The composition of ruffed lemur (Varecia spp.) diets in six UK zoological collections, with reference to the problems of obesity and iron storage disease

Abstract

The formulation and provision of appropriate diets for zoo animals is important in ensuring the continued health of populations. Inappropriate diets can lead to a number of nutritional deficiencies and increase the risk of disease and obesity. Ruffed lemurs (Varecia spp.) are the most intensely frugivorous of extant lemur species. Captive animals are often fed a diet which may not accurately reflect the composition of the wild diet. As such, the species is prone to obesity and can suffer from nutrition-related diseases. Here the historical diets of several populations of ruffed lemurs across UK zoological collections are described, highlighting differences in nutritional content with a focus on the problems of obesity and iron storage disease. Dietary data were collected from six zoological institutions. Comparative calculations were conducted to investigate differences in the amount of metabolisable energy, carbohydrates, sugar and iron provisioned per individual per day, between institutions. The composition of ruffed lemur diets, and the amount of food offered, differed between institutions. Metabolisable energy exceeded suggested maintenance energy requirements at all institutions. One population was found to be obese, and two institutions reported mortalities where excessive iron accumulation and iron storage disease (ISD) was observed. Reducing the relative proportion of sugar-rich fruit, removing food items high in iron and limiting daily iron to 2 mg per individual may be an effective means of decreasing the prevalence of obesity and ISD in the captive population.

Full text

OPEN ACCESS JZAR Research arcle
Journal of Zoo and Aquarium Research 6(2) 2018 41
OPEN ACCESS
Research arcle
The composion of rued lemur (Varecia spp.) diets in six UK zoological
collecons, with reference to the problems of obesity and iron storage
disease
Anthony Caravaggi1,4*, Amy Plowman2, David J Wright3, Charles Bishop1
1Department of Biological Sciences, Bangor University, Gwynedd, LL57 2UW
2Whitley Wildlife Conservaon Trust, Paignton Zoo Environmental Park, Totnes Road, Paignton, Devon, TQ4 7EU
3School of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich, NR4 7TJ
4School of Biological, Earth and Environmental Sciences, University College Cork, Disllery Field, N Mall, Cork, Ireland
*Correspondence: ar.caravaggi@gmail.com
Keywords: husbandry, frugivores, fruit,
vegetables, primates
Arcle history:
Received: 20 Mar 2017
Accepted: 4 Apr 2018
Published online: 31 Jan 2018
Abstract
The formulaon and provision of appropriate diets for zoo animals is important in ensuring the
connued health of populaons. Inappropriate diets can lead to a number of nutrional deciencies
and increase the risk of disease and obesity. Rued lemurs (Varecia spp.) are the most intensely
frugivorous of extant lemur species. Capve animals are oen fed a diet which may not accurately
reect the composion of the wild diet. As such, the species is prone to obesity and can suer from
nutrion-related diseases. Here the historical diets of several populaons of rued lemurs across UK
zoological collecons are described, highlighng dierences in nutrional content with a focus on the
problems of obesity and iron storage disease. Dietary data were collected from six zoological instuons.
Comparave calculaons were conducted to invesgate dierences in the amount of metabolisable
energy, carbohydrates, sugar and iron provisioned per individual per day, between instuons. The
composion of rued lemur diets, and the amount of food oered, diered between instuons.
Metabolisable energy exceeded suggested maintenance energy requirements at all instuons. One
populaon was found to be obese, and two instuons reported mortalies where excessive iron
accumulaon and iron storage disease (ISD) was observed. Reducing the relave proporon of sugar-
rich fruit, removing food items high in iron and liming daily iron to 2 mg per individual may be an
eecve means of decreasing the prevalence of obesity and ISD in the capve populaon.
Introducon
The provision of an appropriate and considered diet is
important in ensuring the connued health of populaons
ex situ (Hile 2004; Donadeo et al. 2016). Designing diets
for animals in capvity is oen dicult, given the variety of
potenal factors (e.g. gastrointesnal physiology, wild diet
composion, foraging behaviour and/or dental morphology),
many of which remain unquaned or poorly understood
for several exoc species (sensu Fidge and Plowman 2009).
Indeed, the provision of inappropriate diets can lead to a
variety of ailments as a result of nutrient deciencies, including
reproducve disorders (Tubbs et al. 2012) and increased
incidence of disease (e.g. Clauss and Paglia 2012), obesity
(D’Eath et al. 2009) and mortality (Hawn 2005).
Rued lemurs (Varecia spp.) are the largest extant lemurid
species (Miermeier et al. 2010). They are endemic to the
eastern rainforests of Madagascar, from the Masoala Peninsula
in the north to the Vangaindrana Farafangana region in the
south (Miermeier et al. 2010) and are classied as crically
endangered in the IUCN Red List of Threatened Species
(Andriaholinirina et al. 2014). Rued lemurs are considered to
be the most intensely frugivorous of the extant lemurs. Wild
diets consist of between 74% and 92% fruit (Bri 2000; Vasey
2002), with the remainder comprising young leaves, owers
and nectar (White 1989; Rigamon 1993; Bri 2000; Vasey
2003). Despite an overt preference for fruit, however, free-
ranging rued lemurs are adaptable in their feeding habits; at
least 132 dierent plant species have been recorded in the diet
in the wild (Morland 1991; Vasey 2000). The quanty of non-
fruit food items consumed varies seasonally and depends on
local availability (Bri 2000).
Obesity is a common problem for many primate species
housed in zoological collecons (Schwitzer and Kaumanns

Journal of Zoo and Aquarium Research 6(2) 201842
Caravaggi et al.
Z1 Z2 Z3
Food Type Cat Weight (g) ME (Kcal) CH (g) Sugar (g) Fe (mg) Weight (g) ME (Kcal) CH (g) Sugar (g) Fe (mg) Weight (g) ME (Kcal) CH (g) Sugar (g) Fe (mg)
Apple F 33.95 87.44 19.89 19.89 0.15 8.83 22.74 5.17 5.17 0.04 23.36 60.18 13.69 13.69 0.11
Banana F 63.98 98.33 24.64 21.97 0.33 140.03 215.22 53.94 48.09 0.72 128.51 197.52 49.50 44.14 0.66
Cherry F 10.67 16.36 3.92 3.92 0.07
Citrus F 8.29 10.27 2.40 2.40 0.02
Grapes F27.74 91.51 22.67 22.67 0.32
Kiwi F 2.18 3.29 0.71 0.70 0.02
Mango F 9.20 11.92 2.95 2.89 0.15 61.95 80.25 19.85 19.43 0.99
Orange F 2.38 6.59 1.50 1.50 0.02
Peach F 9.54 15.74 3.63 3.63 0.19
Pear F41.04 65.43 16.80 16.80 0.21 14.16 22.58 5.80 5.80 0.07
Plum F 2.29 3.92 0.96 0.96 0.04
Table 2a. Weight of food (g, DM), metabolisable energy (ME; Kcal), carbohydrates (CH; g), sugar (g) and iron (Fe; mg) provided per individual per day for rued lemurs at three zoological instuons (Z1–Z3) in the UK in 2008. Data
are sorted by category (Cat: F=fruit; V=vegetable; O=other) and alphabecally by food type.
2001; Videan et al. 2007). Excessive accumulaon of adipose
ssue (i.e. body fat) has been shown to be a contributory factor
in the development of heart disease, diabetes, cancer and
reproducve issues (Goodchild and Schwitzer 2008; Register and
Clarkson 2009). The problem is oen compounded by inacvity
and the onset of lethargy, which reduces energy expenditure
and facilitates connued weight gain (Goodchild and Schwitzer
2008). Zoo lemurs exhibit very dierent behaviours to their wild
counterparts. For example, blue-eyed black lemurs (Eulemur
avifrons) were found to spend 12–14% of their me foraging
and feeding in capvity, compared to 32% in the wild (Schwitzer
et al. 2006). Moreover, diets in capvity, even for ostensibly
folivorous species, are oen dominated by fruit (Plowman
2013). Commercially produced fruit is substanally dierent
from that found in the wild, being higher in sugar content and
metabolisable energy, and lower in bre, protein, minerals and
vitamins (Goodchild and Schwitzer 2008; Solman 2009; Plowman
2013). The nutrional prole and physiological impact of a diet in
capvity may, therefore, be very dierent to that of the diet in the
wild (Fidge and Plowman 2009). In the wild, rued lemurs weigh
about 3.3 kg (females) to 3.6 kg (males; Vasey 2003). Compared
to their wild counterparts, animals in capvity can be prone to
obesity, with some European zoo populaons averaging as much
as 4.3 kg (Schwitzer and Kaumanns 2001).
Iron storage disease (ISD), or hemochromatosis, is another diet-
related complicaon for zoo lemurs. While iron is an essenal
trace element, appropriate dietary quanes are unknown for
the majority of species (Beard 2001). Threshold levels, that is, the
Table 1. The availability of plants in the enclosures of ve populaons
of rued lemurs (Varecia spp.) housed in UK zoological collecons. Year-
round=growing in the outdoor enclosure; seasonal=provisioned when
available. No browse was made available to animals in Z2.
Species Availability Z1 Z3 Z4 Z5 Z6
Bamboo Phyllostachus sp.Year-round 
Bramble Rubus frucosus Year-round 
Buddleia Buddleia davidii Year-round 
Chasun
palm
Trachycarpus
fortunei
Year-round 
European
beech
Fagussylvaca Year-round
Grasses Poaceae sp. Year-round     
Hazel Corylus
avellana
Seasonal 
Horse
chestnut
Aesculus
hippocastanum
Year-round 
Palm
bamboo
Sasa palmaa Year-round 
Red-barked
dogwood
Cornus alba Year-round 
Silver poplar Populus alba Seasonal 
Sycamore
maple
Acer
pseudoplatanus
Year-round 
Willow Salix sp. Seasonal  

Journal of Zoo and Aquarium Research 6(2) 2018 43
Rued lemur diets in UK zoos
Z1 Z2 Z3
Food Type Cat Weight (g) ME (Kcal) CH (g) Sugar (g) Fe (mg) Weight (g) ME (Kcal) CH (g) Sugar (g) Fe (mg) Weight (g) ME (Kcal) CH (g) Sugar (g) Fe (mg)
Pomegranate F 8.67 9.22 2.13 2.13 0.13
Strawberry F 0.88 3.13 0.64 0.64 0.03
Tomato F 0.91 2.36 0.51 0.51 0.04 1.48 3.84 0.82 0.82 0.07
Broccoli V 4.48 12.91 1.21 0.72 0.40
Carrot V 12.01 34.32 7.35 6.86 0.34 1.20 3.43 0.73 0.69 0.03 5.12 14.62 3.13 2.92 0.14
Celery V 2.12 1.32 0.17 0.17 0.08
Chicory V 2.98 5.76 1.47 0.37 0.21
Courgee V
Cucumber V 0.89 3.58 0.31 0.31 0.08
Leuce V2.58 7.27 0.92 0.92 0.09 0.81 2.28 0.29 0.29 0.03
Parsnip V 1.64 5.07 0.99 0.45 0.05 4.95 15.31 2.99 1.36 0.14
Peas V
Pepper V 0.52 1.61 0.33 0.32 0.03
Potato V7.54 33.78 8.08 0.37 0.13 3.55 15.92 3.81 0.17 0.06
Snap peas V 2.22 7.28 1.07 0.79 0.17
Sweet potato V 2.42 7.36 1.80 0.48 0.06
Sweetcorn V55.32 36.08 4.81 1.20 0.41
Bread O 71.61 13.86 0.92 0.79
Egg O 2.73
Low Fe nuts O 55.57 1.23 0.61 0.06
Mashed potato O 54.54 6.38 2.83 0.50 12.86
Peanut O13.40 80.57 1.79 0.89 0.36
Trio Munch1O 19.40
Total 181.41 400.54 92.05 68.25 2.08 245.19 516.25 116.08 100.30 3.10 332.18 581.23 106.69 92.85 3.35
1 Special Diet Services (SDS), UK.
Table 2a (connued). Weight of food (g, DM), metabolisable energy (ME; Kcal), carbohydrates (CH; g), sugar (g) and iron (Fe; mg) provided per individual per day for rued lemurs at three zoological instuons (Z1–Z3) in the UK in
2008. Data are sorted by category (Cat: F=fruit; V=vegetable; O=other) and alphabecally by food type.

Journal of Zoo and Aquarium Research 6(2) 201844
Caravaggi et al.
Z4 Z5 Z6
Food Type Cat Weight (g) ME (Kcal) CH (g) Sugar (g) Fe (mg) Weight (g) ME (Kcal) CH (g) Sugar (g) Fe (mg) Weight (g) ME (Kcal) CH (g) Sugar (g) Fe (mg)
Apple F 19.80 51.00 11.60 11.60 0.09 12.75 32.83 7.47 7.47 0.06 28.71 73.95 16.82 16.82 0.13
Banana F 34.58 53.16 13.32 11.88 0.18 15.48 23.79 5.96 5.32 0.08 105.40 162.00 40.60 36.20 0.54
Blackberries F 0.38 0.63 0.13 0.13 0.02
Dates F 13.76 43.40 10.96 10.96 0.11
Grapes F 7.39 24.38 6.04 6.04 0.09 0.74 2.44 0.60 0.60 0.01
Kiwi F 4.87 7.35 1.59 1.56 0.05
Melon F 9.88 6.00 1.38 1.38 0.06 39.50 24.00 5.50 5.50 0.23
Nectarine F 2.74 5.25 1.18 1.18 0.05
Orange F 7.96 22.05 5.02 5.02 0.07
Peach F2.00 3.30 0.76 0.76 0.04
Pear F23.81 37.95 9.75 9.75 0.12 2.42 3.85 0.99 0.99 0.01 15.53 24.75 6.36 6.36 0.08
Table 2b. Weight of food (g, DM), metabolisable energy (ME; Kcal), carbohydrates (CH; g), sugar (g) and iron (Fe; mg) provided per individual per day for rued lemurs at three zoological instuons (Z4–Z6) in the UK in 2008. Data
are sorted by category (Cat: F=fruit; V=vegetable; O=other) and alphabecally by food type.
level(s) above which iron may have a toxic eect, vary between
organisms and species. Lemurs have been observed to accumulate
excess iron when fed on diets containing less than 300 mg/kg dry
maer (DM) (Spelman et al. 1989). Excessive iron accumulaon
can lead to toxic eects such as lesions in the liver, hepatocellular
adenoma, carcinoma, necrosis and death (Crawshaw et al. 1995;
Andrews et al. 2005; Olsen et al. 2006). ISD has been described in
several lemur species, including rued, ring-tailed (Lemur caa),
black (Eulemur macaco), brown (E. fulvus) and crowned lemurs (E.
coronatus) and Coquerel’s sifaka (Propithecus coquereli; Spelman
et al. 1989; Wood et al. 2003; Glenn et al. 2006; Clauss and Paglia
2012). While it has been suggested that the incidence of excessive
iron accumulaon in lemurs has been exaggerated (Glenn et al.
2006), ISD remains a concern for zoological instuons housing
these species.
To improve husbandry, Donadeo et al. (2016) highlighted a clear
need for addional data on the nutrional composion of lemur
diets so that species-specic guidelines can be developed. Here,
this knowledge gap is addressed by collang and describing the
historical diets of several populaons of black-and-white rued
lemurs (Varecia variegata, Gray 1863) housed in zoos in the UK,
and invesgang dierences in nutrional content with relevance
and reference to the problems of obesity and ISD.
Methods
Data collecon
Dietary data were collected from six UK zoological instuons
(abbreviated as Z1–Z6 from here on) during July and August
2008 with the support of the Brish and Irish Associaon of Zoos
and Aquaria (BIAZA). Zoos were chosen to maximise populaon
sample size, and with consideraon for the project’s nancial and
temporal constraints. Each instuon provided four sequenal
days of data, which consisted of provisioned weights of individual
food types (e.g. apples, carrots) and which were assumed to be
representave of the core diet provided throughout the year.
Normal husbandry procedures were maintained throughout the
study period; no experimental changes were made to the normal
feeding rounes. Animals in all instuons were kept in indoor
enclosures overnight and were allowed access to larger outdoor
enclosures during the day me. Food was provided in both indoor
and outdoor areas; keepers at all instuons reported that all
food items were consumed, with lile waste. Outdoor enclosures
contained trees, branches, climbing frames, ropes and/or other
objects to varying degrees, thus facilitang the species’ arboreal
habits. Although browse may be included in lemur diets at some
instuons and several enclosures contained living vegetaon
(Table 1), keepers reported that the animals in the focal collecons
rarely consumed foliage.
Nutrional composion calculaons
Nutrional data (metabolisable energy [ME; kcal/100g];
carbohydrates [CH; g/100g]; sugar [g/100g]; iron [Fe; mg/100g];
all in dry maer) were extracted from McCance and Widdowson’s
'composion of foods integrated dataset' (Finglas et al. 2015).
Nutrional informaon for supplemental foods produced by
Mazuri, Kasper Faunafood, and SDS were obtained from relevant
product informaon sheets. Non-structural (i.e. readily digesble)
carbohydrates were esmated as: 100% minus crude fat, crude
protein, Neutral Detergent Fibre (NDF) and ash (all in % dry
maer). It was not possible to quanfy the proporon of each
food item consumed by individual animals. Furthermore, Z3
maintained a polytypic collecon consisng of eight rued lemurs,
two red lemurs (Eulemur rufus) and three red-bellied lemurs (E.
rubriventer), and each instuon housed a dierent number of
individuals (n=2–13). Mean food weight and, hence, nutrient

Journal of Zoo and Aquarium Research 6(2) 2018 45
Rued lemur diets in UK zoos
Z4 Z5 Z6
Food Type Cat Weight (g) ME (Kcal) CH (g) Sugar (g) Fe (mg) Weight (g) ME (Kcal) CH (g) Sugar (g) Fe (mg) Weight (g) ME (Kcal) CH (g) Sugar (g) Fe (mg)
Plum F2.11 3.60 0.88 0.88 0.04
Strawberry F 2.63 9.38 1.91 1.91 0.08
Sultanas F 3.71 12.03 3.04 3.04 0.10
Tomato F 3.58 9.28 1.99 1.99 0.16
Aubergine V 0.98 2.06 0.30 0.28 0.04
Broccoli V 0.74 2.13 0.20 0.12 0.07
Cabbage V 2.34 5.69 0.96 0.96 0.10
Carrot V 11.20 32.00 6.85 6.40 0.32 1.40 4.00 0.86 0.80 0.04 11.20 32.00 6.85 6.40 0.32
Celery V 6.72 4.20 0.54 0.54 0.24 1.19 0.74 0.10 0.10 0.04 2.52 1.58 0.20 0.20 0.09
Chicory V
Courgee V2.05 5.85 0.59 0.55 0.26 1.73 4.95 0.50 0.47 0.22
Cucumber V 1.30 5.21 0.45 0.45 0.11
Leek V 2.07 4.95 0.65 0.50 0.25
Leuce V1.94 5.47 0.70 0.70 0.06 1.46 4.13 0.53 0.53 0.05
Peas V 1.43 4.67 0.64 0.13 0.16
Pepper V 1.33 4.13 0.83 0.81 0.08 4.22 13.06 2.64 2.55 0.26
Sweetcorn V6.90 4.50 0.60 0.15 0.05 12.08 7.88 1.05 0.26 0.09
Bread O 2.84 5.56 1.08 0.07 0.06 113.38 21.95 1.46 1.25 124.78 24.15 1.61 1.38
Egg O 28.60 0.39
Leaf-eater pellet1O47.48 14.03 19.31 0.24
Low Fe nuts O 7.54
Panda cake1O 11.25 4.35 5.60 0.04
Primate pellet2O0.28 3.30 4.12 1.17 0.01
SA373O0.00 0.00 27.00
Trio Munch4O 1.51 30.72 33.81 8.05 11.47 1.69 0.09
Total 151.01 290.29 63.07 53.82 2.33 151.08 259.61 72.39 27.51 2.87 294.80 537.67 132.05 94.85 3.48
1Mazuri Zoo Foods, Witham, Essex, UK; 2Kasper Faunafood, Woerden, NL; 3Intervet, Worksop, UK; 4Special Diet Services (SDS), UK.
Table 2b (connued). Weight of food (g, DM), metabolisable energy (ME; Kcal), carbohydrates (CH; g), sugar (g) and iron (Fe; mg) provided per individual per day for rued lemurs at three zoological instuons (Z4–Z6) in the UK in
2008. Data are sorted by category (Cat: F=fruit; V=vegetable; O=other) and alphabecally by food type.

Journal of Zoo and Aquarium Research 6(2) 201846
Caravaggi et al.
content, were calculated per lemur, per day, at each instuon
(hereaer referred to as ‘per individual’). Lemur weights were
obtained post hoc from the zoo aquarium animal management
soware, ZIMS. Weights were only available for three instuons;
with the excepon of Z4, data did not represent all animals in the
collecon: Z1 (n=4 of 5); Z3 (n=2 of 14); Z4 (n=4 of 4). Weights for
Z3 reported herein refer to rued lemurs only.
Stascal analyses
Inial analyses revealed that residuals from one-way ANOVAs
were not normally distributed and variances were not evenly
distributed. Therefore, non-parametric Kruskal–Wallace tests
were used with post-hoc Dunn tests to invesgate signicant
dierences, across collecons, of the following: mean weight
(DM) of provisioned diets per individual; ME content; CH content;
sugar content; and Fe. Stascal analyses were carried out using R
version 3.4.1 (R Core Team 2018).
Results
A total of 44 dierent food items were provided to rued lemurs
over the course of the study (Table 2). Of these, only three items
were given by all instuons on all days. Fruits accounted for
the greatest proporon of the diet in ve of the six instuons
(51%–78%); vegetables accounted for 44% in Z4 and 47% in Z5.
The quanty (weight, DM) of food provided per individual varied
signicantly between instuons (χ2=24.81, df=5, P<0.0001;
Table 3). This variaon was largely accounted for by observed
dierences in the amount of fruit provided by each instuon
(χ2=15.62, df=5, P=0.008). The amount of vegetaon provided to
each populaon also varied signicantly (χ2=13.05, df=5, P=0.023).
Post-hoc tests described inter-instuonal dierences between
several collecons, for all three metrics (Table 3). There were no
signicant dierences in provisioned weights of other food items.
There were signicant dierences in ME content between
instuons (χ2=14.48, df=5, P=0.013), for example, Z2 relave to
Z5 (P=0.011), Z3 relave to Z4 (P=0.045) and Z5 (P=0.009; Table
4). Daily individual ME ranged from 189.52 (±27.17; Z5) to 547.66
(±5.76; Z3; Table 2) kcal/d. Fruit was the primary source (>60%) of
ME in four instuons; other dietary items accounted for 32% of
ME in Z5, with fruit accounng for 43%. Vegetables accounted for
between 9%–25% of ME (Figure 1).
The amount of CH provisioned per individual diered
signicantly between instuons (χ2=16.22, df=5, P=0.006). Post-
hoc tests showed that Z6 (118.42±18.39 g/d) diered signicantly
from Z5 (67.03±18.32 g/d; P=0.013; Table 4). Fruit accounted for
between 64%–89% of CH in Z1–Z4 and 75% in Z6, but only 29%
in Z5 where other dietary items accounted for 60%. Vegetables
accounted for between 6%–18% of CH (Figure 1).
There was a signicant dierence in the amount of dietary
sugars provided per individual, between instuons (χ2=21.33,
df=5, P<0.0001), for example, Z2 (97.72±19.12 g/d) relave to
Z5 (27.17±6.85 g/d; P=0.012), and Z3 (93.38±2.61 g/d) to Z5
Figure 1. Percentage of (a) metabolisable energy (ME; Kcal), (b)
carbohydrates (CH; g), (c) sugar (g), and (d) iron (Fe; mg) accounted for
by fruit, vegetables and other food items over 4 days in the diets of rued
lemurs in six UK zoological collecons (Z1–Z6).
0
20
40
60
80
100
Participating institu tion
Z1 Z2 Z3 Z4 Z5 Z6
Percentage of d iet
0
20
40
60
80
100
b)
a)
c)
Fruit
Vegetables
Other items
Z1 Z2 Z3 Z4 Z5 Z6
d)
Instuon n Weight Fruit Vegetable Other
Z1 5181.41 ±28.83 139.88 ± 25.49 22.13 ± 7.46 19.40 ± 12.97
Z2 8 245.19 ± 47.06 223.50 ± 42.41A18.96 ± 5.97a2.73 ± 5.45a
Z3 13 303.20 ± 58.25A193.55 ± 75.10 52.46 ± 25.23A17.50 ± 15.16
Z4 4 151.01 ± 22.62a102.94 ± 6.87 32.20 ± 12.35 15.87 ± 29.43
Z5 2151.08 ± 44.76a38.21 ± 3.68a27.14 ± 22.54 85.74 ± 23.97A
Z6 5 294.80 ± 14.72A218.54 ± 39.14A15.45 ± 10.55a60.81 ± 25.57A
Table 3. Weight of all provisioned food, fruit, vegetables and other dietary items (g; dry maer) provided to rued lemurs at six zoological collecons (Z1–
Z6) in the UK across 4 days in 2008. Values are given per individual per day; n=total number of animals in the collecon. Uppercase leers indicate post-hoc
Tukey test results, where A>a, B>b, C>c, at P≤0.05.

Journal of Zoo and Aquarium Research 6(2) 2018 47
Rued lemur diets in UK zoos
(P=0.029) and Z6 (34.78±7.74 g /d) relave to Z5 (P=0.018; Table
4). Fruit accounted for between 66%–96% of dietary sugar.
Vegetables contributed 18% in Z4 and 22% in Z5 (Figure 1).
Animals at Z1 weighed an average of 3.77 kg (±0.47 kg; n=4),
those at Z4 weighed an average of 3.48 kg (±0.45 kg), while
animals at Z3 weighed an average of 4.45 kg (±0.28 kg). Using a
threshold value of 4.274 kg to determine obesity (sensu Terranova
and Coman 1997), animals in Z3 were considered obese.
Calculated individual Fe did not generally dier signicantly
across instuons. However, post-hoc analyses showed that Z3
(3.49±0.14 mg/d) diered signicantly from Z5 (1.78±0.31 g/d;
Table 4). Fruit accounted for 18%–63% of dietary iron. Vegetables
accounted for 27%–58%, and other dietary items for 7%–24%
(Figure 1). Two instuons provided veterinary post-mortem
reports describing excessive accumulaon of Fe and the onset
or presence of ISD. Z3 provided three reports, the oldest from
2002, the most recent from 2007, and Z4 provided one report
from 2006. No reports specically excluded ISD and no veterinary
reports were provided by the other instuons.
Discussion
Few studies have invesgated the diet of rued lemurs in capvity
(but see: White 1989; Morland 1991; Rigamon 1993; Bri 2000;
Vasey 2003; Donadeo et al. 2016). The purpose of the present
study was to quanfy the amount of food provisioned to rued
lemurs, and their basic nutrional proles (i.e. metabolisable
energy, carbohydrates, sugars and iron). Quancaon of
these fundamental parameters is essenal in informing the
development of appropriate species-specic diets, parcularly
given the vulnerability of capve lemurs to obesity (Schwitzer
and Kaumanns 2001). As is typical for studies across several
collecons, there was signicant variaon between parcipang
instuons in all aspects. This, combined with the observaon of
obesity in one instuon and historical records of pathologically
relevant stored iron from two instuons, highlights the lack of
consistency and species-specic knowledge employed when
formulang dietary guidelines for rued lemurs.
The data presented herein were derived from an undergraduate
research project that sought to invesgate dietary and retained
iron via non-invasive faecal analyses. Unsuccessful aempts
were made to collect historical body weight and contemporary
dietary data from parcipang instuons in 2015–2016 to
enable invesgaon of changes in both aspects between 2008
and the present day. The inferenal potenal of the present
study is, therefore, limited. Furthermore, it was not possible to
quanfy the food intake of individual animals, hence the use of
average values for food as-fed throughout. It is highly likely that
the amount of food consumed varied considerably between
individuals, as social hierarchy is known to impact food intake
in some lemur species (e.g. Lemur caa; Rasamimanana 1999).
Rued lemurs exhibit a dynamic social structure (Vasey 2006),
which adds further complexity in a social provisioning seng
and would require signicant manipulaon to quanfy individual
intake. Furthermore, individuals may vary in their requirements
for, and/or ability to ulise, nutrients such as carbohydrates and
sugars. Despite these limitaons, the data and results represent
a valuable addion to the literature, clearly demonstrang that
zoo diets for rued lemurs are highly variable, and potenally
contribute to illness and mortality of individual animals. The
study also facilitates informaon exchange across instuons and
provides base data for future meta-analyses.
Rued lemurs may be suscepble to overfeeding in capvity
where there is a lack of seasonal variaon in climate and food
supply (Schwitzer and Kaumanns 2001). In a recent study,
Donadeo et al. (2016) found that the diet of rued lemurs
in the US was enrely unlike that of their wild counterparts,
also with lile consistency between instuons. Certainly,
there is cause for concern given that levels of metabolisable
energy at ve parcipang instuons exceeded the suggested
maintenance energy requirement of 249.3 kcal/d, as suggested
by Schwitzer and Kaumanns (2001). However, the Naonal
Research Council (2003) provides lile in the way of guidance
with regards to the composion of rued lemur diets, with almost
all recommendaons being broadly applied to all nonhuman
primates. Indeed, most capve primate diets are comprised of at
least 50% fruit and vegetables (Kaumanns et al. 2000); the lemur
diets described herein were no excepon, and almost all were
dominated by fruits. Commercially grown fruit oen contains a
substanal amount of non-structural carbohydrates (e.g. sugar),
high levels of which are known to cause health problems in capve
primates (e.g. Kuhar et al. 2013). This contrasts with fruits found
Instuon nME (Kcal) CH (g) Sugar (g) Fe (mg)
Z1 5337.78 ± 21.75 90.81 ± 12.05 69.18 ± 13.03 1.38 ± 0.005
Z2 8 519.22 ± 71.12A111.82 ± 29.01 97.72 ± 19.12A3.28 ±1.01
Z3 13 547.66 ± 5.76B108.03 ±2.18 93.38 ± 2.61B3.49 ± 0.14A
Z4 4 300.34 ± 74.45b71.53 ± 25.47 54.50 ± 6.41a2.37 ±0.73
Z5 2189.52 ± 27.17a,b 67.03 ± 18.32a28.17 ± 6.85a,b 1.78 ±0.31a
Z6 5 420.57 ± 33.19 118.42 ± 18.39A94.78 ± 7.74B2.21 ±0.27
Table 4. Metabolisable energy (ME; Kcal), carbohydrates (CH; g), sugar (g) and iron (Fe; mg) contained in the diets of rued lemurs at six zoological
collecons (Z1–Z6) in the UK across 4 days in 2008. Values are given per individual per day; n=total number of animals in the collecon. Uppercase leers
indicate post-hoc Dunn test results, where A>a, B>b, C>c at P≤0.05.

Journal of Zoo and Aquarium Research 6(2) 201848
Caravaggi et al.
in the wild diet, which have lower energy content (Goodchild
and Schwitzer 2008). Fruits provided the greatest proporon of
metabolisable energy, carbohydrates and sugars in the current
study. It would be reasonable, therefore, to omit food items
with high sugar content from rued lemur diets in capvity, e.g.
sultanas (69.4 g/100 g), dates (31.3 g/100 g), banana (18.1 g/100
g) and mango (13.8 g/100 g). Reducing the availability of sugar
can have addional welfare benets. For example, an average 25%
reducon in non-structural carbohydrates and an increase in bre
resulted in decreased aggression and increased foraging across
four lemur species, including rued lemur (Bri et al. 2015). The
only zoo with obese lemurs was Z3, where the provisioned diet
contained the most metabolisable energy (547.66±5.76 kcal/day)
and the second-most sugar (93.38±2.61 g/day) of all the zoos in the
study. However, lemurs at Z3 were not fed items with parcularly
high sugar content. It is likely, therefore, that the quanty of food
provided (332.18±7.16 g/day, the highest in the study) was the
main contributory factor.
Spelman and colleagues (1989) suggested that the suscepbility
of lemurs to ISD is indicave of specic adaptaons to a wild
diet high in iron-chelang agents. Diets in capvity are low in
secondary plant polyphenols (such as tannins) and high in ascorbic
acid, which may be the main cause of excessive iron accumulaon
(Gonzalez et al. 1984; Spelman et al. 1989), as absorpon is
inhibited by the former and enhanced by the laer (Yip and
Dallman 1996). Indeed, the diets of many free-ranging lemur
species contain high levels of tannins (Jolly 1966; Taersall 1982).
Conversely, the diets of zoo animals oen contain low levels of
tannins, a situaon which may be problemac for those species
that have evolved to rely upon them (Clauss 2003). Diets high in
iron, and without the iron-chelang components of diets in the
wild, may be parcularly problemac for monogastric browsers
such as rued lemurs. As such, adjustments to reduce dietary iron
for the species in capvity are likely to be benecial (Wood et al.
2003). The observaons of iron storage-related issues from two
instuons add to the exisng evidence regarding ISD in capve
lemurs. Notably, no necropsy reports stang the absence of ISD-
related ndings were communicated during our study. It should be
noted that iron is highly variable in its abundance and availability
(Henry and Miller 1995) and the dietary data presented in
this study represent a temporally-limited sample. Moreover,
mortalies occurred at least 1 year before this study, and zoo
diets are subject to ongoing review and manipulaon. Indeed, Z3
began a series of dietary trials focused on lemurs several months
aer the conclusion of this study. It is therefore not possible to
relate iron-related mortality directly to the diets described herein.
Nevertheless, given the potenal risks of diets rich in iron and
taking the reported mortalies and diets into account, foods with
high iron content, such as peas (2.8 mg/100 g), egg (2.4 mg/100
g), sultanas (2.2 mg/100 g) and broccoli (1.1 mg/100 g) should be
avoided and dietary iron should not exceed 2 mg per individual
per day.
Dietary adjustments are oen necessary to deal with obesity
and ISD. Any such changes should be responsive to the issue
at hand but should also consider the composion of the diet
and other inuencing factors (e.g. seasonality, weight, me
spent foraging) in the wild. Dietary changes can also have other
benecial eects, beyond migang disease. For example, animals
may respond more favourably to naturalisc diets, resulng in
welfare benets (e.g. Cabana and Plowman 2014). The diets of
capve populaons are, however, limited by resources available
to the host instuon(s). Nevertheless, instuons should strive
to provide lemurs with as close an approximaon of the wild diet,
including accounng for feeding strategy and seasonal variability,
as possible. Given the degree of variaon in diet, and the evidence
of rued lemur obesity and excess iron accumulaon presented
herein, the development of species-specic diets is an important
aim. Reformulaon of diets to reduce the relave abundance of
fruits, parcularly those high in metabolisable energy and non-
structural carbohydrates, and the removal of food items rich in
iron may prove eecve in decreasing the prevalence of obesity
and ISD in the capve populaon.
Acknowledgements
We thank BIAZA for their endorsement of the original study, and,
parcularly, all parcipang zoological instuons and keepers for
their support and for providing dietary data. We are parcularly
grateful to Vicky Mel (JZAR Managing Editor), Marcus Clauss
and one anonymous reviewer for their insighul feedback, which
greatly improved this manuscript.
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