PLATINUM The Journal of Threatened Taxa (JoTT) is dedicated to building evidence for conservaton globally by publishing peer-reviewed artcles OPEN ACCESS online every month at a reasonably rapid rate at www.threatenedtaxa.org. All artcles published in JoTT are registered under Creatve Commons Atributon 4.0 Internatonal License unless otherwise mentoned. JoTT allows unrestricted use, reproducton, and distributon of artcles in any medium by providing adequate credit to the author(s) and the source of publicaton.
Journal of Threatened Taxa Building evidence for conservaton globally www.threatenedtaxa.org ISSN 0974-7907 (Online) | ISSN 0974-7893 (Print) Review
Ramifications of reproductive diseases on the recovery of the Sumatran Rhinoceros Dicerorhinus sumatrensis (Mammalia: Perissodactyla: Rhinocerotidae)
Nan E. Schafer, Muhammad Agil & Zainal Z. Zainuddin
26 February 2020 | Vol. 12 | No. 3 | Pages: 15279–15288 DOI: 10.11609/jot.5390.12.3.15279-15288
For Focus, Scope, Aims, Policies, and Guidelines visit htps://threatenedtaxa.org/index.php/JoTT/about/editorialPolicies#custom-0 For Artcle Submission Guidelines, visit htps://threatenedtaxa.org/index.php/JoTT/about/submissions#onlineSubmissions For Policies against Scientfc Misconduct, visit htps://threatenedtaxa.org/index.php/JoTT/about/editorialPolicies#custom-2 For reprints, contact
The opinions expressed by the authors do not refect the views of the Journal of Threatened Taxa, Wildlife Informaton Liaison Development Society, Zoo Outreach Organizaton, or any of the partners. The journal, the publisher, the host, and the part- Publisher & Host ners are not responsible for the accuracy of the politcal boundaries shown in the maps by the authors.
Member
Threatened Taxa
Journal of Threatened Taxa | www.threatenedtaxa.org | 26 February 2020 | 12(3): 15279–15288 ISSN 0974-7907 (Online) | ISSN 0974-7893 (Print) PLATINUM OPEN ACCESS DOI: htps://doi.org/10.11609/jot.5390.12.3.15279-15288
#5390| Received 06 September 2019 | Final received 02 December 2019 | Finally accepted 04 February 2020
R e v Ramifcatons of reproductve diseases on the recovery of the i e Sumatran Rhinoceros Dicerorhinus sumatrensis w (Mammalia: Perissodactyla: Rhinocerotdae)
Nan E. Schafer 1 , Muhammad Agil 2 & Zainal Z. Zainuddin 3
1 SOS Rhino; IUCN/SSC Asian Rhino Specialist Group, 2414 Tracy Place, NW, Washington, D.C., USA. 2 Department of Clinic, Reproducton and Pathology, Faculty of Veterinary Medicine, Bogor Agricultural University; IUCN/SSC Asian Rhino Specialist Group , Jl. Agats, Kampas IPB Dramaga, Bogor 16680, Indonesia. 3 Borneo Rhino Alliance; IUCN/SSC Asian Rhino Specialist Group, c/o Fakult Sains Dan Sumbur Alam, Jalan UMS, 88400 Kota Kinabalu, Malaysia. 1 [email protected] (corresponding author), 2 [email protected], 3 [email protected]
Abstract: The Sumatran Rhinoceros Dicerorhinus sumatrensis is on the edge of extncton. The decline of this species was initally atributed to poaching and habitat loss, but evidence presented here indicates that reproductve failure has also been a signifcant cause of loss, and contnues to afect wild populatons. Indonesia’s remaining populatons of Sumatran Rhino are small and scatered, with limited access to breeding opportunites with unrelated mates. This leaves them subject to inbreeding and isolaton-induced infertlity, linked to fertlity problems analyzed here. Sumatran Rhino females in captvity showed high rates (>70%) of reproductve pathology and/or problems with concepton, which has signifcantly hindered the breeding program. Technological advances enabling examinaton immediately afer capture revealed similarly high rates and types of reproductve problems in individuals from wild populatons. The last seven Sumatran Rhino females captured were from areas with small declining populatons, and six had reproductve problems. Going forward, capturing similarly compromised animals will take up valuable space and resources needed for fertle animals. The high risk of infertlity and difculty of treatng underlying conditons, coupled with the decreasing number of remaining animals, means that the success of eforts to build a viable captve populaton will depend upon utlizing fertle animals and applying assisted reproductve techniques. Decades of exhaustve in situ surveys have not provided informaton relevant to populaton management or to ascertaining the fertlity status of individual animals. Thus the frst priority should be the capture of individuals as new founders from areas with the highest likelihood of containing fertle rhinos, indicated by recent camera trap photos of mothers with ofspring. In Sumatra these areas include Way Kambas and parts of the Leuser ecosystem.
Keywords: Extncton, isolaton-induced infertlity, pathology, reproducton.
Editor: Anonymity requested. Date of publicaton: 26 February 2020 (online & print)
Citaton: Schafer, N.E., M. Agil & Z.Z. Zainuddin (2020). Ramifcatons of reproductve diseases on the recovery of the Sumatran Rhinoceros Dicerorhinus sumatrensis (Mammalia: Perissodactyla: Rhinocerotdae). Journal of Threatened Taxa 12(3): 15279–15288. htps://doi.org/10.11609/jot.5390.12.3.15279-15288
Copyright: © Schafer et al. 2020. Creatve Commons Atributon 4.0 Internatonal License. JoTT allows unrestricted use, reproducton, and distributon of this artcle in any medium by providing adequate credit to the author(s) and the source of publicaton.
Funding: SOS Rhino.
Competng interests: The authors declare no competng interests.
For Author details, Author contributon & Bahasa Indonesia abstract see end of this artcle.
Acknowledgements: Authors would like to acknowledge the multtude of keepers, caretakers and animal managers that made this work possible.
15279 J TT Reproductve diseases in Sumatran Rhinos Schafer
INTRODUCTION
The global populaton of Sumatran Rhinoceros Dicerorhinus sumatrensis was estmated at less than 100 individuals at the Sumatran Rhino Crisis Summit of 2013. For decades, the persistent decline has been atributed to uncontrolled poaching and habitat loss. Evidence presented here, however, indicates that reproductve failure (previously only associated with captvity) is an important factor in the contnued decline of this species. The prevalence of reproductve problems across tme and landscapes indicate a need to understand the scope and nature of this failure for successful recovery. Between 1984 and 1995, a total of 41 Sumatran Rhinos were captured in Indonesia (Sumatra) and Malaysia (Peninsular and Sabah) (Rookmaaker 1998). The majority of males and females were placed in breeding facilites in each range country; three were moved to the United Kingdom and seven to the United States. At that tme, the husbandry of this species was poorly understood and insufcient knowledge about diet, habitat, social structure, matng behavior, and reproducton hampered breeding eforts. Introductons of males and females ofen led to violent responses. These husbandry gaps resulted in signifcant losses in the inital captve populaton. Improvements in diet and behavioral management addressed some of these Image 1. Analysis of reproducton in the frst captve females was challenges, yet despite breeding, females were not hampered by the lack of portable ultrasound machines. Pictured is producing ofspring. With the advent of ultrasound in Dr. Nan Schafer with an early prototype in 1998. © SOS Rhino. the 1990s, factors inhibitng concepton were revealed (Schafer et al. 1994) (Image 1). The high rate of pathologic abnormalites observed in the reproductve RESULTS tracts of female rhinos from both Indonesia and Malaysia was initally presented at the 1999 Asian Rhino Specialist This paper is based on records of female Sumatran Group Meetng, and published shortly thereafer Rhinos captured or poached from various sites in (Schafer et al. 2002). In additon, pregnancy failure was Indonesia and Malaysia between 1984 and 2018. linked to early embryonic death (Roth et al. 2001). Available records for husbandry reports, laboratory In early 2001, examinaton of a poached female results, histology, ultrasound images, and reproductve in Sabah, Malaysia signaled that the problem was not tract examinaton were compiled by Schafer (2018). exclusive to captvity (Image 2). In 2011 and 2014, two Source data and additonal details on individual animals more females examined immediately afer capture from are available on the Rhino Resource Center website. the same geographic area in Sabah presented with A summary of the data is provided in Table 1, which extreme pathologic conditons (Fiuza et al. 2015; Schafer includes animal identfcaton, approximate age, dates 2018). The Sumatran Rhino was declared extnct in the and locaton of capture, breeding facility locaton, date rainforests in Malaysia in 2015. This trend will have of death, whether the animal copulated, examinaton serious implicatons for the success of Indonesia’s 2018 results, and name of examiner. Age of adults, parous Emergency Acton Plan to build a productve captve status, and relatedness were unknown with the excepton populaton with the last Sumatran Rhinos, as set forth of one genetcally related breeding pair (Morales et below. al. 1997). Despite wide variability in parameters, the type of reproductve diseases were similar among individuals, and the rate of disease occurrence was high
15280 Journal of Threatened Taxa | www.threatenedtaxa.org | 26 February 2020 | 12(3): 15279–15288 J TT Reproductve diseases in Sumatran Rhinos Schafer L. Lowentne C. Furley Examiner N. Schafer Kretzschmar P. N. Schafer R. Radclife N. Schafer N. Schafer M. Agil N. Schafer R. Radclife R. Radclife N. Schafer C. Furley L. Lowentne Z. Zahari N. Schafer N. Schafer M. Agil N. Schafer N. Schafer R. Radclife T. Roth T. R. Radclife N. Schafer Roth T. Z. Zahari Histology Method Ultrasound Ultrasound Ultrasound Ultrasound Histology Ultrasound Ultrasound Gross Pathology Histology Histology Gross Pathology Ultrasound Histology Ultrasound Histology Ultrasound Ultrasound Ultrasound Ultrasound Ultrasound Ultrasound Gross Pathology No Records Uterine Leiomyoma (noted before death death before (noted Leiomyoma Uterine in 1994) Evidence of pathology date recorded date of pathology Evidence No Records Few uterine cysts (1998); more cysts (2004) cysts (1998); more cysts uterine Few (2010) productve Post Few, Small Uterine Tumors & cysts (1991) & cysts Tumors Small Uterine Few, Same Findings (2001) Uterine Tumors & Cysts (1991) & Cysts Tumors Uterine Multple Corpus Luteum; Enlarged Uterus Uterus Enlarged Multple Corpus Luteum; (1993) No Records No Records Uterine Cysts (1991); Large Tumor (1998); Tumor (1991); Large Cysts Uterine (2002) Cysts Tumors, Birthed SB15 (1987); Cysts (2001) Birthed SB15 (1987); Cysts Immature Reproductve Tract (1992) Tract Reproductve Immature Uterine Leiomyoma Leiomyoma Uterine Cystc endometrial hyperplasia (1995) hyperplasia endometrial Cystc No Pathology Uterine Tumor and cysts (1998) and cysts Tumor Uterine (2001) Leiomyoma Chronic Lactaton (1992-2001); Lactaton Chronic & Ovaries Uterus Irregular Uterine Tumors and cysts (1994) and cysts Tumors Uterine Uterine Cysts (1991); Tumors (2002) (1991); Tumors Cysts Uterine 5 Abortons (1998 – 2001); 3 births (2001, (2002) (resolved) 2004, 2007); Cysts Cysts (2001) Cysts Post productve (2010); productve Post (2019)? (2014); Cycling cysts Few No Pathology Unknown No Evidence of Evidence copulaton Unknown Yes Yes Yes Yes Unknown Unknown Yes Yes No No No No Yes Yes No Yes Yes Yes Yes No 4.xi.1994 Date of Date death 12.xi.1996 11.i.2014 17.xi.2003 10.vii.2002 27.vii.1993 23.xi.1986 23.i.1986 28.x.2003 12.iv.2003 10.v.1992 29.x.1986 22.ii.1995 15.xii.1989 23.viii.2000 7.ii.2001 22.xii.2005 9.xi.2003 5.ix.2009 16.xi.2003 15YRS. 23.ix.1988 25.v.1992 Port Lympne, UK Lympne, Port Captve Captve facilites Surabaya, Indonesia Surabaya, Sepilok, Sabah, Malaysia Melaka, Malaysia Melaka, Melaka, Malaysia Melaka, Taman Safari, Indonesia Safari, Taman Melaka, Malaysia & Malaysia Melaka, Thailand Bangkok, Capture Site Capture Melaka, Malaysia Melaka, Melaka, Malaysia Melaka, Los Angeles & Los Angeles USA Cincinnat, Port Lympne, UK Lympne, Port San Diego, USA San Diego, Melaka, Malaysia Melaka, Sepilok, Sabah, Malaysia Melaka, Malaysia, Malaysia, Melaka, Kambas, & Way Jakarta Indonesia Los Angeles & New & New Los Angeles USA York, Melaka, Malaysia Melaka, Los Angeles & Los Angeles USA Cincinnat, Melaka, Malaysia Melaka, Taman Safari & Way & Way Safari Taman Indonesia Kambas, Melaka, Malaysia Melaka, San Diego, USA San Diego, Adult Age at at Age capture ~4 Yrs. Adult ~8 Yrs. Adult Adult N/A Adult ~10 Yrs. Adult Juvenile Adult ~12 Yrs. Adult ~6 Yrs. ~10 Yrs. ~6 Yrs. ~5 Yrs. ~1 Yr. N/A ~3 Yrs. ~7 Yrs. ~8 Yrs. captured between 1984 and 2018 in Peninsula Malaysia; Sabah, Borneo, East Malaysia; Sumatra, Indonesia and Kalimantan, Kalimantan, and Indonesia Sumatra, Malaysia; East Borneo, Sabah, Malaysia; Peninsula in 2018 and 1984 between captured sumatrensis Dicerorhinus Merant Name Wiwien Gologob Mas Merah Jeram Dalu Melintang Riau Seputh Rima Mahato Subur Barakas Julia Lun Parai Dusun Rapunzel Panjang Emi Minah Bina Seridelima Rami 21.vii.1987 Capture date Capture 17.i.1992 17.vi.1994 26.viii.1987 30.iv.1984 8.vii.1988 18.iv.1985 23.i.1986 11.vii.1988 10.ii.1986 22.vii.1988 22.vi.1986 24.vii.1988 6.vii.1986 22.iv.1989 9.ix.1986 26.viii.1989 25.ii.1987 6.iii.1991 23.v.1987 17.v.1991 1.vii.1987 12.vi.1991 Torgamba, Indonesia Torgamba, Capture Capture locaton Bengkulu, Indonesia Bengkulu, Tabin, Malaysia Tabin, Malaysia Selangor, Malaysia Selangor, Torgamba, Indonesia Torgamba, Malaysia Torgamba, Indonesia Torgamba, Pahang, Malaysia Pahang, Johor, Malaysia Johor, Bengkulu, Indonesia Bengkulu, Torgamba, Indonesia Torgamba, Bengkulu, Indonesia Bengkulu, Selangor, Malaysia Selangor, Lahad Datu, Malaysia Lahad Datu, Malaysia Bengkulu, Indonesia Bengkulu, Selangor, Malaysia Selangor, Bengkulu, Indonesia Bengkulu, Captve Born to SB07 in Born to Captve Malaysia Melaka, Bengkulu, Indonesia Bengkulu, Selangor, Malaysia Selangor, Bengkulu, Indonesia Bengkulu, 18 34 40 19 01 22 03 05 23 07 24 10 25 11 26 12 27 13 29 15 32 16 33 Stud Book # Table 1. Details of the female Sumatran rhinoceros rhinoceros Sumatran female the of Details 1. Table Borneo, Borneo, Indonesia. The informaton includes (where available) date in Sabah. found on a 2001 poached female of as data as well born in captvity, on 3 females capture, includes data The table date used and name of examiner. method pathologies, of death, given name, facility where kept, approximate age at tme of capture, and presence or absence of
Journal of Threatened Taxa | www.threatenedtaxa.org | 26 February 2020 | 12(3): 15279–15288 15281 J TT Reproductve diseases in Sumatran Rhinos Schafer Examiner N. Schafer T. Roth T. Roth T. Z. Zahari Z. Zahari M. Agil M. Agil Method Histology Ultrasound Ultrasound Ultrasound Ultrasound Gross Pathology Ultrasound
Image 2. A poached wild animal’s reproductve tract has extensive pathology. O (ovary), C (cervix), T (tumor). © Nan Schafer.
in all geographic areas of origin and all geographic areas of captvity, including breeding sanctuaries in Indonesia (Sumatra and Kalimantan), Malaysia (Peninsular and Evidence of pathology date recorded date of pathology Evidence Cysts and 3 Leiomyoma (2001) and 3 Leiomyoma Cysts Immature Immature (2015); cycling post 5 years & Cysts Tumors Early loss (2018) Embryo 2 Abortons (2009–2010); 2 Births (2012, 2016) Multple Uterine Cysts (2012) Cysts Multple Uterine Uterine Tumors and Cysts (2014) and Cysts Tumors Uterine Immature No pathology, but ovaries and uterus and uterus but ovaries No pathology, quiescent (2019) Tumor Ovarian Sabah), and all zoos and reserves in the United States and United Kingdom. Reproductve analysis of captured animals prior to Evidence of Evidence copulaton No No Yes Yes No No No No No 2000 was sporadic. Hampered by a lack of equipment and limited expertse, only three animals were examined afer death at capture. Thus, potental disease processes and conditons afectng reproducton such as early Date of Date death N/A 30.iii.2014 15.vi.2017 16.xi.2019 5.iv.2016 embryo death remained unidentfed and unrecorded untl monitoring was implemented on a consistent basis. By 2000, a broader base of available expertse, protocols and reportng standards ensured that the last seven females captured: a poached female, Ratu, Rosa, Puntung, Iman, Najaq, and Pahu were examined Captve Captve facilites Wild, Sabah Cincinnat, USA Cincinnat, Way Kambas, Indonesia Kambas, Way Way Kambas, Indonesia Kambas, Way Sabah, Malaysia Danum Valley, Sabah Danum Valley, Way Kambas, Indonesia Kambas, Way Site Capture Died at Kelian (Kalimantan) (Kalimantan) Kelian Indonesia and reproductvely monitored from the beginning of their captve status. Since 1984, of the 32 females brought into captvity, analyses of the reproductve Age at at Age capture Adult N/A ~3 YRS. ~5 YRS. Adult Adult N/A Old Old tract were available for 25 because three animals had not reached maturity and four had no records. Out of 25, 22 individuals (88%) presented with some kind of reproductve disease. Out of the 22 animals, 14 Name Female Suci Rosa Ratu Puntung Iman Delilah Najaq Pahu females did not conceive despite copulatng a few to several tmes and eight females were without access to a breeding male. Females copulated even if they had pathology. Capture date Capture 2001 30.vii.2004 30.ix.2005 20.ix.2005 18.xii.2011 10.iii.2014 12.v.2016 12.iii.2016 25.xi.2018
Cysts and Tumors Uterine cysts and tumors were the most frequently documented reproductve problems (42%), and were primarily noted on ultrasound evaluaton. Gross Capture Capture locaton Poached Animal Sabah, Poached Malaysia Captve Born to (SB29 Born to Captve USA +28) Cincinnat, Bukit Barisan Selatan, Bukit Barisan Selatan, Indonesia Way Kambas, Indonesia Kambas, Way Malaysia Tabin, Danum Valley, Malaysia Danum Valley, Captve Born to (SB42 Born to Captve Kambas, + 46) Way Indonesia Kutai Barat, Indonesia Barat, Kutai West Kutai, Indonesia Kutai, West visualizaton of intraluminal cysts was noted in a female that died in captvity in 2000 (Lun Parai). A female 43 45 46 51 57 58 poached in 2001 had numerous tumors and cysts. Stud Book # Histology reports regarding the endometrium were
15282 Journal of Threatened Taxa | www.threatenedtaxa.org | 26 February 2020 | 12(3): 15279–15288 J TT Reproductve diseases in Sumatran Rhinos Schafer available for only two females: endometrial edema in the lumen of the uterus. Iman demonstrated a (Dalu) and cystc endometrial hyperplasia (Barakas). large tumor and pyometra that cultured as alpha and Histopathology on the uterine masses of six animals beta hemolytc streptococcus at the tme of capture. confrmed leiomyoma. The ultrasound images of these She subsequently died when the large tumor fnally tumors were consistent with signs of smooth muscle interfered with her urinary tract. fbroma (dense, round circumscribed) and frm on palpaton. Tumors occurred in three obviously older animals (Rapunzel, Jeram, Subur), fve adults (Lun Parai, DISCUSSION Merant, Mas Merah, Iman, and a poached female), and one young female (Rosa). The tumors present in Mas Infectons of the uterus were rarely observed in Merah had not changed when examined 10 years afer the Sumatran Rhino, which is consistent with fndings the original exam. Two animals Panjang and Seputh both reported in other species of rhinoceros by Hermes presented with only a few cysts when initally examined. & Hildebrandt (2011). Nutritonal factors apparently Follow-up exams 10 years later revealed that each had infuenced the development of abnormal conditons in developed tumors in the both the vagina and uterus. two animals. The predominant signs of reproductve Abnormalites were also observed in younger animals. failure identfed in this species are uterine cysts, uterine Minah, who was born in captvity, had cysts by 14 years tumors, uterine hyperplasia, and early embryonic loss, of age, but this may have been due to her exposure to all of which are indicatve of hormonal imbalances. exogenous hormones. Another juvenile, Rosa, began Hormonal imbalances can be associated with the factors cycling in 2010 and began to develop pathology in 2015 of age, lack of parity, and the aberrant genetcs inherent (Ferawat et al. 2018). in non-producing (isolated) and inbred animals.
Early Embryo Death Nutriton When ultrasound was fnally applied consistently Although multple corpora lutea can be a normal enough to monitor for signs of pregnancy, animals were occurrence in horses and camelids, the greatly enlarged found to be losing embryos. Three monitored animals uterine endometrium in one rhinoceros and prolonged (Emi, Ratu and Rosa) entered captvity young, but lactaton in another indicated disease. The unusual subsequently had difculty maintaining pregnancy. First conditons in both Dusun and Dalu occurred in the tme pregnancies might account for frst tme abortons, presence of hemosiderosis. Both of these animals were but it was unclear why multple spontaneous abortons in residental zoo setngs where proper foods were (Emi 5; Ratu 2) occurred thereafer. Rosa was reluctant not readily available, and they died before nutritonal to breed when she began to cycle and a few years later requirements for this species were elucidated. she developed signifcant pathology and is currently Efects on the reproductve system could have losing embryos. stemmed from direct deposits of iron into the reproductve organs of rhinos, a process that can Unusual Findings evidentally turn the endometrium dark brown (Nan Two females in residental zoos, Dalu (Taman Safari, Schafer, pers. obs. 1992), or indirectly from iron Bogor, Indonesia) and Dusun (Melaka, Malaysia and depositon into organs such as the kidney that infuence Ragunan, Jakarta, Indonesia) had unusual histories and hormone levels. Kidney failure was the most commonly pathological fndings. Dalu’s reproductve tract had reported cause of death in the Sumatran Rhinoceros multple corpus luteum and a signifcantly enlarged afer gastrointestnal disease (Foose 1999). uterus that revealed edema with hemosiderin without An uncommon symptom of chronic kidney disease is evidence of infecton. Afer breeding, Dusun lactated for galactorrhea whereby chronic nephrits results in a lack nine years before her death. Findings on necropsy noted of clearance of the hormone prolactn (Hou et al. 1985). chronic cystc kidney disease and darkening of multple Dusun was the only animal to present with this syndrome, organs, including the skin, suggestng hemosiderosis. and she was also the only one that demonstrated signs of late pregnancy loss. The histology report on Barakas Infecton (San Diego Zoo) showed the multple system-wide No signs of infectons were identfed in the few occurrence of hemosiderosis, which was also evident in histological reports provided. One female (Panjang) this animal’s cystc, hyperplastc endometrium. displayed possible infectous processes such as fuid The last two animals to die of hemosiderosis
Journal of Threatened Taxa | www.threatenedtaxa.org | 26 February 2020 | 12(3): 15279–15288 15283 J TT Reproductve diseases in Sumatran Rhinos Schafer
were a breeding female (Emi) and her ofspring (Suci) Reduced Parity with Early Senescence at the Cincinnat Zoo. The fact that their diets had An analysis of reproductve events in the captve been improved considerably over tme may have populaton of Sumatran Rhinoceros suggests that relieved efects on the reproductve system. Deaths premature senescence occurs in non-productve females. from iron overload have become rare as a result of Ordinarily in mammals, except for humans, reproductve the improved diet available in semi-wild sanctuaries life typically lasts up untl the end of life. Three older located in Indonesia and no animals have succumbed to animals had a long period wherein the ovaries were hemosiderosis since Suci’s death in 2014. inactve before death: Jeram was post-productve for 10 years, Rapunzel for 10 years, and Gologob for four years. Age Bina has never conceived despite multple atempts Cysts are most closely associated with age in horses, with one male and is presently reluctant to breed with and are found in 22% of adult mares and 55% of older new males, which may indicate beginning senescence. mares (Wolfsdorf 2002). Even though cysts seem to Premature senescence with high rates of reproductve develop as rhinos aged, some apparently younger pathology, termed “asymmetric reproductve ageing” animals (Minah, Emi and Rosa) also developed cysts. in captve White and Indian Rhinoceroses, reduces Tumors are associated with non-productve females the producton of ofspring in females that experience (Hermes et al. 2004) and have been documented in rhinos a prolonged lack of pregnancy (Hermes et al. 2004). as young as 15 years of age (Montali & Citno 1993). Notably, pregnancy is common in herds of older White The fact that Rosa, a young non-productve Sumatran Rhinoceroses in the wild, suggestng that this may not female, developed pathology fve years afer maturity is be a problem in these herds (Kretzschmar, pers. comm. an ominous sign for animals in the wild that are unable 2018). In the Sumatran Rhinoceros, among the last to stay consistently pregnant. The progressive nature seven captured females fve presented (soon afer of the disease was also evident in Rosa, who initally capture) with either pathology or as older animals had few cysts and then developed a tumor. This was with quiescent reproductve tracts suggestng they had observed in two additonal non-productve animals, who reduced breeding opportunites in the wild. progressed from having cysts to several tumors. The fact that there are fewer and fewer signs of ofspring in many Inbreeding Efects of the small, scatered remaining populatons of the Small populatons ofen sufer the efects of Sumatran Rhino may be an indicaton of development of inbreeding depression. Deleterious alleles may have this disease, which results in the loss of fertlity. been expressed in Sumatran Rhinoceros males and females which can predispose females to disease Protecton of Parity processes such as fbrous tumors (Medikare et al. In other species, parity may provide some protecton 2011). The heritable component of hemosiderosis may from developing reproductve pathology (Parazzini et have been demonstrated when Suci, an ofspring from al. 1988; Hermes et al. 2004). The parous state of the a pair of closely related parents, died from genetcally Sumatran Rhino has been difcult to assess because related iron sensitvity (Morales et al. 1997). While the majority of animals were adult when captured and Suci’s brothers survived and became productve, she and hymens were rarely checked when individuals entered her mother succumbed to hemosiderosis. Moreover, captvity. Most reports of the conditon of the hymen recessive alleles have been directly expressed as are connected with atempts to break the hymen of the problematc reproductve morphologies, including female afer the male had difculty copulatng with her. an abnormal male penile skin atachments and intact Parity was confrmed in only three animals. “imperforate” hymens in two captve females that had Rima gave birth just afer entering captvity, yet their hymens manually broken before copulaton could despite regular breeding thereafer, she did not become succeed (Filkins 1965; Tibary 2016). pregnant. The fact that she did not develop cysts untl Atemptng to breed animals from highly inbred her later years, suggests that her pregnancy protected populatons will severely compromise producton. The her from pathology. efectve number of breeders is now so low that recovery High rates of pathology in females may occur because of genetc vigor will require careful genetc mixing. they were non-productve before they entered captvity Therefore, infusion of genetc resources from animals and remained so aferwards. in Kalimantan and the exchange of genetc resources between rhinos from the northern and southern areas
15284 Journal of Threatened Taxa | www.threatenedtaxa.org | 26 February 2020 | 12(3): 15279–15288 J TT Reproductve diseases in Sumatran Rhinos Schafer of Sumatra will be vital for this species survival. diferences among rhinos in the typical locaton of tumors, in the reproductve tract. Indian Rhinos typically Treatment develop vaginal tumors, White Rhinos typically develop Only afer females could be closely monitored within uterine tumors, and Sumatran Rhinos develop both. a captve setng could early pregnancy loss be diagnosed Early cases of uterine tumor removal were not successful and treated with drugs that prevent embryo loss in other in the Sumatran and Indian Rhinoceros (Klein et al. rhinoceros species (Berkeley et al. 1997; Roth et al. 1997; Foose 1999). Although a few vaginal tumors have 2004). To date, all females that have delivered ofspring been removed, there has not been a further atempt to in captvity have been medicated with progesterone remove uterine tumors thus far (Radclife 2003). Some supplements, as demonstrated by Schafer et al. (1995). hormone treatments show promise in shrinking these Treatments become increasingly less successful the tumors (Hermes et al. 2016). Other treatment regimens more pathology a female develops. Certain types of useful for domestc animals have been explored for non- cysts are more problematc, but this cannot be confrmed productve female Sumatran Rhinoceroses (Radclife without a biopsy. Though only one cystc endometrial 2003). Unfortunately, these animals died before hyperplasia has been reported, this conditon may treatment efects could be ascertained. Animals with have been more common. Uterine biopsy could be a pathology will be difcult and tme consuming to recover. useful tool in elucidatng the reproductve conditon of individuals. Difcultes sampling the uterine tssue of Ramifcatons for Female Sumatran Rhinos larger species of rhinoceros have been overcome and Reproductve problems prevalent in small, isolated, access to the uterus of the Sumatran Rhino has been inbred populatons of Sumatran Rhinos in captvity are accomplished (Radclife et al. 2000; Hermes et al. 2009). also evident in animals in the wild. The frst indicaton Extensive numbers of cysts and/or tumors will that pathology could be a problem in populatons in interfere with maintenance of pregnancy. In domestc the wild was observed in 1986 with the capture of horses, treatment of cysts involves mechanical the frst animal in Indonesia. The discovery of tumors interventon such as aspiraton or hormonal removal. at the necropsy of this female within four months Procedural complicatons and reoccurrence of the cysts of entering captvity suggested that she developed is common. To date, treatment of cysts in Sumatran the tumors before she was captured (Furley 1993). Rhinos with extensive pathology has been unsuccessful Early capture eforts focused on capturing “doomed” and resulted in the return of cysts (Fiuza et al. 2015). Emi animals (Nardelli 2014), many of which had or later developed a few cysts between successful pregnancies, developed reproductve problems. The prevalence of indicatng it may be possible for females to achieve reproductve problems in females, however, became pregnancy when cysts are minimal. Although mares evident in the wild afer 2000 when animals were have achieved pregnancy with mild cases of only a few routnely examined immediately afer capture. Since cysts, Panjang and Seputh were breeding with negligible 2001, newly captured females have also been from cysts, but neither produced ofspring. Unfortunately, like “doomed” areas. Fertlity problems have been pervasive most animals captured during the 1980’s and 1990’s, it in these “rescued” females. All seven of these female was impossible to determine whether or not uterine Sumatran Rhinos captured had reproductve problems: cysts interfered with embryos in these individuals. The fve had reproductve abnormalites that were observed monitoring of Rosa has revealed that she has developed immediately afer capture, and early embryonic death cysts and a tumor. Embryos are also forming with was subsequently observed in two animals. A high rate breeding, but she is not maintaining her pregnancies of infertlity is inherent in small inbred populatons with despite progesterone treatments. Unlike Ratu and isolated females, and it contnues to interfere with the Emi whose healthy, pathology-free uteri responded growth of captve and wild populatons. successfully to progesterone treatments, Rosa is The existence of pathology in females suggests they unlikely to become pregnant even with progesterone. have had few, if any, ofspring in the wild, and indeed Thus, Rosa’s only chance to contribute to the recovery there is no evidence of births in the areas where rhinos of this species is through the applicaton of Advanced have recently been captured in Sumatra (Bukit Barisan Reproductve Techniques. Selatan and Way Kambas Natonal Parks) and Sabah Leiomyomas were the most common type of (Tabin Wildlife Reserve and Danum Valley). These areas reproductve tumors in the rhinoceros (Montali & Citno have seen precipitous drops in rhino populatons. For 1993). Hermes & Hildebrandt (2011) described species example Way Kambas had 26–31 rhinos according to the
Journal of Threatened Taxa | www.threatenedtaxa.org | 26 February 2020 | 12(3): 15279–15288 15285 J TT Reproductve diseases in Sumatran Rhinos Schafer
2015 populaton viability analysis (Miller et al. 2015), while recent observatons indicate the populaton now numbers 4–9 rhinos (Marcellus Adi pers. comm. 2019). Areas with steadily declining populatons and litle evidence of ofspring will contnue to provide predominately reproductvely compromised animals. Credible demographic informaton about populatons is nonexistent, except for the fact that they are disappearing. To date, no populaton assessment tool or combinaton of tools including surveys, camera-traps, and fecal DNA analyses has provided the critcal fertlity informaton required to manage this species in the wild. Camera-trap photographs of a few females with young Image 3. In contrast to decades of unreliable surveys, direct observaton and analysis has been the only source of relevant can only provide informaton on where potentally fertle informaton for productve management. © Nan Schafer. rhinos can be found; it does not defne or confrm the ongoing viability of the current populaton or survival of the species. Realistc informaton applicable to the reproductve events by comparing ultrasound images Sumatran Rhino should have been used for successful with individual hormonal levels in feces or blood. modeling of extncton outcomes for this species (Miller Treatment protocols for pathology have been atempted et al. 2015). For years we have had all the informaton but need further development (Radclife 2003). we needed to show that the Sumatran Rhino in Indonesia Simulaton or inducement of pregnancy may be the can no longer be sustained in the wild, partcularly in the only preventon (Roth 2006; Hermes & Hildebrandt face of mountng infertlity and negatve growth rates, 2011; Hermes et al. 2016; Roth et al. 2018). Females even with the absence of poaching. have been successfully assisted with the maintenance Fertle females are the determinant factor in of their pregnancies, and ofspring have resulted. Other the recovery of this Critcally Endangered species techniques are evolving quickly to optmize producton (Kretzschmar et al. 2016). When numbers are critcally in this species (Galli et al. 2016) even though minimal low and the risk of infertlity so high, the fertlity status and marginal genetc material has been available. As of every female rhinoceros must be ascertained and happened with the Northern White Rhino, soon there constantly monitored, which is not possible when the will be litle genetc material lef for preserving the last status of animals is unknown. Intensive management record of the Sumatran Rhino (Saragusty et al. 2016; zones (IMZs) and/or intensive protecton zones (IPZs) Nardelli 2019). The success of a single genetcally distnct are not suitable for this cryptc rainforest species, union could revitalize this Critcally Endangered species. because the informaton necessary for successful None of these conditons will be identfable or treatable management cannot be obtained within such areas while animals are in the wild. Time is running out for (Ahmad et al. 2013; Payne & Yoganand 2018). Although younger treatable animals, which without pregnancy are these management strategies may apply to the larger at risk of rapidly developing pathology, given that Rosa African and Asian rhinoceros populatons, which can developed pathology in less than fve years. be observed, monitored and sampled at the individual level, these strategies are inappropriate and dangerously non-productve for the Sumatran Rhino (Image 3). The CONCLUSION only way to determine the fertlity status of an individual Sumatran Rhino is through direct, hands-on examinaton The critcally low estmates of numbers in widely in a captve setng. scatered populatons of the Sumatran Rhino, coupled Afer 25 years of perfectng tools and techniques in with the fact that both captve populatons and captvity, the Sumatran Rhino Sanctuary (SRS) design in animals caught from the wild are largely reproductvely Way Kambas is currenly the only opton for successful compromised, means that only a small number of reproductve management of Sumatran Rhinos. Only reproductvely viable animals may be lef in the wild. in this environment can the essental management In additon, the complete lack of relevant informaton, informaton be obtained, and reproducton optmized. and in some cases wild extrapolatons, on the status Fertlity monitoring for this species requires confrming of animals makes addressing these problems in the
15286 Journal of Threatened Taxa | www.threatenedtaxa.org | 26 February 2020 | 12(3): 15279–15288 J TT Reproductve diseases in Sumatran Rhinos Schafer wild impossible. In light of these facts, building a new pp. 546–561. In: Fowler’s Zoo and Wild Animal Medicine: Current productve captve populaton by startng immediately Therapy, vol. 7. Saunders, New York, 688 pp. Hermes, R., T.B. Hildebrandt & F. Goeritz (2004). Reproductve with capturing viable, productve animals from the onset problems directly atributable to long-term captvity–asymmetric and optmizing their producton is essental. Recovery reproductve aging. Animal Reproducton Science 82–83: 49–60. htps://doi.org/10.1016/j.anireprosci.2004.05.015 and use of vital genetc materials must be accelerated Hermes, R., F. Goeritz, T.J. Portas, B.R. Bryant, J.M. Kelly, L.J. Maclellan, before these resources are lost. Fertle animals must be T. Keeley, F. Schwarzenberger, C. Walzer, A. Schnorrenberg, R.E. the frst priority for the few sanctuary spaces that are Spindler, J. Saragusty, S. Kaandorp & T.B. Hildebrandt (2009). Ovarian superstmulaton, transrectal ultrasound-guided oocyte available. The best chance of obtaining fertle founders recovery, and IVF in rhinoceros. Theriogenology 72: 959–968. exists in the few clusters where females with young have htps://doi.org/10.1016/j.theriogenology.2009.06.014 been confrmed with recent camera-trap photos. These Hermes, R., F. Schwarzenberger, F. Goeritz, S. Oh, T. Fernandes, R. Bernardino, A. Leclerc, E. Greunz, A. Mathew, S. Forsyth, J. will also be the areas where females are at risk of fewer Saragusty & T.B. Hildebrandt (2016). Ovarian down regulaton by pregnancies, but may stll be recoverable with treatment. GnRF vaccinaton decreases reproductve tract tumor size in female Only two such areas have provided such evidence: Way white and Greater One-horned Rhinoceroses (abstract). Proceedings of the Scientfc program of the 15th Internatonal Elephant & Rhino Kambas Natonal Park (Lampung, southern Sumatra) and conservaton and research symposium, Singapore, November 14– certain areas of the Leuser ecosystem (Aceh, western 18, 2016: 52. Sumatra). They are the frst focus areas for capturing Hou, S.H., S. Grossman & M.E. Molitch (1985). Hyperprolactnemia in patents with renal insufciency and chronic renal failure requiring viable females, before they, too, are lost. hemodialysis or chronic ambulatory peritoneal dialysis. American Journal of Kidney Diseases 6(4): 245–249. Klein, L.V., R.A. Cook, P.P. Calle, B.L. Raphael & P. Thomas (1997).
Etorphine-Isophlorine-O2-anesthesia for ovariohysterectomy in an REFERENCES Indian rhinoceros (Rhinoceros unicornis), pp. 127–130. Proceedings of the Annual Conference of the American Associaton of Zoo Ahmad, A.H., J. Payne & Z.Z. Zainuddin (2013). Preventng the Veterinarians, 26–30 October 1997, Houston, TX. extncton of the Sumatran Rhinoceros. Journal of Indonesian Medikare, V., L.R. Kandukuri, V. Ananthapur, M. Deenadayal & P. Natural History 1: 11–22. Nallari (2011). The genetc bases of uterine fbroids: a review. Berkeley, E.V., J.F. Kirkpatrick, N.E. Schafer, W.M. Bryant & W.R. Journal of Reproducton & Infertlity 12(3): 181–191. Threlfall (1997). Serum and fecal steroid analysis of ovulaton, Miller, P.S., C. Lees, W. Ramono, A. Purwoto, A. Rubianto, Sectonov, pregnancy, and parturiton in the Black Rhinoceros (Diceros B. Talukdar (Eds.) (2015). Populaton Viability Analysis for the bicornis). Zoo Biology 16(2): 121–132. htps://doi.org/10.1002/ Sumatran Rhino in Indonesia. Apple Valley, MN: IUCN/SSC (SICI)1098-2361 Conservaton Breeding Specialist Group. Ferawat, N.M., Z. Arsan, W.Y. Agvinta Nilam, S. Hasmaran & T. Montali, R.J. & S.B. Citno (1993). Pathological fndings in captve Roth (2018). Pengaruh keberadaan jaringan fbroid pada saluan rhinoceroses, pp. 346-349. In: Ryder, O.A. (ed.). Rhinoceros Biology reproduksi badak sumatera betna terhadap potensi kebuntngannya and Conservaton: Proceedings of an Internatonal Conference, San [Efect of the presence of fbroid tssue on female reproductve track Diego, U.S.A. Zoological Society, San Diego (CA). of the Sumatran rhino to the potental for pregnancy]. Proceedings Morales, J.C., P.M. Andau, J. Supriatna, Z.Z. Zainuddin & D.J. Melnick of the 20th FAVA Congress & 15th KIVNAS PDHI, Bali, Nov 1-3, 2018: (1997). Mitochondrial DNA variability and conservaton genetcs of 322–324. the Sumatran rhinoceros. Conservaton Biology 11(2): 539–543. Filkins, M.E. (1965). Congenital and hereditable defects which Nardelli, F. (2014). The last chance for the Sumatran rhinoceros? interfere with the reproductve efciency of domestc catle (Bos Pachyderm 55: 43–53. taurus). Iowa State University Veterinarian 27(2): 67–75. Nardelli, F. (2019). Observatons on the ex situ management of the Fiuza, R., R. Hermes, F. Goeritz, Z.Z. Zainuddin, P. Kretzschmar, J. Sumatran Rhinoceros Dicerorhinus sumatrensis (Mammalia: Payne & T.B. Hildebrandt (2015). The Sabah Rhino Breeding Perissodactyla: Rhinocerotdae): present status and desiderata for Programme: reproductve pathology and its clinical implicatons conservaton. Journal of Threatened Taxa 11(15): 14927–14941. in wild-caught Sumatran rhinoceroses. Proceedings of the 10th htps://doi.org/10.11609/jot.4952.11.15.14927-14941 Internatonal Conference on Behaviour, Physiology and Genetcs of Parazzini, F., C. La Vecchia, E. Negri, G. Cecchet & L. Fedele (1988). Wildlife, Berlin: 70. Epidemiologic characteristcs of women with uterine fbroids: a Foose, T. (1999). Internatonal Studbook for Sumatran Rhino case-control study. Obstetrics & Gynecology 72: 853–857. (Dicerorhinus sumatrensis), 31 October 1999. Internatonal Rhino Payne, J. & K. Yoganand (2018). Critcally Endangered Sumatran Foundaton, Columbus, 12pp. Rhinoceros: Inputs for Recovery Strategy and Emergency Actons Furley, C.W. (1993). The clinical history of the adult female Sumatran 2017-2027. WWF Indonesia, Jakarta, 114 pp. rhinoceros, called ‘Subur’ in captvity in Sumatra and at Port Radclife, R. (2003). Reproducton and health assessments 2001-2003. Lympne Zoo, Kent, Great Britain, pp. 357–366. In: Ryder, O.A. Sumatran Rhino Conservaton Centre, Sungai Dusun, Malaysia. (ed.). Rhinoceros Biology and Conservaton: Proceedings of an Radclife, R.M., D.A. Hendrickson, G.L. Richardson, J.R. Zuba & R.W. Internatonal Conference, San Diego, U.S.A. Zoological Society, San Radclife (2000). Standing laparoscopic-guided uterine biopsy Diego (CA). in a Southern White Rhinoceros (Ceratotherium simum simum). Galli, C., R. Hermes, F. Goeritz, S. Colleoni, S. Diecke, M. Drukker, Journal of Zoo and Wildlife Medicine 31: 201–207. htps://doi. Katsuhiko Hayashi, S. Holtze, G. Lazzari, J. Payne, E. Sos, J. Stejskal, org/10.1638/1042-7260 M. Wiesner, Z.Z. Zainuddin & T. Hildebrandt (2016). First results Roth, T.L. (2006). A review of the reproductve physiology of rhinoceros of oocyte maturaton and in-vitro-fertlisaton (IVF) in Sumatran species in captvity. Internatonal Zoo Yearbook 40: 130–143. and northern white rhinoceroses. Proceedings of the Scientfc htps://doi.org/10.1111/j.1748-1090.2006.00130.x program of the 15th Internatonal Elephant & Rhino conservaton Roth, T.L., J.K. O’Brien, M.A. McRae, A.C. Bellem, S.J. Romo, J.L. Kroll and research symposium, Singapore, November 14–18, 2016: 51. & J.L. Brown (2001). Ultrasound and endocrine evaluaton of the Hermes, R. & T.B. Hildebrandt (2011). Rhinoceros theriogenology, ovarian cycle and early pregnancy in the Sumatran Rhinoceros,
Journal of Threatened Taxa | www.threatenedtaxa.org | 26 February 2020 | 12(3): 15279–15288 15287 J TT Reproductve diseases in Sumatran Rhinos Schafer
Dicerorhinus sumatrensis. Reproducton 121: 139–149. htps://doi. Bahasa Indonesia Abstrak: Badak Sumatera Dicerorhinus sumatrensis berada org/10.1530/rep.0.1210139 di ujung kepunahan. Penurunan spesies ini pada awalnya dikaitkan dengan Roth, T.L., H.L. Bateman, J.L. Kroll, B.G. Steinmetz & P.R. Reinhart perburuan liar dan hilangnya habitat, tetapi bukt yang disajikan di sini menunjukkan bahwa kegagalan reproduksi juga telah menjadi penyebab utama (2004). Endocrine and ultrasonographic characterizaton of a hilangnya, dan terus mempengaruhi penurunan populasi liar. Populasi badak successful pregnancy in a Sumatran Rhinoceros (Dicerorhinus Sumatera yang tersisa di Indonesia adalah kecil dan tersebar, dengan akses sumatrensis) supplemented with a synthetc progestn. Zoo Biology terbatas ke peluang berkembang biak dengan pasangan yang tdak berkerabat. 23: 219–238. htps://doi.org/10.1002/zoo.10131 Kondidi tersebut mengakibatkan terjadinya inbreeding dan mengakibatkan Roth, T.L., M.W. Schook & M.R. Stoops (2018). Monitoring and infertlitas-akibat terisolasi, berhubungan dengan masalah kesuburan yang controlling ovarian functon in the rhinoceros. Theriogenology 109: dianalisis dalam tulisan ini. Betna badak Sumatera di penangkaran menunjukkan 48-57; htps://doi.org/10.1016/j.theriogenology.2017.12.007 tngkat patologi reproduksi dan / atau masalah dengan konsepsi yang tnggi (> 70%) yang secara signifkan menghambat program pengembangbiakannya. Saragusty, J., S. Diecke, M. Drukker, B. Durrant, I.F. Ben-Nun, C. Kemajuan teknologi memungkinkan pemeriksaan segera setelah penangkapan Galli, F. Goeritz, K. Hayashi, R. Hermes, S. Holtze, S. Johnson, G. dan menunjukkan tngkat dan jenis masalah reproduksi yang sama tngginya Lazzari, P. Loi, J.F. Loring, K. Okita, M.B. Renfree, S. Seet, T. Voracek, pada individu dari populasi liar. Tujuh Badak Sumatera betna yang terakhir J. Stejskal, O.A. Ryder & T.B. Hildebrandt (2016). Rewinding the ditangkap berasal dari daerah dengan populasi kecil yang menurun, dan process of mammalian extncton. Zoo Biology 35(4): 280–292. ditemukan enam badak memiliki masalah reproduksi. Badak-badak yang tdak htps://doi.org/10.1002/zoo.21284 reproduktf selanjutnya akan mengambil ruang berharga dan sumber daya yang Schafer, N.E. (2018). Sumatran rhinoceros: reproductve data 1991- dibutuhkan untuk hewan subur. Risiko tnggi infertlitas dan kesulitan mengobat penyebabnya, ditambah dengan terus menurunnya jumlah badak yang 1999, with updates and addenda to 2018. SOS Rhino, Washington tersisa di alam, maka keberhasilan upaya untuk membangun populasi badak (DC), 78pp.Available from: http://www.rhinoresourcecenter.com/ dipenangkaran yang layak akan sangat tergantung pada pemanfaatan hewan index.php?s=1&act=refs&CODE=ref_detail&id=1537427226. subur dan penerapan teknik reproduksi berbantuan. Survei in situ yang lengkap Schafer, N.E., M. Agil & E. Bosi (2001). Utero-ovarian pathological dalam beberapa dasawarsa belum memberikan informasi yang relevan dengan complex of the Sumatran rhinoceros (Dicerorhinus sumatrensis), manajemen populasi atau untuk memastkan status kesuburan masing-masing p.322. In: Schwammer, H.M. (ed.). Recent Research on Elephants hewan. Dengan demikian Prioritas pertama dalam penyelamatan badak di alam and Rhinos: Abstracts of The Internatonal Elephant and Rhino adalah penangkapan individu sebagai sumber darah baru dari daerah dengan kemungkinan tertnggi mengandung badak subur, ditunjukkan oleh foto dari Research Symposium, June 7–11, 2001. Zoologischer Garten, dari badak betna dengan anak-anaknya dari perangkap kamera yang baru-baru Vienna. ini ditemukan. Daerah tersebut termasuk Way Kambas dan bagian ekosistem Schafer, N.E., W. Bryant, E. Berkeley, J.A. Berry, R. Powell, C. Barnet Leuser untuk saat ini di wilayah Sumatera. & J. Joyce (1995). Case Report: successful birth afer intensive management of an aged Black Rhinoceros (Diceros bicornis) with Author details: Nan Schaffer’s (M.S., D.V.M.), seminal work on reproducton a history of abortons. Proceedings of the Regional Conference of rhinoceroses, since her residency at the Bronx Zoo in 1981, resulted in the Proceedings of the AZA, 1995: 332–337. frst extracton of semen with electroejaculaton and the frst ultrasound of the female reproductve tract. She was the frst to identfy the high prevalence of Schafer, N.E., Z.Z. Zainuddin, M.S.M. Suri, M.R. Jainudeen & R.S. reproductve pathology in female Sumatran Rhino, which she has reported on Jeyendran (1994). Ultrasonography of the reproductve anatomy in since 1991. Muhammad Agil (M.Sc. Agr., D.V.M., Dipl. A.C.C.M.) is a senior the Sumatran Rhinoceros (Dicerorhinus sumatrensis). Journal of Zoo lecturer and researcher at the Faculty of Veterinary Medicine, IPB University. and Wildlife Medicine 25(3): 337–348. He has studied the reproductve biology and conservaton needs of the Tibary, A. (2016). [Internet]. Female genital abnormalites. Merck Sumatran Rhino since 1993. His work and research interests also include the Veterinary Manual Online. Electronic version accessed 9 April 2019. Javan Rhino, Banteng and Sumatran Elephant. Zainal Zainuddin (D.V.M.) is a Wolfsdorf, K.E. (2002). Endometrial cysts. Proceedings of the Bluegrass wildlife veterinarian who was involved with Sumatran Rhino capture, captve management, and assisted reproductve technologies in Malaysia and Indonesia. Equine Reproducton Symposium, Lexington, Ky. (without pages). Since his work began in 1985, he has handled the veterinary care and pathological analysis of over 20 individual rhinos. He has over 20 publicatons on this species.
Author contributon: This paper represents decades of collaboratve feld work and research among these three colleagues in their shared mission to recover the Sumatran Rhino genus. N. Schafer compiled the data and wrote the manuscript. All authors reviewed and approved the fnal manuscript.
Threatened Taxa
15288 Journal of Threatened Taxa | www.threatenedtaxa.org | 26 February 2020 | 12(3): 15279–15288
PLATINUM The Journal of Threatened Taxa (JoTT) is dedicated to building evidence for conservaton globally by publishing peer-reviewed artcles online every month at a reasonably rapid rate at www.threatenedtaxa.org. OPEN ACCESS All artcles published in JoTT are registered under Creatve Commons Atributon 4.0 Internatonal License unless otherwise mentoned. JoTT allows allows unrestricted use, reproducton, and distributon of artcles in any medium by providing adequate credit to the author(s) and the source of publicaton.
ISSN 0974-7907 (Online) | ISSN 0974-7893 (Print)
February 2020 | Vol. 12 | No. 3 | Pages: 15279–15406 Date of Publicaton: 26 February 2020 (Online & Print) www.threatenedtaxa.org DOI: 10.11609/jot.2020.12.3.15279-15406
Review New record of Tulostoma squamosum (Agaricales: Basidiomycota) from India based on morphological features and phylogenetc analysis Ramifcatons of reproductve diseases on the recovery of the – Arun Kumar Duta, Soumitra Paloi & Krishnendu Acharya , Pp. 15375– Sumatran Rhinoceros Dicerorhinus sumatrensis (Mammalia: 15381 Perissodactyla: Rhinocerotdae) – Nan E. Schafer, Muhammad Agil & Zainal Z. Zainuddin, Pp. 15279–15288 Notes
Communicatons An account of a frst record of the Common Goldeneye Bucephala clangula Linnaeus, 1758 (Aves: Anseriformes: Anatdae) Diet ecology of tgers and leopards in Chhatsgarh, central India in Bhutan – Krishnendu Basak, Moiz Ahmed, M. Suraj, B.V. Reddy, O.P. Yadav & – Sangay Nidup, Gyeltshen & Tshering Tobgay, Pp. 15382–15384 Krishnendu Mondal, Pp. 15289–15300 First record of the hawkmoth Theretra lycetus (Cramer, 1775) Building walls around open wells prevent Asiatc Lion Panthera leo persica (Sphingidae: Macroglossinae) from Bhutan (Mammalia: Carnivora: Felidae) mortality in the Gir Lion Landscape, – Sangay Nidup & Jatshwor Singh Irungbam, Pp. 15385–15386 Gujarat, India – Tithi Kagathara & Erach Bharucha, Pp. 15301–15310 Occurrence and associaton of the Scarce Lilacfork Lethe dura gammiei (Moore, [1892]) (Lepidoptera: Nymphalidae: Taxonomic and ecological notes on some poorly known bats Satyrinae) with Woolly-leaved Oak Quercus lanata Smith, 1819 (Mammalia: Chiroptera) from Meghalaya, India (Fabaceae) forest in the Kumaon region of the Indian Himalaya – Utam Saikia, AdoraThabah & Manuel Ruedi, Pp. 15311–15325 – Arun P. Singh & Tribhuwan Singh, Pp. 15387–15390
Angiosperm diversity in Bhadrak region of Odisha, India Additons to the Odonata (Insecta) fauna of Asansol-Durgapur – Taranisen Panda, Bikram Kumar Pradhan, Rabindra Kumar Mishra, Industrial Area, West Bengal, India Srust Dhar Rout & Raj Ballav Mohanty, Pp. 15326–15354 – Amar Kumar Nayak, Pp. 15391–15394
Gynochthodes cochinchinensis (DC.) Razafm. & B. Bremer (Morindeae: Short Communicatons Rubioideae: Rubiaceae): an additon to the woody climbers of India – Pradeep Kumar Kamila, Prabhat Kumar Das, Madhusmita Mallia, Sightng of Petaurista petaurista (Pallas, 1766) (Mammalia: Rodenta: Chinnamadasamy Kalidass, Jagayandat Pat & Pratap Chandra Panda, Sciuridae) on limestone hills in Merapoh, Malaysia Pp. 15395–15399 – Priscillia Miard, Mohd Nur Arifuddin, Izereen Mukri, Sit Syuhada Sapno, Hafz Yazid, Nadine Ruppert & Jayaraj Vijaya Kumaran, Pp. 15355–15358 Record of Oldenlandia hygrophila Bremek. (Spermacoceae: Rubiaceae), a lesser known herb from Palghat Gap of Western Ghats, Kerala, India Molecular detecton of Murshidia linstowi in a free-ranging dead – Vadakkeveedu Jagadesh Aswani, Vasudevan Ambat Rekha, Pathiyil elephant calf Arabhi, Manjakulam Khadhersha Jabeena, Kunnamkumarath Jisha & – Sourabh Ranjan Hota, Sonali Sahoo, Manojita Dash, Avisek Pahari, Maya Chandrashekaran Nair, Pp. 15400–15404 Bijayendranath Mohanty & Niranjana Sahoo, Pp. 15359–15363
Parasite commonality at Swamp Deer (Mammalia: Artodactyla: Book Review Cervidae: Rucervus duvaucelii duvaucelii) and livestock interface – Animesh Talukdar, Bivash Pandav & Parag Nigam, Pp. 15364–15369 The State of Wildlife and Protected Areas in Maharashtra: News and Informaton from the Protected Area Update 1996-2015 Prevalence and seasonal variaton of gastrointestnal parasites – Reviewed by L.A.K. Singh, Pp. 15405–15406 among captve Northern Pig-tailed Macaque Macaca leonina (Mammalia: Primates: Cercopithecidae) – Phoebe Lalremruat & G.S. Solanki, Pp. 15370–15374 Publisher & Host
Member
Threatened Taxa