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Australian Journal of Zoology Australian Journal of Zoology Society
Evolutionary, molecular and comparative zoology
RESEARCH ARTICLE

Changes in urinary testosterone and corticosterone metabolites during short-term confinement with repeated handling in wild male cane toads (Rhinella marina)

Edward J. Narayan A D , Frank C. Molinia B , John F. Cockrem C and Jean-Marc Hero A
+ Author Affiliations
- Author Affiliations

A Environmental Futures Centre, School of Environment, Griffith University, Gold Coast campus, Qld 4222, Australia.

B Landcare Research, Private Bag 92170, Auckland 1142, New Zealand.

C Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Palmerston North, New Zealand.

D Corresponding author. Email: e.narayan@griffith.edu.au

Australian Journal of Zoology 59(4) 264-269 https://doi.org/10.1071/ZO11070
Submitted: 11 August 2011  Accepted: 17 February 2012   Published: 13 March 2012

Abstract

Stressors generally decrease testosterone secretion and inhibit reproduction in animals. Urinary testosterone and corticosterone metabolite concentrations were measured in adult male cane toads (Rhinella marina) at the time of capture from the wild and during 24 h of confinement with repeated handling. Mean urinary testosterone concentrations increased 2 h after capture, were significantly elevated above initial concentrations at 5 h, and then declined. Mean testosterone concentrations remained elevated 24 h after capture. Mean urinary corticosterone concentrations increased after capture, were significantly elevated above initial concentrations at 2 h, and remained elevated thereafter. This is the first report in amphibians of an increase in testosterone excretion after capture from the wild, with previous studies showing either no change or decline in testosterone. This finding may be associated with the mating strategy and maintenance of reproductive effort in the cane toad, a species that shows explosive breeding and agonistic male–male interactions during breeding. The finding that testosterone excretion increases rather than decreases after capture in male cane toads shows that it should not be generally assumed that reproductive hormone secretion will decrease after capture in amphibians.

Additional keywords: amphibian, capture, explosive breeding, non-invasive, stress.


References

Coddington, E. J., and Cree, A. (1995). Effect of acute captivity stress on plasma concentrations of corticosterone and sex steroids in female whistling frogs, Litoria ewingi. General and Comparative Endocrinology 100, 33–38.
Effect of acute captivity stress on plasma concentrations of corticosterone and sex steroids in female whistling frogs, Litoria ewingi.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXosVWnsbg%3D&md5=26edaba0055dcfe5fd361887720e7ff4CAS |

Daugherty, D. R., and Callard, I. P. (1972). Plasma corticosterone levels in the male iguanid lizard Sceloporus cyanogenys under various physiological conditions. General and Comparative Endocrinology 19, 69–79.
Plasma corticosterone levels in the male iguanid lizard Sceloporus cyanogenys under various physiological conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE38XksF2jtb4%3D&md5=578c8147eb7ec9f90523fb8a002a3311CAS |

Duellman, W. E., and Trueb, L. (1994). ‘Biology of Amphibians.’ (Johns Hopkins University Press: Baltimore, MD.)

Emerson, S. B., and Hess, D. L. (1996). The role of androgens in opportunistic breeding, tropical frogs. General and Comparative Endocrinology 103, 220–230.
The role of androgens in opportunistic breeding, tropical frogs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XkvV2rt70%3D&md5=cd938b874b526d475c749d46f7f45d42CAS |

Germano, J. M., Molinia, F. C., Bishop, P. J., and Cree, A. (2009). Urinary hormone analysis assists reproductive monitoring and sex identification of bell frogs (Litoria raniformis). Theriogenology 72, 663–671.
Urinary hormone analysis assists reproductive monitoring and sex identification of bell frogs (Litoria raniformis).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVSit7vP&md5=64154ae99653783d04f66bb58fe82e39CAS |

Gobbetti, A., and Zerani, M. (1996). Possible mechanism for the first response to short captivity stress in the water frog, Rana esculenta. The Journal of Endocrinology 148, 233–239.
Possible mechanism for the first response to short captivity stress in the water frog, Rana esculenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XhtVCrsrw%3D&md5=d759bba44bfa770c4720e113196e924aCAS |

Greenberg, G. N., and Wingfield, J. C. (Eds) (1987). ‘Stress and Reproduction: Reciprocal Relationships. Hormones and Reproduction in Fishes, Amphibians and Reptiles.’ (Plenum: New York.)

Harvey, L. A., Propper, C. R., Woodley, S. K., and Moore, M. C. (1997). Reproductive endocrinology of the explosively breeding desert spadefoot toad, Scaphiopus couchii. General and Comparative Endocrinology 105, 102–113.
Reproductive endocrinology of the explosively breeding desert spadefoot toad, Scaphiopus couchii.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXlslWgtA%3D%3D&md5=d44d24b09bb18c96e2e7dc4ce337b7a0CAS |

Heiblum, R., Arnon, E., Gvaryahu, G., Robinzon, B., and Snapir, N. (2000). Short-term stress increases testosterone secretion from testes in male domestic fowl. General and Comparative Endocrinology 120, 55–66.
Short-term stress increases testosterone secretion from testes in male domestic fowl.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnsVGnsLs%3D&md5=a8ccae6e735f4c4d282f6744b7332d24CAS |

Knol, B. W. (1991). Stress and the endocrine hypothalamus-pituitary-testis system: a review. The Veterinary Quarterly 13, 104–114.
Stress and the endocrine hypothalamus-pituitary-testis system: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXlt1Ogsro%3D&md5=e6aa12739b58ae4fd07ac351a76ca572CAS |

Leboulenger, F., Delarue, C., Tonon, M. C., Jegou, S., Leroux, P., and Vaudry, H. (1979). Seasonal study of the interrenal function of the european green frog, in vivo and in vitro. General and Comparative Endocrinology 39, 388–396.
Seasonal study of the interrenal function of the european green frog, in vivo and in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXmtVOkur8%3D&md5=557dfd68275a339c61069e221cf02b5eCAS |

Lever, C. (2001). ‘The Cane Toad: The History and Ecology of a Successful Colonist.’ (Westbury Publishing: West Yorkshire.)

Licht, P., McCreery, B. R., Barnes, R., and Pang, R. (1983). Seasonal and stress related changes in plasma gonadotropins, sex steroids, and corticosterone in the bullfrog, Rana catesbeiana. General and Comparative Endocrinology 50, 124–145.
Seasonal and stress related changes in plasma gonadotropins, sex steroids, and corticosterone in the bullfrog, Rana catesbeiana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXhsVSrs7s%3D&md5=a5dc7fc240f1f1c3fedb938bfe3d3f5eCAS |

Moore, F. L., and Miller, L. J. (1984). Stress-induced inhibition of sexual behavior: corticosterone inhibits courtship behaviors of a male amphibian (Taricha granulosa). Hormones and Behavior 18, 400–410.
Stress-induced inhibition of sexual behavior: corticosterone inhibits courtship behaviors of a male amphibian (Taricha granulosa).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXlvFOjug%3D%3D&md5=5bfaa4921bdfac5da179a5105b7782b2CAS |

Moore, F. L., and Zoeller, R. T. (1985). Stress-induced inhibition of reproduction: evidence of suppressed secretion of LH-RH in an amphibian. General and Comparative Endocrinology 60, 252–258.
Stress-induced inhibition of reproduction: evidence of suppressed secretion of LH-RH in an amphibian.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXlvFensbc%3D&md5=83e3ddade082295f3b75bcf050f5008fCAS |

Mosconi, G., Palermo, F., Carotti, M., Kikuyama, S., Yamamoto, K., and Polzonetti-Magni, A. M. (2006). Neuroendocrine modulation of stress response in the anuran, Rana esculenta. Amphibia-Reptilia 27, 401–408.
Neuroendocrine modulation of stress response in the anuran, Rana esculenta.Crossref | GoogleScholarGoogle Scholar |

Narayan, E., and Hero, J.-M. (2011). Urinary corticosterone responses and haematological stress indicators in the endangered Fijian ground frog (Platymantis vitiana) during transportation and captivity. Australian Journal of Zoology 59, 79–85.
Urinary corticosterone responses and haematological stress indicators in the endangered Fijian ground frog (Platymantis vitiana) during transportation and captivity.Crossref | GoogleScholarGoogle Scholar |

Narayan, E., Christi, K., Morley, C., and Trevenen, P. (2008). Sexual dimorphism in the cane toad Bufo marinus: a quantitative comparison of visual inspection methods for sexing individuals. The Herpetological Journal 18, 63–65.

Narayan, E., Molinia, F., Christi, K., Morley, C., and Cockrem, J. (2010a). Annual cycles of urinary reproductive steroid concentrations in wild and captive endangered Fijian ground frogs (Platymantis vitiana). General and Comparative Endocrinology 166, 172–179.
Annual cycles of urinary reproductive steroid concentrations in wild and captive endangered Fijian ground frogs (Platymantis vitiana).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhslSrtbY%3D&md5=728c489bc7c0b9b24c684d2b89d1e332CAS |

Narayan, E., Molinia, F., Christi, K., Morley, C., and Cockrem, J. (2010b). Urinary corticosterone metabolite responses to capture, and annual patterns of urinary corticosterone in wild and captive endangered Fijian ground frogs (Platymantis vitiana). Australian Journal of Zoology 58, 189–197.
Urinary corticosterone metabolite responses to capture, and annual patterns of urinary corticosterone in wild and captive endangered Fijian ground frogs (Platymantis vitiana).Crossref | GoogleScholarGoogle Scholar |

Narayan, E. J., Cockrem, J. F., and Hero, J.-M. (2011a). Urinary corticosterone metabolite responses to capture and captivity in the cane toad (Rhinella marina). General and Comparative Endocrinology 173, 371–377.
Urinary corticosterone metabolite responses to capture and captivity in the cane toad (Rhinella marina).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpvFSmtrY%3D&md5=bbf03094c91f468cc8b80873a87488cfCAS |

Narayan, E., Molinia, F., Christina, K., Cockrem, J., and Hero, J.-M. (2011b). Urinary corticosterone responses to capture and toe-clipping in the cane toad (Rhinella marina) indicate that toe-clipping is a stressor for amphibians. General and Comparative Endocrinology 174, 238–245.
Urinary corticosterone responses to capture and toe-clipping in the cane toad (Rhinella marina) indicate that toe-clipping is a stressor for amphibians.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlejt7fL&md5=2f4eac2efee898f65893d4dcdd43b8e4CAS |

Narayan, E., Molinia, F., Cockrem, J., and Hero, J.-M. (2012). Individual variation and repeatability in urinary corticosterone metabolite responses to capture in the cane toad (Rhinella marina). General and Comparative Endocrinology 175, 284–289.
Individual variation and repeatability in urinary corticosterone metabolite responses to capture in the cane toad (Rhinella marina).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVKrtQ%3D%3D&md5=54fb62aabe0cab428feef83bc06733e3CAS |

Orchinik, M., Licht, P., and Crews, D. (1988). Plasma steroid concentrations change in response to sexual behavior in Bufo marinus. Hormones and Behavior 22, 338–350.
Plasma steroid concentrations change in response to sexual behavior in Bufo marinus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXlvVOlu7g%3D&md5=d50af2a72c1da93bb77b475632cd1d91CAS |

Paolucci, M., Esposito, V., Difiore, M. M., and Botte, V. (1990). Effects of short postcapture confinement on plasma reproductive hormone and corticosterone profiles in Rana esculenta during the sexual cycle. Bollettino di Zoologia 57, 253–259.
Effects of short postcapture confinement on plasma reproductive hormone and corticosterone profiles in Rana esculenta during the sexual cycle.Crossref | GoogleScholarGoogle Scholar |

Pukazhenthi, B. S., and Wildt, D. E. (2004). Which reproductive technologies are most relevant to studying, managing and conserving wildlife? Reproduction, Fertility and Development 16, 33–46.
Which reproductive technologies are most relevant to studying, managing and conserving wildlife?Crossref | GoogleScholarGoogle Scholar |

Wingfield, J. C., and Grimm, A. S. (1977). Seasonal changes in plasma cortisol, testosterone and oestradiol-17β in the plaice, Pleuronectes platessa L. General and Comparative Endocrinology 31, 1–11.
Seasonal changes in plasma cortisol, testosterone and oestradiol-17β in the plaice, Pleuronectes platessa L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXktVCmtQ%3D%3D&md5=ec39411d1ac845353f57d8d715116f11CAS |

Woodley, S. K., and Lacy, E. L. (2010). An acute stressor alters steroid hormone levels and activity but not sexual behavior in male and female Ocoee salamanders (Desmognathus ocoee). Hormones and Behavior 58, 427–432.
An acute stressor alters steroid hormone levels and activity but not sexual behavior in male and female Ocoee salamanders (Desmognathus ocoee).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpvVKgs78%3D&md5=69bbad23cac45537586d90642b73ebaaCAS |