ,Vehrencamp S (2011). Principles of Animal Communication,2nd edn. Sinauer Associates,Sunderland, MA.

[19]

BrischouxF,RollandV, Bonnet X,CaillaudM,ShineR (2012). Effects of oceanic salinity on body condition in sea snakes. Integrative and Comparative Biology 52,235–244.

[20]

BrooksR,KempDJ (2001). Can older males deliver the good genes? Trends in Ecology and Evolution 16,308–313.

[21]

CainD,Cidlowski J (2017). Immune regulation by glucocorticoids. Nature Reviews Immunology 17,233–247.

[22]

ClarkeKR,GorleyRN (2006). PRIMER v6: User Manual/Tutorial. PRIMER-E Ltd.,Plymouth, UK.

[23]

ColeKS,SmithRJF (1992). Attraction of female fathead minnows,Pimephales promelas, to chemical stimuli from breeding males. Journal of Chemical Ecology 18,1269–1284.

[24]

CookeSJ,SackL, FranklinCE et al. (2013). What is conservation physiology? Perspectives on an increasingly integrated and essential science. Conservation Physiology 1,cot001.

[25]

CooperWE Jr (1995). Foraging mode, prey chemical discrimination, and phylogeny in lizards. Animal Behaviour 50,973–985.

[26]

CooperWE Jr,López P,SalvadorA (1994). Pheromone detection by an amphisbaenıán. Animal Behaviour 47,1401–1411.

[27]

CôtéIM,Hunte W (1993). Female redlip blennies prefer older males. Animal Behaviour 46,203–205.

[28]

CoteJ,ClobertJ, MeylanS,Fitze PS (2006). Experimental enhancement of corticosterone levels positively affects subsequent male survival. Hormones & Behavior 49,320–327.

[29]

DemasG,NelsonR (2012). Ecoimmunology. Oxford University Press,Oxford, UK.

[30]

EspmarkY,Amundsen T,RosenqvistG (2000). Animal Signals. Signalling and Signal Design in Animal Communication. Tapir Academic Press,Trondheim, Norway.

[31]

FolstadI,KarterAJ (1992). Parasites, bright males and the immunocompetence handicap. American Naturalist 139,603–622.

[32]

GansC (1978). The characteristics and affinities of the Amphisbaenia. Transactions of the Zoological Society of London 34,347–416.

[33]

García-RoaR,Saiz J,GómaraB,LópezP,Martín J (2018). How to tackle chemical communication? Relative proportions versus semiquantitative determination of compounds in lizard chemical secretions. Ecology and Evolution 8,2032–2040.

[34]

Gonzalez-JimenaV,Fitze PS (2012). Blood corticosterone levels and intersexual selection games: Best-of-bad-job strategies of male common lizards. Behavioral Ecology and Sociobiology 66,305–315.

[35]

GonzaloA,CabidoC, MartínJ,LópezP (2004). Detection and discrimination of conspecific scents by the anguid slow-worm Anguis fragilis. Journal of Chemical Ecology 30,1565–1573.

[36]

GreenAJ (2001). Mass/length residuals: Measures of body condition or generation of spurious results? Ecology 82,1473–1483.

[37]

GreeneMJ,StarkSL, MasonRT (2001). Pheromone trailing behavior of the brown tree snake,Boiga irregularis. Journal of Chemical Ecology 27,2193–2201.

[38]

HamiltonWD,ZukM (1982). Heritable true fitness and bright birds: A role for parasites? Science 218,384–387.

[39]

HillGE (2011). Condition-dependent traits as signals of the functionality of vital cellular processes. Ecology Letters 14,625–634.

[40]

HorváthG,Rodríguez-Ruiz G,MartínJ,LópezP,HerczegG (2019). Maternal diet affects juvenile Carpetan rock lizard performance and personality. Ecology and Evolution 9,14476–14488.

[41]

IbáñezA,Marzal A,LópezP,MartínJ (2013). Boldness and body size of male Spanish terrapins affect their responses to chemical cues of familiar and unfamiliar males. Behavioral Ecology and Sociobiology 67,541–548.

[42]

JaredC,Antoniazzi MM,SilvaJRMC,FreymüllerE (1999). Epidermal glands in Squamata: Microscopical examination of precloacal glands in Amphisbaena alba (Amphisbaenia, Amphisbaenidae). Journal of Morphology 241,197–206.

[43]

JohanssonBG,JonesTM (2007). The role of chemical communication in mate choice. Biological Reviews 82,265–289.

[44]

KokkoH,Lindstrom J (1996). Evolution of female preference for old mates. Proceedings of the Royal Society B: Biological Sciences 263,1533–1538.

[45]

LearyCJ,KnappR (2014). The stress of elaborate male traits: Integrating glucocorticoids with androgen-based models of sexual selection. Animal Behaviour 89,85–92.

[46]

LemaîtreJF,Gaillard JM (2017). Reproductive senescence: New perspectives in the wild. Biological Reviews 92,2182–2199.

[47]

LópezP (2015). Culebrilla ciega -Blanus cinereus. In: Salvador A,Marco A, eds. Enciclopedia Virtual de los Vertebrados Españoles. Museo Nacional de Ciencias Naturales,Madrid. http://www.vertebradosibericos.org.

[48]

LópezP,Martín J (1994). Responses by the amphisbaenian Blanus cinereus to chemicals from prey or potentially harmful ant species. Journal of Chemical Ecology 20,1113–1119.

[49]

LópezP,Martín J (2001). Chemosensory predator recognition induces specific defensive behaviours in a fossorial amphisbaenian. Animal Behaviour 62,259–264.

[50]

LópezP,Martín J (2005). Intersexual differences in chemical composition of precloacal gland secretions of the amphisbaenian Blanus cinereus. Journal of Chemical Ecology 31,2913–2921.

[51]

LópezP,Martín J (2009). Potential chemosignals associated with male identity in the amphisbaenian Blanus cinereus. Chemical Senses 34,479–486.

[52]

LópezP,Martín J,BarbosaA (2000). Site familiarity affects antipredator behavior of the amphisbaenian Blanus cinereus. Canadian Journal of Zoology 78,2142–2146.

[53]

LópezP,Martín J,CooperWE Jr (2002). Chemosensory responses to plant chemicals by the amphisbaenian Blanus cinereus. Amphibia-Reptilia 23,348–353.

[54]

LópezP,Martín J,CuadradM (2003). Chemosensory cues allow male lizards Psammodromus algirus to override visual concealment of sexual identity by satellite males. Behavioral Ecology and Sociobiology 54,218–224.

[55]

LópezP,OrtegaJ, MartínJ (2014). Chemosensory prey detection by the amphisbaenian Trogonophis wiegmanni. Journal of Herpetology 48,514–517.

[56]

LópezP,Salvador A (1992). The role of chemosensory cues in discrimination of prey odors by the amphisbaenian Blanus cinereus. Journal of Chemical Ecology 18,87–93.

[57]

LópezP,Salvador A,CooperWE Jr (1997). Discrimination of self from other males by chemosensory cues in the amphisbaenian (Blanus cinereus). Journal of Comparative Psychology 111,105–109.

[58]

LópezP,Salvador A,MartínJ (1998). Soil temperatures, rock selection and the thermal ecology of the amphisbaenian reptile Blanus cinereus. Canadian Journal of Zoology 76,673–679.

[59]

MacDougall-ShackletonA,Bonier F,RomeroLM,MooreIT (2019). Glucocorticoids and “stress” are not synonymous. Integrative and Comparative Biology 1, obz017.

[60]

MartínJ,BarjaI, Rodríguez-RuizG,RecioP,CuervoJJ (2023). Hidden but potentially stressed: A non-invasive technique to quantify fecal glucocorticoid levels in a fossorial amphisbaenian reptile. Animals 13,109.

[61]

MartínJ,BarjaI, Rodríguez-RuizG,RecioP,García LV (2021a). Soil pollution by heavy metals correlates with the levels of faecal glucocorticoid metabolites of a fossorial amphisbaenian reptile. Conservation Physiology 9,coab085.

[62]

MartínJ,Civantos E,AmoL,LópezP (2007a). Chemical ornaments of male lizards Psammodromus algirus may reveal their parasite load and health state to females. Behavioral Ecology and Sociobiology 62,173–179.

[63]

MartínJ,Ibáñez A,GarridoM,Raya-GarcíaE,López P (2021b). Chemical cues may allow a fossorial amphisbaenian reptile to avoid extremely saline soils when selecting microhabitats. Journal of Arid Environments 188,104452.

[64]

MartínJ,López P (2006). Links between male quality, male chemical signals, and female mate choice in Iberian rock lizards. Functional Ecology 20,1087–1096.

[65]

MartínJ,López P (2007). Scent may signal fighting ability in male Iberian rock lizards. Biology Letters 3,125–127.

[66]

MartínJ,López P (2011). Pheromones and reproduction in reptiles. In: Norris DO,Lopez KH, eds. Hormones and Reproduction of Vertebrates, Reptiles, vol. 3. Academic Press,Cambridge, MA, pp. 141–167.

[67]

MartínJ,López P (2015). Condition-dependent chemosignals in reproductive behavior of lizards. Hormones & Behavior 68,14–24.

[68]

MartínJ,López P,GabirotM,PilzKM (2007b). Effects of testosterone supplementation on chemical signals of male Iberian wall lizards: Consequences for female mate choice. Behavioral Ecology and Sociobiology 61,1275–1282.

[69]

MartínJ,López P,GutiérrezE,GarcíaLV (2015). Natural and anthropogenic alterations of the soil affect body condition of the fossorial amphisbaenian Trogonophis wiegamnni in North Africa. Journal of Arid Environments 122,30–36.

[70]

MartínJ,López P,SalvadorA (1991). Microhabitat selection of the amphisbaenian Blanus cinereus. Copeia 1991,1142–1146.

[71]

MartínJ,OrtegaJ, García-RoaR et al. (2021d). Going underground: Short-and long-term movements may reveal the fossorial spatial ecology of an amphisbaenian. Movement Ecology 9,14.

[72]

MartínJ,Raya-García E,OrtegaJ,LópezP (2020). How to maintain underground social relationships? Chemosensory sex, partner and self recognition in a fossorial amphisbaenian. PLoS ONE 15,e0237188.

[73]

MartínJ,Raya-García E,OrtegaJ,LópezP (2021c). Offspring and adult chemosensory recognition by an amphisbaenian reptile may allow maintaining familiar links in the fossorial environment. PeerJ 9,e10780.

[74]

MartinLB,HanP, LewittesJ,Kuhlman JR,KlasingKC,WikelskiM (2006). Phytohemagglutinin-induced skin swelling in birds: Histological support for a classic immunoecological technique. Functional Ecology 20,290–299.

[75]

MasonRT,ParkerMR (2010). Social behavior and pheromonal communication in reptiles. Journal of Comparative Physiology A 196,729–749.

[76]

McCormickGL,Langkilde T (2014). Immune responses of eastern fence lizards (Sceloporus undulatus) to repeated acute elevation of corticosterone. General and Comparative Endocrinology 204,135–140.

[77]

McCormickGL,SheaK, LangkildeT (2015). How do duration, frequency, and intensity of exogenous CORT elevation affect immune outcomes of stress? General and Comparative Endocrinology 222,81–87.

[78]

McGrawKJ,CorreaSM, Adkins-ReganE (2006). Testosterone upregulates lipoprotein status to control sexual attractiveness in a colorful songbird. Behavioral Ecology and Sociobiology 60,117–122.

[79]

MeylanS,Belliure J,ClobertJ,de FraipontM (2002). Stress and body condition as prenatal and postnatal determinants of dispersal in the common lizard (Lacerta vivipara). Hormones & Behavior 42,319–326.

[80]

Müller-SchwarzeD (2006). Chemical Ecology of Vertebrates. Cambridge University Press,Cambridge, UK.

[81]

Navarro-CastillaÁ,DíazM,BarjaI (2017). Does ungulate disturbance mediate behavioural and physiological stress responses in Algerian mice (Mus spretus)? A wild exclosure experiment. Hystrix, Italian Journal of Mammalogy 28,165–172.

[82]

NavasCA,Antoniazzi MM,CarvalhoJE et al. (2004). Morphological and physiological specialization for digging in amphisbaenians, an ancient lineage of fossorial vertebrates. Journal of Experimental Biology 207,2433–2441.

[83]

O’DonnellRP,Ford NB,ShineR,MasonRT (2004). Male red-sided garter snakes,Thamnophis sirtalis parietalis, determine female mating status from pheromone trails. Animal Behaviour 68,677–683.

[84]

RecioP,Rodríguez-Ruiz G,SannoloS,CuervoJJ,López P,MartínJ (2023). Conspecific scent-marks may influence underground site selection by a fossorial reptile. Behavioral Ecology and Sociobiology 77,29.

[85]

RobertKA,VleckC, BronikowskiAM (2009). The effects of maternal corticosterone levels on offspring behavior in fast-and slow-growth garter snakes (Thamnophis elegans). Hormones & Behavior 55,24–32.

[86]

RomeroLM (2004). Physiological stress in ecology: Lessons from biomedical research. Trends in Ecology and Evolution 19,249–255.

[87]

SalaberriaC,MurielJ, de LunaM,Gil D,PuertaM (2013). The PHA test as an indicator of phagocytic activity in a passerine bird. PLoS ONE 8,e84108.

[88]

SapolskyRM,RomeroLM, MunckAU (2000). How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews 21,55–89.

[89]

ScaliS,SacchiR, GozzoE et al. (2023). The size of a smell: Assessment of rival’s relative size from femoral secretions in the common wall lizards,Podarcis muralis (Laurenti, 1768). Behavioral Ecology 34,306–313.

[90]

SecondiJ,HaertyW, LodeT (2005). Female attraction to conspecific chemical cues in the palmate newt Triturus helveticus. Ethology 111,726–735.

[91]

SemhanRV,HalloyM, MonteroR (2010). Chemical prey discrimination of termites in Amphisbaena heterozonata (Reptilia: Squamata): A learned trait? Journal of Herpetology 44,489–492.

[92]

SheldonBC,Verhulst S (1996). Ecological immunology: Costly parasite defence and trade-offs in evolutionary ecology. Trends in Ecology and Evolution 11,317–321.

[93]

SmitsJE,Bortolotti GR,TellaJL (1999). Simplifying the phytohaemagglutinin skin-testing technique in studies of avian immunocompetence. Functional Ecology 13,567–572.

[94]

StoreyAE,RyanMG, FitzsimmonsMG et al. (2017). Balancing personal maintenance with parental investment in a chick-rearing seabird: Physiological indicators change with foraging conditions. Conservation Physiology 5,cox055.

[95]

TibbettM,FraserTD, DuddiganS (2020). Identifying potential threats to soil biodiversity. PeerJ 8,e9271.

[96]

ToumaC,SachserN, MöstlE,Palme R (2003). Effects of sex and time of day on metabolism and excretion of corticosterone in urine and feces of mice. General and Comparative Endocrinology 130,267–278.

[97]

TrompeterWP,Langkilde T (2011). Invader danger: Lizards faced with novel predators exhibit an altered behavioural response to stress. Hormones & Behavior 60,152–158.

[98]

WesterdahlH,AsgharM, HasselquistD,BenschS (2012). Quantitative disease resistance: To better understand parasite-mediated selection on major histocompatibility complex. Proceedings of the Royal Society B: Biological Sciences 279,577–584.

[99]

WikelskiM,CookeSJ (2006). Conservation physiology. Trends in Ecology and Evolution 21,38–46.

[100]

WilderSM,Raubenheimer D,SimpsonSJ (2016). Moving beyond body condition indices as an estimate of fitness in ecological and evolutionary studies. Functional Ecology 30,108–115.

[101]

WingfieldJC (2013). Ecological processes and the ecology of stress: The impacts of abiotic environmental factors. Functional Ecology 27,37–44.

[102]

WingfieldJC,RomeroLM (2001). Adrenocortical responses to stress and their modulation in free-living vertebrates. In: McEwen BS,Goodman HM, eds. Handbook of Physiology, Section 7: The Endocrine System, Vol. IV: Coping with the Environment: Neural and Endocrine Mechanisms. Oxford University Press,Oxford, UK, pp. 211–234.

[103]

WyattTD (2014). Pheromones and Animal Behaviour. Chemical Signals and Signatures. Cambridge University Press,Cambridge, UK.

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