Abstract
In animal husbandry, diets should help in maintaining a healthy body condition, support reproduction, and promote species-specific longevity. It is recommended to feed folivorous primates kept in zoos a high-fiber diet, i.e., leaves, although satisfying such a requirement is challenging in temperate regions because it is difficult to obtain fresh leaves, especially in autumn and winter. As equally important for their appropriate treatment, it is valuable to provide details of clinical reports of medical problems and pathological findings, although such clinical reports are rather limited. Therefore, in foregut-fermenting proboscis monkeys (Nasalis larvatus), we (1) described the individual clinical reports of renal disease and weight loss at the Yokohama Zoological Gardens in Japan, (2) determined the nutritional profile of the diets supplied to these animals because other potential triggers for their renal disease and weight loss could be excluded, (3) modified the diet regimen to minimize weight loss and the development of hypercalcemia and hypophosphatemia, and (4) assessed the effects of such dietary modification by comparing the body weight and the Ca and P concentrations and the Ca/P ratios in the blood before and after diet modification with a comparison of these measurements between zoo and free-ranging individuals. Based on the nutritional profile of the diets, we concluded that the reported cases of renal failure might be caused by consumption of leaves with a Ca/P ratio far above the appropriate level in autumn and winter. Additionally, the dietary modification of minerals and metabolizable energy achieved certain beneficial effects on zoo-kept proboscis monkeys.
Similar content being viewed by others
References
AOAC (2005) Official methods of analysis, 18th edn. Association of Official Analytical Chemists, Arlington, VA, USA
Atwater WO (1910) Principles of nutrition values of food. United states farmer's bulletin 142
Azumano A, Ueda M, Tanaka S (2015) Report of a fatal case of a juvenile proboscis monkey (Nasalis larvatus). Bull Zool Stud 13:30–33
Baker KC, Georoff TA, Ialeggio DM et al (2022) Retrospective review of urolithiasis-related morbidity and mortality in Asian colobine monkeys. J Zoo Wildl Med 53:1–10. https://doi.org/10.1638/2021-0023
Bernard H, Matsuda I, Hanya G et al (2019) Feeding ecology of the proboscis monkey in Sabah, Malaysia, with special reference to plant species-poor forests. Primates in flooded habitats: Ecology and conservation. Cambridge University Press, Cambridge, pp 89–98
Bismark M (2010) Proboscis monkey (Nasalis larvatus): Bio-ecology and conservation. Indonesian primates. Springer, New York, pp 217–233
Boonratana R (2003) Feeding ecology of proboscis monkeys (Nasalis larvatus) in the lower Kinabatangan, Sabah, Malaysia. Sabah Parks Nature Journal 6:1–6
Calle P, Raphael B, Stetter M et al (1995) Gastrointestinal linear foreign bodies in silver leaf langurs Trachypithecus cristatus ultimus. J Zoo Wildl Med 26:87–97
Carroll MF, Schade DS (2003) A practical approach to hypercalcemia. Am Fam Physician 67:1959–1966
Clauss M, Dierenfeld E (2008) The nutrition of browsers. Zoo and wild animal medicine: Current therapy, 6th edn. Saunders Elsevier, St. Louis, pp 444–454
Cline J (2012) Calcium and Vitamin D metabolism, deficiency, and excess. Top Companion Anim Med 27:159–164. https://doi.org/10.1053/j.tcam.2012.09.004
Collins L, Roberts M (1978) Arboreal folivores in captivity- maintenance of a delicate minority. The ecology of arboreal folivores. Smithsonian Institution, Washington DC, pp 5–12
Crissey S, Pribyl L, Pruett-Jones M, Meehan T (1998) Nutritional management of old world primates with special consideration for vitamin D. Int Zoo Yearb 36:122–130. https://doi.org/10.1111/j.1748-1090.1998.tb02894.x
Dierenfeld ES, Koontz FW, Goldstein RS (1992) Feed intake, digestion and passage of the proboscis monkey (Nasalis larvatus) in captivity. Primates 33:399–405. https://doi.org/10.1007/BF02381201
Edwards MS, Crissey SD, Oftedal OT (1997) Leaf-eating primates: nutrition and dietary husbandry. NAG handbook Fact Sheet 7
Emerick R, Embry L (1963) Calcium and phosphorus levels related to the development of phosphate urinary calculi in sheep. J Anim Sci 22:510–513. https://doi.org/10.2527/jas1963.222510x
Ensley P, Rost T, Anderson M et al (1982) Intestinal obstruction and perforation caused by undigested Acacia sp. leaves in langur monkeys. J Am Vet Med Assoc 181:1351–1354
Estrada A, Garber PA, Rylands AB et al (2017) Impending extinction crisis of the world’s primates: why primates matter. Sci Adv 3:e1600946. https://doi.org/10.1126/sciadv.1600946
George JW, Hird DW, George LW (2007) Serum biochemical abnormalities in goats with uroliths: 107 cases (1992–2003). J Am Vet Med 230:101–106. https://doi.org/10.2460/javma.230.1.101
Goff JP (2000) Pathophysiology of calcium and phosphorus disorders. Vet. Clin n Am - Food Anim Pract 16:319–337. https://doi.org/10.1016/S0749-0720(15)30108-0
Han S, Garner MM (2016) Soft tissue mineralization in captive 2-toed sloths. Vet Pathol 53:659–665. https://doi.org/10.1177/0300985815598206
Hayakawa T, Nathan SKSS, Stark DJ et al (2018) First report of foregut microbial community in proboscis monkeys: are diverse forests a reservoir for diverse microbiome? Environ Microbiol Rep 10:655–662. https://doi.org/10.1111/1758-2229.12677
Hill O (1964) The maintenance of langurs (Colobidae) in captivity; Experiences and some suggestions. Folia Primatol 2:222–231. https://doi.org/10.1159/000155018
Hollihn U (1973) Remarks on the breeding and maintenance of colobus monkeys Colobus guereza, proboscis monkeys Nasalis larvatus and douc langurs Pygathrix nemaeus in zoos. Int Zoo Yearb 13:185–188
Hosey G, Melfi V, Pankhurst S (2013) Zoo animals: Behaviour, management and welfare. Oxford University Press, Oxford
Hoshino S, Seino S, Funahashi T et al (2021) Apparent diet digestibility of captive colobines in relation to stomach types with special reference to fibre digestion. PLoS ONE 16:e0256548. https://doi.org/10.1371/journal.pone.0256548
Inoue E, Ogata M, Seino S, Matsuda I (2016) Sex identification and efficient microsatellite genotyping using fecal DNA in proboscis monkeys (Nasalis larvatus). Mammal Study 41:141–148. https://doi.org/10.3106/041.041.0304
Janssen D (1994) Morbidity and mortality of douc langurs (Pygathrix nemaeus) at the San Diego zoo. Proceedings of the American Association of Zoo Veterinarians 221–226
Kagawa Y (2005) Standard tables of food composition in Japan 5th revised and enlarged. Toppan Printing, Japan (in Japanese)
Kato Y, Sato K, Sata A et al (2004) Hypercalcemia induced by excessive intake of calcium supplement, presenting similar findings of primary hyperparathyroidism. Endocr J 51:557–562. https://doi.org/10.1507/endocrj.51.557
Kawasaki R, Kawakita M, Kurosawa K et al (2021) Analysis of fecal nutrients and particle size in captive proboscis monkeys (Nasalis larvatus) fed seasonal dietary foliage at a Japanese zoo. Anim Sci J. https://doi.org/10.1111/asj.13612
Kleiman D, Thompson K, Baer C (2010) Wild mammals in captivity: Principles and techniques for zoo management, 2nd edn. University of Chicago Press, Chicago
Licitra G, Hernandez TM, Van Soest PJ (1996) Standardization of procedures for nitrogen fractionation of ruminant feeds. Anim Feed Sci Technol 57:347–358. https://doi.org/10.1016/0377-8401(95)00837-3
Lindemann DM, Gamble KC, Corner S (2013) Calcium carbonate obstructive urolithiasis in a red kangaroo (Macropus rufus). J Zoo Wildl Med 44:196–199. https://doi.org/10.1638/1042-7260-44.1.196
Loomis M, Britt J, Gendron A et al (1983) Hepatic and gastric amebiasis in black and white colobus monkeys. J Am Vet Med Assoc 83:1188–1191
Matsuda I, Bernard H, Tuuga A et al (2018) Fecal nutrients suggest diets of higher fiber levels in free-ranging than in captive proboscis monkeys (Nasalis larvatus). Front Vet Sci 4:246. https://doi.org/10.3389/fvets.2017.00246
Matsuda I, Chapman CA, Clauss M (2019) Colobine forestomach anatomy and diet. J Morphol 280:1608–1616. https://doi.org/10.1002/jmor.21052
Matsuda I, Clauss M, Tuuga A et al (2017) Factors affecting leaf selection by foregut-fermenting proboscis monkeys: New insight from in vitro digestibility and toughness of leaves. Sci Rep 7:42774. https://doi.org/10.1038/srep42774
Matsuda I, Grueter CC, Teichroeb JA (2022) The colobines: Natural history, behaviour and ecological diversity. Cambridge University Press, Cambridge
Matsuda I, Stark DJ, Saldivar DAR et al (2020) Large male proboscis monkeys have larger noses but smaller canines. Commun Biol 3:522. https://doi.org/10.1038/s42003-020-01245-0
Matsuda I, Tuuga A, Bernard H (2011) Riverine refuging by proboscis monkeys (Nasalis larvatus) and sympatric primates: Implications for adaptive benefits of the riverine habitat. Mamm Biol 76:165–171. https://doi.org/10.1016/j.mambio.2010.03.005
Matsuda I, Tuuga A, Bernard H et al (2013) Leaf selection by two Bornean colobine monkeys in relation to plant chemistry and abundance. Sci Rep 3:1873. https://doi.org/10.1038/srep01873
Matsuda I, Tuuga A, Higashi S (2009) The feeding ecology and activity budget of proboscis monkeys. Am J Primatol 71:478–492. https://doi.org/10.1002/ajp.20677
Miller E, Fowler ME (2015) Fowler’s zoo and wild animal medicine, vol 8. Saunders
Nijboer J, Clauss M (2006) The digestive physiology of colobine primates. Utrecht University Repository, Fibre intake and faeces quality in leaf-eating primates. Ridder. https://doi.org/10.5167/UZH-3520
Nijboer J, Dierenfeld ES (1996) Comparison of diets fed to southeast Asian colobines in North American and European zoos, with emphasis on temperate browse composition. Zoo Biol 15:499–507
Nishiura H, Yamazaki A, Wakakuri K et al (2019) Yersinia infection in two captive guereza colobus monkeys (Colobus guereza). J Vet Med Sci 81:1201–1204. https://doi.org/10.1292/jvms.19-0039
NRC (2003) Nutrient requirements of nonhuman primates, 2nd edn. The National Academies Press, Washington DC
NRC (2007) Nutrient requirements of small ruminants: sheep, goats, cervids, and new world camelids. The National Academies Press, Washington DC
Ogata M, Seino S (2015) Genetic analysis of captive proboscis monkeys: genetic variation of captive proboscis monkeys in a Japanese zoo. Zoo Biol 34:76–79. https://doi.org/10.1002/zoo.21176
Overskei TL, Pirie G Jr, Veazey RS et al (1994) Entamoeba histolytica Infection in Hanuman (Semnopithecus entellus) and purple-faced (Trachypithecus vetulus) langurs. J Zoo Wildl Med 25:240–247
Palmieri J, Dalgard D, Connor D (1984) Gastric amebiasis in a silvered leaf monkey. J Am Vet Med Assoc 185:1374–1375
Pang V, Chang C, Chang W (1993) Concurent gastric and hepatic amebiasis in a dusky leaf monkey (Presbytis obscurus). J Zoo Wildl Med 24:204–207
Rappaport AB, Hochman H (1988) Cystic calculi as a cause of recurrent rectal prolapse in a sloth (Cholepus sp.). J Zoo Wildl Med. https://doi.org/10.2307/20094895
Santos F, Fuente R, Mejia N et al (2013) Hypophosphatemia and growth. Pediatr Nephrol 28:595–603. https://doi.org/10.1007/s00467-012-2364-9
Schubert L, Deluca HF (2010) Hypophosphatemia is responsible for skeletal muscle weakness of vitamin D deficiency. Arch Biochem Biophys 500:157–161. https://doi.org/10.1016/j.abb.2010.05.029
Schwitzer C, Polowinsky S, Solman C (2009) Fruits as foods–common misconceptions about frugivory. Zoo animal nutrition IV. Filander Verlag, Fürth, pp 131–168
Shelmidine N, McAloose D, McCann C (2013) Survival patterns and mortality in the North American population of silvered leaf monkeys (Trachypithecus cristatus). Zoo Biol 32:177–188. https://doi.org/10.1002/zoo.21055
Unwin S, Ancrenaz M, Bailey W (2011) Handling, anaesthesia, health evaluation and biological sampling. In: Field and laboratory methods in primatology: A practical guide, 2nd edn. Cambridge University Press, Cambridge
Van Soest PJ, Robertson JB, Lewis BA (1991) Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. J Dairy Sci 74:3583–3597. https://doi.org/10.3168/jds.S0022-0302(91)78551-2
Watkins BE, Ullrey DE, Whetter PA (1985) Digestibility of a high-fiber biscuit-based diet by black and white colobus (Colobus guereza). Am J Primatol 9:137–144. https://doi.org/10.1002/ajp.1350090207
Weatherall D (2006) The use of non-human primates in research. Medical Research Council, The Royal Society and Wellcome Trust, London, UK, Academy of Medical Sciences
Yeager CP (1989) Feeding ecology of the proboscis monkey (Nasalis larvatus). Int J Primatol 10:497–530. https://doi.org/10.1007/BF02739363
Yeager CP, Silver SC, Dierenfeld ES (1997) Mineral and phytochemical influences on foliage selection by the proboscis monkey (Nasalis larvatus). Am J Primatol 41:117–128. https://doi.org/10.1002/(SICI)1098-2345(1997)41:2%3c117::AID-AJP4%3e3.0.CO;2-%23
Acknowledgements
We thank all staff and veterinarians at YZG who are committed to managing and improving the health management of proboscis monkeys; we are especially grateful to Miya Ueda and Ryuta Kawasaki. We also thank the Sabah Biodiversity Centre, the Sabah Forestry Department, and the Sabah Wildlife Department for granting us permission to conduct this research in Sabah, Malaysia, and the Wildlife Rescue Unit rangers for their assistance in the field. We are grateful for the support from Dr. Danica J. Stark, Dr. Rosa Sipangkui and our research assistants in the field. We would also like to thank Marcus Clauss as well as an unknown reviewer for their very helpful comments on this manuscript. Finally, we would like to commemorate the four monkeys that died of renal disease.
Author information
Authors and Affiliations
Contributions
SH, IM, and MY developed the initial concept; AA performed necropsies of zoo individuals; SH conducted in situ sample collection and analyses; SKSSN, DARS and IM conducted sample collection in the field; BG and MSL analyzed the blood samples from free-ranging individuals; SS, AT, BG, and MSL arranged the sampling from the zoo and free-ranging animals; SH, IM, and MY performed and interpreted the statistical analysis and drafted the manuscript; MY organized the project. All authors contributed to the final version of the manuscript.
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Hoshino, S., Seino, S., Azumano, A. et al. Modifying the diets of captive proboscis monkeys in a temperate zoo to reduce weight loss and renal disease. Primates 64, 123–141 (2023). https://doi.org/10.1007/s10329-022-01031-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10329-022-01031-y