Primate Nutrition

Standards for feeding nonhuman primates

Charlotte Kirk Baer1 and Duane E. Ullrey2

U.S. National Research Council, The National Academies, Washington, D.C. USA

Current affiliations: 1Baer and Associates, LLC, Silver Spring, MD, USA and 2Michigan State University

In 2003 the U.S. National Research Council (NRC) published a second revised edition of its report Nutrient Requirements of Nonhuman Primates (National Research Council, 2003). This report is one of a series of NRC reports on animal nutrition and is an update and expansion of the first edition, which was published 25 years earlier. The revised report takes into account the large number of nonhuman primate species being fed in conservation organizations and research facilities today. The purpose of the recommendations in this report are twofold: (1) to provide science-based information for developing nonhuman primate diets and feeding programs and (2) to provide specific reference points and ranges for determining when dietary nutrient concentrations are adequate or inadequate. Regulatory agencies, industry, and other sectors rely on the NRC to provide these scientifically supported reference values so that when analyses are conducted, foods are formulated, diets are fed, and regulatory decisions are made, they are based on a frame-of-reference supported by scientific evidence and are not subjective. Unlike many reports in the NRC series, recommendations in this report are provided not only for minimum requirements, but also for estimated adequate dietary nutrient concentrations of diets containing conventional ingredients, which can be used to evaluate the adequacy of diets offered to primates.

For purposes of establishing nutrient requirements, nonhuman primates can be divided into six “model” categories based on gastrointestinal morphology, feeding ecology, taxonomic relationships, and the current state of knowledge (i.e., peer-reviewed research), which suggests that the “Old World” and “New World” designations are no longer appropriate in primate nutrition. Reflecting the new knowledge of the past quarter century, variation in feeding ecology and digestive physiology are new topics covered in great detail in the revised NRC report. In addition, comprehensive discussions of individual nutrients are provided throughout the report, with several new additions. Several novel aspects of the revision are noted below.

Although energy is not a nutrient in the sense of being a chemically identifiable substance, animals require energy for metabolic functions. Energy requirements of primates vary, as do their size and characteristics. Smaller primates exhibit higher mass-specific energy requirements for growth than larger primates and many species present unique challenges that could be affected by diet. For example, commercial diets for long-term maintenance of marmosets and tamarins formulated to contain 3.5-4.2 kcal of metabolizable energy∙g-1 may help to address “marmoset wasting syndrome” among Callithrix and Sanguinus species (Barnard et al., 1988; Clapp and Tardif, 1985).

Fiber is also not considered a nutrient but based on what we have learned in the past 25 years, certain fiber forms (fractions described by Van Soest et al., 1991) are known to be beneficial to health for certain groups of primates when fed in certain concentrations and proportions. For example, recommended fiber concentrations in total diet dry matter of extruded diets for callitrichids are 10% neutral detergent fiber and 5% acid detergent fiber; whereas for colobus monkeys (foregut fermenters), 30% NDF and 15% ADF are recommended.

Although quantitative recommendations for amino acid requirements of nonhuman primates cannot be defined, several amino acids are essential. The report discusses evidence for essentiality of methionine, lysine, phenylalanine, tryptophan, and taurine.

Both n-3 and n-6 fatty acids are essential nutrients for nonhuman primates. Fatty acids that could be detrimental include the long-chain, monounsaturated docosaenoic acids. Cholesterol, which is typically not found in manufactured primate diets (with the exception of infants consuming milk or formula), is synthesized in tissues and is likely not required.

For the first time in history, requirements for copper and selenium have been defined. Fat-soluble and water-soluble vitamin requirements have been updated.

In summary, much is known about feeding and nutrient needs of nonhuman primates; however, there are many gaps in our knowledge. The NRC report on primate nutrition, as well as upcoming reports on small ruminants, horses, and mineral tolerance of animals provide the foundation for appropriate nutritional husbandry of exotic animals. For institutions feeding these animals it is essential to utilize respected resources such as the NRC report and expert consultation to interpret current knowledge and to fill in the gaps.

References

Barnard, D., J. Knapka, and D. Renquist. 1988. The apparent reversal of a wasting syndrome by nutritional intervention in Sanguinus mystax. Lab. Anim. Sci. 38:282-288.

Clapp, N.K. and S.D. Tardif. 1985. Marmoset husbandry and nutrition. Digest. Dis. Sci. 30: 17S-23S.

National Research Council, The National Academies. 2003. Nutrient Requirements of Nonhuman Primates, Second Revised Edition. National Academies Press, Washington, D.C.

Van Soest, P.J., J.B. Robertson, and B.A. Lewis. 1991. Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. J. Dairy Sci. 74:3583-3597.

Author’s address:
C. Kirk Baer
U.S. National Research Council
The National Academies, Washington, D.C.
USA
e-mail: ckbaer@att.net

Food intake, nutrient intake and food selection in captive and semi-free Douc langurs (Pygathrix nemaeus ssp.)

C. Ademmer, W. Kaumanns

Cologne Zoo, Germany

Colobines are specialized folivorous primates with a pregastric fermentation system. The endangered Douc langur (Pygathrix nemaeus ssp.), a highly folivorous member of this family, inhabits forests of Vietnam, Laos and Cambodia. Morphological, physiological, social and behavioural adaptations allow this species to feed mainly on a diet characterized by low concentrations of easily accessible energy and nutrients. According to the optimal foraging theory (see Hume 1989), animals should optimize their energy and nutrient intake by choosing food items of the best quality. The quality of leaves highly depends on the protein:fibre ratio (Yeager et al. 1997). If Douc langurs select leaves according to the optimal foraging theory, they should select leaves with a high content of protein and a low content of fibre. One aim of the study presented here was to determine the food and nutrient intake of Douc langurs. Moreover, patterns of food selection should be described. In captivity, food selection is possible only within the range of the food plants offered. However, if patterns of food selection exist, they should be similar under different keeping conditions.
In this study, three keeping conditions were included: first, at Cologne Zoo, where the animals are fed a diet consisting of leaves, vegetables, lettuce, pellets and fruits (n=35 days total); second, at the Endangered Primate Rescue Centre (EPRC), situated in the Cuc Phuong National Park (Vietnam), where the animals are kept in outdoor cages and are fed exclusively with leaves of local plants (n=26 days); third, in an semi-free enclosure, consisting of a 4 ha area of primary forest in the Cuc Phuong National Park, which provides natural food trees (n=10 days). The Cologne data represent three different seasons (summer, winter and spring).
The mean individual food intake was estimated by weighing the food offer and leftovers of the captive groups. The individual food intake behaviour was observed by focal animal sampling, and the number of pick-up’s was counted for each food plant. Preference indices for certain food plants were calculated. Leaves of a large spectrum of food plants were analyzed for their content of nutrients and fibre.
In Vietnam, an animal was offered about 4000g fresh leaves per day of which 41% were consumed. The Douc langurs were observed to feed on 87 plant species belonging to 36 families (EPRC & semi-free condition). Most of the food plant species consumed in Vietnam belonged to the family Leguminosae.
In Cologne, an animal was offered about 370g fresh leaves per day of which 37% were consumed. Leaves constitute about 12% of the total diet in Cologne. The Douc langurs at Cologne Zoo were observed to feed on 28 species belonging to eleven families. Most of the food plant species consumed in Cologne belonged to the family Salicaceae. In spring, the amount of leaves consumed per animal and day was higher than in summer. During winter, leaf intake reached a minimum with only about 40% of the amount eaten in spring. Regarding the nutrient and fibre content, spring leaves showed a higher protein:fibre ratio than summer and winter leaves.
When young leaves were present, they were consumed first. This was observed under all keeping conditions and for all food plant species.
The results suggest that in fact Douc langurs select leaves with a high protein and a low fibre content, although the presence of other nutrients and of secondary plant compounds would have to be considered as well. The selection of leaves showing a high protein:fibre ratio corresponds to findings of other studies (Bleisch et al. 1998, Yeager et al. 1997) and would be compatible to the expectations of the optimal foraging theory. For the first time, the food and nutrient intake of Douc langurs living under different conditions have been described quantitatively. In spite of the small sample size and the restriction to non-experimental study-conditions, this study provides important information with regard to in situ and ex situ conservation of Douc langurs and other Colobines, as well as reference values for further studies.



References
• Bleisch, W.V., Liu, Z.M., Dierenfeld, E.S. & J.H. Xie (1998): Selected nutrient analysis of plants in the diet of the Guizhou Snub-nosed monkey (Rhinopithecus brelichi). In: Jablonski, N.G. (ed.): The Natural History of the Doucs and Snub-nosed monkeys. Singapore: World Scientific Publishing: 241-254
• Hume, I.D. (1989): Optimal digestive strategies in mammalian herbivores. Physiological Zoology 62(6): 1145-1163
• Yeager, C.P., Silver, C.S. & E.S. Dierenfeld (1997): Mineral and phytochemical influences on foliage selection by the proboscis monkey (Nasalis larvatus). Am. J. Primatol. 41(2): 117-128


Author’s address:
C. Ademmer
Cologne Zoo
Working Group Primatology
Riehler Str. 173
D-50735 Cologne
Germany
e-mail: ademmerc@gmx.de

Effect of fruits and vegetables on the diet of Silvered leaf langurs (Trachepithecus auratus auratus)

J. Nijboer1, M. Olsthoorn2, W. Noordermeer2, T.R. Huisman2, A.C. Beynen3

1Rotterdam Zoo, the Netherlands, 2Van Hall Instituut, the Netherlands, 3University of Utrecht, the Netherlands

The natural diet of silvered leaf monkeys consists of 55-80% leaves. In zoos they are often fed on considerable amounts of fruit and vegetables; However, consuming too much fruit and vegetables will cause soft stools. These soft faeces are probably caused by the higher amount of non-structural carbohydrates (NSC) compared to the more fibrous NDF (Neutral Detergent Fibre) character of the diet in situ.
This research focuses on the effect of removing fruit and vegetables from the monkey diet and the resulting altered NDF/NSC-ratio on faecal consistency.
Trials were carried out at Apenheul as well as at Rotterdam Zoom, (two zoological collections in the Netherlands).
Ten animals were involved at Apenheul, five animals at Rotterdam Zoo. The trial consisted of three periods (A1, B and A2). During the control periods (A1 and A2) the usual diet, containing fruit, vegetables, langur pellets and browse was fed. During the experimental period (B), vegetables and fruits were removed and the diet consisted of pellets and browse only. During the entire trial the food offered was weighed and the food remains were collected and weighed. The faeces was collected and classified. The faecal classification system ranged from 1 – 5; 5 being loose stool, and 1 being firm stool.
Samples of the diet, food remains and also of the faeces were analysed following the Van Soest and the Proximate Analysis method at the Nutritional Department of the Veterinary Faculty of Utrecht University.
During the B period the intake of both the langur pellets and the browse increased and the faecal consistency improved in both zoos. The faecal consistency score improved from 4 to 2 at Rotterdam and from 3.5 to 2 at Apenheul. For optimum faeces quality (2) is suggested that the optimal ratio between NDF and NSC should be 1.30. More detailed research is necessary to understand the digestion mechanism in langurs.


Author’s address:
J. Nijboer
Rotterdam Zoo
Postbus 532
3000 AM Rotterdam
The Netherlands
e-mail: J.Nijboer@Rotterdamzoo.nl

Food intake and body weight of the blue-eyed black lemur (Eulemur macaco flavifrons) in captivity

S.Y. Polowinsky, C. Schwitzer

Zoologischer Garten Köln, Riehler Strasse 173, D-50735 Köln, Germany

The blue-eyed black lemur (Eulemur macaco flavifrons) is a highly endangered medium-sized lemur from north-west Madagascar with a mean body weight of 1793 g and a mean body length of about 41 cm. Its habitat consists of mixed forest, dry forest, coffee and citrus plantations. The nutritional ecology of blue-eyed black lemurs in the wild has so far not been studied; generally Eulemur macaco flavifrons is classified as frugivorous.
Under captive conditions, lemurs seem to be susceptible to obesity, especially blue-eyed black lemurs (body weight in captivity: 2800 – 3200 g). It is unknown whether the high susceptibility to obesity in this species can be exclusively attributed to a surplus of food and a lack of locomotion in captivity in combination with a comparatively high efficiency of energy utilisation.
This study deals with aspects of the feeding ecology (quality, quantity, seasonal differences and preferences in food consumption, digestibility, activity budgets) of four blue-eyed black lemurs kept at Cologne Zoo. The aim of this study is to reveal possible correlations between food consumption and weight development and name factors, which influence food intake and body weight.
The following methods are used: All food offered to the animals is weighed daily and leftovers are weighed on the following day respectively. Possible food preferences shall be exposed. Additionally the animals are weighed weekly. Samples of feeds are analyzed for gross energy and according to Weende detergent analysis.
Preliminary data on the effect of food and nutrient intake on the body weight of blue-eyed black lemurs in captivity are presented.
This study is part of a comprehensive project, which includes investigations on free-ranging blue-eyed black lemurs in the Sahamalaza region in north-west Madagascar. It aims in collecting systematically data on the quality, quantity and spatio-temporal distribution of food consumed by wild blue-eyed black lemurs.

Author’s address:
S.Y. Polowinsky
Zoologischer Garten Köln
Riehler Strasse 173
D-50735 Köln
Germany
e-mail: s.polowinsky@worldonline.de

Feeding the Gentle Giant: Aspects of Gorilla Dietary Regimes in Zoos

K. A. Dörnath Aguirre Alvarez1, 2, A. Alonso Aguirre3, 4, E.S. Dierenfeld5, K. Eulenberger1

1Zoo Leipzig,, Germany,2Bristol Clifton and West of England Zoological Society, Bristol Zoo Gardens, Guthrie Road, Clifton, Bristol BS8 3HA, United Kingdom, 3Wildlife Trust, New York, USA, 4Center for Environmental Research and Conservation, Columbia University, Schermerhorn, New York, USA, 5St. Louis Zoo, USA

For the first time, current data on various aspects of gorilla feeding regimes in EEP holdings are being presented. The only similar study, conducted within the SSP, was published by Popovich and Dierenfeld in 1997.
Looking at various zoos, gorillas are being fed very different diets (Hampe,1999). This is probably due to most institutions basing gorilla feeding and diets on empirical knowledge.
In our study, we were primarily interested in collecting qualitative data regarding different aspects of gorilla feeding regimes in captivity, concentrating on EEP holdings. We firstly aimed at finding out differences and similarities amongst feeding regimes of the various institutions; secondly, we wanted to compare natural feeding strategies of wild ranging gorillas with what the current captive feeding regimes can offer to zoo gorillas; thirdly, we were interested in what diseases and behavioural abnormalities might be linked with captive gorilla feeding.
Gorilla diets in the wild as well as in zoological institutions were reviewed by means of an extensive literature review having used the electronic databases Agricola (1970-2004), Biological Abstracts (1969-2004), Medline (1966-2004) and PrimateLit (1940-2004), as well as having manually reviewed a wealth of publications.
Information on the current feeding regimes in various zoos was obtained using a questionnaire. This was sent out to the 57 gorilla EEP holdings (including Israel) listed in the 2003 Gorilla Studbook (Hilsberg and Bender 2004). In addition, other institutions worldwide volunteered to take part in this study after a request was sent out to the electronic gorilla keeper discussion group. All answers were analysed confidentially and the data will be presented anonymously. At the time of writing, 43 out of 57 (i.e. 75,4 %) EEP institutions participated in this study; 10 zoos outside the EEP contributed data.
Certain aspects were identified of particular importance for the survey, hence the following questions were asked offering multiple-choice answers:
· What is the basis for the gorilla diet in your institution?
· How many meals a day do you offer to the gorillas?
· How many different food items do you offer to the gorillas each day?
· Which food items do you offer throughout the year? (Categories: browse, vegetables, fruits, animal products, commercial diets, liquids other than water, other)
· How often do you offer browse to the gorillas?
· If you offer animal products, which are these and how frequently are they being offered?
· Do you change the diet seasonally?
· Do the gorillas have access to a source of potable water at all times?
· Do you supplement the diet? If yes, how?
· Do you separate the gorillas during feeding? If yes, why?
· Do you hand fed the gorillas? If yes, why?
· Have you experienced cases of diseases related to nutrition in your collection?
· Are the gorillas in your collection generally overweight or obese?
· Do the gorillas in your institution show any regurgitation/ reingestion (R/R)?
In addition to offering an overview and a discussion on the results we received, a list of items being fed to zoo gorillas will be provided including an extensive browse list.

Acknowledgement
This survey was only possible with the support and participation of numerous zoological gardens worldwide. We would like to express our enormous gratitude and appreciation to these institutions for having taken their time and effort to fill in the questionnaire.

References
Hampe, K. (1999): Erhebungen zur Ernìhrung ausgewìhlter Primatenspezies in menschlicher Obhut. Inaugural-Diss. Dr. agr. Justus-Liebig-Universitìt Gieÿen, Gieÿen.
Hilsberg, S., U. Bender (2004): International Register and Studbook for the Gorilla (restricted to Gorilla g. gorilla) 2003. Frankfurt Zoological Garden. ISSN 0934-2656
Popovich, D.G., E.S. Dierenfeld (1997): Nutrition. In: Ogden, J., D. Wharton (1997): Management of gorillas in captivity. Husbandry manual. Gorilla Species Survival Plan.
Abbreviations:
EEP – Europìisches Erhaltungszuchtprogramm (European Endangered species
Programme)
SSP – Species Survival Plan

Address of Corresponding Author
K. Alexandra Dörnath Aguirre Alvarez, MSc Wild Animal Health, MRCVS
Bristol Zoo Gardens
Veterinary Department
Guthrie Road
Clifton
Bristol BS8 3HA
United Kingdom
e-mail: adoernath@bristolzoo.org.uk