IS THERE A RELATION BETWEEN PARASITISM AND TAIL AUTOTOMY IN LIZARDS? CASE STUDY IN LIOLAEMUS DARWINII (IGUANIA: LIOLAEMIDAE)
DOI:
https://doi.org/10.24039/rnh20221621500Keywords:
Argentina, behavior, Liolaemus darwinii, parasitism, tail loss, San JuanAbstract
Tail autotomy acts as anti-predatory mechanism in a great diversity of lizard species. Research links tail loss with various aspects of lizard life history. However, parasitic aspects are not taken into consideration, despite being a variable that greatly influences reptile ecology. For the first time, it is proposed that the existence of a relationship between the caudal autotomy of a lizard species is related to its parasitic condition. We studied 30 adult specimens of Liolaemus darwinii Bell, 1843 in the desert of Monte, San Juan province, Argentina. Autotomy was used as a direct measure of predator-prey interaction. A series of variables were analyzed that could be related to tail autotomy. The following variables were studied using generalized linear models: sex, environments (disturbed vs. conserved), condition (parasitized vs. not parasitized), parasitic intensity, weights (g) and snout-vent length (Lhc). The dependent variable (presence of tail: 1, absence of tail: 0) was adjusted to a binomial distribution, whose link function is logit (logistic regression). Only the variable parasitized vs. non-parasitized condition was significantly associated with tail autotomy. Parasitized individuals all have cut tails or in some stage of regeneration. Individuals that were not parasitized had complete tails (intact). The results establish for the first time a relationship between parasitism and tail loss in L. darwinii. The results are discussed in a behavioral ecological context and physiological resource allocation. In addition, our work is an approach to understanding the role of parasites in the ecology of L. darwinii in the Monte desert in Argentina.
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Abdala, CS, Acosta, JL, Acosta, JC, Blanca, BA, Arias, F, Avila, LJ, Blanco, MG, Bonino, M, Boretto, JM, Brancatelli, G, Breitman, MF, Cabrera, MR, Cairo, S, Corbalan, V, Hernando, A, Ibarguengoytia, NR, Kacoliris, F, Laspiur, A, Montero, R, Morando, M, Pelegrin, N, Perez, CHF, Quinteros, AS, Semhan, RV, Tedesco, ME, Vega, L & Zalba, SM. 2012. Categorización del estado de conservación de las lagartijas y anfisbenas de la República Argentina. Cuadernos de herpetología, vol. 26, pp. 215–248.
Acosta, JC, Blanco, GM, Gómez-Alés, R, Acosta, R, Piaggio-Kokot, L, Victorica, AE, Villavicencio, HJ & Fava, GA. 2017. Los reptiles de San Juan. Editorial Brujas.
Anderson, RC, Chabaud, AG & Willmott, S. 2009. Keys to the nematode parasites of vertebrates. CAB International.
Arnold, EN. 1984. Evolutionary aspects of tail shedding in lizards and their relatives. Journal of Natural History, vol. 18, pp. 127-169.
Ávila, L, Acosta, JC. 1993. Notas sobre el comportamiento de Liolaemus darwinii (Sauria: Tropiduridae). Facena, vol. 10, pp. 57-61.
Bateman, PW & Fleming, PA. 2009. To cut a long tail short: a review of lizard caudal autotomy studies carried out over the last 20 years. Journal of zoology, vol. 277, pp. 1-14.
Bauwens, D & Thoen, C. 1981. Escape tactics and vulnerability to predation associated with reproduction in the lizard Lacerta vivipara. The Journal of Animal Ecology, vol. 50, pp. 733-743.
Bels, V & Russell, A. 2019. Behavior of lizards: evolutionary and mechanistic perspectives. Crc Press.
Bower, DS, Brannelly, LA, McDonald, CA, Webb, RJ, Greenspan, SE, Vickers, M & Greenlees, MJ. 2019. A review of the role of parasites in the ecology of reptiles and amphibians. Austral Ecology, vol. 44, pp. 433-448.
Bush, AO, Lafferty, KD, Lotz, JM & Shostak, AW. 1997. Parasitology meets ecology on its own terms. Journal of Parasitology, vol. 83, pp. 575–583.
Castañeda, G, García De la Peña, C, Gadsden H, Contreras-Balderas, AJ & Cooper, Jr, WE. 2011. Tail loss incidence in the Chihuahuan fringe toed-lizard Uma paraphygas (Squamata: Phrynosomatidae). Revista Mexicana de Biodiversidad, vol. 82, pp. 193-198.
Castillo, GN, Acosta JC, González-Rivas, CJ & Ramallo, G. 2020. Checklist of nematode parasites of reptiles from Argentina. Annals of Parasitology, vol. 66, pp. 425-432.
Casas, MH, Aráoz, E & Montero, R. 2016. Prevalence of Autotomy and Tail Regeneration in Teius teyou (Reptilia,Teiidae). Journal of Herpetology, vol. 50, pp. 449-456.
Cei, JM. 1986. Reptiles del Centro, Centro-Oeste y Sur de la Argentina. Herpetofauna de Zonas Áridas y Semiáridas. Museo Regionale di Scienze Naturali Torino. Monografía IV, pp. 112-120.
Cooper, WE & Blumstein, DT. 2015. Escaping from predators: an integrative view of escape 346 decisions. Cambridge University Press.
Cooper, WE, Jr & Frederick, WG. 2010. Predator lethality optimal escape behavior and autotomy. Behavior Ecology, vol. 21, pp. 91-96.
Cooper, WE, Pérez-Mellado, V & Vitt, LJ. 2004. Ease and effectiveness of costly autotomy vary with predation intensity among lizard populations. Journal of Zoology, vol. 262, pp. 243-255.
Dial, BE & Fitzpatrick, LC. 1981. The energetic costs of tail autotomy to reproduction in the lizard Coleonyx brevis (Sauria: Gekkonidae). Oecologia, vol. 51, pp. 310-317.
Er-Rguibi, O, Laghzaoui, EM, Aglagane, A, Kimdil, L, Abbad, A & Mouden, EH. 2021. Determinants of prevalence and co-infestation by ecto-and endoparasites in the Atlas day gecko, Quedenfeldtia trachyblepharus, an endemic species of Morocco. Parasitology Research, vol 120, pp. 2543-2556.
Emberts, Z, Escalante, I & Bateman, PW. 2019. The ecology and evolution of autotomy. Biological Reviews, vol 94, pp. 1881-1896.
Fischer, JD, Cleeton, SH, Lyons, TP & Miller, JR. 2012. Urbanization and the predation paradox: the role of trophic dynamics in structuring vertebrate communities. Bioscience, vol. 62, pp. 809-818.
Fox, SF & Rostker, MA. 1982. Social cost of tail loss in Uta stansburiana. Science, vol. 218 pp. 692-693.
García de la Peña, C, Castañeda, G, Gadsden, H, Contreras-Balderas, AJ & Lazcano, D. 2004. Autotomía caudal de Uma exsul (Sauria: Phrynosomatidae). Boletín de la Sociedad Herpetológica Mexicana, vol. 12, pp. 43-48.
García-Rosales, A & Martínez-Coronel, M. 2016. Frecuencia de pérdida de la cola en un ensamble de lagartijas de Oaxaca, México. Acta zoológica mexicana, vol. 32, pp. 174-181.
Garrido, M & Pérez-Mellado, V. 2014. Sprint speed is related to blood parasites, but not to ectoparasites, in an insular population of lacertid lizards. Canadian journal of zoology, vol. 92, pp. 67-72.
Garrido, M, Pérez‐Mellado, V & Cooper, WE. 2014. Complex relationships amongst parasite load and escape behaviour in an insular lizard. Ethology, vol. 12, pp. 116-124.
Genovart, M, Negre, N, Tavecchia, G, Bistuer, A, Parpal, L & Oro, D. 2010. The young, the weak and the sick: evidence of natural selection by predation. PLoS One, vol. 5, e9774.
Goldberg, SR & Bursey, CR. 1989. Physaloptera retusa (Nematoda, Physalopteridae) in naturally infected sagebrush lizards, Sceloporus graciosus (Iguanidae). Journal of Wildlife Diseases, vol. 25, pp. 425-429.
Hannah, L, Lohse D, Hutchinson, C, Carr, JL & Lankerani, A. 1994. A Preliminary Inventory of Human Disturbance of World Ecosystems. Ambio, vol. 23, pp. 246-250.
Hernandez-Caballero, I, Garcia-Longoria, L, Gomez-Mestre, I & Marzal, A. 2022. The Adaptive Host Manipulation Hypothesis: Parasites Modify the Behaviour, Morphology, and Physiology of Amphibians. Diversity, vol.14, pp. 1-18.
Higham, TE, Russell, AP & Zani, PA. 2013. Integrative biology of tail autotomy in lizards. Physiological and Biochemical Zoology, 86, pp. 603-610.
Itescu, Y, Schwarz, R, Meiri, S & Pafilis, P. 2017. Intraspecific competition, not predation, drives lizard tail loss on islands. Journal of Animal Ecology, vol 86, pp. 66-74.
Keehn, JE & Feldman, CR. 2018. Predator attack rates and antipredator flight behavior of side-blotched lizards (Uta stansburiana) at disturbed wind farms in Southern California, USA. Herpetological Conservation and Biology, vol. 13, pp. 194-204.
Klasing, KC. 2004. The costs of immunity. Dong Wu Xue Bao [acta Zoologica Sinica], vol 50, pp. 961-969.
Kuo, CC, Yao, CJ, Lin, TE, Liu HC, Hsu, YC, Hsieh, MK & Huang, WS. 2013. Tail loss compromises immunity in the many-lined skink, Eutropis multifasciata. Naturwissenschaften, vol. 100, pp. 379-384.
Lazić, MM, Carretero, MA, Živković, U & Crnobrnja-Isailović, J. 2017. City life has fitness costs: reduced body condition and increased parasite load in urban common wall lizards, Podarcis muralis. Salamandra, vol. 53, pp. 10-17.
Maginnis, TL. 2006. The costs of autotomy and regeneration in animals: a review and framework for future research. Behavioral Ecology, vol. 17, pp. 857-872.
Main, AR & Bull, CM. 2000. The impact of tick parasites on the behaviour of the lizard Tiliqua rugosa. Oecologia, vol. 122, pp. 574-581.
Marquez, J, Carretero, EM & Dalmaso, A. 2016. Provincias Fitogeográficas de la Provincia de San Juan. In: Carretero, E. M. & Garcia A. edts. 2016. San Juan Ambiental. San Juan, Editorial Universidad Nacional de San Juan. p. 187-197.
Moller, AP & Nielsen, JT. 2007. Malaria and risk of predation: a comparative study of birds. Ecology, vol. 88, pp. 871-881
Moore, J. 2002. Parasites and the Behavior of Animals. Oxford University Press on Demand.
Morello, J. 1958. La Provincia Fitogeográfica del Monte. Opera Lilloana II, Tucumán.
Oppliger, A, Celerier, ML & Clobert, J. 1996. Physiological and behaviour changes in common lizards parasitized by haemogregarines. Parasitology, vol. 113, pp. 433-438.
Oppliger, A & Clobert, J. 1997. Reduced tail regeneration in the common lizard, Lacerta vivipara, parasitized by blood parasites. Functional Ecology, vol. 11, pp. 652- 655.
Ramallo, GR & Díaz, F. 1998. Physaloptera lutzi (Nematoda, Physalopteridae) parasite de Liolaemus (Iguania, Tropiduridae) del noroeste Argentino. Boletín chileno de parasitologia, vol. 53, pp. 19-22.
Rodríguez, D, Pedroso-Reyes, JG, Olivares, MJL, Sánchez-Castilleja, YM & Arece- García, J. 2014. La interacción hospedero-parásito. Una visión evolutiva. Revista de Salud Animal, vol. 36, pp. 1-6.
Sanderson, EW, Jaiteh, M, Levy, MA, Redford, KH, Wannebo, AV & Woolmer, G. 2002. The human footprint and the last of the wild: the human footprint is a global map of human influence on the land surface, which suggests that human beings are stewards of nature, whether we like it or not. BioScience vol. 52, pp. 891-904.
Savvides, P, Poliviou, V, Stavrou, M, Sfenthourakis, S & Pafilis, P. 2018. Insights into how predator diversity, population density and habitat type may affect defensive behaviour in a Mediterranean lizard. Ethology Ecology & Evolution, vol. 31, pp. 12-27.
Schall, JJ & Sarni, GA. 1987. Malarial parasitism and the behavior of the lizard, Sceloporus occidentalis. Copeia, vol 1, pp. 84–93.
Sinclair, AR, Fryxell, JM & Caughley, G. 2006. Wildlife ecology, conservation, and management. Blackwell Publishing.
Temple, SA. 1987. Do predators always capture substandard individuals disproportionately from prey populations?. Ecology, vol. 68, pp. 669-674.
Videla, F. 1983. Hábitos alimentarios en Iguanidos del oeste árido de la Argentina. Deserta, vol. 7, pp. 192-202.
Vitt, LJ & Caldwell, JP. 2009. Herpetology: An Introductory Biology of Amphibians and Reptiles. 3rd Edition. Elsevier Inc.
Vitt, LJ, Congdon, JD & Dickson, NA. 1977. Adaptive strategies and energetics of tail autonomy in lizards. Ecology, vol. 58, pp. 326-337.
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