Advertisement

Mammalian Biology

, Volume 72, Issue 1, pp 14–26 | Cite as

Non-invasive assessment of reproductive status in Chinese water deer (Hydropotes inermis): Correlation with sexual behaviour

  • Robert MaugetEmail author
  • Christiane Mauget
  • Gérard Dubost
  • Florence Charron
  • Aurélie Courcoul
  • Aurélie Rodier
Original investigation

Abstract

The annual reproductive cycle of Chinese water deer (Hydropotes inermis), a nearly threatened small cervid species, was studied by means of fecal steroid analysis coupled with behavioural observations. Data showed a clearly seasonal reproductive pattern. In adult males, the onset of androgen secretion, in October, was concomitant with the first manifestations of territoriality. Androgen metabolites concentrations reached significant peak values in December, when matings occurred. In mature females, there was a close synchrony in reproductive states: lactational/seasonal anoestrus from June to November, pregnancy from December to May. Fecal progesterone metabolites profiles suggested that silent ovulations occurred at the onset of breeding season and that females conceived at their first ovulation with behavioural estrus. The female sexual receptivity state might last only a few hours. High levels of sniffing, parades and pursuits, concomitant of the highest concentrations of androgen, could allow the males to detect the furtive estrus in the females present in their territory. We concluded that the non-invasive method applied for the first time in this species was useful for the evaluation of the endocrine status and its relation with behaviour.

Key words

Water deer reproduction fecal steroids 

Nicht-invasive Abschätzung des Fortpflanzungsstatus beim chinesischen Wasserreh (Hydropotes inermis): Korrelation mit Sexualverhalten

Zusammenfassung

Der jährliche Fortpflanzungszyklus chinesischer Wasserrehe (Hydropotes inermis), einer kleinen Hirschart, die beinahe als bedroht einzustufen ist, wurde mittels Analyse des Steroidinhalts im Kot zusammen mit Verhaltensbeobachtungen untersucht. Die Daten zeigten ein deutliches jahreszeitliches Fortpflanzungsmuster. Bei erwachsenen Männchen ging der Beginn der Testosteronausschüt-tungen im Oktober mit den ersten Anzeichen von Revierverhalten einher. Signifikante Höchstwerte der Testosteronkonzentrationen wurden im Dezember erreicht, als Begattungen stattfanden. Bei erwachsenen Weibchen war der Fortpflanzungsstand eng synchron: Laktation/jahreszeitlicher Anöstrus von Juni bis November, Trächtigkeit von Dezember bis Mai. Durchschnittswerte von Progesteron deuteten darauf hin, daß bei Beginn der Fortpflanzungszeit stille” Eisprünge ” stattfanden, sowie daß die Weibchen beim ersten Eisprung mit östrus trächtig wurden. Zeitweilig dauerte die weibliche Paarungswilligkeit nur wenige Stunden. Das besonders häufig beobachtete Beriechen, Imponierlaufen und Verfolgen, das gleichzeitig mit den höchsten Konzentrationen von Testosteron vorkam, hat den Männchen möglicherweise erlaubt, den verdeckten östrus bei den im Revier anwesenden Weibchen aufzuspüren. Wir folgern daraus, daß die erstmalig bei dieser Art angewandte, nicht invasive Vorgehensweise eine nützliche Methode ist zur Abschätzung des endokrinen Status und seiner Beziehung zum Verhalten.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Altmann, J. (1974): Observational study of behavior: sampling methods. Behaviour 49, 227–267.PubMedPubMedCentralCrossRefGoogle Scholar
  2. Asher, G. W.; ONeill, K. T.; Scott, I. C.; Mockett, B. G.; Fisher, M. W. (2000): Genetic influences on reproduction of female red deer (Cervus elaphus) (1) Seasonal luteal cyclicity. Anim. Reprod. Sci. 59, 43–59.PubMedCrossRefGoogle Scholar
  3. Barrette, C. (1987): The comparative behavior and ecology of chevrotains, musk deer, and morphologically conservative deer. In: Biology and Management of the Cervidae, Research Symposia of the National Zoological Park. Ed. by C. Wemmer. Washington, DC, London: Smith sonian Institution Press. Pp. 200–213.Google Scholar
  4. Berger, J.; Testa, J. W.; Roffe, T.; Monfort, S. L. (1999): Conservation endocrinology: a nonin-vasive tool to understand relationships between carnivore colonization and ecological carrying capacity. Conserv. Biol. 13, 980–989.CrossRefGoogle Scholar
  5. Blanvillain, C.; Berthier, J. L.; Bomsel-Demontoy, M. C.; Sempere, A. J.; Olbricht, G. (1997): Analysis of reproductive data and measurement of fecal progesterone metabolites to monitor the ovarian function in the Pudu, Pudu puda Artiodactyla, Cervidae. Mammalia 61, 589–602.Google Scholar
  6. Caraty, A.; Skinner, D. C. (1999): Progesterone priming is essential for the full expression of the positive feedback effect of estradiol. Endocrinology 140, 165–170.PubMedCrossRefGoogle Scholar
  7. Clutton-Brock, T. H.; Guinness, F. E.; Albon, S. D. (1982): Red Deer: Behaviour and Ecology of Two Sexes. Chicago: University of Chicago Press.Google Scholar
  8. Curlewis, J. D.; Loudon, A. S. I.; Coleman, A. P. M. (1988): Oestrous cycles and the breeding season of the Pere David’s hind (Elaphurus davidianus). J. Reprod. Fertil. 82, 119–126.PubMedCrossRefGoogle Scholar
  9. Feer, F. (1982): Some ethological observations on Hydropotes inermis (Swinhoe, 1870) in captivity. Z. Saugetierkunde 47, 175–184.Google Scholar
  10. Geist, V. (1999): Water deer. In: Deer of the World. Their Evolution Behaviour and Ecology. Ed. by V. Geist. Shrewsbury: Swan Hill Press. Pp. 26–28.Google Scholar
  11. Guan, L.; Su, T. (2004): [The resource conservation and breeding of wild Hydropotes inermis in China]. Zhong Yao Cai 27, 5–6.PubMedGoogle Scholar
  12. Hamasaki, S.; Yamauchi, K.; Ohki, T.; Murakami, M.; Takahara, Y.; Takeuchi, Y.; Mori, Y. (2001): Comparison of various reproductive status in Sika deer (Cervus nippon) using fecal steroid analysis. J. Vet. Med. Sci. 63, 195–198.PubMedCrossRefPubMedCentralGoogle Scholar
  13. Harris, S.; Morris, P.; Wray, S.; Yalden, D. (1995): A Review of British Mammals: Population Estimates and Conservation Status of British Mammals other than Cetaceans. London. J.N.N.C. Publications UK.Google Scholar
  14. Hassanin, A.; Douzery, E. J. P. (2003): Molecular and morphological phylogenies of Ruminantia and the alternative position of the Moschidae. Syst. Biol. 52, 206–228.PubMedCrossRefGoogle Scholar
  15. Hastings, B. E.; Abbott, D. E.; George, L. M.; Stadler, S. G. (1992): Stress factors influencing plasma cortisol levels and adrenal weights in Chinese water deer (Hydropotes inermis). Res. Vet. Sci. 53, 375–380.PubMedCrossRefPubMedCentralGoogle Scholar
  16. Hofmann, R. R.; Kock, R. A.; Ludwig, J.; Axmacher, H. (1988): Seasonal changes in rumen papillary development and body condition in free ranging Chinese water deer (Hydro-potes inermis). J. Zool. (London) 216, 103–117.CrossRefGoogle Scholar
  17. IUCN. (2004): The IUCN Red List of Threatened Species. Gland, Switzerland: IUCN.Google Scholar
  18. Jabbour, H. N.; Hayssen, V.; Bruford, M. W. (1997): Conservation of deer: contributions from molecular biology, evolutionary ecology, and reproductive physiology. J. Zool. (London) 243, 461–484.CrossRefGoogle Scholar
  19. Kapke, C. A.; Arcese, P.; Ziegler, T. E.; Scheffler, G. R. (1999): Estradiol and progesterone metabolite concentration in white-tailed deer (Odocoileus virginianus) feces. J. Zoo Wildl. Med. 30, 361–371.PubMedPubMedCentralGoogle Scholar
  20. Kirkwood, J. K.; Williams, P.; Moxey, T.; Wallbank, H.; Stadler, S. G.; Howlett, J.; Markham, J.; Dean, C.; Watts, E.; Eva, J. (1988): Management and formula intake of young hand-reared Chinese water deer Hydropotes inermis and their growth compared with mother-reared fawns. Internat. Zoo Yearbook 27, 308–316.CrossRefGoogle Scholar
  21. Lasley, B. L.; Kirkpatrick, J. F. (1991): Monitoring ovarian function in captive and free-ranging wildlife by means of urinary and fecal steroids. J. Zoo Wildl. Med. 22, 23–31.Google Scholar
  22. Li, C.; Jiang, Z.; Jiang, G.; Fang, J. (2001): Seasonal changes of reproductive behavior and fecal steroid concentrations in Pere David’s deer. Horm. Behav. 40, 518–525.PubMedCrossRefGoogle Scholar
  23. Li, C. W.; Jiang, Z. G.; Zeng, Y.; Yan, C. (2004): Relationship between serum testosterone, dominance and mating success in Pere David’s deer stags. Ethology 110, 681–691.CrossRefGoogle Scholar
  24. Lincoln, G. A.; Guinness, F. E.; Short, R. V. (1972): The way in which testosterone controls the social and sexual behavior of the red deer stag (Cervus elaphus). Horm. Behav. 3, 375–396.CrossRefGoogle Scholar
  25. Matsuura, Y.; Sasamoto, Y.; Sato, K.; Takahashi, Y.; Suzuki, M.; Ohtaishi, N. (2004): Monitoring ovarian cycle and conception by fecal progesterone analysis in sika deer. Ecol. Res. 19, 397–404.CrossRefGoogle Scholar
  26. Montfort, S. L.; Schwartz, C. C.; Wasser, S. K. (1993): Monitoring reproduction in captive moose using urinary and fecal steroid metabolites. J. Wildl. Manage. 57, 400–407.CrossRefGoogle Scholar
  27. Montfort, S. L.; Wemmer, C.; Kepler, T. H.; Bush, M.; Brown, J. L.; Wildt, D. E. (1990): Monitoring ovarian function and pregnancy in Eld’s deer (Cervus eldi thamin) by evaluating urinary steroid metabolite excretion. J. Reprod. Fertil. 88, 271–281.CrossRefGoogle Scholar
  28. Morrow, C. J.; Asher, G. W.; Smith, J. F.; Jabbour, H. N.; Mulley, R. C.; McLeay, L. M. (1982): Seasonal effects on the efficacy of intravaginal CIDR devices for oestrous synchronization of farmed fallow deer (Dama dama). Proc. New Zealand Soc. Animal Prod. 52, 165–170.Google Scholar
  29. Oldham, C. M.; Lindsay, D. R. (1980): Laparo-scopy in the ewe: a photographic record of the ovarian activity of ewes experiencing normal or abnormal oestrous cycles. Anim. Reprod. Sci. 3, 119–124.CrossRefGoogle Scholar
  30. Palme, R.; Fischer, P.; Schildorfer, H.; Ismail, M. N. (1996): Excretion of infused 14C-steroid hormones via faeces and urine in domestic livestock. Anim. Reprod. Sci. 43, 43–63.CrossRefGoogle Scholar
  31. Pereira, R. J. G.; Duarte, J. M. B.; Negrao, J. A. (2005): Seasonal changes in fecal testosterone concentrations and their relationship to the reproductive behavior, antler cycle and grouping patterns in free-ranging male Pampas deer (Ozotoceros bezoarticus bezoarticus). Therio-genology 63, 2113–2125.CrossRefGoogle Scholar
  32. Plotka, E.; Seal, U.; Verme, L.; Ozoga, J. (1983): The adrenal gland in white-tailed deer: a significant source of progesterone. J. Wildl. Manage. 47, 38–44.CrossRefGoogle Scholar
  33. Randi, E.; Mucci, N.; Pierpaoli, M.; Douzery, E. J. P. (1998): New phylogenetic perspectives on the Cervidae (Artiodactyla) are provided by the mitochondrial cytochrome b gene. Proc. R. Soc. London B: Biol. Sci. 265, 793–801.CrossRefGoogle Scholar
  34. Scherpe, W. P. (1971). Beobachtungen am Verhalten des chinesischen Wasserrehs (Hydropotes inermis, Swinhoe) des indischen Muntjaks (Muntiacus muntjak muntjak, Zimmermann) und des chinesischen Muntjaks (Muntiacus muntjak reevesi, Ogilby). Diss. thesis, Veteri-narmedizin, Freien Universitat Berlin.Google Scholar
  35. Schwarzenberger, F.; Mostl, E.; Palme, R.; Bamberg, E. (1996): Faecal steroid analysis for non-invasive monitoring of reproductive status in farm, wild and zoo animals. Anim. Reprod. Sci. 42, 515–526.CrossRefGoogle Scholar
  36. Schwarzenberger, F.; Patzl, M.; Francke, R.; Ochs, A.; Buiter, R.; Schaftenaar, W.; De Meurichy, W. (1993): Fecal progestagen evaluations to monitor the estrous cycle and pregnancy in the Okapi (Okapia johnstoni). Zoo Biol. 12, 549–559.CrossRefGoogle Scholar
  37. Sheng, H.; Ohtaishi, N. (1993): The status of deer in China. In: Deer of China. Ed. by N. Ohtaishi, H. Sheng. Amsterdam: Elsevier Science Publishers B.V.. Pp. 1–11.Google Scholar
  38. Stadler, S. G. (1991). Behaviour and social organisation of Chinese water deer (Hydropotes inermis) under semi-natural conditions. Diss. thesis, Universitat Bielefeld, Germany.Google Scholar
  39. Stoops, M. A.; Anderson, G. B.; Lasley, B. L.; Shideler, S. E. (1999): Use of fecal steroid metabolites to estimate the pregnancy rate of a free-ranging herd of tule elk. J. Wildl. Manage. 63, 561–569.CrossRefGoogle Scholar
  40. Sun, L. (2002): Anti-predation does not fully explain grouping in the Chinese water deer (Hydropotes inermis). Acta Zool. Sinica 48, 302–308.Google Scholar
  41. Sun, L.; Dai, N. (1995): Male and female association and mating system in the Chinese water deer (Hydropotes inermis). Mammalia 59, 171–178.CrossRefGoogle Scholar
  42. Sun, L.; Xiao, B. (1995): The effect of female distribution on male territoriality in Chinese water deer (Hydropotes inermis). Z. Saugetierkunde 60, 33–40.Google Scholar
  43. Thibier, M.; Pothelet, D.; Jean Guyot, N.; De Montiguy, G. (1981): Estrous behavior, progesterone in peripheral plasma and milk in dairy goats at onset of breeding season. J. Dairy Sci. 64, 513–519.PubMedCrossRefGoogle Scholar
  44. Ward, A. I. (2005): Expanding ranges of wild and feral deer in Great Britain. Mammal Rev. 35, 165–173.CrossRefGoogle Scholar
  45. Wang, S. (1998): China Red Data Book of Endangered Animals (Mammalia). Beijing: Science Press.Google Scholar
  46. Welsh, T. J.; Johnson, B. (1981): Stress-induced alterations in secretion of corticosteroids, progesterone, luteinizing hormone, and testosterone in bulls. Endocrinology 109, 185–190.PubMedCrossRefGoogle Scholar
  47. Wildt, D. E.; Wemmer, C. M. (1999): Sex and wildlife: the role of reproductive science in conservation. Biodiv. Conserv. 8, 965–976.CrossRefGoogle Scholar
  48. Wingfield, J. C.; Hegner, R. E.; Dufty, A. M. J.; Ball, G. F. (1990): The “challenge hypothesis”: theoretical implications for patterns of testosterone secretion, mating systems and breeding strategies. Am. Nat. 136, 829–846.CrossRefGoogle Scholar
  49. Yamauchi, K.; Hamasaki, S.; Takeuchi, Y.; Mori, Y. (1997): Assessment of reproductive status of Sika deer by fecal steroid analysis. J. Reprod. Dev. 43, 221–226.CrossRefGoogle Scholar
  50. Zhang, E. (1998a): Chinese water deer, Hydropotes inermis. In: Deer, Status Survey and Conservation Action Plan. Ed. by C. Wemmer. Gland, Switzerland, and Cambridge, UK: IUCN/SSC Deer Specialist Group. Pp. 69–70.Google Scholar
  51. Zhang, E. (1998b): Uniparental female care in the Chinese water deer at Whipsnade Wild Animal Park, England. Acta Theriol. Sinica 18, 173–183.Google Scholar
  52. Zhang, E. (2000): Daytime activity budgets of the Chinese water deer. Mammalia 64, 163–172.CrossRefGoogle Scholar
  53. Zhu, H.; Qin, P.; Wang, H. (2004): Functional group classification and target species selection for Yancheng Nature Reserve, China. Biodiv. Conserv. 13, 1335–1353.CrossRefGoogle Scholar

Copyright information

© Deutsche Gesellschaft für Säugetierkunde 2006

Authors and Affiliations

  • Robert Mauget
    • 1
    Email author
  • Christiane Mauget
    • 1
  • Gérard Dubost
    • 1
  • Florence Charron
    • 1
  • Aurélie Courcoul
    • 1
  • Aurélie Rodier
    • 1
  1. 1.Muséum National d’Histoire NaturelleCNRS-UMR 5173/MNHN-USM 305, Conservation des Espèces, Restauration et Suivi et des Populations, Ménagerie du Jardin des PlantesParis Cedex 05France

Personalised recommendations