Seasonal and reproductive variation in chemical constituents of scent signals in wild giant pandas
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摘要
Seasonally reproducing animals show many behavioral and physiological changes during the mating period, including increased signaling for intrasexual competition and mate attraction. We collected 102 anogenital gland secretions(AGS) from marking trees in Foping Nature Reserve, and used gas chromatography mass spectrometry to analyze these chemical composition. Of these marks, all but one were from males, confirmed with DNA analysis. We found that several chemical constituents, especially volatile compounds, were present only during the mating season and that the relative abundance of many compounds changed as a function of breeding season, whereas nonvolatile compounds were lower in the mating season. This seasonal variation in chemical composition of AGS most likely plays an important role in governing giant panda reproduction, including mate location, attraction, and male-male competition. The chemical properties of many of these putative chemosignals—such as volatility and longevity—are suggestive of these roles, and undoubtedly contribute to successful reproduction for this species with a characteristically sophisticated chemical communication system. We also found a number of important differences between the chemical constituents of AGS from wild pandas and those found in previous studies with captive pandas, suggesting that inappropriate chemosignal composition may contribute to poor reproductive success in captive breeding programs.
Seasonally reproducing animals show many behavioral and physiological changes during the mating period, including increased signaling for intrasexual competition and mate attraction. We collected 102 anogenital gland secretions(AGS) from marking trees in Foping Nature Reserve, and used gas chromatography mass spectrometry to analyze these chemical composition. Of these marks, all but one were from males, confirmed with DNA analysis. We found that several chemical constituents, especially volatile compounds, were present only during the mating season and that the relative abundance of many compounds changed as a function of breeding season, whereas nonvolatile compounds were lower in the mating season. This seasonal variation in chemical composition of AGS most likely plays an important role in governing giant panda reproduction, including mate location, attraction, and male-male competition. The chemical properties of many of these putative chemosignals—such as volatility and longevity—are suggestive of these roles, and undoubtedly contribute to successful reproduction for this species with a characteristically sophisticated chemical communication system. We also found a number of important differences between the chemical constituents of AGS from wild pandas and those found in previous studies with captive pandas, suggesting that inappropriate chemosignal composition may contribute to poor reproductive success in captive breeding programs.
Seasonally reproducing animals show many behavioral and physiological changes during the mating period, including increased signaling for intrasexual competition and mate attraction. We collected 102 anogenital gland secretions(AGS) from marking trees in Foping Nature Reserve, and used gas chromatography mass spectrometry to analyze these chemical composition. Of these marks, all but one were from males, confirmed with DNA analysis. We found that several chemical constituents, especially volatile compounds, were present only during the mating season and that the relative abundance of many compounds changed as a function of breeding season, whereas nonvolatile compounds were lower in the mating season. This seasonal variation in chemical composition of AGS most likely plays an important role in governing giant panda reproduction, including mate location, attraction, and male-male competition. The chemical properties of many of these putative chemosignals—such as volatility and longevity—are suggestive of these roles, and undoubtedly contribute to successful reproduction for this species with a characteristically sophisticated chemical communication system. We also found a number of important differences between the chemical constituents of AGS from wild pandas and those found in previous studies with captive pandas, suggesting that inappropriate chemosignal composition may contribute to poor reproductive success in captive breeding programs.
引文
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Alberts,A.C.(1992).Constraints on the design of chemical communication systems in terrestrial vertebrates.Am Nat 139,S62-S89.
Breiman,L.(2001).Random forests.Mach Learn 45,5-32.
Brennan,P.A.,and Keverne,E.B.(2004).Something in the air?New insights into mammalian pheromones.Curr Biol 14,R81-R89.
Brennan,P.A.,and Kendrick,K.M.(2006).Mammalian social odours:attraction and individual recognition.Philos Trans R Soc B 361,2061-2078.
Brown,R.E.,Macdonald,D.W.(1985).Social Odours in Mammals.(Oxford:Clarendon Press).
Burgener,N.,Dehnhard,M.,Hofer,H.,and East,M.L.(2009).Does anal gland scent signal identity in the spotted hyaena?Anim Behav 77,707-715.
Burger,B.V.(2005).Mammalian semiochemicals:the chemistry of pheromones and other semiochemicals II.(Berlin:Springer Berlin Heidelberg),pp.231-278.
Dorries,K.M.,Adkins-Regan,E.,and Halpern,B.P.(1997).Sensitivity and behavioral responses to the pheromone androstenone are not mediated by the vomeronasal organ in domestic pigs.Brain Behav Evol 49,53-62.
Escobar,C.A.,Labra,A.,and Niemeyer,H.M.(2001).Chemical composition of precloacal secretions of Liolaemus lizards.J Chem Ecol 27,1677-1690.
Escobar,C.M.,Escobar,C.A.,Labra,A.,and Niemeyer,H.M.(2003).Chemical composition of precloacal secretions of two Liolaemus fabiani populations:are they different?J Chem Ecol 29,629-638.
Ezenwa,V.O.,and Williams,A.E.(2014).Microbes and animal olfactory communication:where do we go from here?Bioessays 36,847-854.
Ferrero,D.M.,and Liberles,S.D.(2010).The secret codes of mammalian scents.WIREs Syst Biol Med 2,23-33.
Gilfillan,G.D.,Vitale,J.D.T.,McNutt,J.W.,and McComb,K.(2017).Spontaneous discrimination of urine odours in wild African lions,Panthera leo.Anim Behav 126,177-185.
Greene,L.K.,Grogan,K.E.,Smyth,K.N.,Adams,C.A.,Klager,S.A.,and Drea,C.M.(2016).Mix it and fix it:functions of composite olfactory signals in ring-tailed lemurs.R Soc Open Sci 3,160076.
Hagey,L.,and MacDonald,E.(2003).Chemical cues identify gender and individuality in giant pandas(Ailuropoda melanoleuca).J Chem Ecol29,1479-1488.
Harris,R.L.,Davies,N.W.,and Nicol,S.C.(2012).Chemical composition of odorous secretions in the Tasmanian short-beaked echidna(Tachyglossus aculeatus setosus).Chem Senses 37,819-836.
Harris,R.L.,Holland,B.R.,Cameron,E.Z.,Davies,N.W.,and Nicol,S.C.(2014).Chemical signals in the echidna:differences between seasons,sexes,individuals and gland types.J Zool 293,171-180.
Hu,Y.,Zhan,X.,Qi,D.,and Wei,F.(2010).Spatial genetic structure and dispersal of giant pandas on a mountain-range scale.Conserv Genet 11,2145-2155.
Hurst,J.L.(2005).Scent marking and social communication.Animal communication networks.(Cambridge:Cambridge University Press),pp.219-243.
Jemiolo,B.,Alberts,J.,Sochinski-Wiggins,S.,Harvey,S.,and Novotny,M.(1985).Behavioural and endocrine responses of female mice to synthetic analogues of volatile compounds in male urine.Anim Behav33,1114-1118.
Jemiolo,B.,Xie,T.M.,and Novotny,M.(1991).Socio-sexual olfactory preference in female mice:attractiveness of synthetic chemosignals.Physiol Behav 50,1119-1122.
Johansson,B.G.,and Jones,T.M.(2007).The role of chemical communication in mate choice.Biol Rev 82,265-289.
Jordan,N.R.,Mwanguhya,F.,Kyabulima,S.,Rüedi,P.,and Cant,M.A.(2010).Scent marking within and between groups of wild banded mongooses.J Zool 280,72-83.
Khannoon,E.R.,El-Gendy,A.,and Hardege,J.D.(2011).Scent marking pheromones in lizards:cholesterol and long chain alcohols elicit avoidance and aggression in male Acanthodactylus boskianus(Squamata:Lacertidae).Chemoecology 21,143-149.
Khazanehdari,C.,Buglass,A.J.,and Waterhouse,J.S.(1996).Anal gland secretion of European mole:volatile constituents and significance in territorial maintenance.J Chem Ecol 22,383-392.
Liaw,A.,Wiener,M.(2002).Classification and regression by randomforest.R News 2,18-22.
Liu,D.,Yuan,H.,Tian,H.,Wei,R.,Zhang,G.,Sun,L.,Wang,L.,and Sun,R.(2006).Do anogenital gland secretions of giant panda code for their sexual ability?Chin Sci Bull 51,1986-1995.
Lizé,A.,McKay,R.,Lewis,Z.(2013).Gut microbiota and kin recognition.Trends Ecol Evol 28,325-326.
Lu,Z.,Johnson,W.E.,Menotti-Raymond,M.,Yuhki,N.,Martenson,J.S.,Mainka,S.,Shi-Qiang,H.,Zhihe,Z.,Li,G.,Pan,W.,et al.(2001).Patterns of genetic diversity in remaining giant panda populations.Conserv Biol 15,1596-1607.
Martín,J.,and López,P.(2006a).Links between male quality,male chemical signals,and female mate choice in Iberian rock lizards.Funct Ecol 20,1087-1096.
Martín,J.,and López,P.(2006b).Vitamin D supplementation increases the attractiveness of males'scent for female Iberian rock lizards.Proc R Soc B-Biol Sci 273,2619-2624.
Martín,J.,Barja,I.,and López,P.(2010).Chemical scent constituents in feces of wild Iberian wolves(Canis lupus signatus).Biochem Systatics Ecol 38,1096-1102.
Martin-Wintle,M.S.,Shepherdson,D.,Zhang,G.,Huang,Y.,Luo,B.,and Swaisgood,R.R.(2017).Do opposites attract?Effects of personality matching in breeding pairs of captive giant pandas on reproductive success.Biol Conserv 207,27-37.
Martin-Wintle,M.S.,Shepherdson,D.,Zhang,G.,Zhang,H.,Li,D.,Zhou,X.,Li,R.,and Swaisgood,R.R.(2015).Free mate choice enhances conservation breeding in the endangered giant panda.Nat Commun 6,10125.
Müller-Schwarze,D.(2006).Chemical ecology of vertebrates.(Cambridge:Cambridge University Press).
Nie,Y.,Swaisgood,R.R.,Zhang,Z.,Hu,Y.,Ma,Y.,and Wei,F.(2012).Giant panda scent-marking strategies in the wild:role of season,sex and marking surface.Anim Behav 84,39-44.
Nielsen,B.L.,Jer?me,N.,Saint-Albin,A.,Thonat,C.,Briant,C.,Boué,F.,Rampin,O.,and Maurin,Y.(2011).A mixture of odorant molecules potentially indicating oestrus in mammals elicits penile erections in male rats.Behav Brain Res 225,584-589.
Pan,W.S.,Lu,Z.,Zhu,X.,Wang,D.J.,Wang,H.,Long,Y.,Fu,D.L.,Zhou,X.(2001).A chance for lasting survival.(Beijing:Beijing University).
Pause,B.(2004).Are androgen steroids acting as pheromones in humans?Physiol Behav 83,21-29.
Rasmussen,L.E.L.,Lee,T.D.,Zhang,A.,Roelofs,W.L.,and Daves Jr,G.D.(1997).Purification,identification,concentration and bioactivity of(Z)-7-dodecen-1-yl acetate:sex pheromone of the female asian elephant.Elephas maximus.Chem Senses 22,417-437.
Rosell,F.,Jojola,S.M.,Ingdal,K.,Lassen,B.A.,Swenson,J.E.,Arnemo,J.M.,and Zedrosser,A.(2011).Brown bears possess anal sacs and secretions may code for sex.J Zool 283,143-152.
Royer,L.,and McNeil,J.N.(1993).Effect of relative humidity conditions on responsiveness of European corn borer(Ostrinia nubilalis)males to female sex pheromone in a wind tunnel.J Chem Ecol 19,61-69.
Schaller,G.B.,Hu,J.C.,Pan,W.S.Zhu,J.(1985).The Giant Pandas of Wolong.(Chicago:The University of Chicago Press).
Scordato,E.S.,Dubay,G.,and Drea,C.M.(2007).Chemical composition of scent marks in the ringtailed lemur(Lemur catta):glandular differences,seasonal variation,and individual signatures.Chem Senses 32,493-504.
Shen,F.J.,Watts,P.,Zhang,Z.H.,Zhang,A.J.,Sanderson,S.,Kemp,S.J.,Yue,B.S.(2005).Enrichment of giant panda microsatellite markers using dynal magnet beads.Acta Genet Sinica 32,457-462.
Stoffel,M.A.,Caspers,B.A.,Forcada,J.,Giannakara,A.,Baier,M.,Eberhart-Phillips,L.,Müller,C.,and Hoffman,J.I.(2015).Chemical fingerprints encode mother-offspring similarity,colony membership,relatedness,and genetic quality in fur seals.Proc Natl Acad Sci USA112,E5005-E5012.
Strobl,C.,Boulesteix,A.L.,Zeileis,A.,and Hothorn,T.(2007).Bias in random forest variable importance measures:Illustrations,sources and a solution..BMC BioInf 8,25.
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Swaisgood,R.R.,Lindburg,D.G.,Zhou,X.,and Owen,M.A.(2000).The effects of sex,reproductive condition and context on discrimination of conspecific odours by giant pandas.Anim Behav 60,227-237.
Swaisgood,R.R.,Lindburg,D.G.,and Zhang,H.(2002).Discrimination of oestrous status in giant pandas(Ailuropoda melanoleuca)via chemical cues in urine.J Zool 257,381-386.
Swaisgood,R.R.,Lindburg,D.G.,White,A.M.,Zhang,H.M.,Zhou,X.P.(2004).Chemical communication in giant pandas:experimentation and application.In Lindburg,D.&Baragona,K.,eds,Giant pandas:Biology and Conservation.(California:University of California Press),pp.106-120.
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Tobey,J.R.,Nute,T.R.,and Bercovitch,F.B.(2009).Age and seasonal changes in the semiochemicals of the sternal gland secretions of male koalas(Phascolarctos cinereus).Aust J Zool 57,111-118.
Trabalon,M.,and Assi-Bessekon,D.(2008).Effects of web chemical signatures on intraspecific recognition in a subsocial spider,Coelotes terrestris(Araneae).Anim Behav 76,1571-1578.
Wang,Y.J.,and Liu,L.(2012).Recent progress of sensory system research in China.Sci China Life Sci 55,1026-1028.
Wei,F.,Swaisgood,R.,Hu,Y.,Nie,Y.,Yan,L.,Zhang,Z.,Qi,D.,and Zhu,L.(2015).Progress in the ecology and conservation of giant pandas.Conserv Biol 29,1497-1507.
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Alberts,A.C.(1992).Constraints on the design of chemical communication systems in terrestrial vertebrates.Am Nat 139,S62-S89.
Breiman,L.(2001).Random forests.Mach Learn 45,5-32.
Brennan,P.A.,and Keverne,E.B.(2004).Something in the air?New insights into mammalian pheromones.Curr Biol 14,R81-R89.
Brennan,P.A.,and Kendrick,K.M.(2006).Mammalian social odours:attraction and individual recognition.Philos Trans R Soc B 361,2061-2078.
Brown,R.E.,Macdonald,D.W.(1985).Social Odours in Mammals.(Oxford:Clarendon Press).
Burgener,N.,Dehnhard,M.,Hofer,H.,and East,M.L.(2009).Does anal gland scent signal identity in the spotted hyaena?Anim Behav 77,707-715.
Burger,B.V.(2005).Mammalian semiochemicals:the chemistry of pheromones and other semiochemicals II.(Berlin:Springer Berlin Heidelberg),pp.231-278.
Dorries,K.M.,Adkins-Regan,E.,and Halpern,B.P.(1997).Sensitivity and behavioral responses to the pheromone androstenone are not mediated by the vomeronasal organ in domestic pigs.Brain Behav Evol 49,53-62.
Escobar,C.A.,Labra,A.,and Niemeyer,H.M.(2001).Chemical composition of precloacal secretions of Liolaemus lizards.J Chem Ecol 27,1677-1690.
Escobar,C.M.,Escobar,C.A.,Labra,A.,and Niemeyer,H.M.(2003).Chemical composition of precloacal secretions of two Liolaemus fabiani populations:are they different?J Chem Ecol 29,629-638.
Ezenwa,V.O.,and Williams,A.E.(2014).Microbes and animal olfactory communication:where do we go from here?Bioessays 36,847-854.
Ferrero,D.M.,and Liberles,S.D.(2010).The secret codes of mammalian scents.WIREs Syst Biol Med 2,23-33.
Gilfillan,G.D.,Vitale,J.D.T.,McNutt,J.W.,and McComb,K.(2017).Spontaneous discrimination of urine odours in wild African lions,Panthera leo.Anim Behav 126,177-185.
Greene,L.K.,Grogan,K.E.,Smyth,K.N.,Adams,C.A.,Klager,S.A.,and Drea,C.M.(2016).Mix it and fix it:functions of composite olfactory signals in ring-tailed lemurs.R Soc Open Sci 3,160076.
Hagey,L.,and MacDonald,E.(2003).Chemical cues identify gender and individuality in giant pandas(Ailuropoda melanoleuca).J Chem Ecol29,1479-1488.
Harris,R.L.,Davies,N.W.,and Nicol,S.C.(2012).Chemical composition of odorous secretions in the Tasmanian short-beaked echidna(Tachyglossus aculeatus setosus).Chem Senses 37,819-836.
Harris,R.L.,Holland,B.R.,Cameron,E.Z.,Davies,N.W.,and Nicol,S.C.(2014).Chemical signals in the echidna:differences between seasons,sexes,individuals and gland types.J Zool 293,171-180.
Hu,Y.,Zhan,X.,Qi,D.,and Wei,F.(2010).Spatial genetic structure and dispersal of giant pandas on a mountain-range scale.Conserv Genet 11,2145-2155.
Hurst,J.L.(2005).Scent marking and social communication.Animal communication networks.(Cambridge:Cambridge University Press),pp.219-243.
Jemiolo,B.,Alberts,J.,Sochinski-Wiggins,S.,Harvey,S.,and Novotny,M.(1985).Behavioural and endocrine responses of female mice to synthetic analogues of volatile compounds in male urine.Anim Behav33,1114-1118.
Jemiolo,B.,Xie,T.M.,and Novotny,M.(1991).Socio-sexual olfactory preference in female mice:attractiveness of synthetic chemosignals.Physiol Behav 50,1119-1122.
Johansson,B.G.,and Jones,T.M.(2007).The role of chemical communication in mate choice.Biol Rev 82,265-289.
Jordan,N.R.,Mwanguhya,F.,Kyabulima,S.,Rüedi,P.,and Cant,M.A.(2010).Scent marking within and between groups of wild banded mongooses.J Zool 280,72-83.
Khannoon,E.R.,El-Gendy,A.,and Hardege,J.D.(2011).Scent marking pheromones in lizards:cholesterol and long chain alcohols elicit avoidance and aggression in male Acanthodactylus boskianus(Squamata:Lacertidae).Chemoecology 21,143-149.
Khazanehdari,C.,Buglass,A.J.,and Waterhouse,J.S.(1996).Anal gland secretion of European mole:volatile constituents and significance in territorial maintenance.J Chem Ecol 22,383-392.
Liaw,A.,Wiener,M.(2002).Classification and regression by randomforest.R News 2,18-22.
Liu,D.,Yuan,H.,Tian,H.,Wei,R.,Zhang,G.,Sun,L.,Wang,L.,and Sun,R.(2006).Do anogenital gland secretions of giant panda code for their sexual ability?Chin Sci Bull 51,1986-1995.
Lizé,A.,McKay,R.,Lewis,Z.(2013).Gut microbiota and kin recognition.Trends Ecol Evol 28,325-326.
Lu,Z.,Johnson,W.E.,Menotti-Raymond,M.,Yuhki,N.,Martenson,J.S.,Mainka,S.,Shi-Qiang,H.,Zhihe,Z.,Li,G.,Pan,W.,et al.(2001).Patterns of genetic diversity in remaining giant panda populations.Conserv Biol 15,1596-1607.
Martín,J.,and López,P.(2006a).Links between male quality,male chemical signals,and female mate choice in Iberian rock lizards.Funct Ecol 20,1087-1096.
Martín,J.,and López,P.(2006b).Vitamin D supplementation increases the attractiveness of males'scent for female Iberian rock lizards.Proc R Soc B-Biol Sci 273,2619-2624.
Martín,J.,Barja,I.,and López,P.(2010).Chemical scent constituents in feces of wild Iberian wolves(Canis lupus signatus).Biochem Systatics Ecol 38,1096-1102.
Martin-Wintle,M.S.,Shepherdson,D.,Zhang,G.,Huang,Y.,Luo,B.,and Swaisgood,R.R.(2017).Do opposites attract?Effects of personality matching in breeding pairs of captive giant pandas on reproductive success.Biol Conserv 207,27-37.
Martin-Wintle,M.S.,Shepherdson,D.,Zhang,G.,Zhang,H.,Li,D.,Zhou,X.,Li,R.,and Swaisgood,R.R.(2015).Free mate choice enhances conservation breeding in the endangered giant panda.Nat Commun 6,10125.
Müller-Schwarze,D.(2006).Chemical ecology of vertebrates.(Cambridge:Cambridge University Press).
Nie,Y.,Swaisgood,R.R.,Zhang,Z.,Hu,Y.,Ma,Y.,and Wei,F.(2012).Giant panda scent-marking strategies in the wild:role of season,sex and marking surface.Anim Behav 84,39-44.
Nielsen,B.L.,Jer?me,N.,Saint-Albin,A.,Thonat,C.,Briant,C.,Boué,F.,Rampin,O.,and Maurin,Y.(2011).A mixture of odorant molecules potentially indicating oestrus in mammals elicits penile erections in male rats.Behav Brain Res 225,584-589.
Pan,W.S.,Lu,Z.,Zhu,X.,Wang,D.J.,Wang,H.,Long,Y.,Fu,D.L.,Zhou,X.(2001).A chance for lasting survival.(Beijing:Beijing University).
Pause,B.(2004).Are androgen steroids acting as pheromones in humans?Physiol Behav 83,21-29.
Rasmussen,L.E.L.,Lee,T.D.,Zhang,A.,Roelofs,W.L.,and Daves Jr,G.D.(1997).Purification,identification,concentration and bioactivity of(Z)-7-dodecen-1-yl acetate:sex pheromone of the female asian elephant.Elephas maximus.Chem Senses 22,417-437.
Rosell,F.,Jojola,S.M.,Ingdal,K.,Lassen,B.A.,Swenson,J.E.,Arnemo,J.M.,and Zedrosser,A.(2011).Brown bears possess anal sacs and secretions may code for sex.J Zool 283,143-152.
Royer,L.,and McNeil,J.N.(1993).Effect of relative humidity conditions on responsiveness of European corn borer(Ostrinia nubilalis)males to female sex pheromone in a wind tunnel.J Chem Ecol 19,61-69.
Schaller,G.B.,Hu,J.C.,Pan,W.S.Zhu,J.(1985).The Giant Pandas of Wolong.(Chicago:The University of Chicago Press).
Scordato,E.S.,Dubay,G.,and Drea,C.M.(2007).Chemical composition of scent marks in the ringtailed lemur(Lemur catta):glandular differences,seasonal variation,and individual signatures.Chem Senses 32,493-504.
Shen,F.J.,Watts,P.,Zhang,Z.H.,Zhang,A.J.,Sanderson,S.,Kemp,S.J.,Yue,B.S.(2005).Enrichment of giant panda microsatellite markers using dynal magnet beads.Acta Genet Sinica 32,457-462.
Stoffel,M.A.,Caspers,B.A.,Forcada,J.,Giannakara,A.,Baier,M.,Eberhart-Phillips,L.,Müller,C.,and Hoffman,J.I.(2015).Chemical fingerprints encode mother-offspring similarity,colony membership,relatedness,and genetic quality in fur seals.Proc Natl Acad Sci USA112,E5005-E5012.
Strobl,C.,Boulesteix,A.L.,Zeileis,A.,and Hothorn,T.(2007).Bias in random forest variable importance measures:Illustrations,sources and a solution..BMC BioInf 8,25.
Swaisgood,R.R.,Lindburg,D.G.,and Zhou,X.(1999).Giant pandas discriminate individual differences in conspecific scent.Anim Behav57,1045-1053.
Swaisgood,R.R.,Lindburg,D.G.,Zhou,X.,and Owen,M.A.(2000).The effects of sex,reproductive condition and context on discrimination of conspecific odours by giant pandas.Anim Behav 60,227-237.
Swaisgood,R.R.,Lindburg,D.G.,and Zhang,H.(2002).Discrimination of oestrous status in giant pandas(Ailuropoda melanoleuca)via chemical cues in urine.J Zool 257,381-386.
Swaisgood,R.R.,Lindburg,D.G.,White,A.M.,Zhang,H.M.,Zhou,X.P.(2004).Chemical communication in giant pandas:experimentation and application.In Lindburg,D.&Baragona,K.,eds,Giant pandas:Biology and Conservation.(California:University of California Press),pp.106-120.
Symonds,M.R.E.,and Elgar,M.A.(2008).The evolution of pheromone diversity.Trends Ecol Evol 23,220-228.
Tobey,J.R.,Nute,T.R.,and Bercovitch,F.B.(2009).Age and seasonal changes in the semiochemicals of the sternal gland secretions of male koalas(Phascolarctos cinereus).Aust J Zool 57,111-118.
Trabalon,M.,and Assi-Bessekon,D.(2008).Effects of web chemical signatures on intraspecific recognition in a subsocial spider,Coelotes terrestris(Araneae).Anim Behav 76,1571-1578.
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