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Another potential cost of tail autotomy: tail loss may result in high ectoparasite loads in Sceloporus lizards

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Tail autotomy is a common phenomenon in lizards that increases the chances of immediate survival during a predation event or agonistic encounter. However, despite short-term benefits, tail regeneration may also impose costs. Several studies have demonstrated that tail loss compromises other vital functions such as lipid storage, reproduction, and the immune system. Several lizard species are hosts of mites and ticks. Here we evaluated in three lizard species from the genus Sceloporus, whether individuals that have lost their tails and invested energy in tail regeneration are more susceptible to ectoparasites. Using a multimodel inference framework, we examined if tail loss and regeneration, as well as sex, body condition, and season (dry or rainy) predict ectoparasite load. Our results indicate that investing energy and resources in tail regeneration compromises defence against ectoparasites. These costs differed between sexes and among species. Overall, ectoparasite load increases during the rainy season and is on average higher in males. In S. grammicus, during the rainy season, males with regenerated tails and in poor body condition had more ectoparasites than males with intact tails in good body condition. In S. megalepidurus, we observed the same effect during the rainy season but in females rather than males. In S. torquatus, we found no effect of tail loss on ectoparasite load. We discuss the possibility that differences observed among species reflect differences in both species-specific physiological trade-offs and local environmental conditions.

Affiliations: 1: Departamento de Ecología y Recursos Naturales, Facultad de Ciencias, Universidad Nacional Autónoma de México, Ciudad de México 04510, México

*Corresponding author; e-mail: jzuniga@ciencias.unam.mx
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1. Akaike H. (1973): "Information theory and an extension of the maximum likelihood principle". In: 2nd International Symposium on Information Theory, p.  267-281. Petrov B.N., Czáki F., Eds. Akademiai Kiadó, Budapest.
2. Ardia D.R. (2005): "Super size me: an experimental test of the factors affecting lipid content and the ability of residual body mass to predict lipid stores in nestling European Starlings". Funct. Ecol. Vol 19: 414-420. [Crossref]
3. Arévalo E., Porter C.A., González A., Mendoza F., Camarillo J.L., Sites J.W. Jr (1991): "Population cytogenetics and evolution of the Sceloporus grammicus Complex (Iguanidae) in Central Mexico". Herpetol. Monogr. Vol 5: 79-115. [Crossref]
4. Arnold E.N. (1984): "Evolutionary aspects of tail shedding in lizards and their relatives". J. Nat. Hist. Vol 18: 127-169. [Crossref]
5. Bastiaans E., Morinaga G., Castañeda Gaytán J.G., Marshall J.C., Sinervo B. (2013): "Male aggression varies with throat color in 2 distinct populations of the mesquite lizard". Behav. Ecol. Vol 24: 968-981. [Crossref]
6. Bateman P.W., Fleming P.A. (2009): "To cut a long tail short: a review of lizard caudal autotomy studies carried out over the last 20 years". J. Zool. Vol 277: 1-14. [Crossref]
7. Belliure J., Smith L., Sorci G. (2004): "Effect of testosterone on T cell-mediated immunity in two species of Mediterranean lacertid lizards". J. Exp. Zool. Part A. Vol 301: 411-418. [Crossref]
8. Bonnet X., Naulleau G., Mauget R. (1994): "The influence of body condition on 17-beta estradiol levels in relation to vitellogenesis in female Vipera aspis (Reptilia, Viperidae)". Gen. Comp. Endocrinol. Vol 93: 424-437. [Crossref]
9. Brossard M., Wikel S.K. (1997): "Immunology of interactions between ticks and host". Med. Vet. Entomol. Vol 11: 270-276. [Crossref]
10. Burnham K.P., Anderson R.P. (2002): Model Selection and Multimodel Inference. A Practical Information–Theoretic Approach, 2nd Edition. Springer-Verlag, New York.
11. Burnham K.P., Anderson R.P. (2004): "Multimodel inference: understanding AIC and BIC in model selection". Sociol. Method. Res. Vol 33: 261-304. [Crossref]
12. Chapple D.G., Swain R. (2002): "Distribution of energy reserves in a viviparous skink: does tail autotomy involve the loss of lipid stores?" Austral Ecol. Vol 27: 565-572. [Crossref]
13. Clopton R.E., Gold R.E. (1993): "Distribution and seasonal and diurnal activity patterns of Eutrombicula alfreddugesi (Acari: Trombiculidae) in a forest edge ecosystem". J. Med. Entomol. Vol 30: 47-53. [Crossref]
14. Cox R.M., John-Alder H.B. (2007): "Increased mite parasitism as a cost of testosterone in male striped plateau lizards Sceloporus virgatus". Funct. Ecol. Vol 21: 327-334. [Crossref]
15. Cox R.M., Zilberman V., John-Alder H.B. (2008): "Testosterone stimulates the expression of a social color signal in Yarrow’s spiny lizard, Sceloporus jarrovii". J. Exp. Zool. Part A. Vol 309: 505-514.
16. Cox R.M., Skelly S.L., Leo A., John-Alder H.B. (2005): "Testosterone regulates sexually dimorphic coloration in the eastern fence lizard, Sceloporus undulatus". Copeia Vol 2005: 597-608. [Crossref]
17. Cromie G.L., Chapple D.G. (2012): "Impact of tail loss on the behaviour and locomotor performance of two sympatric lampropholis skink species". PLoS One Vol 7: e34732. [Crossref]
18. Doughty P., Shine R. (1998): "Reproductive energy allocation and long-term energy stores in a viviparous lizard (Eulamprus tympanum)". Ecology Vol 79: 1073-1083. [Crossref]
19. Doughty P., Shine R., Lee M.S.Y. (2003): "Energetic costs of tail loss in a montane scincid lizard". Comp. Biochem. Phys. Part A Vol 135: 215-219. [Crossref]
20. Dudek K., Skórka P., Sajkowska Z.A., Ekner-Grzyb A., Dudek M., Tryjanowski P. (2016): "Distribution pattern and number of ticks on lizards". Ticks and Tick-Borne Diseases Vol 7: 172-179. [Crossref]
21. Dunlap K.D., Mathies T. (1993): "Effects of nymphal ticks and their interaction with malaria on the physiology of male fence lizards". Copeia Vol 1993: 1045-1048. [Crossref]
22. Eisen L., Eisen R.J., Lane R.S. (2004): "The roles of birds, lizards, and rodents as hosts for the western black-legged tick Ixodes pacificus". J. Vector Ecol. Vol 29: 295-308.
23. Eisen R.J., Eisen L., Lane R.S. (2001): "Prevalence and abundance of Ixodes pacificus immatures (Acari: Ixodidae) infesting western fence lizards (Sceloporus occidentalis) in northern California: temporal trends and environmental correlates". J. Parasitol. Vol 87: 1301-1307. [Crossref]
24. Ekner A., Sajkowska Z., Dudek K., Tryjanowski P. (2011): "Medical cautery units as a permanent and non-invasive method of marking lizards". Acta Herpetologica Vol 6: 229-236.
25. Folstad I., Karter A.J. (1992): "Parasites, bright males, and the immunocompetence handicap". Am. Nat. Vol 139: 603-622. [Crossref]
26. Fox S.F., McCoy J.K. (2000): "The effects of tail loss on survival, growth, reproduction, and sex ratio of offspring in the lizard Uta stansburiana in the field". Oecologia Vol 122: 327-334. [Crossref]
27. Fox S.F., Heger N.A., Delay L.S. (1990): "Social cost of tail loss in Uta stansburiana: lizard tails as status-signalling badges". Anim. Behav. Vol 39: 549-554. [Crossref]
28. Fuxjager M.J., Foufopoulos J., Diaz-Uriarte R., Marler C.A. (2011): "Functionally opposing effects of testosterone on two different types of parasite: implications for the immunocompetence handicap hypothesis". Funct. Ecol. Vol 25: 132-138. [Crossref]
29. Gillis G.B., Bonvini L.A., Irschick D.J. (2009): "Losing stability: tail loss and jumping in the arboreal lizard Anolis carolinensis". J. Exp. Biol. Vol 212: 604-609. [Crossref]
30. Godínez-Cano E. (1985): Ciclo reproductivo de Sceloporus megalepidurus Smith (Reptilia: Sauria: Iguanidae), en la parte oriental de Tlaxcala, México. Bch. Thesis, ENEP Iztacala, Universidad Nacional Autónoma de México, México.
31. Goldberg S.R., Holshuh H.J. (1992): "Ectoparasite-induced lesions in mite pockets of the Yarrow’s spiny lizard, Sceloporus jarrovii (Phrynosomatidae)". J. Wildl. Dis. Vol 28: 537-541. [Crossref]
32. González-Ruíz G.A. (1991): Aspectos de la ecología poblacional de Sceloporus megalepidurus en el oriente de Tlaxcala, México. Bch. Thesis, ENEP Iztacala, Universidad Nacional Autónoma de México, México.
33. Hews D.K., Quinn V.S. (2003): "Endocrinology of species differences in sexually dimorphic signals and aggression: using the organization and activation model in a phylogenetic framework". In: Lizard Social Behavior, p.  253-277. Fox S.F., McCoy J.K., Baird T.A., Eds. Johns Hopkins University Press, Baltimore.
34. Hews D.K., Hara E., Anderson M.C. (2012): "Sex and species differences in plasma testosterone and in counts of androgen receptor-positive cells in key brain regions of Sceloporus lizard species that differ in aggression". Gen. Comp. Endocrinol. Vol 176: 493-499. [Crossref]
35. Hunsaker D. (1962): "Ethological isolating mechanisms in the Sceloporus torquatus group of lizards". Evolution Vol 16: 62-74. [Crossref]
36. Jackman S. (2015): Package “pscl”. http://pscl.stanford.edu/.
37. Jakob E.M., Marshall S.D., Uetz G.W. (1996): "Estimating fitness: a comparison of body condition indices". Oikos Vol 77: 61-67. [Crossref]
38. Jiménez-Cruz E., Ramírez-Bautista A., Marshall J.C., Lizana-Avia M., Nieto-Montes De Oca A. (2005): "Reproductive cycle of Sceloporus grammicus (Squamata: Phrynosomatidae) from Teotihuacán, México". Southwest. Nat. Vol 50: 178-187. [Crossref]
39. John-Alder H.B., Cox R.M., Haenel G.J., Smith L.C. (2009): "Hormones, performance and fitness: natural history and endocrine experiments on a lizard (Sceloporus undulatus)". Integr. Comp. Biol. Vol 49: 393-407. [Crossref]
40. Klasing K. (2004): "The costs of immunity". Acta Zoolog. Sin. Vol 50: 961-969.
41. Klein S.L. (2004): "Hormonal and immunological mechanisms mediating sex differences in parasite infection". Parasite. Immunol. Vol 26: 247-264. [Crossref]
42. Klukowski M. (2004): "Seasonal changes in abundance of host-seeking chiggers (Acari: Trombiculidae) and infestations on fence lizards, Sceloporus undulatus". J. Herpetol. Vol 38: 141-144. [Crossref]
43. Klukowski M., Nelson C.E. (2001): "Ectoparasite loads in free-ranging northern fence lizards, Sceloporus undulatus hyacinthinus: effects of testosterone and sex". Behav. Ecol. Sociobiol. Vol 49: 289-295. [Crossref]
44. Kuo C.C., Yao C.J., Lin T.E., Liu H.C., Hsu Y.C., Hsieh M.K., Huang W.S. (2013): "Tail loss compromises immunity in the many-lined skink, Eutropis multifasciata". Naturwissenschaften Vol 100: 379-384. [Crossref]
45. Lin J., Chen Y., Wang Y., Hung K., Lin S., Lin S. (2017): "Tail regeneration after autotomy revives survival: a case from a long-term monitored lizard population under avian predation". Proc. R. Soc. B. Vol 284: 20162538. [Crossref]
46. Lindsay W.R., Wapstra E., Silverin B., Olsson M. (2016): "Corticosterone: a costly mediator of signal honesty in sand lizards". Ecology and Evolution. Vol 6: 7451-7461. [Crossref]
47. Lucas L.D., French S.S. (2012): "Stress-induced tradeoffs in a free-living lizard across a variable landscape: consequences for individuals and populations". PLoS One. Vol 7: e49895.
48. Martín P.B., Bateson P. (1986): Measuring Behaviour: an Introductory Guide. Cambridge University.
49. Martín J., Salvador A. (1993): "Tail loss reduces mating success in the Iberian rock-lizard, Lacerta monticola". Behav. Ecol. Sociobiol. Vol 32: 185-189. [Crossref]
50. Martin L.B. (2009): "Stress and immunity in wild vertebrates: timing is everything". Gen. Comp. Endocrinol. Vol 163: 70-76. [Crossref]
51. Martínez-Méndez N., Méndez-de la Cruz F.R. (2007): "Molecular phylogeny of the Sceloporus torquatus species-group (Squamata: Phrynosomatidae)". Zootaxa Vol 1609: 53-68.
52. McElroy E.J., Bergmann P.J. (2013): "Tail autotomy, tail size, and locomotor performance in lizards". Physiol. Biochem. Zool. Vol 86: 669-679. [Crossref]
53. Moore M.C. (1986): "Elevated testosterone levels during nonbreeding-season territoriality in a fall-breeding lizard, Sceloporus jarrovi". J. Comp. Physiol. A. Vol 158: 159-163. [Crossref]
54. Olsson M., Wapstra E., Madsen T., Silverin B. (2000): "Testosterone, ticks and travels: a test of the immunocompetence-handicap hypothesis in free-ranging male sand lizards". Proc. Biol. Sci. Vol 267: 2339-2343. [Crossref]
55. Oppliger A., Giorgi M.S., Conelli A., Nembrini M., John-Alder H.B. (2004): "Effect of testosterone on immunocompetence, parasite load, and metabolism in the common wall lizard (Podarcis muralis)". Can. J. Zool. Vol 82: 1713-1719. [Crossref]
56. Pinheiro J., Bates D., DebRoy S., Sarkar D., R Core Team (2016): Package “nlme”. http://CRAN.R-project.org/package=nlme>.
57. Pollock N.B., Vredevoe L.K., Taylor E.N. (2012): "The effect of exogenous testosterone on ectoparasite loads in free-ranging western fence lizards". J. Exp. Zool. PART A. Vol 317: 447-454.
58. R Core Team (2016): R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.
59. Ritzman T.B., Stroik L.K., Julik E., Hutchins E.D., Lasku E., Denardo D.F., Wilson-Rawls J., Rawls J.A., Kusumi K., Fisher R.E. (2012): "The gross anatomy of the original and regenerated tail in the green anole (Anolis carolinensis)". Anat Rec. Vol 295: 1596-1608. [Crossref]
60. Salvador A., Martín J., López P. (1995): "Tail loss reduces home range size and access to females in male lizards, Psammodromus algirus". Behav. Ecol. Vol 6: 382-387. [Crossref]
61. Salvador A., Veiga J.P., Martín J., López P. (1997): "Testosterone supplementation in subordinate, small male lizards: consequences for aggressiveness, color development, and parasite load". Behav. Ecol. Vol 8: 135-139. [Crossref]
62. Salvador A., Veiga J.P., Martín J., López P., Abelenda M., Puerta M. (1996): "The cost of producing a sexual signal: testosterone increases the susceptibility of male lizards to ectoparasitic infestation". Behav. Ecol. Vol 7: 145-150. [Crossref]
63. Schall J.J., Smith T.C. (2006): "Detection of a malaria parasite (Plasmodium mexicanum) in ectoparasites (mites and ticks), and possible significance for transmission". J. Parasitol. Vol 92: 413-415. [Crossref]
64. Sites J.W. Jr. (1982): "Morphological variation within and among three chromosome races of Sceloporus grammicus (Sauria: Iguanidae) in the north-central part of its range". Copeia Vol 1982: 920-941. [Crossref]
65. Venables W.N., Ripley B.D. (2002): Package “MASS”. http://www.stats.ox.ac.uk/pub/MASS4.
66. Wikelski M., Steiger S.S., Gall B., Nelson K.N. (2005): "Sex, drugs, and mating role: testosterone-induced phenotype-switching in Galapagos marine iguanas". Behav. Ecol. Vol 16: 260-268. [Crossref]
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2018-04-24
2018-08-14

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