Reproductive endocrinology of zoo-housed aardwolves

• Autorzy: Marneweck D. G. , Ganswindt A. , Rhodes S. , Bellem A. , Bryant J. , Wielebnowski N. , Dalerum F.
• Języki publikacji: EN

Abstrakty

EN

Knowledge regarding the relationship between endocrine parameters and reproductive activity can offer important insights into how social and environmental factors influence the reproductive success of mammals. Although components of both the physical and social environment affect endocrine regulation of reproduction, less is understood about the potential role of interactions between different endocrine axes on reproductive activity. We evaluated temporal patterns of reproductive and adrenocortical steroids in two male and three female aardwolves (Proteles cristata) housed in captivity at Brookfield Zoo, Chicago, IL, USA. We found seasonal variation in faecal androgens, estrogens, and progestagens, which provide support for previous observations of the aardwolf as a seasonal breeder. However, the timing of peak endocrine activity did not correspond to observations from wild populations. Our interpretation is that this discrepancy is caused by photoperiodic regulation of reproductive activity. We found a positive relationship between faecal androgens and faecal glucocorticoid metabolites in males and a positive relationship between faecal estrogens and faecal glucocorticoid metabolites in females when housed with conspecifics but not when housed alone. We also found a positive but asymptotic relationship between faecal progestagens and faecal glucocorticoid metabolites. We argue that these observations indicate a potential effect of reproductive endocrine activity on the hypothalamic–pituitary–adrenal axis, which could result in interesting physiological trade-offs in male reproductive tactics and female pre-partum maternal investment because of the negative effects of long-term glucocorticoid elevation on reproductive performance. Finally, our results suggest that social and environmental factors interact in regulating many aspects of endocrine fluctuations in this mostly solitary species.

• Wydawca: -
• Czasopismo: Acta Theriologica
• Rocznik: 2013
• Tom: 58
• Numer: 2
• Opis fizyczny: p.223-232,fig.,ref.

Twórcy

autor

Marneweck D. G.

• Department of Zoology and Entomology, Mammal Research Institute, University of Pretoria, Private Bag X20, Pretoria 0028, South Africa

autor

Ganswindt A.

• Department of Zoology and Entomology, Mammal Research Institute, University of Pretoria, Private Bag X20, Pretoria 0028, South Africa
• Department of Production Animal Studies, Faculty of Veterinary Science, University of Pretoria, Private Bag X04, Onderstepoort 0110, South Africa

autor

Rhodes S.

• Animal Programs, Chicago Zoological Society, 3300 Golf Road, Brookfield, IL 60513, USA

autor

Bellem A.

• Department of Conservation Science, Chicago Zoological Society, 3300 Golf Road, Brookfirld, IL 60513, USA

autor

Bryant J.

• Department of Conservation Science, Chicago Zoological Society, 3300 Golf Road, Brookfirld, IL 60513, USA

autor

Wielebnowski N.

• Department of Conservation Science, Chicago Zoological Society, 3300 Golf Road, Brookfirld, IL 60513, USA
• Ocegon Zoo, 4001 SW Canyon Road, Portland, OR 97221, USA

autor

Dalerum F.

• Centre for Wildlife Management, Hatfield Experimental Farm, Unievrsity of Pretoria, Private Bag. X20, Pretoria 0028, South Africa

Bibliografia

• Atsalis S, Margulis S, Bellem A, Wielebnowski N (2004) Sexual behavior and hormonal estrus cycles in captive aged lowland gorillas (Gorilla gorilla). Am J Primatol 62:123–132
• Bekoff M (1972) The development of social interaction, play, and metacommunication in mammals: an ethological perspective. Quart Rev Biol 47:412–434
• Blanchard RJ, McKittrick CR, Blanchard DC (2001) Animal models of social stress: effects on behaviour and brain neurochemical systems. Physiol Behav 73:261–271
• Brown JL (2006) Comparative endocrinology of domestic and nondomestic felids. Theriogenology 66:25–36
• Brown JL, Bellem AC, Fouraker M, Wildt DE, Roth TL (1994) Comparative analysis of gonadal and adrenal activity in the black and white rhinoceros in North America by noninvasive endocrine monitoring. Zoo Biol 20:463–486
• Carlstead K (1996) Effects of captivity on the behaviour of wild mammals. In: Kleiman DG, Allen ME, Thompson KV, Lumpkin S (eds) Wild mammals in captivity. University of Chicago Press, Chicago, pp 317–333
• deCatanzaro D, Muir C, Beaton E, Jetha M, Nadella K (2003) Enzyme immunoassay of oestradiol, testosterone and progesterone in urine samples from female mice before and after insemination. Reproduction 126:407–414
• Dloniak SM, French JA, Place NJ, Weldele ML, Glickman SE, Holekamp KE (2004) Non-invasive monitoring of fecal androgens in spotted hyenas (Crocuta crocuta). Gen Comp End 135:51–61
• Dloniak SM, French JA, Holekamp KE (2006a) Rank-related maternal effects of androgens on behaviour in wild spotted hyenas. Nature 440:1190–1193
• Dloniak SM, French JA, Holekamp KE (2006b) Faecal androgen concentrations in adult male spotted hyaenas, Crocuta crocuta, reflect interactions with socially dominant females. Anim Behav 71:27–37
• Dobson H, Smith RF (2000) What is stress, and how does it affect reproduction? Anim Repr Sci 60–61:743–752
• Estep DQ, Dewsbury DA (1996) Mammalian reproductive behavior. In: Kleiman DG, Allen ME, Thompson KV, Lumpkin S (eds) Wild mammals in captivity. University of Chicago Press, Chicago, pp 379–389
• Fanson KV, Wielebnowski NC, Shenk TA, Jakubas WJ, Squires JR, Lucas JR (2010a) Patterns of testicular activity in captive and wild Canada lynx (Lynx canadensis). Gen Comp End 169:210–216
• Fanson KV, Wielebnowski NC, Shenk TA, Jakubas WJ, Squires JR, Lucas JR (2010b) Patterns of ovarian and luteal activity in captive and wild Canada lynx (Lynx canadensis). Gen Comp End 169:217–224
• Fanson KV, Wielebnowski NC, Shenk TM, Lucas JR (2012) Comparative patterns of adrenal activity in captive and wild Canad lynx (Lynx Canadensis). J Comp Phys B 182:157–165
• Fuller G, Margulis SG, Santymire R (2009) The effectiveness of indigestible markers for identifying individual animal feces and their prevalence of use in North American zoos. Zoo Biol 30:379–398
• Ganswindt A, Muenscher S, Henley M, Henley S, Heistermann M, Palme R, Thompson P, Bertschinger H (2010) Endocrine correlates of musth and the impact of ecological and social factors in free-ranging African elephants (Loxodonta africana). Horm Behav 57:506–510
• Ganswindt A, Muijlwijk C, Engelkes M, Muenscher S, Bertschinger H, Paris M, Palme R, Cameron EZ, Bennett NC, Dalerum F (2012) Validation of non-invasive monitoring of adrenocortical endocrine activity in ground feeding aardwolves (Proteles cristata); exemplifying the influence of consumption of inorganic material for fecal steroid analysis. Phys Biochem Zool 85:194–199
• Goldman BD (1999) The circadian timing system and reproduction in mammals. Steroids 64:679–685
• Goymann W, East WL, Wachter B, Höner OP, Möstl E, Van’t Hof TJ, Hofer H (2001) Social, state dependent and environmental modulation of faecal glucocorticoid levels in free ranging female spotted hyenas. Proc Roy Soc B 268:2453–2459
• Graham L, Schwarzenberger F, Möstl E, Galama W, Savage A (2001) A versatile enzyme immunoassay for the determination of progestogens in feces and serum. Zoo Biol 20:227–236
• Hesterman H, Wasser SK, Cochrem JF (2005) Longitudinal monitoring of fecal testosterone in male Malayan sun bears (U. malayanus). Zoo Biol 24:403–417
• Kraaijeveld-Smit FJL, Ward SJ, Temple-Smith PD, Paetkau D (2002) Factors influencing paternity success in Antechinus agilis: last-male sperm precedence, timing of mating and genetic compatibility. J Evol Biol 15:100–107
• Kretzschmar P, Ganslosser U, Dehnhard M (2004) Relationship between androgens, environmental factors, and reproductive behavior in male white rhinoceros (Ceratotherium simum simum). Horm Behav 45:1–9
• Lindburg DG, Fitch-Snyder H (1994) Use of behaviour to evaluate reproductive problems in captive mammals. Zoo Biol 13:433–455
• Lovic V, Gonzalez A, Madden M, Sinopoli K, Fleming AS (2006) Maternal and littermate deprivation disrupts maternal behaviour and social-learning of food preference in adulthood: Tactile stimulation, nest odor, and social rearing prevent these effects. Dev Psych 48:209–219
• Marchlewska-Koj A (1997) Sociogenic stress and rodent reproduction. Neurosc Biobehav Rev 21:699–703
• McAllan BM, Dickman CR (1985) The role of photoperiod in the timing of reproduction in the Dasyurid marsupial Antechinus stuartii. Med Biol Eff Light 453:182–204
• Meier GW (1965) Other data on the effects of social isolation during rearing upon adult reproductive behaviour in the rhesus monkey (Macaca mulatta). Anim Behav 13:228–232
• Monclus R, Palomares F, Tablado Z, Martinez-Fontúrbel A, Palme R (2009) Testing the threat-sensitive predator avoidance hypothesis: physiological responses and predator pressure in wild rabbits. Oecologia 158:615–623
• Monfort SL, Dahl KD, Czekala NM, Stevens L, Bush M, Wildt DE (1989) Monitoring ovarian function and pregnancy in the giant panda (Ailuropoda melanoleuca) by evaluating urinary bioactive FSH and steroid metabolites. J Repr Fert 85:203–212
• Monfort SL, Wasser SK, Mashburn KL, Burke M, Brewer BA, Creel SR (1997) Steroid metabolism and validation of noninvasive endocrine monitoring in the African wild dog (Lycaon Pictus). Zoo Biol 16:533–548
• Paape SR, Shille VM, Seto H, Stabenfeldt GH (1975) Luteal activity in the pseudopregnant cat. Biol Reprod 13:470–474
• Pinheiro JC, Bates DM (2000) Mixed effect models in S and S-plus. Springer Verlag, New York
• Pinheiro JC, Bates DM, DebRoy S, Sarkar D (2012). nlme: linear and nonlinear mixed effects models. R package version 3.1-104.
• Rasmussen HB, Ganswindt A, Douglas-Hamilton I, Vollrath F (2008) Endocrine and behavioural changes in male African elephants: linking hormone changes to sexual state and reproductive tactic. Horm Behav 54:539–548
• Richardson PRK (1987) Aardwolf mating system: overt cuckoldry in an apparently monogamous mammal. S Afr J Sc 83:405–410
• Rothschild DM, Serfass TL, Seddon WL, Hegde L, Fritz RS (2008) Using fecal glucocorticoids to assess stress levels in captive river otters. J Wildl Man 72:138–142
• Sapolsky RM (2002) Endocrinology of the stress response. In: Becker JB, Breedlove SM, Crews D, McCarthy M (eds) Behavioral endocrinology, 2nd edn. MIT Press, Cambridge, pp 409–450
• Schwarzenberger F (2007) The many uses of non-invasive faecal steroid monitoring in zoo and wildlife species. Int Zoo Yearb 41:52–74
• Schwarzenberger F, Möstl E, Palme R, Bamberg E (1996) Fecal steroid analysis for non-invasive monitoring of reproductive status in farm, wild and zoo animals. Anim Repr Sc 42:515–526
• Scott MP (1986) The timing and synchrony of seasonal breeding in the marsupial, Antechinus stuartii: interaction of environmental and social cues. J Mamm 67:551–560
• Tilbrook AJ, Turner AI, Clarke IJ (2000) Effects of stress on reproduction in non-rodent mammals: the role of glucocorticoids and sex differences. Rev Repr 5:105–113
• Tsutsui T, Stabenfeldt GH (1993) Biology of ovarian cycles, pregnancy and pseudopregnancy in the domestic cat. J Repr Fert 47:29–35
• Van Meter PE, French JA, Dloniak SM, Watts HE, Kolowski JM, Holekamp KE (2009) Fecal glucocorticoids reflect socio-ecological and anthropogenic stressors in the lives of wild spotted hyenas. Horm Behav 55:329–337
• Weingrill T, Gray DA, Barrett L, Henzi SP (2004) Fecal corticosteroid levels in free-ranging female chacma baboons: relationships to dominance, reproductive state and environmental factors. Horm Behav 45:259–269
• Wildt DE, Chan SYW, Seager SWJ, Chakraborty PK (1981) Ovarian activity, circulating hormones, and sexual behavior in the cat: I. Relationships during the coitus induced luteal phase and the estrous period without mating. Biol Repr 25:15–28
• Wingfield JC, Hegner RE, Dufty AM Jr, Ball GF (1990) The "challenge hypothesis": theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am Nat 136:829–846

Uwagi

Rekord w opracowaniu