The effect of testosterone suppression on health and parasite burden in male eastern grey kangaroos (Macropus giganteus)
Maquel E. Brandimarti
A E , Rachael Gray B , Zoe J. Hilton A , Tamara Keeley C , ‘Kangaroo’ Phil Murray D and Catherine A. Herbert A
+ Author Affiliations
- Author Affiliations
A School of Life and Environmental Science, The University of Sydney, JD Stewart building, Camperdown, NSW 2006, Australia.
B Sydney School of Veterinary Science, The University of Sydney, McMaster building, Camperdown, NSW 2006, Australia.
C School of Agriculture and Food Sciences, The University of Queensland, Building 8117A, Ground Floor, Gatton, Qld 4343, Australia.
D Nelson Bay Golf Club, 57 Dowling St, Nelson Bay, NSW 2315, Australia.
E Corresponding author. Email: maquel.brandimarti@live.com.au
Australian Mammalogy 44(2) 213-224 https://doi.org/10.1071/AM21017
Submitted: 21 May 2021 Accepted: 5 July 2021 Published: 9 August 2021
Abstract
Testosterone has a dualistic effect in males by promoting sexual ornamentation at the cost of immune defence. This trade-off has been demonstrated in several taxa, such that males often host a greater parasite burden compared with female conspecifics. We suppressed testosterone in wild male eastern grey kangaroos (Macropus giganteus) for 10 weeks using a novel gonadotropin-releasing hormone (GnRH) vaccine, Bopriva. We evaluated the impact of testosterone suppression on testes width, parameters of health, tick and worm burden in kangaroos using a before-after-control-impact (BACI) experimental design. Given the potential impact of animal movement on parasite burden, core area use of a subset of males was also determined. Bopriva significantly reduced testosterone in male kangaroos as well as reducing the combined size of testes by 9.6% (P = 0.01). There was no detectable effect of testosterone suppression on parasite burden and core area use in Treated kangaroos compared to Control (placebo) and Before treatment animals. Our results suggest that a duration of suppression longer than 10 weeks may be required to observe changes in parasite burden. Overall, this study provides a suitable framework for future studies to test whether reproductive hormones influence energy allocation, parasitism, and reproductive strategies in marsupials.
Keywords: immunocompetence, kangaroo, Macropus giganteus, marsupial, parasite burden, sexual signals, testosterone, ticks.
References
Alexander, J., and Stimson, W. H. (1988). Sex hormones and the course of parasitic infection. Parasitolgy Today 4, 189–193.| Sex hormones and the course of parasitic infection.Crossref | GoogleScholarGoogle Scholar |
Amatayakul-Chantler, S., Jackson, J. A., Stegner, J., King, V., Rubio, L. M. S., Howard, R., Lopez, E., and Walker, J. (2012). Immunocastration of Bos indicus × Brown Swiss bulls in feedlot with gonadotropin-releasing hormone vaccine Bopriva provides improved performance and meat quality. Journal of Animal Science 90, 3718–3728.
| Immunocastration of Bos indicus × Brown Swiss bulls in feedlot with gonadotropin-releasing hormone vaccine Bopriva provides improved performance and meat quality.Crossref | GoogleScholarGoogle Scholar | 22665672PubMed |
Arbor Assays (2020). ‘ISWE Testosterone Mini-Kit.’ Available at https://www.arborassays.com/documentation/inserts/ISWE001.pdf (accessed 15 September 2018.)
Arundel, J. H., Dempster, K. J., Harrigan, K. E., and Black, R. (1990). Epidemiological observations on the helminth parasites of Macropus giganteus Shaw in Victoria. Wildlife Research 17, 39–51.
| Epidemiological observations on the helminth parasites of Macropus giganteus Shaw in Victoria.Crossref | GoogleScholarGoogle Scholar |
Beldomenico, P. M., and Begon, M. (2010). Disease spread, susceptibility and infection intensity: vicious circles? Trends in Ecology and Evolution 25, 21–27.
| Disease spread, susceptibility and infection intensity: vicious circles?Crossref | GoogleScholarGoogle Scholar | 19782425PubMed |
Benhamou, S. (2011). Dynamic approach to space and habitat use based on biased random bridges. PLoS One 6, e14592.
| Dynamic approach to space and habitat use based on biased random bridges.Crossref | GoogleScholarGoogle Scholar | 21297869PubMed |
Beveridge, I., and Emery, D. (2015). ‘Australasian animal parasites: inside and out.’ pp. 279–340. (Australian Society for Parasitology).
Bradley, A. J. (1987). Stress and mortality in the red-tailed Phascogale, Phascogale calura (Marsupialia: Dasyuridae). General and Comparative Endocrinolgy 67, 85–100.
| Stress and mortality in the red-tailed Phascogale, Phascogale calura (Marsupialia: Dasyuridae).Crossref | GoogleScholarGoogle Scholar |
Bradley, A. J., McDonald, I. R., and Lee, A. K. (1980). Stress and mortality in a small marsupial (Antechinus stuartii, Macleay). General and Comparative Endocrinolgy 40, 188–200.
| Stress and mortality in a small marsupial (Antechinus stuartii, Macleay).Crossref | GoogleScholarGoogle Scholar |
Brandimarti, M. E., Gray, R., Coulson, G., Cripps, J. K., Wilson, M. E., Death, C., Snape, M., Wimpenny, C., Silva, F. R. O., Miller, E. J., Scanes, E., Spielman, D., Thomas, G., and Herbert, C. A. (2020). Reference intervals for parameters of health of eastern grey kangaroos (Macropus giganteus) and management implications across their geographic range. Wildlife Biology 2020, .
| Reference intervals for parameters of health of eastern grey kangaroos (Macropus giganteus) and management implications across their geographic range.Crossref | GoogleScholarGoogle Scholar |
Brandimarti, M. E., Gray, R., Silva, F. R. O., and Herbert, C. A. (2021). Kangaroos at maximum capacity: health assessment of free-ranging eastern grey kangaroos on a coastal headland. Journal Mammalogy 102, 387–851.
| Kangaroos at maximum capacity: health assessment of free-ranging eastern grey kangaroos on a coastal headland.Crossref | GoogleScholarGoogle Scholar |
Brunton, E. A., Srivastava, S. K., and Burnett, S. (2019). Spatial ecology of an urban eastern grey kangaroo (Macropus giganteus) population: local decline driven by kangaroo–vehicle collisions. Wildlife Research 45, 685–695.
| Spatial ecology of an urban eastern grey kangaroo (Macropus giganteus) population: local decline driven by kangaroo–vehicle collisions.Crossref | GoogleScholarGoogle Scholar |
Cabaret, J., Gasnier, N., and Jacquiet, P. (1998). Faecal egg counts are representative of digestive-tract strongyle worm burdens in sheep and goats. Parasite 5, 137–142.
| Faecal egg counts are representative of digestive-tract strongyle worm burdens in sheep and goats.Crossref | GoogleScholarGoogle Scholar | 9754309PubMed |
Calenge, C. (2015). ‘Home range estimation in R: the adehabitatHR package.’ (The Comprehensive R Archive Network (CRAN).)
Colditz, I. G. (2008). Six costs of immunity to gastrointestinal nematode infections. Parasite Immunology 30, 63–70.
| 18186766PubMed |
Coulson, G. M. (2008). Eastern grey kangaroo. In ‘The mammals of Australia’. (Eds S. V. Dyck and R. Strahan.) pp. 335–338. (New Holland Publishers.)
Coulson, G., Cripps, J. K., and Wilson, M. E. (2014). Hopping down the main street: eastern grey kangaroos at home in an urban matrix. Animals 4, 272–291.
| Hopping down the main street: eastern grey kangaroos at home in an urban matrix.Crossref | GoogleScholarGoogle Scholar | 26480041PubMed |
Craney, T. A., and Surles, J. G. (2002). Model-dependent variance inflation factor cutoff values. Quality Engineering 14, 391–403.
| Model-dependent variance inflation factor cutoff values.Crossref | GoogleScholarGoogle Scholar |
Cripps, J. K., Beveridge, I., Ploeg, R., and Coulson, G. (2014). Experimental manipulation reveals few subclinical impacts of a parasite community in juvenile kangaroos. International Journal of Parasitology: Parasites and Wildlife 3, 88–94.
| Experimental manipulation reveals few subclinical impacts of a parasite community in juvenile kangaroos.Crossref | GoogleScholarGoogle Scholar |
Cripps, J. K., Beveridge, I., Martin, J. K., Borland, D., and Coulson, G. (2015). Temporal dynamics of helminth infections in eastern grey kangaroos (Macropus giganteus) in Victoria. Australian Journal of Zoology 63, 163–174.
| Temporal dynamics of helminth infections in eastern grey kangaroos (Macropus giganteus) in Victoria.Crossref | GoogleScholarGoogle Scholar |
Decristophoris, P. M. A., von Hardenberg, A., and McElligott, A. G. (2007). Testosterone is positively related to the output of nematode eggs in male alpine ibex (Capra ibex) faeces. Evolutionary Ecology Research 9, 1277–1292.
De La Peña, E., Martín, J., Barja, I., Pérez‐Caballero, R., Acosta, I., and Carranza, J. (2020). The immune challenge of mating effort: steroid hormone profile, dark ventral patch and parasite burden in relation to intrasexual competition in male Iberian red deer. Integrative Zoology 15, 262–275.
| The immune challenge of mating effort: steroid hormone profile, dark ventral patch and parasite burden in relation to intrasexual competition in male Iberian red deer.Crossref | GoogleScholarGoogle Scholar | 31912636PubMed |
Demas, G. E., Zysling, D. A., Beechler, B. R., Muehlenbein, M. P., and French, S. S. (2011). Beyond phytohaemagglutinin: assessing vertebrate immune function across ecological contexts. Journal of Animal Ecology 80, 710–730.
| Beyond phytohaemagglutinin: assessing vertebrate immune function across ecological contexts.Crossref | GoogleScholarGoogle Scholar |
Emerson, S. B. (2000). Vertebrate secondary sexual characteristics – physiological mechanisms and evolutionary patterns. The American Naturalist 156, 84–91.
| Vertebrate secondary sexual characteristics – physiological mechanisms and evolutionary patterns.Crossref | GoogleScholarGoogle Scholar | 10824023PubMed |
Fisher, D. O., and Lara, M. C. (1999). Effects of body size and home range on access to mates and paternity in male bridled nailtail wallabies. Animal Behaviour 58, 121–130.
| Effects of body size and home range on access to mates and paternity in male bridled nailtail wallabies.Crossref | GoogleScholarGoogle Scholar | 10413548PubMed |
Folstad, I., and Karter, A. J. (1992). Parasites, bright males, and the immunocompetence handicap. The American Naturalist 139, 603–622.
| Parasites, bright males, and the immunocompetence handicap.Crossref | GoogleScholarGoogle Scholar |
Grear, D. A., Perkins, S. E., and Hudson, P. J. (2009). Does elevated testosterone result in increased exposure and transmission of parasites? Ecology Letters 12, 528–537.
| Does elevated testosterone result in increased exposure and transmission of parasites?Crossref | GoogleScholarGoogle Scholar | 19392718PubMed |
Gulland, F. M. D. (1995). The impact of infectious diseases on wild animal populations: a review. In ‘Ecology of infectious diseases in natural populations’. (Eds B. T. Grenfell and A. P. Dobson.) pp. 20–51. (Cambridge University Press.)
Henderson, T., Vernes, K., Körtner, G., and Rajaratnam, R. (2018). Using GPS technology to understand spatial and temporal activity of kangaroos in a peri-urban environment. Animals 8, 97.
| Using GPS technology to understand spatial and temporal activity of kangaroos in a peri-urban environment.Crossref | GoogleScholarGoogle Scholar |
Herbert, C. A., Trigg, T. E., Renfree, M. B., Shaw, G., Eckery, D. C., and Cooper, D. W. (2004). Effects of a gonadotropin-releasing hormone agonist implant on reproduction in a male marsupial, Macropus eugenii. Biology of Reproduction 70, 1836–1842.
| Effects of a gonadotropin-releasing hormone agonist implant on reproduction in a male marsupial, Macropus eugenii.Crossref | GoogleScholarGoogle Scholar | 14973259PubMed |
Herbert, C. A., Dassis, M., Pye, M., Jones, P. W., Leong, P. H. W., Thomas, G., Cope, H., Jarman, A., Hobbs, R., Murray, P. E., and Machovsky Capuska, G. E. (2020). Development of light-weight video-tracking technology for use in wildlife research: a case study on kangaroos. Australian Zoology 40, 364–378.
| Development of light-weight video-tracking technology for use in wildlife research: a case study on kangaroos.Crossref | GoogleScholarGoogle Scholar |
Janett, F., Gerig, T., Tschuor, A. C., Amatayakul-Chantler, S., Walker, J., Howard, R., Bollwein, H., and Thun, R. (2012a). Vaccination against gonadotropin-releasing factor (GnRF) with Bopriva significantly decreases testicular development, serum testosterone levels and physical activity in pubertal bulls. Theriogenology 78, 182–188.
| Vaccination against gonadotropin-releasing factor (GnRF) with Bopriva significantly decreases testicular development, serum testosterone levels and physical activity in pubertal bulls.Crossref | GoogleScholarGoogle Scholar | 22541323PubMed |
Janett, F., Gerig, T., Tschuor, A. C., Amatayakul-Chantler, S., Walker, J., Howard, R., Piechotta, M., Bollwein, H., Hartnack, S., and Thun, R. (2012b). Effect of vaccination against gonadotropin-releasing factor (GnRF) with Bopriva in the prepubertal bull calf. Animal Reproduction Science 131, 72–80.
| Effect of vaccination against gonadotropin-releasing factor (GnRF) with Bopriva in the prepubertal bull calf.Crossref | GoogleScholarGoogle Scholar | 22440457PubMed |
Jarman, P. J. (2000). Males in macropod society. In ‘Primate males: causes and consequences of variation in group composition’. (Ed. P. M. Kappeler.) pp. 21–33. (Cambridge University Press.)
Keeley, T., O’brien, J. K., Fanson, B. G., Masters, K., and McGreevy, P. D. (2012). The reproductive cycle of the Tasmanian devil (Sarcophilus harrisii) and factors associated with reproductive success in captivity. General and Comparative Endocrinology 176, 182–191.
| The reproductive cycle of the Tasmanian devil (Sarcophilus harrisii) and factors associated with reproductive success in captivity.Crossref | GoogleScholarGoogle Scholar | 22306283PubMed |
Klein, S. L., and Nelson, R. J. (1998). Adaptive immune responses are linked to the mating system of arvicoline rodents. The American Naturalist 151, 59–67.
| Adaptive immune responses are linked to the mating system of arvicoline rodents.Crossref | GoogleScholarGoogle Scholar | 18811424PubMed |
Martínez‐Padilla, J., Mougeot, F., Webster, L. M. I., Pérez Rodríguez, L., and Piertney, S. B. (2010). Testing the interactive effects of testosterone and parasites on carotenoid‐based ornamentation in a wild bird. Journal of Evolutionary Biology 23, 902–913.
| Testing the interactive effects of testosterone and parasites on carotenoid‐based ornamentation in a wild bird.Crossref | GoogleScholarGoogle Scholar | 20536879PubMed |
Massei, G., Cowan, D., Coats, J., Gladwell, F., Lane, J. E., and Miller, L. A. (2008). Effect of the GnRH vaccine GonaCon on the fertility, physiology and behaviour of wild boar. Wildlife Research 35, 540–540.
| Effect of the GnRH vaccine GonaCon on the fertility, physiology and behaviour of wild boar.Crossref | GoogleScholarGoogle Scholar |
McKenna, P. B. (1981). The diagnostic value and interpretation of faecal egg counts in sheep. New Zealand Veterinary Journal 29, 129–132.
| The diagnostic value and interpretation of faecal egg counts in sheep.Crossref | GoogleScholarGoogle Scholar | 6945520PubMed |
Miller, E. J., Eldridge, M. D. B., Cooper, D. W., and Herbert, C. A. (2010). Dominance, body size and internal relatedness influence male reproductive success in eastern grey kangaroos (Macropus giganteus). Reproduction, Fertility and Development 22, 539–549.
| Dominance, body size and internal relatedness influence male reproductive success in eastern grey kangaroos (Macropus giganteus).Crossref | GoogleScholarGoogle Scholar |
Nakanishi, H., Horii, Y., Terashima, K., and Fujita, K. (1989). Effect of testosterone on the susceptibility of C57BL/6 mice to infection with Brugia pahangi with reference to inflammatory cell response. The Journal of Parasitology , 455–460.
| Effect of testosterone on the susceptibility of C57BL/6 mice to infection with Brugia pahangi with reference to inflammatory cell response.Crossref | GoogleScholarGoogle Scholar | 2723929PubMed |
Negro, S. S., Caudron, A. K., Dubois, M., Delahaut, P., and Gemmell, N. J. (2010). Correlation between male social status, testosterone levels, and parasitism in a dimorphic polygynous mammal. PLoS One 5, e12507.
| Correlation between male social status, testosterone levels, and parasitism in a dimorphic polygynous mammal.Crossref | GoogleScholarGoogle Scholar | 20856933PubMed |
Pedersen, A. B., and Fenton, A. (2015). The role of anti-parasite treatment experiments in assessing the impact of parasites on wildlife. Trends in Parasitology 31, 200–211.
| The role of anti-parasite treatment experiments in assessing the impact of parasites on wildlife.Crossref | GoogleScholarGoogle Scholar | 25778845PubMed |
Pfizer. (2020). ‘Transform bull management with Bopriva. Veterinary guide Pfizer animal health.’ Available at https://www.zoetis.co.nz/_locale-assets/doc/species-products/bopriva-veterinary-guide.pdf (accessed 15 September 2018.)
Pollock, N. B., Vredevoe, L. K., and Taylor, E. N. (2012). How do host sex and reproductive state affect host preference and feeding duration of ticks? Parasitology Research 111, 897–907.
| How do host sex and reproductive state affect host preference and feeding duration of ticks?Crossref | GoogleScholarGoogle Scholar | 22526292PubMed |
Poole, W. E. (1973). A study of breeding in grey kangaroos, Macropus giganteus Shaw and M. fuliginosus (Desmarest), in central New South Wales. Australian Journal of Zoology 21, 183–212.
| A study of breeding in grey kangaroos, Macropus giganteus Shaw and M. fuliginosus (Desmarest), in central New South Wales.Crossref | GoogleScholarGoogle Scholar | 4803461PubMed |
Poole, W. E., Carpenter, S. M., and Wood, J. T. (1982). Growth of grey kangaroos and the reliability of age determination from body meausrements I. The eastern grey kangaroo, Macropus giganteus. Wildlife Research 9, 9–20.
| Growth of grey kangaroos and the reliability of age determination from body meausrements I. The eastern grey kangaroo, Macropus giganteus.Crossref | GoogleScholarGoogle Scholar |
Powell, R., and Mitchell, M. (2012). What is a home range? Journal of Mammalogy 93, 948–958.
| What is a home range?Crossref | GoogleScholarGoogle Scholar |
Randall, D., Burggren, W., French, K., and Eckert, R. (1997). ‘Animal physiology: mechanisms and adaptations’, 2nd edn. (W.H. Freeman & Co.)
R Core Team. (2017). ‘R: a language and environment for statistical computing.’ (R foundation for statistical computing: Vienna. Austria.) Available at https://www.R-project.org/ (accessed 29 February 2020.)
Rice, W. R. (1989). Analyzing tables of statistical tests. Evolution 43, 223–225.
| Analyzing tables of statistical tests.Crossref | GoogleScholarGoogle Scholar | 28568501PubMed |
Rioux-Paquette, E., Garant, D., Martin, A. M., Coulson, G., and Festa-Bianchet, M. (2015). Paternity in eastern grey kangaroos: moderate skew despite strong sexual dimorphism. Behavioral Ecology 26, 1147–1155.
| Paternity in eastern grey kangaroos: moderate skew despite strong sexual dimorphism.Crossref | GoogleScholarGoogle Scholar |
Roberts, M. L., Buchanan, K. L., and Evans, M. R. (2004). Testing the immunocompetence handicap hypothesis: a review of the evidence. Animal Behaviour 68, 227–239.
| Testing the immunocompetence handicap hypothesis: a review of the evidence.Crossref | GoogleScholarGoogle Scholar |
Seivwright, L. J., Redpath, S. M., Mougeot, F., Leckie, F., and Hudson, P. J. (2005). Interactions between intrinsic and extrinsic mechanisms in a cyclic species: testosterone increases parasite infection in red grouse. Proceedings: Biological Science 272, 2299–2304.
| Interactions between intrinsic and extrinsic mechanisms in a cyclic species: testosterone increases parasite infection in red grouse.Crossref | GoogleScholarGoogle Scholar |
Shaw, A. K., Sherman, J., Barker, F. K., and Zuk, M. (2018). Metrics matter: the effect of parasite richness, intensity and prevalence on the evolution of host migration. Proceedings of the Royal Society B 285, 20182147.
| Metrics matter: the effect of parasite richness, intensity and prevalence on the evolution of host migration.Crossref | GoogleScholarGoogle Scholar | 30429312PubMed |
Sheldon, B. C., and Verhulst, S. (1996). Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends in Ecology and Evolution 11, 317–321.
| Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology.Crossref | GoogleScholarGoogle Scholar | 21237861PubMed |
Smith, A. (2018). Movement patterns of eastern grey kangaroos (Macropus giganteus) in relation to road infrastructure. BSc Honours thesis. The University of Sydney, Australia.
Snape, M. A. (2012). Reproductive and behavioural effects of a GnRH-targeted immunocontraceptive vaccine in macropodids. PhD thesis. Australian National University, Canberra, Australia.
Sokal, R. F., and Rohlf, F. J. (1995). The principles and practice of statistics in biological research. Biometry , 451–554.
Stark, D. J., Vaughan, I. P., Ramirez Saldivar, D. A., Nathan, S. K. S. S., and Goossens, B. (2017). Evaluating methods for estimating home ranges using GPS collars: a comparison using proboscis monkeys (Nasalis larvatus). PLoS One 12, e0174891.
| Evaluating methods for estimating home ranges using GPS collars: a comparison using proboscis monkeys (Nasalis larvatus).Crossref | GoogleScholarGoogle Scholar | 28362872PubMed |
Teitelbaum, C. S., Huang, S., Hall, R. J., and Altizer, S. (2018). Migratory behaviour predicts greater parasite diversity in ungulates. Proceedings of the Royal Society B: Biological Sciences 285, 20180089.
| Migratory behaviour predicts greater parasite diversity in ungulates.Crossref | GoogleScholarGoogle Scholar | 29563269PubMed |
Theubet, G., Thun, R., Hilbe, M., and Janett, F. (2010). Effect of vaccination against GnRH (Bopriva) in the male pubertal calf. Schweizer Archiv Fur Tierheilkunde 152, 459–469.
| Effect of vaccination against GnRH (Bopriva) in the male pubertal calf.Crossref | GoogleScholarGoogle Scholar | 20886442PubMed |
Tompkins, D. M., and Begon, M. (1999). Parasites can regulate wildlife populations. Parasitolgy Today 15, 311–313.
| Parasites can regulate wildlife populations.Crossref | GoogleScholarGoogle Scholar |
Tompkins, D. M., Dunn, A. M., Smith, M. J., and Telfer, S. (2011). Wildlife diseases: from individuals to ecosystems. Journal of Animal Ecology 80, 19–38.
| Wildlife diseases: from individuals to ecosystems.Crossref | GoogleScholarGoogle Scholar |
Tschirren, B., Fitze, P. S., and Richner, H. (2003). Sexual dimorphism in susceptibility to parasites and cell‐mediated immunity in great tit nestlings. Journal of Animal Ecology 72, 839–845.
| Sexual dimorphism in susceptibility to parasites and cell‐mediated immunity in great tit nestlings.Crossref | GoogleScholarGoogle Scholar |
Turkstra, J. A., van der Staay, F. J., Stockhofe-Zurwieden, N., Woelders, H., Meloen, R. H., and Schuurman, T. (2011). Pharmacological and toxicological assessment of a potential GnRH vaccine in young-adult male pigs. Vaccine 29, 3791–3801.
| Pharmacological and toxicological assessment of a potential GnRH vaccine in young-adult male pigs.Crossref | GoogleScholarGoogle Scholar | 21439319PubMed |
Veiga, J. P., Salvador, A., Merino, S., and Puerta, M. (1998). Reproductive effort affects immune response and parasite infection in a lizard: a phenotypic manipulation using testosterone. Oikos , 313–318.
| Reproductive effort affects immune response and parasite infection in a lizard: a phenotypic manipulation using testosterone.Crossref | GoogleScholarGoogle Scholar |
Zuk, M., Johnsen, T. S., and Maclarty, T. (1995). Endocrine-immune interactions, ornaments and mate choice in red jungle fowl. Proceedings of the Royal Society B: Biological Sciences 260, 205–210.
| Endocrine-immune interactions, ornaments and mate choice in red jungle fowl.Crossref | GoogleScholarGoogle Scholar |
