NUTRITION GUIDELINES for CROWNED LEMURS (Eulemur coronatus ) 1,4 – 1,8 Kg RED BELLIED LEMURS (Eulemur rubriventer ) 1,7 2,0 Kg SCLATER'S BLACK LEMURS (Eulemur macaco flavifrons ) 1,9 – 2,6 Kg
Edited by David GOMIS Contributors : Pierre MOISSON and Sara DE MICHELIS ACKNOWLEDGEMENTS Thanks to animal keepers’ staff from Mulhouse Zoo, for their collaboration to the intake surveys. Especially to Corinne Fromm for the plant database, Claire Prieur, Aline Drouin and Frédéric Seyffarth for the body weight survey, Fanny Huth for the hemosiderosis survey and Caroline Kammerer for the english text reviewing. Thanks to Roland Bulliard (Servion Zoo), Graham Catlow (Edinburgh Zoo), Clare Jenkinson (Banham Zoo), Jana Kálnová (Ostrava Zoo), Alexander Sliwa (Cologne Zoo), Cédric Libert (Montpellier Zoo), William Magnone (Parco Natura Viva), Thierry Petit (La Palmyre Zoo), Frank Rietkerk (Apenheul Primate Park), Claire Saunders (Colchester Zoo), Emma Stanley (Linton Zoo) and Ewa Trzesowska (Poznan Zoo) for providing their datas on Scalter’s black lemurs. Thanks to Christoph Schwitzer (Bristol Zoo) and Sandra Polowinsky (University of Bonn, Institute of Animal Science) for providing their data and expertise on the Sclater’s black lemur ecology in Sahamalaza Reserve and in captivity. Thanks to Andrea L. Fidgett (Chester Zoo), Ellen Dierenfeld (Novus International, Inc.), Joeke Nijboer (Rotterdam Zoo) and Christoph Schwitzer (Bristol Zoo) for their comments and reviewing the document. Thanks to Aline Drouin (Mulhouse Zoo) and Thierry Petit (La Palmyre Zoo) for their photographs. Thanks to the members of the ‘Association Européenne pour l’Etude et la Conservation des Lémuriens’ (AEECL) for promoting field research projects in Madagascar since more than 10 years.
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 2 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 Preliminar note: Meeting the nutritional needs of lemurs is essential to assure their survival and their reproduction in captivity. Present guidelines are not formal nutrition recommendations, but a first evaluation mainly focussed on Sclater’s black lemurs zoo diets and constitute the major nutrition guidelines we should respect in captive conditions. We hope that you will find in this work some valuable information in order to improve your feeding regimes for Sclater’s black lemurs, Crowned lemurs and Red bellied lemurs. David Gomis, DVM Note from the Coordinator: As coordinator of these EEPs, I can only stress that nutrition is an essential part for the success of any reproduction/conservation program. You can have all the the ARKS, SPARKS, MedARKS or PM2000 data published with precision, without good food (and of course good social and medical follow up), population management of your species is impossible to perform with positive results. I encourage any holder to be careful of the quality and of the quality of the food thay give to their lemurs, in order to maintain healthy red bellied, Sclater’s and crowned lemurs in their facilities. And of course thank you to all contributors of these guidelines, especially to David. Pierre Moisson, DVM Red bellied lemur EEP Coordinator Sclater's black lemur EEP Coordinator Crowned lemur ESB Studbook keeper
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 3 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 TABLE OF ABBREVIATIONS ADF ______Acid detergent fiber AF ______As fed Al ______Animal BMR ______Basal metabolic rate BW______Body weight CP ______Crude protein (D) DM ______(Dietary) Dry matter DMI ______Dry matter intake IU ______International Unit ME ______Metabolisable energy nd ______Number of days NDF ______Neutral detergent fiber ng ______Number of groups ni ______Number of individuals NRC ______National Research Council ns ______Number of studies NSC ______Non structural carbohydrate SD ______Standard deviation SE ______Standard error TDF ______Total dietary fiber Vit. ______Vitamin
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 4 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 CONTENTS page 1 Introduction 7 2 Feeding ecology, gastrointestinal physiology and requirement establishment 8 2.1 Geographic range and habitat 8 2.2 Gastrointestinal physiology of diurnal generalist lemurs 8 2.3 Feeding ecology and requirement establishment 10 2.3.1 Feeding ecology studies 10 2.3.2 Cathemeral activity 10 2.3.3 Nutritional studies 11 2.3.4 Requirement establishment 15 3 Nutritional related problems in captivity 19 3.1 Behavioural problems 19 3.2 Coprophagy 19 3.3 Obesity and reproductive failure 19 3.4 Dental problems 22 3.5 Hepatic iron storage disease (hemochromatosis) 23 3.6 Diabetes mellitus 25 3.7 Renal failure and periarticular hyperostosis 25 4 Practical feeding strategy 26 4.1 How to control the global intake 26 4.2 How to choose fruits and vegetables 29 4.3 How to meet the protein requirement 30 4.4 How to control the mineral & vitamin supplementation 31 4.5 How to control the energy intake 31 4.6 How to manage an overweight lemur 33 Appendixes 35 Appendix 1: Eg. of an intake study for Crowned lemurs at Mulhouse Zoo, France 35 Appendix 2: Eg. of an intake study for Red bellied lemurs at Mulhouse Zoo, France 36 Appendix 3: Eg. of an intake study for Blue eyed Black lemurs at Mulhouse Zoo, France 37 Appendix 4: Eg. of the feeding regime for Blue eyed Black lemurs at Banham Zoo, UK 38 Appendix 5: Eg. of the feeding regime for Blue eyed Black lemurs at Edinburgh Zoo, UK 40 Appendix 6: Eg. of the feeding regime for Blue eyed Black lemurs at Montpellier Zoo, France 41 Appendix 7: Eg. of the feeding regime for Blue eyed Black lemurs at Colchester Zoo, UK 42 Appendix 8: Survey on the BW of captive Blue eyed Black lemurs in European zoos 43 Appendix 9: Nutrient composition of the pellets used at Mulhouse Zoo, France 45 Appendix 10: List of fruits and vegetables given to Eulemur sp. at Mulhouse Zoo, France 46 Appendix 11: Recipe and composition of the “milk bread mixture” at Mulhouse Zoo, France 47 Appendix 12: Plants’ database for Eulemur sp. at Mulhouse Zoo, France 48 Appendix 13: Proposed requirement ranges for diet formulation and analysis 49 Appendix 14: Some BW records for captive Red belied lemurs in Mulhouse Zoo 50 Appendix 15: Some BW records for captive Crowned lemurs in Mulhouse Zoo 51 References 52 Summary box 56
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 5 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 6 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 1 Introduction: The isolated adaptative radiation of lemurs on Madagascar and their food intake strategy Most lemurs are generalist feeders, omnivorous with fruits or leaves dominating other plant parts, and usually fed in zoos with fruits, vegetables, pellets, seeds, etc. As with many other primates, feeding behaviour in wild conditions differs a lot from captive one: in zoos, animals spend less time feeding, are usually offered large amounts of food in order to reduce conflicts and appear to be more suceptible to obesity (Schaaf et al. , 1983; Pereira et al. , 1995; Schwitzer, 2003). Existing studies of their feeding ecology are often based on a qualitative, more than on a quantitative aspect. Thus, food intake regulation is poorly known. Among primates, the isolated adaptive radiation of lemurs on Madagascar may explain their food intake strategy as an adaptative response to a harsh and unpredictable island environment. The abundance of resources (flowers, seeds, fruits, nectar, insects, etc.) vary significantly from dry to wet season, with irregular, asynchronous or alternate vegetal production cycles. Also frequent cyclones and droughts destroy large proportions of resources, even though the nutrient intake may not vary between seasons (Wright, 1999; Curtis, 2003; Schwitzer, 2003; Schwitzer et al. , 2007). The nutritional ecology and the low metabolism of lemurs constitute only one feature of their adaptation to the seasonal occurrence of food with relatively low nutritional quality. Some authors propose an “energy conservation hypothesis” (ECH) or an “evolutionary disequilibrium hypotheses” (EVDH) to explain also other behavioural features of lemurs, like the female dominance, the targeted female female aggression, the sperm competition coupled with male male aggression, the lack of sexual dimorphism regardless of mating system, the high infant mortality, the strict seasonal breeding, and the cathemerality. Wright [1999] suggests a more comprehensive “energy frugality hypothesis” (EFH) “which postulates that the majority of lemur traits are either adaptations to conserve energy (e.g., low basal metabolic rate (BMR), torpor, sperm competition, small group size, seasonal breeding) or to maximize use of scarce resources (e.g., cathemerality, territoriality, female dominance, fibrous diet, weaning synchrony)”. This “energy frugality hypothesis” may explain the high susceptibility to obesity of this taxon in captivity: low energy expenditure in captive conditions, combined with a low BMR and an over provision of unvaried and to richer food, can certainly promote obesity (Mc Cormic, 1981; Müller, 1983; Daniels, 1984; Richard et al. , 1987; Schmid et al ., 1996). The high energy input/low energy output foraging strategy from lemurs, and their high efficiency of energy utilisation, may not explain all. The specialization of lemurs on fruit results in protein requirements being achieved probably by a narrow margin, like for frugivorous birds (Simmen et al. , 2007). Thus, quantitative or qualitative poor dietary proteins of an unbalanced zoo diet may also lead to an energy intake excess (Gomis, 2008). In the same manner, preliminary data obtained from an in vitro fermentation system seem to prove that fermentation in the gut may be more flexible for Eulemur sp. than for Varecia sp. and Hapalemur sp. , depending on the type of fiber present in the diet (Campbell et al. , 2002). Thus, dietary fiber content and quality may interact differently with energy intake, nutrient digestibility and transit time from one species to another, and also lead to an excessive white adipose tissue deposition. Food resources availability in wild or semi captive conditions may have a major limiting effect on population size, through feeding competition and proportion of multiple births: an increase in the abundance of food usually leads to an immediate change in the reproductive output of the population (Pereira, 1993; Simmen et al. , 2007). Superabundant and unbalanced zoo diets have the opposite effect, with lower or nil breeding rates for obese females. Thus, meeting the nutritional needs through present nutrition guidelines is essential to assure the reproduction in captivity and the future of these endangered species breeding programmes.
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 7 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 2 Feeding ecology, gastrointestinal physiology and requirement establishment 2.1 Geographic range and habitat Sclater’s black lemurs occur in the semi deciduous forests just east of and on Sahamalaza Peninsula, in northwest Madagascar. They seem to be able to adapt to the different types of habitat (highly fragmented stretches of primary or secondary forest) in this transition zone between the western dry deciduous forest region in the south and the wetter Sambirano region in the north. Their ecological and behavioural flexibility has only recently been analysed in Ankarafa forest, highlighting that home range size (which correlates with the distribution of food resources), use of habitat and population densities vary from primary to secondary forest (Robins et al. , 2006; Schwitzer et al. , 2007). Thus, blue eyed black lemur cannot be classified as a habitat generalist. Crowned lemurs occur from the extreme north, on the Cap d’Ambre Peninsula, southwest to Ambilobe and probably some distance down the Mahavavy River. To the east the Bemarivo River is possibly the limit. They exist throughout this range in all forests, semi deciduous dry tropical and humid ones (Mittermeir et al ., 1994 and 2006). Home range size has not been reported for this species. They seem to occur more in dense forests than damaged or secondary ones (Wilson et al. , 1989). Red belied lemurs occur in the eastern rainforest, from the Tsaratanana Massif to the Pic d’Ivohibe Special Reserve and the Manampatrana River (Mittermeir et al ., 2006). They seem restricted to dense evergreen forests, with a canopy of Fig. 1: Map of Eulemur ssp (part) from MITTERMEIR et al., 2006 (p.271) 25 to 35 m. None of these 3 threatened and sexually dichromatic Eulemur species seem to be a real habitat generalist, their ecological and behavioural flexibility depending on the quality of the forested cover. 2.2 Gastrointestinal physiology of diurnal generalist lemurs Gastrointestinal morphology among the Eulemur species is quite similar with a simple stomach, a moderately long small intestine, a large and capacious cecum, and a short colon (Campbell, 2003, Fig.2). No considerable difference is seen in comparison with frugivorous lemur species. A larger and sacculated cecum and/or colon are found on folivores or bamboo feeders, related to the important fermentation of the fibrous components of the diet. Among all of the diurnal lemurs, numerical data (Table I) are similar with the exception of the data from Propithecus species. They possess a much larger ratio of total intestine length to body length (Table II) compared to all other species reported. No species differences are observed among the diurnal lemurs in length of either small or large intestine as a percentage of total intestine length. Among the generalists, only L. catta posses the largest ratio of total intestine to body length (Campbell, 2003).
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 8 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 GASTROINTESTINAL TRACTS FROM GENERALIST FEEDERS: Brown lemur Crowned lemur Ring tailed lemur Eulemur fulvus Eulemur coronatus Lemur catta COMPARED TO THOSE FROM: FRUGIVORES FOLIVORES BAMBOO FEEDERS Red ruffed lemur Coquerel’s sifaka Gentle grey lemur Varecia variegata rubra Propithecus verreauxi coquereli Hapalemur griseus griseus
Fig. 2: Gastrointestinal tracts from diurnal prosimian species from CAMPBELL J.L. (2003), illustrations of STEVENS & HUME (1995) Table I: Mean measurements of length of the small intestine, cecum, and colon from diurnal prosimian species from CAMPBELL J.L. (2003)
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 9 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 Table II: Mean measurements of body weight and gastrointestinal tract length ratios for diurnal lemurs. from CAMPBELL J.L. (2003): 2 Diet categories are based on published observations as follows: Generalist (Mittermeier et al., 1994); Frugivore (Britt, 2000); Bamboo (Tan, 1999); Folivore (Richard, 1977; Meyers, 1993). The gastrointestinal tracts of Sclater’s black lemurs, Crowned lemurs and Red bellied lemurs are all three similar to those illustrated for E. fulvus and E. coronatus in Fig. 2. The three species are diurnal generalists that consume a diet consisting of leaves, fruits, seeds, nuts, and occasionally small animal prey. The presence of a large cecum suggests that there is potential for some fermentation of the fibrous components of foods consumed (Campbell, 2003). This morphological adaptation may certainly help these species to adapt to an unpredictable environment, and to maximize the use of alternative resources such as leaves. 2.3 Feeding ecology and requirement establishment 2.3.1 Feeding ecology studies In general, reported data from feeding ecology studies across Eulemur species did not differ greatly. All are generalists, omnivorous with fruits or leaves dominating other plant parts (see table III), consuming abundant arthropods during the wet season – such as millipedes, spiders, froghoppers and cicadae ( Pycna madagascariensis ) (Birkinshaw, 2003; Schwitzer pers. com. , 2006) , rarely small animal prey, and adapting their regimes to available food resources (Campbell, 2003; Sussman, 1999). The potential for feeding flexibility may however be lower than expected when species tend to specialize more on fruits, as revealed by recent observations of Eulemur macaco macaco in an old coastal secondary forest of north western Madagascar. Protein requirements being achieved probably by a narrow margin, the patchy distribution of preferred cash crop plants and indigenous species has a major limiting effect on population size through feeding competition (Simmen, 2007). Table III: Dietary data for comparison between Varecia and Eulemur sp. from GODFREY et al. (2004)
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 10 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 The observations undertaken on Eulemur macaco flavifrons in the fragmented habitat of the Sahamalaza peninsula also demonstrate the importance of the quality of the forested cover : this species use differently primary (even with higher human pressure and less dense canopy) and secondary forests. The density of Sclater’s black lemurs was higher and home range size smaller, in primary forest. Primary dense forest may be necessary, not only for facing bad weather conditions (stormy dry season) and aerial predation, but also for its higher plant biodiversity (Schwitzer et al. , 2007). 2.3.2 Cathemeral activity Eulemur species are known to have a cathemeral behaviour, affected by a variety of environmental factors including temperature, rainfall, habitat structure (primary / secondary forest), canopy cover, predation, food resources availability and quality, as well as nocturnal moon luminosity (Colquhoun, 1998; Curtis et al. , 1999, 2002 and 2006; Kappeler et al. , 2003; Erkert et al. , 2006; Tatersall, 2006; Tarnaud, 2006; Donati et al. , 2006; Schwitzer et al. , 2007). Seasonal shift from more nocturnal activity to more diurnal activity is observed for E. mongoz, E. rufus , E. fulvus fulvus and E. fulvus collaris , while E. macaco macaco and E. m. flavifrons tend to exhibit cathemeral activity throughout all of the year. This seems best explained as a flexible response to varying environmental factors that inhibit or enhance activity. 2.3.3 Nutritional studies Overall, fruits consumed by wild primates are more comparable in their nutrient composition to vegetables used in zoo diets (Schwitzer at al. , 2008). Phytochemical analysis of wild diets are highly important to understand better the nutritional mistakes made in captivity. Sadly, these data are quite scarce for Eulemur species, but those available reveal that frugivorous zoo fed diets do not consider frugivory on a right nutritional basis: protein, fiber and metabolizable energy content, as well as sugar composition, are often inadequate. Recent phytochemical analysis undertaken on Mongoose lemurs ( Eulemur mongoz ) wild diets in north western Madagascar (Curtis, 2003) revealed that: immature leaves were richest in protein and essential amino acids, mature fruit and flowers contained the most water soluble carbohydrates, the limiting amino acids in all plant foods were methionine and cystine, mineral content was highest in petioles and mature leaves, crude lipid content was highest in seeds, crude fiber content was indistinguishable between immature and mature fruit and leaves, high fiber foods were eaten during both seasons, the wet season diet was dominated by high energy foods (mature fruit, nectar, and seeds), the dry season diet contained foods high in energy (mature fruit and flowers) and high in protein (immature leaves) and minerals (mature leaves and petioles), nutrient intake did not vary between seasons. A nutritional study was also undertaken in captivity for Mongoose lemurs ( Eulemur mongoz ) at Bristol Zoo Gardens (Willis et al. 2008). Activity budgets were established and five day digestibility trials were
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 11 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 organised with samples analysed for dry matter (DM), crude protein (CP), crude ash (CA), crude fiber (CF) and ether extract (EE) as well as for neutral detergent fiber (NDF) and acid detergent fiber (ADF). Nitrogen free extracts (NFE) were calculated as 100 CP CA CF EE. The results of this study showed that: the diet consumed was high in easily available carbohydrates and relatively low in fiber, the animals preferred fruits and vegetables over the rest of their diet, dry matter and nutrient digestibility was high these captive lemurs consumed more energy than their wild conspecifics. Concerning Sclater’s black lemurs ( Eulemur macaco flavifrons ), a recent survey was undertaken in the Sahamalaza peninsula in 2004 2005, as part of AEECL’s Programme Sahamalaza (Association Européenne pour l’Etude et la Conservation des Lémuriens). 68 fruit samples and 60 leaf samples from 48 plant species utilized as food resources, as well as from 10 species growing in the lemurs’ habitat but not utilized, were analyzed and compared to 13 fruit samples and 29 vegetable samples at Cologne Zoo (Schwitzer, 2006; Schwitzer et al. , 2008; Polowinsky & Schwitzer, 2008). These analysis demonstrated that: Malagasy fruits and leaves did not differ considerably from each other (see table IV), fruits consumed differed from those not consumed in having a lower fiber and a higher fat content (see table V), leaves consumed only showed a slightly lower lignin and higher protein content than leaves not consumed (see table VI), wild fruits had a considerably higher content of Neutral Detergent Fiber (NDF), Acid Detergent Fiber (ADF) and Acid Detergent Lignine residue (ADL) than fruits fed in Cologne Zoo (see table VIII), wild fruits were higher in Crude Protein (CP) and NFC as well as in Metabolizable Energy (ME) content, wild and zoo fed fruits moreover differed in sugar composition, with the domesticated fruits being higher in sucrose and the wild fruits higher in glucose and fructose content. This research project was continued by S.Y. Polowinsky for her doctoral thesis (Polowinsky, 2008), who compared not less than 112 Malagasy plant samples to 75 food samples collected in Cologne Zoo and 32 food samples collected in Mulhouse Zoo. This tremendous work confirmed that: the mean nutritional compositions of Malagasy plants collected during the wet season (68 samples) and the dry season (44 samples) did not differ significantly, the mean nutritional compositions of Malagasy plants collected in primary forests (22 samples) and in secondary forests (19 samples) did not differ significantly, excepted for the ash content, this being higher in primary forests’ plant items (55.8 g/Kg versus 45.2 g/Kg, p=0.041), the mean nutritional compositions of Malagasy plants consumed (26 samples) and not consumed (18 samples) during the dry season did not differ significantly, excepted for the crude protein content, this being higher for consumed plant items (this may suggest a possible discrimination
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 12 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 Table IV: Comparison of Malagasy fruits and Malagasy leaves Table V: Comparison of Malagasy fruits consumed and Malagasy fruits not consumed Table VI: Comparison of Malagasy leaves consumed and Malagasy leaves not consumed Table VII: Comparison of Malagasy leaves to vegetables consumed at Cologne Zoo Table VIII: Comparison of Malagasy fruits to fruits consumed at Cologne Zoo All tables from SCHWITZER C. (2006) Nutritional ecology of the blue eyed black lemur ( Eulemur macaco flavifrons ) In: Scientific report to the board of AEECL - Programme Sahamalaza 2006/2007. Please note that data from tables IV to VIII cannot be produced or transmitted in any form without written permission from C. Schwitzer.
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 13 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 of protein content or CP/TDF ratio, even if no data is currently available for Eulemur species: see next chapter 2.3.4), the mean nutritional compositions of Malagasy fruits consumed and not consumed during the dry season did not differ significantly, while the leaves consumed during this season showed a lower ADL content (178 g/Kg versus 274 g/Kg) (this confirms the previous data from Schwitzer, 2006: see table VI), the mean nutritional compositions of ex situ and i n situ diets significantly differ, excepted for ash and crude fat contents (see table IX below) Table IX: Comparison of ex situ (Cologne and Mulhouse Zoos) and in situ mean diets (Polowinsky, 2008: p.70) the NDF, ADF, ADL and crude fat contents were significantly higher in the fruits collected in situ versus the vegetables offered ex situ , while their ash, crude protein and NFC contents were significantly lower (see table X below), the ash, NDF, ADF, ADL and crude fat contents were significantly higher in the fruits collected in situ versus the fruits offered ex situ , while their NFC and energy content were significantly lower (see table X below, this confirms the previous comments about the sugar composition in domesticated fruits, the ash, NDF, ADF, ADL and crude protein contents were significantly higher in the leaves collected in situ versus the fruits offered ex situ , while their NFC and energy content were significantly lower (see table X below), the NDF, ADF and ADL contents were significantly higher in the leaves collected in situ versus the vegetables offered ex situ, while their ash, NFC and energy contents were significantly lower (see table X below, this confirming the data of table VII too), the NFC and energy contents were significantly higher in the fruits versus the vegetables, both offered ex situ , while their ash, NDF and crude protein were significantly lower (see table X below), the NFC content was significantly higher in the fruits versus the leaves, both collected in situ , while their ash and crude protein content were significantly lower (see table X below, this confirms data from table IV: Malagasy fruits and leaves do not differ considerably from each other) Table X: Comparison of fruits and leaves collected in situ and offered ex situ (Polowinsky, 2008: p.72)
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 14 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 2.3.4 Requirement establishment Specific dietary requirements have not been determined for most lemur’s species. Accurate data concerning nutrient requirements and their digestibility are scarce and the only recommendations published by the National Research Council, Committee on Animal Nutrition (NRC, 2003) concern the fiber content of the diets (20% NDF and 10% ADF in DDM; Table 11 1) and the energy requirement (110 176 BMR in Kcal / day / Kg BW and 278 454 MMR in kcal of ME / day / Kg BW; Table 2 1: see table XI of this report). Carbohydrates and fiber The values proposed by the NRC concerning fiber concentrations in total DDM for the Lemurs are based on Varecia variegata model and recommended for extruded diets, for which higher fiber concentrations than 30% NDF and 15% ADF in DM are difficult to extrude with present technology ( 1) for an acceptable waste (see NRC, 2003: Table 3 5). Fiber concentrations in wild Eulemur diets have been described to reach higher contents, eg. 58,7% NDF DM and 49,0% ADF DM for Eulemur fulvus (Ganzhorn, 1988; see also NRC, 2003: Table 3 3). Non folivorous Lemurs are considered to have a medium ability to utilize plant cell wall, as previously illustrated with the presence of a large cecum suggesting that there is potential for some fermentation of the fibrous components of foods consumed (Campbell, 2003; see previous § 2.2). However, their relative digestibility of NDF may be comparable with that seen in domestic mammalian species (Edwards, 1995: Ruffed lemurs as Lemur model). As previously seen with nutritional studies undertaken on both wild and captive Eulemur sp. , the fiber and carbohydrate contents of captive diets are very different than those observed for wild conspecifics. Frugivory is commonly adapted wrongly in zoo diets with low fiber, low protein, high energy and high sucrose fruits (Curtis, 2003; Schwitzer, 2006; Willis et al. 2008; Schwitzer et al. , 2008; Polowinsky & Schwitzer, 2008). Minerals Possibly, lemurs are efficient at mobilizing calcium from the diet because of the marginal amounts in natural foods. When provided complete and balanced diets, excessive calcium may be absorbed (eg. of metastatic calcifications reported for diademed sifaka) (Junge, 2003). Opposing this, given the opportunity for free choice among mixtures of nutritionally “complete” biscuits or pellets, fruits, vegetables, browse, and insects, the likelihood of calcium (Ca) deficiency is real. With the exception of primate biscuits and some green, leafy vegetables, most of these foods are inadequate sources of Ca. In spinach, much of the Ca is bound to oxalate and unavailable. Sprinkling on Ca supplements does not necessarily prevent Ca deficiencies that might appear when mixed diets are fed. That practice was attempted with two species of lemurs ( Lemur catta and V. variegata ) at the Cincinnati Zoo, but much of the supplement did not adhere to the foods; signs of nutritional secondary hyperparathyroidism were seen, including hyperphosphatemia, hypocalcemia, increased alkaline phosphatase activity, impaired mobility, bowing of the long bones, poorly mineralized skeleton, and soft tissue mineralization (NRC, 2003; Tomson and Lotshaw, 1978). Concerning iron : report to § 3.5. Vitamins Lemurs may be sensitive to vitamin D and maintain themselves with low levels (Junge, 2003). Gray et al. (1982) offered brown lemurs ( Lemur fulvus ) a commercial primate diet containing 1 Experimental pellets for leaf eating monkeys can however rich up to 55% NDF and 40% ADF in DM: eg. those produced by Hope Farms (Woerden, the Netherlands) and used in Nijboer et al. , 2001 study.
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 15 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 −1 vitamin D 3 at 6,600 IU kg plus fresh fruit and a “supplement” containing oats, soy flour, eggs, wheat germ, evaporated milk, sugar, and bananas. Calcium concentrations in the serum from 20 lemurs were 9.6 −1 −1 12.6 mg dL . Serum 25(OH) D3 concentrations were 3.4 94.8 ng mL , and serum 1, 25(OH) 2D3 concentrations were less than 4 to 220 pg mL −1 . Because the lemurs could make a variety of food choices, it was not possible to relate the composition of the diet consumed directly to animals whose biochemical measures appeared to be outside a normal range. Nevertheless, the researchers suggested that some lemurs were hypercalcemic and might have had increased 25(OH)D 3 or 1,25(OH) 2D3 because of episodic intoxication by vitamin D from the commercial diet. Some animals had low 25(OH)D 3 or 1,25(OH) 2D3 concentrations, so it is also possible that some lemurs consumed a diet that was low in vitamin D 3, although no clinical signs of deficiency were reported (NRC, 2003). Many mammals have the ability to synthesize ascorbic acid from glucose, but most primates, including humans, lack gulonolactone oxidase, the enzyme required for ascorbic acid synthesis. Many, perhaps most, prosimians possess this enzyme and presumably do not require a dietary source of vitamin C . Fifteen species of prosimians—including sifakas ( Propithecus verreauxi ), pottos ( Perodicticus potto ), and a number of species of lemurs, bushbabies, and lorises—have substantial liver concentrations of gulonolactone oxidase; these species might be able to synthesize ascorbic acid endogenously (Nakajima et al. , 1969; Pollock and Mullen, 1987). However, the enzyme is not found in the liver of western tarsiers (Tarsius bancanus ), so perhaps prosimians are not all alike in their ability to synthesize this vitamin (Pollock and Mullin, 1987). Confirmatory studies in which diets devoid of vitamin C have been fed to prosimians for extended periods have not been conducted. The ability to synthesize vitamin C is clearly lacking in all other higher primates that have been studied to date (NRC, 2003). Concerning the extent of vitamin C ’s enhancement on iron absorption: report to § 3.5. Proteins As far as we know, no accurate data have been published on protein requirement of non folivorous prosimians. The report of the National Research Council, Committee on Animal Nutrition (NRC, 1978) suggested that New World monkeys (NWM) have higher protein requirements than Old World monkeys (OWM), and manufacturers of formulated primate feeds developed 15% protein diets for OWM and 25% protein diets for NWM, and many zoos and primate research centres have followed this lead. The second revised edition of the National Research Council, Committee on Animal Nutrition (NRC, 2003) does not suggest any change concerning the protein requirement of Lemurs: the table 11 1, which lists estimated minimum nutrient requirements in diets for model primate species in six categories, only includes amounts of NDF and ADF. Sclater’s black lemurs, Crowned lemurs and Red bellied lemurs are diurnal generalists that consume a diet consisting of leaves, fruits, seeds, nuts, and occasionally small animal prey. The morphological adaptation of the large cecum and the flexible behavioural response of a cathemeral activity depending also on food resources availability and quality, suggest that the protein requirements are frequently achieved by a narrow margin. Thus, depending on protein quality and digestibility, the range of 12 to 15% of CP in DDM may be sufficient and reasonable in captivity. Targeting their diets to 15% of CP in DDM, Mulhouse Zoo obtained theorical intake values that ranged from 13.7 to 17.7% (see appendix 1 to 3). Blood urea nitrogen levels of free ranging ruffed lemurs are significantly lower than published captive reference values (5 vs. 20 mg/dL) suggesting that the natural diet is lower in protein (Pollock, 1985; Junge & Garell, 1995; Junge, 2003). Although pathologic protein excess is rarer in monkeys than in other species, such as the rat, monkeys can develop pathologic changes in the kidney, which sometimes lead to terminal renal failure (Burek et al. , 1988). It is common practice in all species, including humans, to limit protein intake to prolong the preterminal period in renal disease (Bourgoignie, 1992). It has not been shown in humans that a high protein diet will compromise an otherwise healthy kidney. In humans, it has been clearly shown that excess dietary protein increases urinary calcium loss (see Chapter 6) and thus calcium requirements. There is no data on calcium requirements of nonhuman primates relative to
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 16 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 different dietary protein intakes. Therefore, the conservative approach is to keep dietary protein within reasonable bounds (NRC, 2003). The mother’s milk protein content may also be indicative for this requirement approach. Prosimians that carry their young during lactation (the case of these Eulemur species) produce more dilute milk than species that leave their young unattended for long periods, but analysis still range the Eulemur milks from 10.6 to 14.8% CP DM (Tilden and Oftedal, 1997; NRC, 2003: see table XI). Milk proteins being more amino acid balanced and easily digestible for young, the range of 12 to 15% of CP in DDM seem definitively reasonable for zoo fed diets. % CP DM 13.5 14.8 10.6 13.2 30.0 Table XI: Proximate composition of milk from several Lemuridae species from NRC, 2003 (Table 9-4, p. 165) Energy As seen in the introduction the “energy frugality hypothesis” (EFH) postulates “that the majority of lemur traits are either adaptations to conserve energy (e.g., low basal metabolic rate (BMR), torpor, sperm competition, small group size, seasonal breeding) or to maximize the use of scarce resources (e.g., cathemerality, territoriality, female dominance, fibrous diet, weaning synchrony)” (Wright; 1999). Lemurs are known to have a low BMR, thus, lower energy requirements than other primates. Even the cost of reproduction, benchmarked against either maternal mass or metabolic rate, is not usually high in lemurs when compared to other groups of primates (Kappeler, 1996; see also Godfrey, 2004). Examples of energy requirements are given in § 4.5 of this report. As far as we know, the adaptative role of taste to maximize food choice has only been investigated with threshold and supratheshold ingestive responses to various sweeteners (fructose, sucrose, alitame, aspartame, thaumatin, monellin, stevioside, neohesperidinedihydrochalcone, D tryptophan) for several lemurid species (Glaser, 1993; Bonnaire & Simmen, 1994; Glaser et al. , 1995). No data is currently available for Eulemur species concerning the discrimination of protein content (or CP/TDF ratio), fat content, secondary compounds such as alkaloids and tannins, or other potential toxic substances. Therefore, discriminative abilities of these species to high energy content food sources (ie. readily assimilable sugars or fats) have not been completely investigated. On one side the special energetical physiology of lemurs seem to be an adaptative response to a harsh and unpredictable island environment. On the other side, their detoxifying abilities (bamboo lemurs so far: Garbutt, 1999; Sussman, 1999) are an adaptative response to the sympatric use of resources without
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 17 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 competing. The question of these two digestive adaptations allowed by extraordinary taste sensitivity remain poorly investigated… A better knowledge to recognize the adaptative role of taste in the food choice and the dietary adaptation is presently needed. Table XII: Estimated Daily Metabolizable Energy (ME) Requirements (as Multiples of BMR) for Adult Captive Lemurs from NRC, 2003 (Table 2-1, p. 45) a Kilocalories of ME intake relative to estimates of basal metabolic rate (BMR, 70BW 0.75 ) provide factors by which basal energy requirements can be multiplied to accommodate energy costs of physical activity typical of captivity. Averaged factors × 70BW 0.75 provide estimates of daily energy requirements. b Total energy expenditures (TEE) was measured with the doubly labeled water method. Ratios of TEE:BMR provide factors by which basal energy requirements can be multiplied to accommodate energy costs of physical activity typical of captivity. When TEE was reported separately for males and females, there were no apparent differences between sexes in magnitude of factors (FAO/WHO/UNU, 1985). c Energy expenditure analyzed with indirect calorimetry used as above to determine multiple of BMR. d 0.716 BMR in kcal per day as function of body weight (kg) for eutherians: BMR = 57.2BW kg (McNab, 1988). e MMR (maintenance metabolic rate) in kcal of ME per day as function of body weight (kg) to meet daily maintenance energy requirements for 0.75 placental mamm als: MR = 140BW kg (Scott, 1986; Robbins, 1993a). f Diet type: M = mixed, N = natural ingredient, P = purified, SP = semipurified, ADF15 = 15% acid detergent fiber, ADF30 = 30% acid detergent fiber. Summary table: see appendix 13 Mixing several bibliographical sources and Mulhouse Zoo experience, the table in Appendix 13 shows the nutrient ranges we could use for the lemurs.
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 18 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 3 Nutritional related problems in captivity 3.1 Behavioural problems Foraging and food intake patterns in the wild differ considerably from those in captive environments (Fernandes, 1996; Schwitzer, 2003). This may contribute to explain behavioural problems we encounter in captivity, particularly aggravated female dominance or targeted female female aggressions. Therefore, many zoos tend to feed in excess their Lemurs (and generally all the primates living in social groups) in order to “prevent” aggressions and to ensure that even the lowest ranking individual can meet its requirement (Haumanns et al. , 2000; Schwitzer, 2003). Recorded transit times for Eulemur species can be rapid, eg. for E. fulvus ranging from 2,7 to 4,6 hours (Klein, 1991; Ganzhorn, 1986). Thus, it is preferable to distribute smaller multiple meals during the day (at least three) than overfeeding once a day. Also, enrichment of the environment seem extremely important for prosimians, despite the fact that many zoos tend to first “concentrate” their efforts for great apes. Multiple meals and environment enrichment should help to prevent aggressions. Only in cases of targeted breeding female breeding male aggressions, the breeding male should be preferably separated from the group the time of the evening and last meal. Mulhouse Zoo experienced this method with success on breeding males which were to “stressed” and loosing weight. But, this should only be undertaken if the composition of the family group is stable and the aggressions are not generated by conflicts with the elder daughter or son. Stereotypies, especially prior to feeding times, can also be encountered; but Eulemur species do not seem so prone to this behavioural problem than other primates or captive mammals do (Kolter, 1995; Carlstead, 1996). 3.2 Coprophagy Coprophagy has been documented in several species of prosimians, and commonly related in captivity to stress, boredom or food scarcity. Fish et al. (2007) report that wild ring tailed lemurs ( Lemur catta ) consumed dried faecal matter from cattle, dogs and even humans, during the dry seasons at the Beza Mahafaly Special Reserve. De Michelis et al. (2005) report that captive crowned lemurs ( Eulemur coronatus ) showed a marked behaviour of auto and allo coprophagy. Although attempts in improving dietary fiber content (NDF/NSC ratio) and the number of meals (2 to 4/day) did not show any behavioural modification, poor environmental enrichment in night indoor facilities was also suspected to promote coprophagy. Such as described in sportive lemurs ( Lepilemur sp.; Hladik et al. , 1980), coprophagy could also be interpretated in Lemur or Eulemur species as an opportunity to increase the recovery of nutrients from relatively indigestible feeds. A better knowledge to recognize the role of coprophagy as a dietary adaptation or a behavioural stress marker is presently needed among prosimians. 3.3 Obesity and reproductive failure Feeding in excess or unbalanced diets commonly lead all the Malagasy lemurs to obesity (Schaaf & Stuart, 1983; Pereira & Pond., 1995; Terranova & Coffman, 1997, Schwitzer, 2003). Changes in the reproductive biology are observed in captivity with lower or nil breeding rate for obese animals (Pereira & Pond., 1995). Thus, it is important to control body weight condition for enhancing breeding rate among EPPs/ESBs and preventing obesity related problems such as bad dentition, shorter longevity, diabetes mellitus, etc.
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 19 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 Although the abundance of food provisions have been suggested to enhance the reproductive output of wild or semi captive populations with higher proportion of multiple births (Pereira, 1993: Ring tailed lemur as model), it is evident among captive populations of Crowned lemurs, Red bellied lemurs and more particularly Sclater’s black lemurs that obese animals tend to show a poor breeding rate. Fig. 3 & 4: Obese female Sclater’s black lemur Courtesy of T. Petit at La Palmyre Zoo, France Normal BW range for Sclater’s black lemurs: In order to explore possible causes of the reproductive failure among the European captive population of Sclater’s black lemurs, a survey on body weight records was sent to participants in 2008. The results of this survey are shown on appendix 8, table XIII and fig.5. To determine whether an animal was obese, a weight based definition was used following Kemnitz et al. (1989): an obese animal was identified when weighing more than two standard deviations (SD) over the mean wild weight. For Sclater’s black lemurs: Terranova & Coffman (1997) report a mean wild weight of 1,793 Kg (n = 7; SD = 209g; min. = 1,607 Kg and max = 2,188 Kg) and a mean captive weight of 2,339 Kg at Duke University Primate Center (n = 21; SD = 185g; min. = 1,730 Kg and max = 3,110 Kg) (sexes combined), Kappeler (1991) reports a mean captive weight of 2,321 Kg for males (n = 3; standard error (SE) = 110g) and of 2,290 Kg for females (n = 5; SE = 92g) also at Duke University Primate Center, Schwitzer (2003) reports a mean captive weight of 2,504 Kg (n = 10; SD = 294g) in several european zoos (sexes combined), Field data (Sahamalaza AEECL project, Schwitzer pers. com. , 2008) indicate a mean wild weight of 2,04 Kg for females (n = 9; SD = 0,7 Kg) and 1,87 Kg for males (n = 12; SD = 0,9 Kg) (SD values seem high). Thus, according to Terranova & Coffman (1997), a Slater’s black lemur weighing more than 2,211 Kg should be considered as obese. But the number of wild individuals used to determinate the mean wild weight is low, therefore this definition of obesity for Slater’s black lemurs remains open for discussion. According to mean weights obtained from non obese lemurs, ranging from 2,290 Kg to 2,504 Kg, and Mulhouse Zoo experience , the range of 1,9 to 2,6 Kg seem acceptable for captive Sclater’s black lemurs and individuals exceding 2,8 Kg should be considered obese . Using this discriminating upper limit of 2.8 Kg, 50% of living females and 43% of living males will be declared obese by the end of 2008. Females tend to have an higher BW than males: the mean BW for
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 20 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 obese females is 3,373 Kg (n = 7; SD = 437g) and 3,197 Kg (n = 6; SD = 280g) for obese males , and the mean BW for non obese females is 2,353 Kg (n = 11; SD = 322g) and 2,225 Kg (n = 13; SD = 430g) for non obese males (see table XIII). Among the animals declared non obese, at least 3 females (EEP # 17 (dead), # 21 and # 71) and 3 males (EEP # 6 (dead), # 34 and # 43) were obese (at least one BW record ≥ 2,8Kg). This high incidence of obesity may certainly constitute a major cause of the noted reproductive failure in this EEP: the rate of obese or ex obese females experiencing lower or nil breeding success is too high and represents 64% of current EEP female population . Total population studied (N=37; 1998 2008) Sex BW [Kg] SD N % N obese individuals (BW > 2,8Kg) m 3,197 0,280 6 32% f 3,373 0,437 7 39% non obese individuals (BW < 2,8Kg) m 2,225 0,430 13 68% f 2,353 0,322 11 61% Total population alive (N=28; Nov 2008) Sex BW [Kg] SD N % N obese individuals (BW > 2,8Kg) m 3,197 0,280 6 43% f 3,373 0,437 7 50% non obese individuals (BW < 2,8Kg) m 2,419 0,303 8 57% f 2,457 0,182 7 50% Table XIII: Results of the Body Weight Survey for Sclater’s black lemur EEP (see detailed data on Appendix 8).
4,250
4,000
3,750
3,500 BW > 2,8 Kg
3,250 obesity category
3,000
2,750
2,500 BW (Kg)
2,250
2,000
1,750
1,500 wild BW (Sahamalaza): females ( n = 9 ) 2.04 ± 0.7 and males ( n =12 ) 1.87±0.9 1,250
1,000 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 age (Y) Fig. 5: Body weights records for EEP E. m. flavifrons (n=37: 19 males (in blue), 18 females (in red)) (see detailed data on Appendix 8)
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 21 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 Normal BW range for Red bellied lemurs: The range of 1,7 to 2,0 Kg seems acceptable for captive Red bellied lemurs and individuals exceeding 2,3 Kg should be considered obese : According to the BW records obtained at Mulhouse Zoo (see Appendix 14), the mean BW observed is 1,839 Kg for the males (n = 7 with 14 records; SD = 176g; excluding # 76, # 227 and last young “Dionysos”) and 1,713 Kg for the females (n = 6 with 20 records; SD = 112g; excluding # 137, # 149, # 210 and last BW record for # 10), Schwitzer (2003) reports a mean captive weight of 1,968 Kg (n = 13; SD = 205g) in several European zoos (sexes combined), Terranova & Coffman (1997) report a mean wild weight of 1,956 Kg (n = 29; SD = 195g) and a mean captive weight of 2,060 Kg at Duke University Primate Centre (n = 15; SD = 178g), Glander et al. (1992) report a mean wild weight of 2,067 Kg for males (n = 9; SD = 195g) and of 1,960 Kg for females (n = 13; SD = 140g), Kappeler (1991) reports a mean captive weight of 2,267 Kg for males (n = 4; SE = 124g) and of 2,139 Kg for females (n = 4; SE = 92g) at Duke University Primate Centre. Normal BW range for Crowned lemurs: The range of 1,4 to 1,8 Kg seems acceptable for captive Crowned lemurs and individuals exceeding 2,0 Kg should be considered obese : According to the BW records obtained at Mulhouse Zoo (see Appendix 15), the mean BW observed is 1,529 Kg for males (n = 5 with 14 records; SD = 221g; excluding # 49 and last BW record for # 56) and 1,431 Kg for females (n = 7 with 10 records; SD = 266g; excluding # 196 except for its last BW record), Schwitzer (2003) reports a mean captive weight of 1,618 Kg (n = 9, SD = 225g) in several European zoos (sexes combined), Terranova & Coffman (1997) report a mean wild weight of 1,177 Kg (n = 4; SD = 224g) and a mean captive weight of 1,660 Kg at Duke University Primate Centre (n = 30; SD = 238g), Kappeler (1991) reports a mean captive weight of 1,712 Kg for males (n = 11; SE = 80g) and of 1,687 Kg for females (n = 8, SE = 88g) also at Duke University Primate Centre. 3.4 Dental problems Unbalanced and soft zoo diets, especially when containing high levels of simple saccharids or acid compounds, are commonly associated with dental problems such as chemical deterioration of teeth, caries, tartar accumulation, parodontopathies and subsequent tooth loss. But severe tooth wear is also observed on wild animals (Junge & Sauther, 2007; Cuozzo et al. , 2008), suggesting that lemurs may be naturally susceptible to this concern and that zoo diets only accelerate the process. A recent investigation on salivary pH of wild and captive lemurs (Cuozzo et al. , 2008) suggest that: salivary pH varies between lemur species (ring tailed lemurs compared to sympatric Verreaux’s sifakas), corresponding to broad dietary categories,
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 22 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 lemur saliva seem to have a strong buffering capacity, indicating that the impact of acidic foods on dental wear is short lived, likely having a limited effect, tannins in tamarind fruit may increase friction between teeth, thereby increasing attrition and wear in lemurs. Even if the salivary pH of the captive ring tailed lemurs included in this study did not differ significantly from those of wild ring tailed lemurs (8.125, n=16, SD=0.289 versus 8.098, n=41, SD=0.550 and 8.080, n=25, SD=0.746), further investigations are needed to determine whether the zoo diets may or may not influence this pH and thus, explain the high incidence of tooth wear in captivity. Fig.6: E. m. flavifrons , male, captive born, 21years old Fig.7: E. m. flavifrons , male, wild born, 16 years in captivity Mulhouse Zoo, D. Gomis 2008 Mulhouse Zoo, D. Gomis 2003 Some modified diets have been experimentally tested on lemurs in order to prevent the dental calculus accumulation (eg. with sodium hexametaphosphate: Willis et al. , 1999) but this kind of prophylactic measure seems complicated to generalize and properly evaluate in zoo conditions. Regular clinical exams and dietary evaluation may help to maintain satisfactory oral health. 3.5 Hepatic iron storage disease (hemochromatosis) Hepatic iron overload has been historically considered a common problem in lemurs in captivity, especially in Eulemur species: Gonzales et al. (1984) reported most pronounced signs in the black lemur (Eulemur macaco ) and least in the ring tailed lemur ( Lemur catta ). Non pathologic accumulation of iron pigment (hemosiderosis) should be distinguished from conditions in which there is functional or morphologic evidence of toxicity (hemochromatosis) (AZA PTAG, 2003). This toxicity can also lead to the transformation of damaged cells into hepatocellular carcinomas (Brygoo et al. , 1964; Junge, 2003). Spelman et al. (1989) reported 100% incidence of hemosiderosis in all 49 lemurs that had been necropsied during a 10 year period in the studied colony, and that severity increased with age. A suggested explanation was that captive lemurs received diets high in Fe (commercial monkey diets) and in ascorbic acid (citrus fruits), which enhanced the reduction of Fe 3+ to Fe 2+ and its absorption, while they received few inhibitors of Fe absorption, such as tannins (polyphenols), that are constituents of the diet consumed in the wild (leaves, fruits, and bark). Because hemosiderosis can lead to liver and kidney disease, the authors suggested that lemur diets should be modified to reduce this risk (NRC, 2003).
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 23 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 Concerning the extent of vitamin C ’s enhancement on iron absorption, there is no sufficient data to determine whether dietary levels of vitamin C contribute to the development of hemosiderosis in lemurs. On one hand, it has been shown that in humans with sufficient tissue stores of iron, vitamin C in the diet does not increase the iron absorption (Rossander Hulthen & Hallberg, 1996); on the other hand, most prosimians have no dietary requirement for vitamin C, having the ability to generate it endogenously (Nakajima et al. , 1969; Pollock and Mullen, 1987)… Glenn et al. (2006) studied the iron concentration and hemosiderin accumulation in banked tissues from 15 different species (n=153) of lemurs necropsied over a 12 year period at the Duke University Primate Center (only animals > 6 months of age were included in the data set). 32% of the animals were considered positive for the presence of hemosiderin in the liver, lymph node, duodenum, and kidney. Most of these positive cases (73%) showed deposition of iron in the liver. Total iron scores (TIS, range = 0 60; Deugnier et al ., 1992) ranged from 0.3±0.3 in Lemur catta to 33.3±1.7 in Cheirogaleus medius . The mean liver iron concentration (LIC) ranged from 209±21 g/g wet weight in L. catta to 2957±414 g/g in C. medius . Although evidence of excess iron deposition in the liver was present across several species studied, hemochromatosis was not observed, and excess iron was not related to the cause of death in any of the animals studied. These findings suggest that the incidence of hemosiderosis in captive lemurs may not be as high as previously suspected and that there may be species and institutional differences in the tendency to develop hemosiderosis (AZA PATG, 2003). Among 69 necropsy reports available at Cologne Zoo from 1978 to 2003, altogether 13 species of lemurs, only 6 cases of hemosiderosis were reported ( i.e. 8% of the 69 cases and 17% of the 35 adult individuals included) (Schwitzer et al. , 2004). Unpublished data from Mulhouse Zoo also confirms that frequent necropsial findings of hemosiderosis in captive lemurs seem often not related to the cause of death, and that toxic hemochromatosis may not be so common in the last decade. Among 170 necropsy reports available at Mulhouse Zoo from 1973 to 2008, altogether 13 lemur species or subspecies, only 7 cases of excess iron deposition are described among the 65 histological examinations available (see table XIV below). NEWBORNS / JUVENILES (< 2 years old) ADULT INDIVIDUALS (> 2 years old) species N total N histol. N hemosid. % hemosid. ser [Fe] M/L N total N histol. N hemosid. % hemosid. ser [Fe] M/L 1 Propithecus v. coronatus 4 2 0 0% 0 0 0 55,63 (N=2) Hapalemur g. alaotrensis 0 0 0 4 4 1 25% 37,91 (N=5) Hapalemur g. occidentalis 6 4 0 0% 5 1 0 0% Lemur catta 8 1 0 0% 35,90 (N=3) 7 4 0 0% 43,65 (N=1) Eulemur f. albifrons 34 10 0 0% 1 1 0 0% 26,70 (N=2) Eulemur f. albocollaris 0 0 0 2 0 0 0% Eulemur m. flavifrons 8 0 0 0% 9 9 6 67% 57,70 (N=8) 3 Eulemur m. macaco 8 2 0 0% 7 7 0 0% Eulemur mongoz 5 4 0 0% 47,10 (N=3) 2 2 0 0% 49,03 (N=3) Eulemur coronatus 8 0 0 0% 25,10 (N=1) 4 3 0 0% 26,84 (N=4) 2 Eulemur rubriventer 8 2 0 0% 2 0 0 0% 32,20 (N=5) Varecia v. variegata 14 6 0 0% 1 0 0 0% 37,40 (N=1) Varecia v. rubra 23 3 0 0% 0 0 0 44,08 (N=2) TOTAL 126 34 0 0% 39,16 (N=7) 44 31 7 16% 42,44 (N=33) Table XIV: Necropsy reports and hemosiderosis at Mulhouse Zoo between 1973 and 2008 (D. Gomis, F. Huth) N total: total number of post-mortem reports available; N histol.: number of reports including an histological examination; % hemosid.: number 1 of histologies reporting iron deposition; ser [Fe]: total serum iron; : some tissue iron deposits were found in the liver of a 4 months old hand- 2 reared juvenile, but not excessive enough to be counted as a case of hemosiderosis; : some hemosiderin was found in the phagocytic cells of the 3 duodenum of a one year and a half old female, but associated to the hemorragy of the spleen caused by a nematode infestation; : some hemosiderin was found in the phagocytic cells of the duodenum of a eight years old female, but associated to the hemorragy of the endothelium caused by a bacterial infection. At Mulhouse Zoo the cases of hemosiderosis (not hemochromatosis) represent 4% of the necropsy reports and 16% of the adult individuals . Even if all the non folivorous lemurs are fed with the same feeding regime, 6 of the 7 cases are found on adult Sclater’s black lemurs (6, 16, 18, 19, 21 and 24 years old) and
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 24 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 associated to the highest total serum iron values (Ser [Fe] = 57,70±11,53 Mol/ L 1). 3 of these deaths were clearly caused by the iron overload, the oldest individual was even found with a hepatocellular carcinoma. This confirms that Eulemur macaco ssp. are more sensitive to the progressive accumulation of iron (Gonzales et al. , 1984; Benirschke et al. , 1985), this is perhaps linked to a special metabolism of the species, explaining also the higher incidence of obesity and of reproductive failure seen in captivity for ssp. flavifrons (see previous § 3.3). The bioavailability and absorption of iron depend on numerous factors including the iron status of the animal, its age and sex, the chemical form of the iron in the diet, and levels of other components including vitamins, minerals, fiber and secondary plant compounds (polyphenols, tannins, phytates, etc.). The term tannin often describes a variety of chemicals with marked variability in chemistry, toxicity and binding specificity, affecting not only the availability of iron but also of other micronutrients as well. Therefore, the addition of tannins to the captive diets may result in secondary deficiencies and may not have the desired impact for preventing hemosiderosis (Hagerman & Carlson, 1998; AZA PTAG, 2003). The report of the National Research Council, Committee on Animal Nutrition (NRC, 2003) estimates the adequate dietary iron concentration for nonhuman primates to be 100 mg/Kg DM (no safe upper limit has been established). Lowering the iron content of primate chows and reducing or eliminating the feeding of citrus fruits with chow seem to have reduced greatly the incidence of hemochromatosis in lemurs in the last 10 years (Junge, 2003). 3.6 Diabetes mellitus Diabetes mellitus has been documented in obese prosimians, and the effect of the diet on this syndrome is being investigated (Meier, 1981; Walzer & Kübber Heiss, 1995; Walzer, 1999; Junge, 2003). In the course of overt ketoacidotic type II diabetes in obese ring tailed lemurs ( Lemur catta ), the hyperinsulinemic stage seem to be an early hormonally impaired stage, which is followed by the hypoinsulinemic late to end stage overt diabetes. Although the data available on type II diabetes mellitus in prosimians is limited, the disease progression seem to be similar as described for concurrent peripheral insulin resistance and an excessive insulin secretion on aging, obese rhesus monkeys (Walzer, 1999). 3.7 Renal failure and periarticular hyperostosis Familial periosteal new bone proliferation at the metaphyseal regions of proximal femora and digits (enlargement of knee and ankle joints) have been described in black lemurs ( Eulemur macaco ), and associated to kidney degeneration (chronic interstitial nephritis and glomerulonephritis) (Junge et al., 1994; Junge, 2003). Although age related renal degeneration is a common cause of mortality in older prosimians 2, protein or mineral excesses could also contribute to develop pathologic changes in the kidney. But the effect of the diet on this bone disease is not yet established. 1 Ser [Fe] was the only data available for this study. Ideally, a complete investigation includes the serum ferritine, the unsaturated iron binding capacity (UIBC), the total iron binding capacity (TIBC = ser [Fe] + UIBC) and the transferrin saturation (% TS = ser [Fe] x 100 / TIBC) (see Wood et al. , 2003). 2 At Mulhouse Zoo, renal lesions are found in 5% of the total number of necropsy reports (N=170), representing 18% of the dead adult individuals (N=44) (D. Gomis, F. Huth, 2008).
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 25 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 4 Practical feeding strategy 4.1 How to control the global intake The safe way to feed Sclater’s black lemurs, Crowned lemurs and Red bellied lemurs in captivity is to restrict the daily amounts of food, this given in at least 2 meals, and to compose each group regime on a scale. This method prevents effectively from obesity, but needs to be evaluated accurately to each individual need: the “intake young coefficient” and the already observed intakes may help this. Young versus adult intake: establishment of an “intake young coefficient” When evaluating the real intake of lemurs in captive family groups, the total food intake per group is divided by the amount of animals to determine the food intake per animal. If an adult animal is counted as one animal, a young eating 50% of an adult ration can be counted as 0.50 animal, 25% as 0.25, etc. Mulhouse Zoo keepers observed an evolution of the intake with growth and were able to modelize this for some lemur species (Gomis et al. , 2007). This coefficient also takes into account the potential extra dietary need of lactating females (see § 4.5). As shown in the fig.8 below, the prosimians when young adult animals can eat more than mature adult ones, thus young coefficient can reach 1.10 or 1.15 between 10 and 11 months of age. Generally, a young Eulemur usually eats as much as an adult at the age of 11 months .
"Young Factor" for Eulemur sp. compared to Varecia sp. (Mulhouse Zoo, 2007)
1,15 1,10 1,05 1,00 0,95 0,90 0,85 0,80 0,75 0,70 0,65 0,60 0,55 0,50 0,45 0,40 0,35 0,30 0,25 0,20 0,15 0,10 0,05 0,00 1 2 3 4 5 6 7 8 9 10 11 12 age (in months) adult intake around the age of 11 months Varecia sp. Eulemur sp. Fig.8: Lemurs intake young coefficient between age of 1 and 12 months the coefficient can be approximated with: “y = 0,1014x 0,0008” for Varecia sp. and “y = 0,1019x 0,1083” for Eulemur sp . Godfrey et al. (2004) studied the prenatal and postnatal growth rate of prosimians related to maternal investment. Contrary to the expectations of Janson and van Schaik’s “ecological risk aversion hypothesis” (RAH), they showed that folivorous lemurs (such as indriids) grow and mature more slowly than like sized frugivorous lemurs (most lemurids), but tend to exhibit faster dental development (see figs.9 and 10 below). This study also shows that fetal and infant growth rates in lemurids are higher than in inrdiids of similar body size, and that lemurids attain adult values for cranial traits at a relatively earlier age. Among lemurids Varecia is considered as an highly frugivorous species and shows an higher postnatal growth rate (10,67 g/day: Pereira et al. , 1987) than several Eulemur species (eg. 6,75 g/day for E. macaco : Leigh & Terranova, 1998). This is concordant with the “intake young coefficient” courves obtained at Mulhouse Zoo, and the fact that Eulemur sp. carry their youngs while Varecia sp . do not.
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 26 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 Fig.9: Postnatal growth rate benchmarked Fig.10: Instrantaneous cranial growth rate at birth against maternal body mass benchmarked against maternal body mass from Godfrey et al., 2004 from Godfrey et al., 2004 Using observed intake averages in zoos When using the “intake young factor” previously described, it is possible to determinate the intake average per adult animal, per day. According to the experience of Mulhouse Zoo (Gomis et al. , 2007; see also detailed data at Appendixes 1 to 3), an adult Eulemur eats between 7,32 and 13,23 % of its BW (AF basis) per day, which represents between 1,94 and 3,46 % on a DM basis (averages including not only Sclater’s black lemurs, Crowned lemurs and Red bellied lemurs, but also a fourth Eulemur species: the Mongoose lemurs). The feeding method used at Mulhouse Zoo restricts the amounts offered, thus these ones are very similar to intake amounts (near nil leftovers) and represent: 148 (+/ 25) g AF / adult animal / day for E. coronatus (n = 10 x 7 consecutive days), 245 (+/ 26) g AF / adult animal / day for E. rubriventer (n = 10 x 7 consecutive days), 261 (+/ 49) g AF / adult animal / day for E. m. flavifrons (n = 12 x 7 consecutive days), and 177 (+/ 22) g AF / adult animal / day for E. mongoz (n = 5 x 7 consecutive days). SIMIAL Milk bread pellet: 7% Milk bread mix: 11% mix: 12% SIMIAL CROUSTI' pellet: 25% CROC pellet: 5% => ~26% DM CROUSTI' CROC FRUITS + FRUIT + pellet: 18 AF VEGETABLES: 77% VEGETABLES: 45% DM Fig.11: Intake composition on as fed (AF) and dry matter (DM) basis at Mulhouse Zoo, average for 4 sp.: E. coronatus, E. rubriventer, E. m. flavifrons and E. mongoz Mulhouse Zoo lemurs are fed 3 times a day with the first meal in the morning consisting of pellets. The pellet intake for these 4 Eulemur sp . represents 12,5 (+/ 0,5) % of the total intake AF (43,8 (+/ 1,8) %
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 27 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 DMI). A major part of the diet is represented by fruits and vegetables (76,4 (+/ 0,8) % of the total intake AF, 44,2 (+/ 0,9) % DMI), with an important part of apples (44,1 (+/ 3,8) % of the fruits and vegetables DMI) and a reduced and controled part of bananas (only 7,1 (+/ 0,7) % of the total intake AF). amounts in g/ animal /day Banham (male) Banham (female) Mulhouse (average) Edinburgh Colchester Montpellier problem of obesity no no no yes yes yes/no fruits & vegetables 660 605 206 550 223 560 pellet 1 20 pellet 2 21 21 15 100 50 30 in house cake or mix 20 cooked Meat 29 29 hard boiled egg 21 21 TOTAL (AF) 731 676 261 650 273 590 approx.TOTAL (DM) 125 83 68 130 55 118 approx. pellet incorp. (%DM) 15,4% 23,2% 46,4% 69,2% 82,6% 22,9% number of meals 2 2 3 1 1 2 number of meals for scatter feeds 2 % banana 14% 0% 6% 0% 3% 25% % apple 14% 7% 47% 18% 18% 20% pellet 1 Sanders Simial pellet 2 Mazuri basix Mazuri basix Sanders Crousti' croc Mazuri Trio Munch Mazuri basix Mazuri leaf eater approx. CP cont. Pellet 1 (DM) 31% approx. CP cont. Pellet 2 (DM) 22% 22% 22% 24% 22% 26% approx. CP cont. Cake/Mix (DM) 17% approx. CP cont. Cooked Meat (DM) 80% 80% approx. CP cont. Hard boiled egg (DM) 55% 55% approx. CP cont. F&V (DM) 3% 3% 3% 3% 3% 3% approx. diet. CP content (DM) 14,8% 22,0% 15,7% 18,6% 20,6% 8,3% CP content (DM) Zootrition ® 16,3% 24,7% 16,0% Table XV: Approximative diet composition for Sclater’s black lemurs in 5 european zoos (see also App. 3 to 7) When comparing the previously described intake diets from Mulhouse Zoo to other offered diets in european zoos, we note that for Sclater’s black lemurs (see table XV above): the total amount of food in an AF basis ranges from 261 to 731 g/animal/day, the total amount of food in a DM basis ranges from 68 to 130 g/animal/day, water content of the diets are not in a similar ranges, thus the highest amounts of food in an AF basis are not proportionnally the highest in an DM basis (eg. Banham versus Mulhouse), therefore, the DM intake should be prefered for controling the global intake , the pellet incorporation ranges from 15,4 to 82,6% in a DM basis, however, the pellet incorporation ratios higher than 40 50% in a DM basis should be controlled with intake studies (values seem really too high and leftovers may be important), resulting theorical CP content in a DM basis ranges from 8,3 to 24,7%, while the range of 12 to 15% seem more reasonable (see § 2.3.4), without any accurate data for the nutrient digestibility on Eulemur sp. , these dietary protein contents may be overestimated and more likely ranging from 5,8 to 17,3% (using 70% as a mean DM digestibility for proteins, see Schwitzer, 2003: V. variegata as model) theorical CP content may be overestimated for Edinburgh and Colchester diets (pellet incorporation), far too low for Montpellier diet and quite accurate for Banham and Mulhouse diets, for restricted diets, the use of high protein content feeds (egg, meat) or pellets (Simial) in Banham and Mulhouse allows to balance better the dietary protein content, this explains that the Banham diets, with controled DM intakes (despite the high AF amounts) and quite high protein contents (despite the low pellet incorporation), succeeed in reducing and controling the BW of their female (see Appendix 8: EEP # 71) and controling the BW of their
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 28 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 male (despite the high % of banana allowed to him) (see Appendix 8: EEP # 34) (see also Goodchild & Schwitzer, 2008), therefore, for generalist lemurs such as Sclater’s black lemurs, meeting the dietary requirements of proteins may be important for preventing obesity (see also § 4.3). Please note that these comments are of course an approximative analysis of the dietary compositions. Further datas are lacking, especially concerning the dietary energetical density and digestibility, as well as the daily energy requirements of the animals (depending on activity, enclosure size, age, reproductive status, etc). Multiple meals prefered As ad-libitum feeding management is indeed not an option for Sclater’s black lemurs, Crowned lemurs and Red bellied lemurs in captive conditions, restricted amounts of food should be offered in at least 2 meals. Pellets or poor palatable high protein content feeds preferably given appart, and prior to any other food item, in the early morning. This constituing to 3 rd meal. Greater meal frequency is reported to enhance the control of appetite (possibly linked to an attenuation in insulin response) and has been prescribed in the treatment and management of obesity in humans (Speechy & Buffenstein, 1999). Schwitzer (2003) also notes that an addittional meal offered to E. m. flavifrons at Cologne Zoo helped to reduce their BW, even if this experience couldn’t be tested for significance. According to the experience of Mulhouse Zoo, multiple meals (at least 2 and preferably 3) may really help to control satiety and prevent from obesity . This feeding method should be prefered, even if multiple small meals can be difficult to manage in family groups with dominance aggressions (see § 3.1): lower dietary dry matter and energetical densities can help to increase the food amounts (see § 4.5). 4.2 How to choose fruits and vegetables In captivity, fruits and vegetables are more nutrient diluted (Schwitzer et al. , 2008). The variety and the nutritional content of the feeds available on the market seem to be very different from those that are consumed in the wild (see § 2.3.3). Analysis of fruits from the same botanical classification showed, that fruits in the wild are higher in fiber and proteins but lower in sugars and water, than those cultivated for human use (Calvert, 1985; Ganzhorn, 1988; Oftedal and Allen, 1997; Schwitzer, 2003). Also, fruits consumed in the wild may be primarily unripe and lower in energy, while those available to zoos are usually very ripe. Ripening increases the sugar level in the fruit. The problem of choosing the fruits and vegetables that we can offer to Sclater’s black lemurs, Crowned lemurs and Red bellied lemurs in captive conditions is more a question of proportions than a problem of nutritional quality. Almost all the fruits and vegetables can be used (see Appendixes 4, 5 and 10), but respecting the following recommendations: Reduce and control the amounts of items being high in: sugars or starch : bananas, melon, grapes, dates, potatoes, etc. vit.C (see § 3.5): kiwi, oranges, etc. iron (see § 3.5): broccoli, spinach, sultanas, etc. fats : sunflower seeds, nuts, etc. Use apples as a safe dietary basis: In Mulhouse Zoo, the apples represent around 53% AF (44% DM) of all the fruits and vegetables given, and 45% AF of the total diets offered to Lemur and Eulemur species, with good health conditions and breeding results for more than 25 years. Increase with preference the vegetables/fruits ratio
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 29 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 and select, when available, fiber rich vegetables (ADF, NDF, NDF/NSC). Never guess amounts, always weigh food items! 4.3 How to meet the protein requirement In diets not including high animal protein food items (hard boiled egg, boiled chicken or beef meat, arthropods, etc.) the dietary proteins are mainly delivered by the pellets. In the Mulhouse diet for example, both pellets used deliver 76,5 (+/ 4,9) % of the total proteins (see fig. 12 below). Lemuridae: % of proteins delivered by diet components OTHERS (milk-bread mix) 14% FRUIT + VEGETABLES 10% SIMIAL 49% CROUSTI' CROC 27% Fig.12: Origin of the dietary proteins, average for all the Lemurids, at Mulhouse Zoo, How to choose the pellets and calculate the amount needed in the diet Eg. if we consider a 1 Kg lemur: the DMI can be approximated to 3% of the BW (1,94 3,46 %, see § 4.1) resulting intake diet should be: 1Kg x 0,03 = 30g DM total intake / Kg BW lemur diets having commonly 25% of DM content, resulting intake should be: 30g x 100 / 25 = 120g AF total intake / Kg BW if the expected pellet incorporation is 40% DM, the total pellet amount should be: 30 x 0,4 = 12 g DM pellets monkey pellet having usually 90% of DM content, resulting pellet amount should be: 12 x 100 / 90 = 13,3 g AF pellets / Kg BW if we approximate that all the dietary proteins may be delivered by these pellets except 3% by the fruits and vegetables (it’s a minimum observed in zoo diets) and that the target of protein content is fixed to 15% in the DMI( *), the pellets should contain: (0,15 0,03) x 30 = 0,12 x 30 = 3,6 g of proteins, thus, be at least: 3,6 / 13,3 = 27 % CP DM pellets common available monkey pellets and biscuits are only 20% CP DM (Mazuri, Nutrazu, Zupreem, etc), therefore it will be necessary to mix them with at least a second and more dense source of proteins, for example pup pellets (at least 30% CP DM), hard boiled egg, boiled chicken or beef meat, some insects, etc. eg.: 5g AF of a 20% CP DM pellets and 10 g AF of a 30% CP DM pellets / Kg BW the rest of the diet can be composed by: 120g – 5g – 10g = 105 g AF of fruits and vegetables / Kg BW
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 30 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 apples can represent 50 60% AF of them, thus 52 63 g AF of apples / Kg BW resulting diet will deliver between 2,9 x 30 = 87 Kcal and 3,9 x 30 = 117 Kcal / Kg BW (*) we can use the upper value of the range (12 15% CP DM) in order to minimize the problem of their unknown digestibility Protein quality Analysing pellet intake and CP dietary level is not enough to ensure adequate amounts of essential amino acids required for growth and for synthesis of all structural and functional proteins. “High quality” proteins for Lemurids are not known, but for most primate species they are often mostly derived from animal sources. Proteins from plant sources generally contain low levels of one or more amino acids and most, if not all, primates may need protein sources other than vegetal ones. Therefore it is important to diversify the items in a diet: a mixture of plants will provide complementary ratios of amino acids. Comparison: % of amino acids Lem diets. Beef meat Casein lactic Chicken meat Soybeans (Zootrition® v.2.6)
Nutrient Unit Arginine % 0,58 3,00 3,85 4,28 2,92 CP % 15,37 44,42 95,00 68,42 42,29 Cystine % 0,20 0,43 0,34 0,91 0,51 Histidine % 0,18 1,41 2,86 2,01 1,12 Isoleucine % 0,50 1,90 6,32 3,42 1,87 Leucine % 1,08 3,56 9,71 4,98 3,03 Lysine % 0,55 3,71 7,88 5,58 2,43 Methionine % 0,25 1,04 3,10 1,82 0,45 Phenylalanine % 0,56 1,69 5,31 2,66 2,07 Threonine % 0,41 1,86 4,32 2,83 1,63 Tryptophan % 0,12 0,55 1,19 0,77 0,51 Tyrosine % 0,42 1,39 5,41 2,21 1,54 Valine % 0,55 2,15 7,40 3,32 2,00 Table XVI: Comparison % of amino acids in Mulhouse Zoo lemur diets and different feed components (DM base) 4.4 How to control the mineral & vitamin supplementation Most diets, when broadly diversified and well balanced with “complete” pellets, may not need any additional min & vit supplementation, moreover if lemurs have regular access to natural soil and sun in natural outside enclosures. Some min & vit supplementations may be needed in particular cases (see eg. in Appendixes 7 and 11) but should always been undertaken after an accurate intake evaluation and a complete dietary analysis (see proposed requirement ranges in Appendix 13; see also Schwitzer, 2003, and Gomis et al. , 2007: p.147 149). 4.5 How to control the energy intake As seen previously in § 2.3.4, the lemurs are known to have lower energy requirements than other primates; even the cost of reproduction is not usually high in lemurs when compared to other groups of primates (Kappeler, 1996; see also Godfrey, 2004). Thus, in captive conditions and with healthy individuals, no special consideration is needed in a family group when the breeding female is in gestation or lactation: it’s BW condition should be monitored but there is no need to give her extra food 1. The “intake young coefficient” (see § 4.1) seems to mix in well both requirements, young solid intake when weaning and mother’s extra expenditure (at least in the experience of Mulhouse Zoo).
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 31 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 Eg. if we consider non obese E. m. flavifrons ♂ EEP # 45 (2,309 Kg) ♀ EEP # 25 (2,240 Kg) the total BW for this couple is 4,549 Kg their average intake is known to be 503 g AF = 131 g DM / pair / day (see Appendix 3: “g4”) according to analysis ME = 2,89 Kcal / g DM (Zootrition ®; see Gomis, 2007: p.142) thus, the couple receives 2,89 x 131 = 378,6 Kcal ME / day representing 378,6 / 4,549 = 83,2 Kcal ME / Kg BW using the approximation ME = 4CP+9CFat+4CHO, we obtain 3,50 Kcal / g DM for this diet thus, the couple receives 3,5 x 131 = 458,5 Kcal ME / day representing 458,5 / 4,549 = 100,8 Kcal ME / Kg BW that fits with recommendation for OWM of 100 Kcal ME /Kg BW (NRC 1978) using the approximation for required BMR [Kcal EM] = 1,35 . 95 PV[Kg]0.75 (according to King, 1978: for E. fulvus mayottensis 86.3 122.8 kcal PV [kg]0.75 = 78 kcal / kg BW / day; and Edwards & Ullrey, 1999: for E. mongoz et L. catta ) (see table XII): we obtain 87,8 Kcal ME /Kg BW and using a second approximation for required BMR [Kcal EM] = 24 . 4,8 MMR /1000 where MMR [ml O2/h] = 2(696.0 PV[Kg]0.76) 0,6 (according to Stahl, 1967; Justice & Smith, 1992) (see Schwitzer, 2003): we obtain 66,9 Kcal ME /Kg PV therefore, the approximate values of 83,2 to 100,8 Kcal ME / Kg BW obtained for this couple seem to be adequate according to published approximations for the energy requirement. Eg. if we consider E. m. flavifrons obese ♂ EEP # 53 (3,550 Kg) ♀ EEP # 51 (3,510 Kg): the total BW for this couple is 7,060 Kg their average intake is not known, but can be approximated to be near 3,5% of the BW (1,94 3,46 %, see § 4.1), thus: 7060 x 0,035 = 247,1 g DM / pair / day dietary energetical density is not known but can be also approximated to be near 3,9 Kcal / g DM thus, the couple can receive 3,90 x 247,1 = 963,7 Kcal ME / day representing 963,7 / 7,060 = 136,5 Kcal ME / Kg BW using the approximation for required BMR [Kcal EM] = 1,35 . 95 PV[Kg]0.75 (according to King, 1978: for E. fulvus mayottensis 86.3 122.8 kcal PV [kg]0.75 = 78 kcal / kg BW / day; and Edwards & Ullrey, 1999: for E. mongoz et L. catta ) (see table XII): we obtain 78,7 Kcal ME /Kg BW 1 Primate milks are typically diluted (8.5 34.1% DM) with energy concentrations ranging from 0.5 to 0.85 kcal GE g 1 for Lemuroidea and 1.1 to 1.8 kcal GE g 1 for several prosimian species (Tilden and Oftedal, 1995; Tilden 0.75 and Oftedal, 1997). Estimated GE outputs during a single lactation are 5,100 7,500 kcal BW kg for bushbabies and 0.75 2,100 3,100 kcal BWkg for lemurs . Thus, despite the shorter lactation in bushbabies than with the lemurs, the estimated total milk energy transfer of bushbabies is nearly twice that of lemurs relative to maternal metabolic size (Tilden and Oftedal, 1995). Differences in milk composition might be related to differences in maternal care. For example, prosimians that carry their young during lactation produce more dilute milks than do species that leave their young unattended for long periods (Tilden and Oftedal, 1997) (NRC, 2003). and using the second approximation for required BMR [Kcal EM] = 24 . 4,8 MMR /1000 where MMR [ml O2/h] = 2(696.0 PV[Kg]0.76) 0,6 (according to Stahl, 1967; Justice & Smith, 1992) (see Schwitzer, 2003): we obtain 60,2 Kcal ME /Kg BW therefore, the approximate value of 136,5 Kcal ME / Kg BW (high intake and energetical density hypothesis) obtained for this couple is higher than published approximations for the energy requirement, but not so much higher
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 32 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 we can also note that for obese animals the energy requirements tend to decrease when benchmarked against BW and that the energetical overprovision may not explain all the obesity situations: in fact it is more likely that all the unbalanced diets (with either low protein content, low fiber content, high simple saccharids and carbohydrates content, and/or high energy density) may gradually install and maintain the obesity. 4.6 How to manage an overweight lemur As seen previously in § 3.3, all the Malagasy lemurs are prone to obesity in captive conditions. The over provision of unvaried and too rich food may not explain all the situations: obesity seems to develop gradually and several factors make it difficult to control, as illustrated in figure 13 above. This schematic representation shows that four main factors should be revised when attempting to reduce the body weight of an overweight individual: nutritional knowledge, feeding regime control (quantitative and qualitative), frequency of meals and environmental enrichment. POOR INADEQUATE NUTRITIONAL FOODS OR UNBALANCED KNOWLEDGE PROPORTIONS FEEDING REGIME & CONTROL
TOO LOW LOW FIBRE CONTENT PROTEIN CONTENT & HIGH SIMPLE SACCHARIDS & CARBOHYDRATES CONTENT POOR FOOD FOOD UNBALANCED ENVIRONMENTAL OVERPROVISION DISTRIBUTION INTAKE ENRICHMENT COMPETITION LOW BMR ! FOR FOOD & LOWER ENERGY AGGRAVATED INTAKE ENERGY EXPENDITURE FEMALE INCREASED OVERPROVISION DOMINANCE LOW MEAL MODIFIED OBESITY BREEDING FAILURE FREQUENCY APPETITE CONTROL & DIABETES Fig.13: Factors promoting and maintaining the obesity among captive lemurs (D. Gomis 2008)
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 33 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 As seen previously, obesity can be defined as more than two standard deviations (SD) over the mean wild weight (Kemnitz et al. , 1989). But this mean wild weight and the SD values remain open for discussion; thus we are now only able to formulate acceptable captive weight ranges (see § 3.3). The definition of an obese lemur can neither be determined with a standard measure such as the body mass index (BMI) used by the human medical profession. Therefore, an easier way to determine whether a lemur can be considered as obese or not, is to estimate the overweight as a percentage: 10% being commonly admitted by the veterinary profession as a simple definition for obesity, and 20% as the upper limit often associated to health problems. % overweight = 100 x (BW – max. value of the acceptable range)/ max. value of the acceptable range eg.: a ♀ Sclater’s black lemur weighing 3,510Kg has (3,510 2,800)/2,800 = 25% of overweight. A safe method to reduce the BW of an obese animal is to first reduce the energy provision to 25%, and then to 10% every 2 or 3 weeks, in order to lose 1% of BW each week. This method is only possible when the dietary energy density is known and controlled (eg. using Zootrition® software), which is often not the case in European zoos. And a stress free weighing method must be undertaken on a regular basis. eg. for the ♀ Sclater’s black lemur weighing 3,510Kg: the BW reduction of 696g will take at least 5 months: week 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 BW [Kg] 3,510 3,475 3,440 3,406 3,372 3,338 3,305 3,272 3,239 3,206 3,174 3,143 3,111 3,080 3,049 3,019 2,989 2,959 2,929 2,900 2,871 2,842 2,814 BW loss [g] 35,1 34,7 34,4 34,1 33,7 33,4 33,0 32,7 32,4 32,1 31,7 31,4 31,1 30,8 30,5 30,2 29,9 29,6 29,3 29,0 28,7 28,4 Of course, the energy provision is a useful tool when inducing a body weight loss, but the dietary nutritional balance has to be ensured first (see previous §§ 4.2, 4.3 and 4.4). The use of higher protein content pellets or foods (eg. hard boiled egg, boiled chicken or beef meat, arthropods, etc.: see table XV and Appendix 4), offered as a first breakfast meal, may help to meet the protein requirement and to control the intake increase, induced by low protein diets (see figure 13). Also, in order to reduce the BW by controlling the total amount eaten, it is obligatory to offer multiple meals (preferably 3 a day). 5 KEY POINTS FOR OVERWEIGHT MANAGEMENT 1. CONTROL THE AMOUNTS & THE NUTRITIONAL BALANCE OF THE GIVEN DIET 2. GIVE THE FOOD IN MULTIPLE MEALS [ preferably 3 a day ] 3. WEIGH REGULARLY [ at least each 3rd week ]: THE BW LOSS MUST BE GRADUAL 4. STICK TO NEW FEEDING REGIME & METHODS [ even if the BW loss seem poor initially! ] 5. IMPROVE THE ENVIRONMENTAL ENRICHMENT [ when food used = part of the diet! ] 3,7 3,5 BW LOSS STEP BY STEP 3,3
3,1 BW [Kg] STICK TO FEEDING REGIME & FEEDING 2,9 METHOD, EVEN IF THE BW LOSS SEEM POOR 2,7 > 20% OVERWEIGHT = NOT SHORTER THAN 5 6 MONTHS 2,5 0 1 2 3 4 5 6 7 8 9 10111213141516171819202122 Months
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 34 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 Appendix 1: Eg. of an intake study for Crowned lemurs at Mulhouse Zoo, France (datas 2002-2004) study n° date age of young Number TOTAL INTAKE SIMIAL CROUSTI CP % CP from CROC young coefficient of g AF g AF / g g DM / % g g AF / % g g AF / % % SIMIAL C. Animals Al DM Al DM AF Al DM AF Al DM DM CROC coro g1 (1) juil 02 2m 1j 0,098557 2,10 323 154 74 35 23 16 8 20 10 5 12 13,8 44,8 19,6 coro g1 (2) janv 03 7m 0,663083 2,66 496 186 126 47 25 36 14 26 17 6 12 14,9 54,1 18,2 17j coro g1 (3) juin 03 3,00 460 153 112 37 24 32 11 26 20 7 16 15,5 51,4 22,8 coro g1 (4) oct 03 3,00 383 128 104 35 27 27 9 23 30 10 26 16,7 43,6 34,6 coro g2 (1) juil 02 3m 8j 0,224913 4,22 619 146 145 34 23 31 7 19 25 6 15 13,7 44,1 25,1 coro g2 (2) janv 03 8m 0,78842 4,79 753 157 211 44 28 73 15 31 32 7 14 16,5 58,5 18,4 24j coro g2 (3) juin 03 1m 0,078177 4,08 762 187 181 44 24 43 11 21 29 7 14 14,5 45,6 21,8 25j coro g2 (5) févr 04 9m 5j 0,826123 4,83 519 108 143 30 28 38 8 24 40 8 25 16,2 45,7 34,5 coro g3 (4) oct 03 3,00 371 124 103 34 28 31 10 27 30 10 26 17,7 47,0 32,9 coro g4 (5) févr 04 2,00 283 141 78 39 28 26 13 30 18 9 20 17,3 53,2 26,5 AVERAGE E. coronatus 148 38 26 11 25 7 18 16 49 25 Eulemur coronatus: intake composition (%AF), ns=6, ng=4, ni=13, nd=42 APPLES, WITH SKIN BANANAS CARROTS MILK-BREAD MIX SIMIAL 7001 LETTUCE CROUSTI' CROC CHICORY CUCUMBER 0% LEEKS SIMIAL 7001 7% LETTUCE 4% 0% CAULIFLOWER CROUSTI' CROC 5% 1% SQUASH, SUMMER ZUCCHINI 0% 0% MILK-BREAD MIX 11% CUCUMBER 3% CELERY 1% 1% BROCCOLI PINEAPPLE 2% RADISHES CARROTS 4% GRAPES 2% 0% FENNEL, BULB 1% CABBAGE TOMATOES, RED RIPE BANANAS 7% REST 12% 2% 1% TURNIPS PEPPERS 0% EGGPLANT 0% 0% BRUSSELS SPROUTS 0% SULTANINES 1% 0% KIWI 0% APPLES 41% 0% 1% ORANGE MELONS 0% PEARS 0% STRAWBERRIES 0% PINEAPPLE GRAPES PEACHES CHERRIES BLUEBERRIES Mulhouse Zoo basical diet composition for Crowned lemurs (amounts per adult animal and per day): 6. 110g of fruits and vegetables (see list on Appendix 10), with a minimum of 60 g of apple 7. 10 g of “Simial” powder (see composition on Appendix 9) 8. 10 g of Milk bread (see composition on Appendix 11) 9. 10 g of “Crousti’ Croc” dog pellets (see composition on Appendix 9) => TOTAL: 140 g per adult animal and per day
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 35 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 Appendix 2: Eg. of an intake study for Red bellied lemurs at Mulhouse Zoo, France (datas 2002-2004) study n° date age of young Number TOTAL INTAKE SIMIAL CROUSTI CP % CP from CROC young coefficient of g AF g AF / g g DM / % g g AF / % g g AF / % % SIMIAL C. Animals Al DM Al DM AF Al DM AF Al DM DM CROC rubri g1 (1) juil 02 3,00 704 235 166 55 24 36 12 19 35 12 19 13,8 43,5 30,6 rubri g1 (2) janv 03 3,00 824 275 220 73 27 71 24 29 29 10 12 15,5 57,9 16,8 rubri g1 (3) juin 03 2,00 548 274 137 68 25 39 20 26 24 12 16 15,8 50,7 22,5 rubri g1 (4) janv 04 4m 1j 0,302357 2,30 515 224 146 63 28 51 22 31 31 14 19 16,9 57,4 25,4 rubri g1 (5) mars 04 6m 3j 0,53367 2,53 592 234 168 66 28 50 20 27 45 18 24 16,7 49,8 32,1 rubri g2 (1) juil 02 3m 7j 0,220837 3,22 784 243 197 61 25 39 12 18 55 17 25 14,3 39,0 39,0 rubri g2 (2) janv 03 9m 0,856693 3,86 1101 285 292 76 27 88 23 27 44 11 13 14,8 56,8 20,2 14j rubri g2 (3) juin 03 2m 0,163773 4,16 1056 254 261 63 25 66 16 23 43 10 15 14,4 49,3 22,8 20j rubri g2 (4) janv 04 9m 2j 0,815933 4,82 1072 223 282 59 26 86 18 28 50 10 16 15,3 55,8 23,1 rubri g2 (5) mars 04 11m 1,025847 5,03 1042 207 284 57 27 78 15 25 75 15 24 16,0 47,9 33,0 4j AVERAGE E. rubriventer 245 64 26 18 25 13 18 15 51 27 Eulemur rubriventer: intake composition (% AF,) ns=5, ng=2, ni=8, nd=35 APPLES, WITH SKIN BANANAS CARROTS MILK-BREAD MIX SIMIAL 7001 LETTUCE CROUSTI' CROC CHICORY CUCUMBER LEEKS SIMIAL 7001 7% SQUASH, SUMMER ZUCCHINI MILK-BREAD MIX 10% LETTUCE 3% 1% CELERY 1% CROUSTI' CROC 5% 1% BROCCOLI CARROTS 4% CUCUMBER 2% RADISHES 0% FENNEL, BULB BANANAS 7% PINEAPPLE 2% 1% CABBAGE 1% 0% TOMATOES, RED RIPE REST TURNIPS 11% 0% PEPPERS 1% 0% EGGPLANT 0% BRUSSELS SPROUTS 1% 0% SULTANINES 0% ORANGE 1% APPLES 48% 1% 0% MELONS 0% 0% PEARS STRAWBERRIES 0% PINEAPPLE 0% 0% 0% GRAPES PEACHES CHERRIES PLUMS DATES Mulhouse Zoo basical diet composition for Red bellied lemurs (amounts per adult animal and per day): 10. 180g of fruits and vegetables (see list on Appendix 10), with a minimum of 100 g of apple 11. 10 g of “Simial” powder (see composition on Appendix 9) 12. 20 g of Milk bread (see composition on Appendix 11) 13. 15 g of “Crousti’ Croc” dog pellets (see composition on Appendix 9) => TOTAL: 225 g per adult animal and per day
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 36 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 Appendix 3: Eg. of an intake study for Blue eyed black lemurs at Mulhouse Zoo, France (data 2002-2004) study n° date age of young Number TOTAL INTAKE SIMIAL CROUSTI CP % CP from CROC young coefficient of g AF g AF / g g DM / % g g AF / % g g AF / % % SIMIAL C. Animals Al DM Al DM AF Al DM AF Al DM DM CROC flavi g1 (1) juil 02 2,00 496 248 132 66 27 33 16 22 35 18 24 15,4 45,2 34,4 flavi g1 (2) janv 03 1,00 350 350 97 97 28 39 39 36 10 10 9 17,1 65,8 12,1 flavi g1 (3) juin 03 2,00 502 251 129 65 26 37 19 26 26 13 18 15,7 51,1 25,7 flavi g2 (1) juil 02 2,00 554 277 141 71 25 31 16 20 35 18 22 14,4 42,6 34,5 flavi g2 (4) oct 03 2,00 406 203 112 56 28 33 16 26 30 15 24 16,3 50,3 32,9 flavi g2 (5) févr 04 2,00 451 226 123 62 27 39 19 28 30 15 22 16,7 52,4 29,2 flavi g3 (2) janv 03 2,00 598 299 151 76 25 51 26 31 13 6 8 15,0 63,2 11,4 flavi g4 (3) juin 03 2,00 634 317 152 76 24 32 16 19 30 15 18 14,1 41,8 28,0 flavi g4 (4) oct 03 2,00 442 221 124 62 28 38 19 27 29 14 20 16,4 51,9 28,1 flavi g4 (5) févr 04 2,00 432 216 117 59 27 37 19 28 30 15 23 16,6 53,2 30,8 AVERAGE E. macaco flavifrons 261 69 26 20 26 14 19 16 52 27 APPLES, WITH SKIN Eulemur flavifrons: intake composition (%AF), ns=5, ng=4, ni=8, nd=35 BANANAS CARROTS MILK-BREAD MIX SIMIAL 7001 LETTUCE CROUSTI' CROC CHICORY CUCUMBER 0% LEEKS 0% CAULIFLOWER SQUASH, SUMMER ZUCCHINI SIMIAL 7001 8% 0% CELERY MILK-BREAD MIX 10% 1% LETTUCE 3% 2% BROCCOLI RADISHES CARROTS 5% 0% CROUSTI' CROC 6% FENNEL, BULB 0% CUCUMBER 3% 2% CABBAGE BANANAS 6% 0% 1% TOMATOES, RED RIPE 0% TURNIPS PEPPERS 0% REST 13% 0% EGGPLANT 0% SULTANINES 1% KIWI 0% ORANGE 0% GRAPEFRUIT MELONS 1% 0% 1% MANGO APPLES 47% 0% 1% PEARS 0% STRAWBERRIES 0% 0% 0% PINEAPPLE 0% GRAPES 0% PEACHES 0% APRICOTS CHERRIES PASSION-FRUIT PLUMS TANGERINES Mulhouse Zoo basical diet composition for Blue eyed black lemurs (amounts per adult animal and per day): 14. 160g of fruits and vegetables (see list on Appendix 10), with a minimum of 100 g of apple 15. 10 g of “Simial” powder (see composition on Appendix 9) 16. 20 g of Milk bread (see composition on Appendix 11) 17. 15 g of “Crousti’ Croc” dog pellets (see composition on Appendix 9) => TOTAL: 205 g per adult animal and per day
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 37 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 Appendix 4: Eg. of the feeding regime for Blue eyed Black lemurs at Banham Zoo, UK Provided by Clare Jenkinson (26/09/2008)
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 38 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 39 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 Appendix 5: Eg. of the feeding regime for Blue eyed Black lemurs at Edinburgh Zoo, UK Provided by Graham Catlow (12/09/2008)
Edinburgh Zoo
Mon/Thurs Tues/Weds/Fri/Sat/Sun Pellets (trio munch) 100g 100g Apple 100g 100g Greens 100g 100g Fruit 50g Root veg (two types if available) 300g 350g
Sclater’s Lemur Diet Please use a variety of feeding devices to encourage activity. NO banana to be fed unless medication is being given. Foodstuff the Sclater’s lemur should not be fed: Banana, Kiwi fruit, Melon, Oranges. Broccoli, Spinach, Potatoes. Sunflower seeds. Blue eyed black lemur food lists Greens – courgette, celery, spring onion, fennel, leek, cucumber, chicory Root vegetable – turnip, beetroot, carrot, parsnip, celeriac Fruits – plums, peaches, nectarines, pears, grapes, strawberries, blueberries, raspberries, pomegranate, papaya, apricots, Scatter feed items – raisins, soaked wheat, flaked maize, dates, currants, mealworms, papaya chunks, peanuts in shells, popcorn (no oil or flavour), sprouted pulses General notes – Scatter feeds are fed twice daily, once am and once pm, and item fed differs each time according to a rota to ensure variation. Only very small amounts are given to prevent weight gain whilst still encouraging foraging behaviours. Fruits, root vegetables and greens – combinations of items given vary each day so that no two days feeds are the same throughout the week. Items also vary depending on what is in season throughout the year. Feeds are placed in differing positions around the enclosure, fed inside and outside and using various feeding devices to encourage activity and foraging behaviours. Fruit is now restricted in the diet with an increase in root vegetables and banana has been removed as both animals were overweight.
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 40 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 Appendix 6: Eg. of the feeding regime for Blue eyed Black lemurs at Montpellier Zoo, France Provided by Cédric Libert (08/09/2008) FEEDING REGIME AT ZOO LUNARET BLUE EYED BLACK LEMURS ( Eulemur macaco flavifrons ) MARCH 2008 Daily amounts per adult animal : INGREDIENTS QUANTITIES DISTRIBUTION pellets given first in the morning Leaf eating primate pellets 30g (09h00) and fruits/vegetables given later (11h00) Apple 1 (~ 120 g*) Cut into 4 pieces Banana 1(~ 150 g*) Cut into 4 pieces Orange ½ (~ 90 g*) Cut into 4 pieces Kiwi ½ (~ 55 g*) Cut into 4 pieces Carrot ½ (~ 80 g*) Cut into 4 pieces Tomato ½ (~ 50 g*) Cut into 2 pieces Lettuce 1 leaf (~ 15g*) Min & Vit supplementation : SOFCANIS : 1/4 coffee spoon / day, during the first 10 days of each month Enrichment with bamboos, fresh branches every week. * approximative weights added by D. Gomis
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 41 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 Appendix 7: Eg. of the feeding regime for Blue eyed Black lemurs at Colchester Zoo, UK Provided by Claire Saunders (17/09/2008) Blue Eyed Black Lemurs Group size 2 Day 1 Day 2 Day 3 Day 4 Day 5 Day 6 Day 7 Lettuce Carrot 100g Carrot Green bean Plums 190g Carrots 50g Apple 200g Green Beans 100g 100g Apples 200g Red Pepper 200g Turnip 250g Tomato Celery 50g Cherry 50g Tomato 100g Courgette 100g Tomato 50g tomato 100g Lettuce 150g 100g Cucumber 150g Apple Mixed Salad Green Beans Celery 100g 150g 150g 50g 100g Banana Courgette Carrots 100g 75g 150g
Plus – 50g Mazuri Primate Pellets Basix per animal on a daily basis.
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 42 Gomis D., Moisson P. and De Michelis S. – Mulhouse Zoo, v2. Sept. 2009 Appendix 8: Survey on the BW of captive Blue eyed Black lemurs in European zoos: MALES (Data 2000-2008) EEP# house name birth date BW date BW date BW date BW date BW date BW date BW date BW date BW date 1 DANOS W ??? 2,570 01/09/01 2,140 09/12/02 3 BIE W 01/06/82 2,000 31/10/00 5 KOOT W 01/06/83 1,900 25/09/02 6 SAARTJE W 01/06/83 2,730 18/08/05 2,881 26/11/05 2,758 09/02/06 2,360 15/07/08 8 JACQUES W 01/06/84 2,670 01/09/01 1,180 24/02/03 21 EDOUARD C 22/04/92 2,350 21/11/08 34 LILIAN C 04/04/95 2,300 28/01/02 2,300 11/04/02 2,500 19/06/03 2,450 05/02/04 2,100 26/05/04 2,600 13/06/05 2,900 19/03/07 2,500 04/02/08 2,400 01/04/08 36 BOBBY C 17/03/96 2,950 18/08/05 2,591 26/11/05 2,600 09/02/06 3,300 26/08/08 38 MYNOS C 23/03/96 2,800 01/12/07 2,660 24/04/08 2,670 26/05/08 2,960 25/08/08 43 NAMOS C 31/03/97 3,500 05/08/07 2,500 19/11/08 45 OLIVIER C 24/03/98 2,427 26/11/05 2,256 09/02/06 2,277 06/09/08 53 SAROH C 16/06/99 2,120 07/09/01 3,550 03/09/08 60 RODOLPHE C 01/04/00 2,120 07/09/01 3,470 01/11/08 64 MICHA C 11/03/01 2,700 16/09/04 2,470 04/10/05 2,050 25/05/06 2,200 29/08/06 2,050 12/10/06 2,700 13/10/08 67 SCOTCH C 10/04/01 2,690 22/09/08 68 BOB C 20/03/02 2,650 14/11/08 75 RANO C 04/03/04 2,900 08/09/08 78 ATTILA C 28/02/05 1,280 01/02/06 1,672 01/06/06 3,000 17/10/08 81 CESAR C 05/05/07 1,784 12/09/08 (see averages and comments pp.20 21) NON OBESE ANIMAL OBESE ANIMAL 2,201 BW dead animal 2,758 BW alive animal Appendix 8: Survey on the BW of captive Blue eyed Black lemurs in European zoos: FEMALES (data 1998-2008) EEP# house name birth date BW date BW date BW date BW date BW date BW date BW date BW date BW date 7 BERNADETTE W 01/06/84 2,680 10/09/01 2,559 26/11/05 2,462 01/02/06 2,174 01/06/06 2,382 12/09/08 10 GOLDI C 16/04/86 1,756 20/12/05 11 KIMJUNG C 31/03/87 2,477 26/11/05 2,398 09/02/06 2,386 01/06/06 2,201 18/06/08 17 DORIANE C 27/03/91 2,800 26/03/98 25 SIDOINE C 03/04/93 2,477 26/11/05 2,000 09/02/06 2,477 06/09/08 27 GUNDI C 27/03/94 2,450 28/01/02 2,400 11/04/02 2,450 03/12/02 2,600 19/06/03 2,300 25/11/03 2,700 05/02/04 2,600 06/01/05 3,250 05/08/07 2,500 19/11/08 30 JOELLE C 22/05/94 2,600 08/09/08 33 DIANE C 01/04/95 1,925 20/02/01 37 MELANIE C 18/03/96 1,992 21/05/04 2,440 04/10/05 2,350 25/05/06 2,000 29/08/06 2,210 12/10/06 2,300 13/10/08 41 NADIA C 22/03/97 2,910 14/11/08 42 NOEMIE C 29/03/97 3,740 17/10/07 3,740 26/08/08 44 GILA C 16/04/97 3,180 02/01/06 3,000 17/10/08 47 ZAZOU C 11/04/98 3,770 01/11/08 51 FUORO C 19/03/99 3,510 03/09/08 52 PATTY C 25/03/99 2,610 07/09/01 2,740 22/09/08 57 TOULOUSE C 22/03/00 3,800 01/12/07 3,630 24/04/08 3,540 26/05/08 3,830 25/08/08 71 BELLE C 08/05/02 3,200 23/11/06 3,200 03/02/07 3,200 19/03/07 3,100 24/04/07 2,700 05/07/07 2,500 28/10/07 2,300 11/12/07 2,400 04/02/08 2,200 01/04/08 73 SJAAN C 27/03/03 3,920 14/09/06 2,850 21/11/08 (see averages and comments pp.20 21) NON OBESE ANIMAL OBESE ANIMAL 2,201 BW dead animal 2,758 BW alive animal Appendix 9 : Nutrient composition of the pellets used at Mulhouse Zoo, France Nutrient Category: Ash/Minerals Nutrient Category: Carbohydrates Nutrient Qty Unit Nutrient Qty Unit Ash 12.86 % Crude Fiber 6.46 % Calcium 2.78 % NDF 13.75 % Copper 47.44 mg/kg ADF 8.16 % Iodine 0.14 % Lignine 1.68 % Iron 291.86 mg/kg Total Dietary Fiber 18.00 % Magnesium 0.22 % Phosphorus 1.67 % Selenium 0.41 mg/kg Nutrient Category: Fat Sodium 0.59 % Nutrient Qty Unit Zinc 41.94 mg/kg Crude Fat 6.67 % Calcium/Phosphor ratio 1.66:1 Nutrient Category: Protein Nutrient Category: Vitamins Nutrient Qty Unit Nutrient Qty Unit Arginine 1.70 % Choline 2332.10 mg/kg Crude Protein 31.03 % Vit. A 22.23 IU A/g or RE/g Cystine 0.55 % Vit. B1 (Thiamin) 2.67 mg/kg Isoleucine 1.33 % Vit. D3 5.33 IU Vit. D3/g Leucine 3.17 % Vit. E 55.56 mg/kg Lysine 1.44 % Vit. K 2.22 mg/kg Methionine 0.74 % Threonine 1.11 % Nutrient composition of “Simial” pellets (v.7001; SANDERS ®), DM base (10.01 % water) Nutrient Category: Ash/Minerals Nutrient Category: Carbohydrates Nutrient Qty Unit Nutrient Qty Unit Ash 8.99 % Crude Fiber 4.49 % Calcium 1.35 % Copper 5.62 mg/kg Nutrient Category: Fat Phosphorus 1.12 % Nutrient Qty Unit Calcium/Phosphor ratio 1.21:1 Crude Fat 6.74 %
Nutrient Category: Vitamins Nutrient Category: Protein Nutrient Qty Unit Nutrient Qty Unit Vit. A 7.87 IU A/g or RE/g Crude Protein 22.47 % Vit. D3 0.79 IU Vit. D3/g Vit. E 89.89 mg/kg Nutrient composition of “Crousti Croc” dog pellets (SANDERS ®), DM base (11.00 % water) Appendix 10 : List of fruits and vegetables given to Eulemur sp. at Mulhouse Zoo, France FRUITS VEGETABLES DAILY OFFERED Apples Carrots Bananas Salad (especially Lettuce) FREQUENTLY OFFERED Tangerines Cucumber Kiwi Courgettes Oranges Chicory Grapes Fennel Pineapples Leeks Melons Green and red peppers Aubergine LESS FREQUENTLY OFFERED Apricots Broccoli Nectarines Celery Cherries Cauliflower Pears Radishes Strawberries Turnips Peaches Plums Sultanas Tomatoes RARELY OFFERED Dates Cabbage Figs Dried figs Raspberries, Bilberries Mirabelle plums Grapefruits Water Melon Avocado Carambola Litchis Mango Passion fruits Walnuts
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 46 Gomis D. – Mulhouse Zoo, December 2008 Appendix 11: Recipe and composition of the “milk bread mixture” at Mulhouse Zoo, France Note: This mixture of bread, water and milk powder was made at Mulhouse Zoo in order to include Vitapaulia M (INTERVET®) in Lemuridae diets. The receipt can change depending on the type of bread used -usually it’s white commercially prepared bread- and final consistency that animals eat better. As this mixture contains milk, the CP level in DM is around 15 to 17% and proteins delivered by this mixture can indeed reach 13,6 % of the total intake proteins in Lemuridae diets. Intake studies revealed higher incorporation than first expected (see Appendix 1 to 4).
Ingredients: Bread, white 1000 g Milk powder 220 g Water 660 mL Vitapaulia M 12 mL Nutrient Category: Ash/Minerals Nutrient Category: Vitamins Nutrient Qty Unit Nutrient Qty Unit Cobalt 1580.00 mg/kg Vit. A 210000.00 IU A/g or RE/g Copper 4000.00 mg/kg Vit. B1 (Thiamin) 21000.00 mg/kg Magnesium 0.37 % Vit. B3 (niacin) 63000.00 mg/kg Manganese 307830.00 mg/kg Vit. B6 (Pyridoxine) 10500.00 mg/kg Zinc 3395.00 mg/kg Vit. D3 21000.00 IU Vit. D3/g Vit. E 23100.00 mg/kg Nutrient composition of Vitapaulia M, DM base (98.00 % water) Nutrient Category: Ash/Minerals Nutrient Category: Protein Nutrient Qty Unit Nutrient Qty Unit Ash 3.93 % Arginine 0.65 % Calcium 0.40 % Crude Protein 17.24 % Cobalt 0.46 mg/kg Cystine 0.28 % Copper 2.84 mg/kg Histidine 0.41 % Iron 37.49 mg/kg Isoleucine 0.83 % Magnesium 0.06 % Leucine 1.42 % Manganese 93.35 mg/kg Lysine 0.85 % Phosphorus 0.32 % Methionine 0.36 % Potassium 0.49 % Threonine 0.62 % Selenium 0.39 mg/kg Tryptophan 0.22 % Sodium 0.76 % Tyrosine 0.64 % Zinc 17.09 mg/kg Valine 0.93 %
Nutrient Category: Vitamins Nutrient Category: Fat Nutrient Qty Unit Nutrient Qty Unit Folacin 1.25 mg/kg Crude Fat 8.59 % Pantothenic Acid 11.79 mg/kg Linoleic Acid 0.95 % Vit. A 65.07 IU A/g or RE/g Linolenic Acid 0.10 % Vit. B1 (Thiamin) 12.59 mg/kg Vit. B2 (Riboflavin) 7.76 mg/kg Nutrient Category: Carbohydrates Vit. B3 (Niacin) 67.72 mg/kg Nutrient Quantity Unit Vit. B12 0.01mg/kg TDF 2.76 % Vit. B6 (Pyridoxine) 4.75 mg/kg Vit. C (Ascorbic acid) 21.10 mg/kg Vit. D3 6.05 IU Vit. D3/g Vit. E 12.79 mg/kg Nutrient composition of Milk bread Lemurs, DM basis (70.90 % water)
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 47 Gomis D. – Mulhouse Zoo, December 2008 Appendix 12: Plants’ database for Eulemur sp. at Mulhouse Zoo, France Provided by Corinne Fromm Eulemur coronatus
in the outside
enclosure
animals can Amelanchier sp, Carex pendula, Carum carvi, Foeniculum vulgare, Hedera helix, Melissa officinalis, Mentha, catch near the Origanum vulgare mesh
Acaena magellanica, Acer capillipes, Bambou, Aucuba japonica variegata, Berberis thunbergii, Betula utilis var jacquemonti, Calycanthus occidentalis, Catharanthus roseus, Corylus avellana, Crataegom espilusXdardarii, Davidia involucrata, Decaisnea fargesii, Deutzia sp, Dipelta floribunda, Elaeagnus animals umbellatus, Epimedium pinnatum, Euonymus alatus, Euonymus myrianthus, Geranium himalayense, cannot catch Helleborus orientalis,Hypericum androsaemum, Ilex aquifolium, Iris sp cultivars, Lonicera tatarica, but < 20m Ophiopognon planiscapus 'Nigrescens', Pennisetum alopecuroides,Picea abies, Pinus pumita, Prunus tenella, Rhodotypos scandens, RibesXgordonianum, Rosa moyesii, Sedum spurium, Sorbus pratii, Symphoricarpos albus, Syringa X 'Josée', Taxcus baccata, Viburnum farreri, Vinca major, Waldsteinia geoides, Waldsteinia ternata
Eulemur macaco flavifrons
in the outside Achillea millefolium, Bellis perenis, Foeniculum vulgare, Melissa officinalis, Mentha, Miscantus gracillimus, enclosure Miscantus sinensis
animals can catch near the Carex pendula, Carum carvi, Foeniculum vulgare, Melissa officinalis, Mentha, Origanum vulgare, mesh
Acaena magellanica, Acer capillipes, Calycanthus occidentalis, Catharanthus roseus, Crataegom espilusXdardarii, Davidia involucrata, Decaisnea fargesii, Dipelta floribunda, Elaeagnus umbellatus, animals Epimedium pinnatum, Euonymus alatus, Euonymus myrianthus, Geranium himalayense, Helleborus cannot catch orientalis, Hypericum androsaemum, Iris sp cultivars, Lonicera tatarica, Ophiopognon planiscapus but < 20m 'Nigrescens', Pennisetum alopecuroides, Picea abies, Pinus pumita, Prunus Tenella, Rhodotypos scandens, RibesXgordonianum, Sedum spurium, Sorbus pratii, Syringa X 'Josée', Taxcus baccata, Viburnum farreri, Vinca major, Waldsteinia geoides, Waldsteinia ternata Eulemur mongoz
in the outside Bambou, Carex pendula enclosure
animals can catch near the Parrotia persica, Robinia pseudoacacia, Rosa canina mesh Chamaecyparis sp, Cornus alternifolia, Crataegus monogyna, Elaeagnus umbellatus, Euonymus fortunei ' animals vegetus ', Lonicera morrowii, Magnolia stellata, Malus sargentii, Nandina domestica, NepetaXfaassenii 'Six cannot catch Hills Giants', Picea pungens 'Glauca Globosa', Pleioblastus graminus, Prunus Tenella, Rhododendron sp, but < 20m Vitis vinifera, Waldsteinia geoides Eulemur rubriventer
in the outside Bambou, Matteucia struthiopteris, Miscantus sinensis enclosure
animals can catch near the Carum carvi, Cornus alternifolia, Elaeagnus umbellatus, Hedera helix, Origanum vulgare mesh animals Euonymus fortunei ' vegetus ', Magnolia stellata, NepetaXfaassenii 'Six Hills Giants', Picea pungens 'Glauca cannot catch Globosa', Pennisetum alopecuroides, Pleioblastus graminus, Prunus Tenella, Rhododendron sp, Robinia but < 20m pseudoacacia, Vitis vinifera, Waldsteinia geoides
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 48 Gomis D. – Mulhouse Zoo, December 2008 Appendix 13: Proposed requirement ranges for diet formulation and analysis From GOMIS D. et al. (2007) Mulhouse Zoo Dietary Manual, descriptions of the feeding regimes currently in use. p. 125. DM base : Unit Min Max Metabolic Energy Kcal/Kg BW/day 100* __ d) __ d) __ d) Crude Protein % 16.7 c) __ d) Crude Protein % 12 e) 15 e) Carbohydrates % 50 a) 60 a) Crude Fat % traces a) 10 a) Fiber % NDF 10* 30 % ADF __ d) __ d) Calcium % 0.55 0.8 b) Phosphorus % 0.33 0.6 b) Potassium % 0.4 0.89 a) Sodium % 0.2 b) 0.65 Magnesium % 0,1 g) 0.2 c) Chloride % 0.2 0.55 Copper mg/kg DM 12 20 100 b) Zinc mg/kg DM 11 c) Main source: Manganese mg/kg DM 20 b) 100 a) NRC, National Research Council, Committee on Iodine mg/kg DM __ d) 0.35 b) Animal Nutrition (2003) Nutrients requirements of Nonhuman Primates : second revised edition. The Iron mg/kg DM 80 a) 140 c) National Academies Press, Washington. Vit A IU/kg DM 8000 b) 14000 c) Vit D3 IU/kg DM 1000 3000 Excepted for a) to e) : Vit E mg/kg DM 56 c) 100 b) a) NRC, Nutrient Requirements for Nonhuman Primates, Vit K mg/kg DM 0.5** b) 12 1978 Vit C mg/kg DM 55 111* b) NRC, Nutrient Requirements for Non Human Primates, 2003. Table 11 2 : Estimated Adequate Nutrient Vit B1 mg/kg DM 1.1 5.6* Concentrations (Dry Matter basis) in diets for post weaning Vit B2 mg/kg DM 1.7 5.6* Non human c) W. L. Jansen and Joeke Nijboer, 2003: Zoo Animal Vit B3 mg/kg DM 16 56 Nutrition, Tables and Guidelines, Recommendations d) No reliable data found Vit B5 mg/kg DM 12 b) __ d) e) practical values, used at Mulhouse Zoo Vit B6 mg/kg DM 2.5 a) 4.4 (M) Maintenance Vit B 12 mg/kg DM 0.6* __ d) (G) Growth Folacin mg/kg DM 0.2 a) 4 b) * AZA PTAG Lemur catta – table 3. Based on NRC requirements for Old World primates (1978) and human Biotin mg/kg DM 0.1* 0.2 b) RDA values (1989) Choline mg/kg DM __d) 750 b) ** As Phylloquinone
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 49 Gomis D. – Mulhouse Zoo, December 2008 Appendix 14: Some BW records for captive Red belied lemurs in Mulhouse Zoo (data 1998-2008) EEP# sex house name birth date BW date BW date BW date BW date BW date BW date BW date BW date BW date 7 M BEBE W ~ 1983 1,940 00/09/01 1,730 17/02/04 1,766 07/12/05 1,806 25/08/06 1,824 04/09/08 31 M SANDY C 21/06/89 1,850 00/09/01 2,173 07/12/05 2,085 17/02/04 1,947 27/11/08 76 M LARRY C 13/04/95 1,650 28/12/98 86 M MARTIN C 29/04/96 1,445 25/11/97 119 M PIERROT C 10/04/99 1,710 00/09/01 120 M POLY C 14/04/99 1,800 00/09/01 164 M TOVO C 24/03/02 1,929 07/12/05 188 M URRIKAN C 04/04/03 1,747 07/12/05 227 M ARGOS C 01/05/05 1,590 25/08/06 M DIONYSOS C 26/02/08 1,206 27/11/08 10 F BRIGITTE W ~ 1984 1,630 25/11/97 1,350 03/10/01 33 F DIANE W ~ 1990 1,710 00/09/01 1,600 24/10/05 1,674 29/11/05 1,781 07/12/05 1,810 07/03/06 1,648 04/09/08 1,585 27/11/08 67 F JODY C 21/04/94 1,900 00/09/01 1,780 17/02/04 1,500 13/04/04 1,818 07/12/05 1,620 26/08/06 1,600 19/09/06 1,600 05/11/06 1,810 23/02/07 1,773 07/09/08 137 F RUDY C 20/05/00 2,100 28/10/01 149 F SARA C 03/04/01 1,050 00/09/01 197 F URSULA C 04/09/03 1,872 07/12/05 210 F VERACRUZ C 11/04/04 1,500 24/10/05 1,358 29/11/05 1,433 07/12/05 221 F APHRODITE C 25/03/2005 1,714 27/11/08 248 F BASTET C 14/06/06 1,838 04/09/08 (see averages and comments p.22) NON OBESE ANIMAL OBESE ANIMAL 2,201 BW dead animal 2,758 BW alive animal Appendix 15: Some BW records for captive Crowned lemurs in Mulhouse Zoo (data 1993-2008) ESB# sex house name birth date BW date BW date BW date BW date 49 M ALAIN W ~ 1986 1,000 25/10/93 52 M SERAPIS C 14/04/81 1,447 26/11/05 1,490 01/12/05 1,320 04/07/07 56 M ELOI W ~ 1992 1,170 25/10/03 1,540 17/02/04 1,554 00/06/06 1,140 12/06/07 57 M FELIX C 30/04/93 1,440 07/09/01 1,455 17/02/04 1,364 30/09/06 190 M RAK C 22/04/00 1,840 06/01/04 1,885 13/01/04 1,800 03/02/04 1,790 17/02/04 212 M UGO C 29/04/03 1,310 30/09/06 11 F ELISE C 13/09/91 1,245 09/10/97 44 F DEBORAH W ~ 1982 1,250 27/09/94 1,245 20/09/94 55 F ELISE W ~ 1982 1,245 09/10/97 60 F JULIE C 07/06/94 1,445 02/12/03 1,776 30/09/06 177 F PAULINE C 20/04/99 1,250 01/06/06 178 F PIA C 18/07/99 1,295 02/12/03 1,576 01/06/06 196 F ROSALIE W ~ 2000 0,970 16/03/01 0,687 26/04/01 1,985 02/12/03 (see averages and comments p.22) NON OBESE ANIMAL OBESE ANIMAL 2,201 BW dead animal 2,758 BW alive animal References 1. 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Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 55 Gomis D. – Mulhouse Zoo, December 2008 Nutritional recommendations for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs in captivity • Total amount of food: - depends on the body weight condition and the balance of the offered diet, ad libitum feeding is never recommended - multiple meals prefered: enchance the control of appetite - the total amount of food ranges from 260 to 730 g as fed / animal / Eulem ur coronatus Crowned lemur day, i.e . 70 to 130 g dry matter / animal / day • Pellets - the lower quantity ingested, the higher protein content needed - pellets are the main source of proteins of the diet: fruits and vegetables only bring about 3 -4 % of crude proteins (dry matter) and the intake diet should contain around 12 – 15 % of crude proteins (dry matter) - commonly available monkey pellets and biscuits only contain 20 % of crude proteins (dry matter) and other protein sources are therefore Eulemur rubriventer Red bellied lemur needed: a richer pellet (eg. pup pellets), hard-boiled eggs, boiled chicken, beef meat, insects… - eg. mixing 2 different pellets in the same diet per Kg of body weight: 5 g as fed of a 20% crude protein pellet + 10 g as fed of a 30% crude protein pellet + 105 g as fed of fruits and vegetables • Fruits and vegetables - Malagasy fruits ≈ Malagasy leaves ≠ Zoo fed fruits !!! Eulemur m. flavifrons - reduce and control the amounts of items being high in sugars or Sclater’s black lemur starch (bananas, melon, grapes, dates, potatoes, etc) and fats (sunflower seeds, nuts, etc) • Obesity - Eulemur species are prone to obesity in captive conditions: their energy requirement is lower than other - obesity = breeding failure & diabetes BW (Kg) 1 1,8 2,0 2,6 3 MAXIMUM FOR: CROWNED RED BELLIED SCLATER’S • Iron storage disease - Eulemur species are prone to hemochromatosis: lower the iron content of primates chows (< 200 ppm) - reduce and control the amounts of items being high in iron (broccoli, spinach, sultanas, etc) and vit.C (kiwi, oranges, etc)
Nutrition guidelines for Crowned lemurs, Red bellied lemurs and Sclater’s black lemurs 56 Gomis D. – Mulhouse Zoo, December 2008