Urinary hormone metabolites identify sex and imply unexpected winter breeding in an endangered, subterranean-nesting frog

General and Comparative Endocrinology

Volumn 175, Issue 3, 2012, Pages 464-472

  Germano, J M ^a   Molinia, F C ^b   Bishop, P J ^a   Bell, B D ^c   Cree, A ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b LANDCARE RESEARCH   (New Zealand)

^c VICTORIA UNIVERSITY OF WELLINGTON   (New Zealand)

Author keywords

Anura; Conservation; Reproduction; Sex identification; Urinary hormone metabolite

Indexed keywords

ESTRONE; PROGESTERONE; TESTOSTERONE;

ADULT ANIMAL; ANIMAL BEHAVIOR; ARTICLE; BIOLOGICAL TRAIT; BODY HEIGHT; BODY SIZE; BREEDING METHOD; CONTROLLED STUDY; ENDANGERED SPECIES; FEMALE; FROG; HORMONE DETERMINATION; HORMONE URINE LEVEL; LEIOPELMA PAKEKA; MALE; NESTING; NONHUMAN; ORGAN SIZE; OVARY FOLLICLE; PRIORITY JOURNAL; SEASONAL VARIATION; SEX DIFFERENCE; SEXUAL BEHAVIOR; SPECIES CONSERVATION; WILD ANIMAL; WINTER;

EID: 84856092429     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2011.12.003     Document Type: Article

References (51)

1. Bagnara J.T. Mexican Leaf Frog (Pachymedusa dacnicolor) as a model in endocrine research. Journal of Experimental Zoology 1990, 145-147.
2. Bauer B., Palme R., Machatschke I.H., Dittami J., Huber S. Non-invasive measurement of adrenocortical and gonadal activity in male and female guinea pigs (Cavia aperea f. porcellus). General and Comparative Endocrinology 2008, 156:482-489.
3. Bell B.D. Observations on the ecology and reproduction of the New Zealand leiopelmid frogs. Herpetologica 1978, 34:340-354.
4. Bell B.D. Conservation Status of the Endemic New Zealand Frogs. Biology of Australasian Frogs and Reptiles 1985, 449-458. Royal Zoological Society of New South Wales, New South Wales. G. Grigg, R. Shine, H. Ehmann (Eds.).
5. Bell B.D. Development and Parental-Care in the Endemic New Zealand Frogs. Biology of Australasian Frogs and Reptiles 1985, 269-278. Royal Zoological Society of New South Wales, New South Wales. G. Grigg, R. Shine, H. Ehmann (Eds.).
6. Bell B.D. Experience of Captive Breeding the Four Extant Leiopelma Species 2002, Unpublished report for the Department of Conservation, School of Biological Sciences, Victoria University of Wellington, p. 17.
7. Bell B.D. The Discovery of Maud Island frogs Leiopelma pakeka Breeding in Karori Wildlife Sanctuary and the Rearing of their Young 2008, Centre for Biodiversity and Restoration Ecology Report, Victoria University of Wellington, Wellington, New Zealand, p. 21.
8. Bell B.D. Breeding phenology of Leiopelma pakeka: a threatened frog never found breeding in the wild. Herpetological Review 2011, 42:29-32.
9. Bell B.D., Pledger S.A. How has the remnant population of the threatened frog Leiopelma pakeka (Anura: Leiopelmatidae) fared on Maud Island, New Zealand, over the past 25 years?. Australian Ecology 2010, 35:241-256.
10. Bell B.D., Pledger S., Dewhurst P.L. The fate of a population of the endemic frog Leiopelma pakeka (Anura: Leiopelmatidae) translocated to restored habitat on Maud Island, New Zealand. New Zealand Journal of Zoology 2004, 31:123-131.
11. Bercovitz A.B., Czekala N.M., Lasley B.L. New method of sex determination in monomorphic birds. Journal of Zoo Animal Medicine 1978, 9:114-124.
12. Bishop P.J., Germano J.M., Bell B.D. Leiopelmatid Frogs: the World's Most Archaic Frogs. Threatened Amphibians of the World 2008, 71-72. Lynx Edicions, Barcelona, Spain. S.N. Stuart, M. Hoffman, J. Chanson, N.A. Cox, R. Berridge, P. Ramani, B. Young (Eds.).
13. Bishop P.J., Daglish L.A., Haigh A., Marshall L.J., Tocher M.D. Native Frog (Leiopelma species) Recovery Plan 2010-2015. Threatened Species Recovery Plan 2011, DOC Scientific Publications, Department of Conservation, Wellington, New Zealand.
14. Blanvillain G., Wood L.D., Meylan A.B., Meylan P.A. Sex ratio prediction of juvenile Hawksbill Sea Turtles (Eretmocheyls imbricata) from South Florida, USA. Herpetological Conservation and Biology 2008, 3:21-27.
15. Brown J.L., Wasser S.K., Wildt D.E., Graham L.H. Comparative aspects of steroid-hormone metabolism and ovarian activity in felids, measured noninvasively in feces. Biology of Reproduction 1994, 51:776-786.
16. Coddington E., Cree A. Effect of acute captivity stress on plasma concentrations of corticosterone and sex steroids in female whistling frogs, Litoria ewingi. General and Comparative Endocrinology 1995, 100:33-38.
17. Cree A. Low annual reproductive output in female reptiles from New Zealand. New Zealand Journal of Zoology 1994, 21:351-372.
18. Cree A., Daugherty C.H. Induction of egg-laying in terrestrial-breeding leiopelmatid frogs 1991, Unpublished report for the Department of Conservation, School of Biological Science, Victoria University of Wellington, p. 18.
19. Cree A., Guillette L., Cockrem J., Joss J. Effects of capture and temperature stresses on plasma steroid concentrations in male tuatara (Sphenodon punctatus). Journal of Experimental Zoology 1990, 253:38-46.
20. Cyr N.E., Romero L.M. Fecal glucocorticoid metabolites of experimentally stressed captive and free-living starlings: Implications for conservation research. General and Comparative Endocrinology 2008, 158:20-28.
21. deCatanzaro D., Muir C., Beaton E., Jetha M., Nadella K. Enzyme immunoassay of oestradiol, testosterone and progesterone in urine samples from female mice before and after insemination. Reproduction 2003, 126:407-414.
22. Delgado M.J., Gutierrez P., Alonzo-Bedate M. Seasonal cycles in testicular activity in the frog, Rana perezi. General and Comparative Endocrinology 1989, 73:1-11.
23. Duellman W., Trueb L. Biology of Amphibians 1986, Johns Hopkins University Press Ltd.
24. Forster R. The use of inulin and creatinine as glomerular filtrate measuring substances in the frog. Journal of Cellular and Comparative Physiology 1938, 12:213-222.
25. Germano J. Sex Identification and Reproductive Biology of the Endangered Maud Island Frog, Leiopelma pakeka 2010, Department of Zoology, University of Otago, Dunedin, p. 128.
26. Germano J.M., Bishop P.J. Leiopelma pakeka (Maud Island Frog) reproduction. Herpetological Review 2007, 38:187-188.
27. Germano J.M., Molinia F.C., Bishop P.J., Cree A. Urinary hormone analysis assists reproductive monitoring and sex identification of bell frogs (Litoria raniformis). Theriogenology 2009, 72:663-671.
28. Germano J.M., Cree A., Bishop P.J. Ruling out the boys from the girls: can subtle morphological differences identify sex of the apparently monomorphic frog, Leiopelma pakeka?. New Zealand Journal of Zoology 2011, 38:161-171.
29. Goymann W. Noninvasive monitoring of hormones in bird droppings: physiological validation, sampling, extraction, sex differences, and the influence of diet on hormone metabolite levels. Annals of the New York Academy of Sciences 2005, 1046:35-53.
30. Graham L., Schwarzenberger F., Mostl E., Galama W., Savage A. A versatile enzyme immunoassay for the determination of progestogens in feces and serum. Zoo Biology 2001, 20:227-236.
31. Gregory L.F., Schmid J.R. Stress responses and sexing of wild Kemp's ridley sea turtles (Lepidochelys kempii) in the Northeastern Gulf of Mexico. General and Comparative Endocrinology 2001, 124:66-74.
32. Kirkpatrick J., Bancroft K., Kincy V. Pregnancy and ovulation detection in bison (Bison bison) assessed by means of urinary and fecal steroids. Journal of Wildlife Diseases 1992, 28:590-597.
33. Kouba A.J., Vance C.K., Willis E.L. Artificial fertilization for amphibian conservation: Current knowledge and future considerations. Theriogenology 2009, 71:214-227.
34. Lance V.A., Elsey R.M. Stress-induced suppression of testosterone secretion in male alligators. Journal of Experimental Zoology 1986, 239:241-246.
35. Licht P., McCreery B., Barnes R., Pang R. Seasonal and stress related changes in plasma gonadotropins, sex steroids, and corticosterone in the bullfrog, Rana catesbeiana. General and Comparative Endocrinology 1983, 50:124-145.
36. Lukis K. Returning an endemic frog to the New Zealand mainland: transfer and adaptive management of Leiopelma pakeka at Karori Sanctuary, Wellington. Vol. MSc 2009, Victoria University of Wellington, Wellington, New Zealand, p. 135.
37. Mahmoud I.Y., Guillette L.J., McAsey M.E., Cady C. Stress-induced changes in serum testosterone, estradiol-17-beta and progesterone in the turtle, Chelydra serpentina. Comparative Biochemistry and Physiology A 1989, 93:423-427.
38. Monfort S.L. Non-invasive Endocrine Measures of Reproduction and Stress in Wild Populations. Reproductive Science and Integrated Conservation 2003, 147-165. Cambridge University Press, Cambridge, UK. W.V. Holt, A.R. Pickard, J.C. Rodger, D.E. Wildt (Eds.).
39. Morris P.J., Jackintell L.A., Alberts A.C. Predicting the gender of subadult Komodo dragons (Varanus komodoensis) using two-dimensional ultrasound imaging and plasma testosterone concentration. Zoo Biology 1996, 15:341-348.
40. Munro C., Stabenfeldt G., Cragun J., Addiego L., Overstreet J., Lasley B. Relationship of serum estradiol and progesterone concentrations to the excretion profiles of their major urinary metabolites as measured by enzyme immunoassay and radioimmunoassay. Clinical Chemistry 1991, 37:838-844.
41. Nakagawa S., Mostl E., Waas J.R. Validation of an enzyme immunoassay to measure faecal glucocorticoid metabolites from Adelie penguins (Pygoscelis adeliae): a non-invasive tool for estimating stress?. Polar Biology 2003, 26:491-493.
42. Narayan E.J., Molinia F.C., Christi K.S., Morley C.G., Cockrem J.F. Annual cycles of urinary reproductive steroid concentrations in wild and captive endangered Fijian ground frogs (Platymantis vitiana). General and Comparative Endocrinology 2009, 166:172-179.
43. Narayan E.J., Molinia F.C., Kindermann C., Cockrem J.F., Hero J. 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 2011, 174:238-245.
44. Newman D.G., Bell B.D., Bishop P.J., Burns R., Haigh A., Hitchmough R.A., Tocher M. Conservation status of New Zealand frogs, 2009. New Zealand Journal of Zoology 2010, 37:121-130.
45. Pukazhenthi B.S., Wildt D.E. Which reproductive technologies are most relevant to studying, managing, and conserving wildlife?. Reproduction, Fertility, and Development 2004, 16:33-46.
46. Rastogi R., Iela L., Delrio G., Bagnara J. Reproduction in the Mexican leaf frog Pachymedusa dacnicolor. II. The Male, General and Comparative Endocrinology 1986, 62:23-35.
47. Sharbel T.F., Green D.M. Captive maintenance of the primitive New Zealand frog, Leiopelma hochstetteri. Herpetological Review 1992, 23:77-79.
48. Szymanski D.C., Gist D.H., Roth T.L. Anuran gender identification by fecal steroid analysis. Zoo Biology 2006, 25:35-46.
49. Tell L.A., Lasley B.L. An automated-assay for fecal estrogen conjugates in the determination of sex in avian species. Zoo Biology 1991, 10:361-367.
50. Tocher M.D., Fletcher D., Bishop P.J. A modelling approach to determine a translocation scenario for the endangered New Zealand frog Leiopelma hamiltoni. Herpetological Journal 2006, 16:97-106.
51. Woolley S.C., Sakata J.T., Crews D. Evolutionary insights into the regulation of courtship behavior in male amphibians and reptiles. Physiology & Behavior 2004, 83:347-360.