Reproductive problems directly attributable to long-term captivity--asymmetric reproductive aging
Abstract
Problems attributable to long-term captivity have been identified and are responsible for the difficulties in establishing successful reproduction in captive populations of wildlife, specifically, elephants and rhinoceroses. Historically, non-reproductive periods of 10-15 years in nulliparous female rhinoceroses and elephants have not been considered problematic. New evidence suggests that prolonged exposure to endogenous sex steroids and that long stretches of non-reproductive periods induce asymmetric reproductive aging in captive animals. The consequences are reduced fertility, shortened reproductive life-span and, eventually, irreversible acyclicity. Although age-related reproductive lesions have also been documented in male rhinoceroses, they continue to maintain a longer reproductive life-span than females. Since human and domestic animal models have already indicated that early pregnancy provides natural protective mechanism against asymmetric reproductive aging processes and premature senescence, it is imperative that appropriate counter measures such as assisted reproductive technologies (ART) be utilized to ensure early pregnancy in captive animals for their preservation and to ensure increased genetic diversity of the captive populations.
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BackgroundSelf-citationLudwig, C., Wachter, B., Silinski-Mehr, S., Ganswindt, A., Bertschinger, H. J., Hofer, H., & Dehnhard, M. (2012) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2012.10.005 · Cited by 36 · see citing works
“In captivity, females often start to reproduce later than in the wild which diminishes their reproductive performance, as also found in other species [11,12].”
BackgroundTHITARAM, C. (2012) · Japanese Journal of Zoo and Wildlife Medicine · doi:10.5686/jjzwm.17.91 · Cited by 34 · see citing works
Enhancing captive Indian rhinoceros genetics via artificial insemination of cryopreserved sperm
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Proctor, C. M., Freeman, E. W., & Brown, J. L. (2009) · Zoo Biology · doi:10.1002/zoo.20238 · Cited by 31 · see citing works
Reproductive Tract Tumours: The Scourge of Woman Reproduction Ails Indian Rhinoceroses
Hermes, R. E., Göritz, F., Saragusty, J., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0092595 · Cited by 29 · see citing works
“In rhinocerotidae, leiomyomata were reported in individual white (Ceratotherium simum), Sumatran, and Indian rhinoceroses [13,31,41–43].”
Self-citationFarquharson, K., Hogg, C., & Grueber, C. (2017) · Journal of Heredity · doi:10.1093/jhered/esx030 · Cited by 28 · see citing works
“Long non-reproductive periods have also been seen to reduce fertility and shorten the reproductive life of captive elephants and rhinoceroses (Hermes et al. 2004), suggesting the generality of this pattern, in mammals at least.”
BackgroundManaged wildlife breeding-an undervalued conservation tool?
Lüeders, I., & Allen, W. R. T. (2020) · Theriogenology · doi:10.1016/j.theriogenology.2020.01.058 · Cited by 31 · see citing works
Boedeker, N. C., Hayek, L. C., Murray, S. Z., de Avila, D. M., & Brown, J. L. (2012) · Journal of Zoo and Wildlife Medicine · doi:10.1638/2011-0270.1 · Cited by 29 · see citing works
“Because older cycling cows appear to be particularly susceptible, it has been speculated that continuous steroid hormone (estrogens and/or progestagens) exposure associated with ovarian cyclicity of nonbred females has a negative and cumulative effect on reproductive health and urogenital tract integrity.(1,24,28) To…”
BackgroundCollection planning for the next 100 years: What will we commit to save in zoos and aquariums?
Powell, D. (2018) · Zoo Biology · doi:10.1002/zoo.21453 · Cited by 25 · see citing works
Monitoring and controlling ovarian function in the rhinoceros
Roth, T. L., Schook, M. W., & Stoops, M. A. (2017) · Theriogenology · doi:10.1016/j.theriogenology.2017.12.007 · Cited by 24 · see citing works
Zywitza, V., Frahm, S., Krüger, N., Weise, A., Göritz, F., Hermes, R. E., Holtze, S., Colleoni, S., Galli, C., Drukker, M., et al. (2022) · iScience · doi:10.1016/j.isci.2022.105414 · Cited by 24 · see citing works
“development of reproductive tract pathologies as a result of repeated ovarian cycling activity due to the absence of naturally occurring long acyclic gestation and lactation phases.(3) Reintroduction of genetic material is crucial to support a healthy and self-sustaining SR population.”
Self-citationFacilitating the social behaviour of bull elephants in zoos
Hartley, M., Wood, A., & Yon, L. (2019) · International Zoo Yearbook · doi:10.1111/izy.12245 · Cited by 24 · see citing works
Update on Comparative Biology of Elephants: Factors Affecting Reproduction, Health and Welfare
Brown, J. L. (2019) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-23633-5_9 · Cited by 22 · see citing works
Estrus induction in white rhinoceros (Ceratotherium simum)
Hermes, R. E., Hildebrandt, T. B., Walzer, C., et al. (2012) · Theriogenology · doi:10.1016/j.theriogenology.2012.05.015 · Cited by 23 · see citing works
“Ultrasonography of the eproductive tract in aged females, 15 yr of age, evealed that long non-reproductive periods were assoiated with extensive pathologies limiting or even exluding successful reproduction [4,6].”
BackgroundSelf-citationScheun, J., Nowack, J., Bennett, N. C., & Ganswindt, A. (2015) · Journal of Comparative Physiology B · doi:10.1007/s00360-015-0947-z · Cited by 23 · see citing works
Proctor, C. M., Freeman, E. W., & Brown, J. L. (2009) · Zoo Biology · doi:10.1002/zoo.20292 · Cited by 20 · see citing works
Sperm sex-sorting in the Asian elephant (Elephas maximus)
Hermes, R. E., Behr, B., Hildebrandt, T. B., et al. (2008) · Animal Reproduction Science · doi:10.1016/j.anireprosci.2008.05.007 · Cited by 21 · see citing works
“But, as particularly in slow reproducing species, females are the limiting factor concerning the effort to enlarge the captive population, and are greatly affected by an asymmetric aging process (Hermes et al., 2004; Faust et al., 2006), it is rather more important to breed female offspring.”
BackgroundSelf-citationProspects for managing African elephant population growth by immunocontraception: a review
Perdok, A. A., de Boer, W. F., & Stout, T. A. E. (2007) · Pachyderm · doi:10.69649/pachyderm.v42i.115 · Cited by 21 · see citing works
“Moreover, even if vaccination does not directly damage the ovaries, there are indications that long non-reproductive periods may accelerate the onset of reproductive senescence in elephant cows (Hermes et al. 2004).”
BackgroundBiasetti, P., Hildebrandt, T. B., Göritz, F., Hermes, R. E., Holtze, S., Galli, C., Lazzari, G., Colleoni, S., Pollastri, I., Spiriti, M. M., et al. (2022) · Frontiers in Veterinary Science · doi:10.3389/fvets.2022.831675 · Cited by 20 · see citing works
“Given the particular vulnerability of captive female rhinoceros to reproductive tract pathologies, such as tumors (42, 94, 96, 97), this is not an aspect to consider lightly.”
BackgroundSelf-citationFreeman, E. W., Schulte, B. A., & Brown, J. L. (2009) · Zoo Biology · doi:10.1002/zoo.20235 · Cited by 20 · see citing works
Ultrasonography: an important tool in captive breeding management in elephants and rhinoceroses
Hildebrandt, T. B., Göritz, F., & Hermes, R. E. (2005) · European Journal of Wildlife Research · doi:10.1007/s10344-005-0012-4 · Cited by 20 · see citing works
“It is now known that the incidence of these reproductive disorders increases with age and is greater in nulliparous than in similarly aged parous individuals (Hermes et al. 2004; Hildebrandt et al. 2000b).”
Self-citationFreeman, E. W., Meyer, J. M., Putman, S. B., Schulte, B. A., & Brown, J. L. (2013) · Conservation Physiology · doi:10.1093/conphys/cot025 · Cited by 20 · see citing works
“Hermes et al. (2004) referred to the decline in zoo elephant reproductive function as asymmetric or premature reproductive ageing.”
Backgroundde Mori, B., Spiriti, M. M., Pollastri, I., Normando, S., Biasetti, P., Florio, D., Andreucci, F., Colleoni, S., Galli, C., Göritz, F., et al. (2021) · Animals · doi:10.3390/ani11020312 · Cited by 20 · see citing works
Self-citationKretzschmar, P., Kramer‐Schadt, S., Ambu, L. N., Bender, J., Bohm, T., Ernsing, M., Göritz, F., Hermes, R. E., Payne, J., Schaffer, N. E., et al. (2016) · Global Ecology and Conservation · doi:10.1016/j.gecco.2016.02.006 · Cited by 19 · see citing works
Self-citationEdwards, K. L., Trotter, J., Jones, M., Brown, J. L., Steinmetz, H. W., & Walker, S. L. (2016) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2015.09.011 · Cited by 18 · see citing works
“…with irregular reproductive cyclicity, asymmetric reproductive ageing, reduced survivorship, high infant mortality and insufficient breeding males amongst the issues being reported (Brown et al., 2004b; Clubb and Mason, 2002; Clubb et al., 2008, 2009; Hermes et al., 2004; Hutchins and Keele, 2006).”
BackgroundInfluentialWeighing the options for limiting surplus animals
Asa, C. (2016) · Zoo Biology · doi:10.1002/zoo.21293 · Cited by 18 · see citing works
Behr, B., Rath, D., Mueller, P., et al. (2009) · Theriogenology · doi:10.1016/j.theriogenology.2009.03.001 · Cited by 18 · see citing works
“In addition, sex-preselection by sperm sorting has the potential to offset breeding losses from premature female aging [4] and to balance skewed sex ratios in the black [5,6] and Indian rhinoceros [7,8].”
BackgroundSelf-citationRoth, T. L. (2023) · Theriogenology Wild · doi:10.1016/j.therwi.2023.100065 · Cited by 17 · see citing works
Hermes, R. E., Schwarzenberger, F., Göritz, F., et al. (2016) · PLoS ONE · doi:10.1371/journal.pone.0157963 · Cited by 17 · see citing works
Self-citationPinya, S., Renga, E., Fernández, G., Mateu‐Vicens, G., Tejada, S., Capó, X., & Sureda, A. (2020) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2020.143930 · Cited by 17 · see citing works
Wilson, M., Hermes, R. E., Bainbridge, J., et al. (2010) · Journal of Zoo and Wildlife Medicine · doi:10.1638/2009-0128.1 · Cited by 17 · see citing works
“The use of ultrasonography in recent years as an aid to captive breeding programs has greatly enhanced scientific knowledge of age-related changes in the white rhinoceros uterus.(2,3,4,5,9,11) The most common uterine pathology documented in the white rhinoceros is endometrial hyperplasia, and it has been described wit…”
BackgroundMethodInfluentialSelf-citationSchulman, M. L., Kirberger, R. M., Tordiffe, A. S. W., et al. (2015) · Theriogenology · doi:10.1016/j.theriogenology.2015.08.011 · Cited by 16 · see citing works
Black rhino conservation in Tanzania: translocation efforts and further challenges
Fyumagwa, R., & Nyahongo, J. W. (2010) · Pachyderm · doi:10.69649/pachyderm.v47i.212 · Cited by 16 · see citing works
“Permanent infertility brought about by such damage is called ‘Asymmetric Reproductive Aging’ (Hermes et al. 2004).”
BackgroundStoops, M. A., West, G. D., Roth, T. L., et al. (2013) · Zoo Biology · doi:10.1002/zoo.21106 · Cited by 16 · see citing works
“Many reproductive problems in captive female rhinoceroses are directly attributed to prolonged periods of estrous cyclicity without breeding and/or pregnancy [Jones, 1979; Hermes et al., 2004, 2006].”
BackgroundPrado, N. A., Malloy, E. J., Deng, X., & Brown, J. L. (2013) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2013.03.035 · Cited by 16 · see citing works
Schulte, B. A. (2006) · Wiley eBooks · doi:10.1002/9780470344484.ch4 · Cited by 16 · see citing works
Toin, P., Brown, J. L., Punyapornwithaya, V., Bansiddhi, P., Somgird, C., & Thitaram, C. (2020) · Animal Reproduction Science · doi:10.1016/j.anireprosci.2020.106606 · Cited by 15 · see citing works
Factors impacting the success of post-mortem sperm rescue in the rhinoceros
Roth, T. L., Stoops, M. A., Robeck, T. R., et al. (2016) · Animal Reproduction Science · doi:10.1016/j.anireprosci.2016.01.019 · Cited by 15 · see citing works
Doyle, C., Rally, H., O’Brien, L., Tennison, M., Marino, L., & Jacobs, B. (2024) · PeerJ · doi:10.7717/peerj.18161 · Cited by 14 · see citing works
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Pringproa, K., Madarame, H., Sritun, J., et al. (2015) · The Thai Journal of Veterinary Medicine · doi:10.56808/2985-1130.2648 · Cited by 14 · see citing works
“In the large mega-herbivores like elephants and rhinoceroses, uterine leiomyoma is usually associated with age and non-reproductive status in which the cystic uterine hyperplasia might also occur with leiomyomas (Hermes et al., 2004; Hildebrandt et al., 2006).”
BackgroundSchmitt, D. L. (2006) · doi:10.1002/9780470344484.ch26 · Cited by 14 · see citing works
Heidegger, E. M., von Houwald, F., Steck, B. L., et al. (2016) · Zoo Biology · doi:10.1002/zoo.21307 · Cited by 13 · see citing works
Circus Animal Welfare: analysis through a five-domain approach
Mota‐Rojas, D., Ghezzi, M. D., Domínguez-Oliva, A., Vega, L. T. D. L., Boscato-Funes, L., Torres-Bernal, F., & Mora‐Medina, P. (2022) · Journal of Animal Behaviour and Biometeorology · doi:10.31893/jabb.22021 · Cited by 14 · see citing works
“In female elephants, this has been associated with stress, reproductive tumors, and cystic hyperplasia that can lead to reproductive aging and a gradual loss of fertility (Agnew et al 2004; Hermes et al 2004).”
BackgroundEndometrial Polyp in an African Wild Dog (Lycaon pictus)
Cho, H. S., & Park, N. Y. (2006) · Zentralblatt für Veterinärmedizin Reihe A · doi:10.1111/j.1439-0442.2006.00873.x · Cited by 12 · see citing works
Autoimmune abnormality affects ovulation and oocyte-pick-up in MRL/MpJ-Fas lpr/lpr mice
Hosotani, M., Ichii, O., Nakamura, T., et al. (2017) · Lupus · doi:10.1177/0961203317711772 · Cited by 12 · see citing works
Monitoring and controlling ovarian activity in elephants
Thitaram, C., & Brown, J. L. (2017) · Theriogenology · doi:10.1016/j.theriogenology.2017.12.009 · Cited by 12 · see citing works
Advanced assisted reproduction technologies in endangered mammalian species
Hildebrandt, T. B., & Holtze, S. (2024) · Reproduction in Domestic Animals · doi:10.1111/rda.14700 · Cited by 13 · see citing works
Self-citationThe Effect of Size on Postrelease Survival of Head-Started Mojave Desert Tortoises
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“Reducing time spent in captivity may also hold physiological benefits, in addition to saving limited conservation dollars (Warkentin and West 1990; Hermes et al. 2004; de Assis et al. 2015).”
BackgroundJenikejew, J., Wauters, J., Dehnhard, M., & Scheumann, M. (2021) · Conservation Physiology · doi:10.1093/conphys/coab026 · Cited by 11 · see citing works
“Despite long-standing research on reproduction and husbandry as well as intensive breeding efforts, the European WR population in captivity still experiences low reproductive rates and, hence, remains not self-sustaining (Hermes et al., 2004; Swaisgood et al., 2006; van der Goot, 2015; Versteege, 2018).”
BackgroundFlacke, G. L., Schwarzenberger, F., Penfold, L. M., Walker, S. L., Martin, G. B., Millar, R. P., & Paris, M. C. J. (2017) · Theriogenology · doi:10.1016/j.theriogenology.2017.07.017 · Cited by 11 · see citing works
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Ultrasonographically documented early pregnancy loss in an Asian elephant (Elephas maximus)
Lüeders, I., Drews, B., Niemuller, C., et al. (2010) · Reproduction Fertility and Development · doi:10.1071/rd09305 · Cited by 11 · see citing works
“Leiomyomas, benign tumours of the smoothmuscle tissue of themyometrium, are known to occur typically in aged Asian elephants (‘asymmetric reproductive ageing’) and its ultrasonographic appearance is pathognomic (Hildebrandt and Goeritz 1995; Montali et al. 1997; Hildebrandt et al. 2000a; Hermes et al. 2004).”
BackgroundSelf-citationReproductive and Diagnostic Ultrasonography
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Self-citationSexual maturation in the sumatran rhinoceros (Dicerorhinus sumatrensis)
Roth, T. L., Reinhart, P. R., Romo, J. S., et al. (2013) · Zoo Biology · doi:10.1002/zoo.21089 · Cited by 10 · see citing works
“, 2001] indicating that this species, like many others in captivity, can lose its fertility to reproductive pathology that develops in females maintained for an extended period in a non‐pregnant state [Hermes et al., 2004; Roth, 2006].”
BackgroundHartman, M. J., Monnet, E. L., Kirberger, R. M., et al. (2015) · Journal of Zoo and Wildlife Medicine · doi:10.1638/2015-0109.1 · Cited by 10 · see citing works
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Cloning the Mammoth: A Complicated Task or Just a Dream?
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Powell, D., Beetem, D., Breitigan, R., Eyres, A., & Speeg, B. (2023) · Zoo Biology · doi:10.1002/zoo.21772 · Cited by 8 · see citing works
- Authors
- Hermes, R., Hildebrandt, T. B., & Göritz, F.
- Affiliations
- Leibniz Institute for Zoo and Wildlife Research (DE)
- Corresponding author
- Hermes, R
- Venue
- Animal Reproduction Science
- Publisher
- Elsevier BV
- Published
- 2004-07
- Volume
- 82-83
- Pages
- 49-60
- ISSN
- 0378-4320 (ISSN-L)
- OpenAlex
- W2106762429
- Semantic Scholar
- 64eb615875c8e2c567878d25bc1c60ce670828b7
- Cited by
- 155
- References
- 35
- Citations by year
- 2026: 5 · 2025: 4 · 2024: 9 · 2023: 7 · 2022: 7 · 2021: 6 · 2020: 9 · 2019: 5 · 2018: 9 · 2017: 9 · 2016: 9 · 2015: 8 · 2014: 9 · 2013: 7 · 2012: 11
- FWCI
- 1.13
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Animal Reproduction Science (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Agronomy and Crop Science › Reproductive Physiology in Livestock
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Reproductive Biology and Fertility
- Health Sciences › Medicine › Reproductive Medicine › Sperm and Testicular Function
- Keywords
- elephants, rhinoceros, reproductive aging, reproductive period, acyclicity, assisted reproduction, genetic diversity
- MeSH terms
- Aging, Animals, Animals, Zoo, Elephants, Female, Infertility, Male, Perissodactyla, Pregnancy, Reproduction, Estrous Cycle
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