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OPEN ACCESS JZAR Research arcle
Journal of Zoo and Aquarium Research 1(2) 2013 73
Research arcle
Diet review and change for monkeys at Paignton Zoo Environmental
Park
Amy Plowman
Whitley Wildlife Conservaon Trust, Paignton Zoo Environmental Park, Totnes Road, Paignton, Devon TQ4 7EU, UK
Correspondence: amy.plowman@paigntonzoo.org.uk
Keywords:
fruit, dental health, obesity, primates,
vegetables
Arcle history:
Received: 6 December 2012
Accepted: 1 September 2013
Published online: 31 October 2013
Abstract
Between 2003 and 2010 the diets of all medium-sized monkeys at Paignton Zoo Environmental Park
were subjected to a connual process of review and improvement. This resulted in the removal of
all fruit, bread, eggs and seeds from the diets and changes to commercial products used for some
species. All species are now provided with similar diets consisng of a suitable commercial pelleted
feed, a variety of fresh vegetables and small amounts of dog biscuits and cooked brown rice to provide
opportunies for scaer feeding. Compared with the 2003 diets the 2010 diets have higher levels
of protein (3–47% increase) and bre (36–77% more NDF) and lower levels of readily digesble
carbohydrate (6–14% decrease). Resultant health benets have been improved dental health and
weight loss in some previously overweight individuals. In addion, the 2010 diets are also considerably
less expensive than the 2003 diets resulng in an esmated annual cost saving of £9717 based on
current prices and animals held.
Introducon
Although primates are tradionally regarded as relavely
easy to feed, there is growing recognion that inappropriate
diets contribute to several common health problems seen in
capve omnivorous primates (e.g. see Oedal and Allen 1996;
Schwitzer et al. 2009). Most common among these is obesity
(e.g. Schwitzer and Kaumanns 2001; Videan et al. 2007), which
is associated with many other illnesses such as heart disease,
cancer, diabetes and reproducve problems (Register and
Clarkson 2009).
Obesity can have a number of contributory factors,
including low acvity levels in capvity, but is largely due to
capve diets that are high in energy without the foraging and
digesve costs associated with the species’ natural nutrive
strategies (Schwitzer at al. 2009). This is parcularly common
in omnivorous primates, which are oen fed a wide variety of
food items, including fruit, vegetables, insects and vertebrate
prey, reecng assumpons about their food selecon in the
wild. Tradionally, most tend to be regarded as fruit eaters, at
least to some extent, and are therefore fed fruit in capvity.
This is even the case for some highly folivorous species.
Unfortunately, fruit culvated for human consumpon is very
dierent in terms of nutrient composion to leaves and wild
fruits eaten by free-living primates (e.g. Oedal and Allen
1996). Selecve breeding and modern culvaon methods
produce fruit that is high in sugars and low in bre, and
therefore high in readily digesble energy. Culvated fruit also
tends to be lower in protein, minerals and vitamins than most
foodstus consumed by primates in the wild (see Schwitzer et
al. 2009 for an excellent review). In addion to contribung
to obesity, capve primate diets containing large amounts of
culvated fruit may cause gastrointesnal problems due to low
bre content (Edwards and Ullrey 1999) and poor dental health
due to high sugar levels (Johnson-Delaney 2008).
Between 2003 and 2010 we underwent a connual process of
review and improvement of diets fed to medium-sized monkeys
at Paignton Zoo Environmental Park. These were iniated as a
result of a number of dierent issues of concern that could be
related to diet, although most of the individuals were generally
healthy. The rst of these, and the main trigger for diet review,
was the poor dental health of several of the Abyssinian colobus
(Colobus guereza) and king colobus (C. polykomos) monkeys.
Following reviews of these diets, increased awareness of
potenal nutrional problems, parcularly obesity, smulated
keepers on the secon to insgate similar reviews of the diets
for the rest of the monkeys in their care. Addional species
present in this secon of the zoo (echidna, pygmy slow loris,
Journal of Zoo and Aquarium Research 1(2) 2013 74
Plowman
African porcupine, meerkat, sloth and red panda) were also
subject to similar diet reviews over the same period but are not
discussed in this paper.
Methods
Study animals
All animals studied were housed at Paignton Zoo Environmental
Park, Devon, UK, and remained in their usual enclosures with
normal husbandry throughout the study period. Subjects included
all medium-sized monkey species included in the “Monkey
Heights” secon (Table 1).
Diet review process
Starng in 2003 we conducted collaborave, mul-department,
nutrion meengs involving keepers on the Monkey Heights
secon, veterinary and research sta approximately every three
or four months. Issues of concern possibly related to diets were
raised by keepers, discussed and if felt necessary invesgated
further by the research team. A paern very quickly emerged
that the rst step in any review was to assess exactly what the
animals were currently eang. Dietary intake studies were inially
conducted by researchers but all keepers on the secon were soon
trained in the method and then conducted the trials themselves.
Dietary intake
For all species the daily food intake was measured for at least ve
days and up to three blocks of ve days over three weeks. All food
items provided to the monkeys were prepared in the normal way
and weighed immediately before presentaon. A small amount
of the same food items was placed in a desiccaon dish at the
same me to adjust for water loss in the leovers. Food was
presented as normal, usually in three feeds per day. Any uneaten
food remaining the next day was collected and weighed along
with food in the desiccaon dish. Weight of remaining food was
adjusted according to the desiccaon rate and deducted from
Table 1. Monkey species included in diet reviews at Paignton Zoo Environmental Park between 2003 and 2010.
Species Diet review period Group size and structure Main concerns
Abyssinian colobus
Colobus guereza
March 2003–July 2008 Inially 2 family groups. Gradually phased
out; 1 group of 2 males by 2010
Many individuals had serious dental problems
including tooth decay and gingivis
King colobus
Colobus polykomos
March 2003–July 2008 Single male, mul-female plus young Dental problems as above, but not so severe
Diana monkey
Cercopithecus diana
April–September 2007 Adult pair plus young Adult male overweight
Hamadrayas baboon
Papio hamadrayas
July 2007 Large mul-male, mul-female group with
many young (>50 individuals)
Cost of the diet for such a large group
Variegated spider monkey
Ateles belzebuth hybridus
September 2007–July 2010 Adult pair, arrived at zoo 2007 Frequent loose faeces and diarrhoea
Sulawesi crested black
macaque Macaca nigra
September 2007–July 2010 Group of mixed sex and age, 1 dominant
adult male (10–15 individuals)
Frequent loose faeces and diarrhoea. Some
overweight individuals
Table 2. Weight of food (g, as fed) provided per individual per day for six species of monkey at Paignton Zoo Environmental Park prior to (2003) and
following diet reviews (2010).
Food type
Abyssinian colobus King colobus Diana monkey
Hamadryas
baboon Spider monkey
Sulawesi crested
black macaque
2003 2010 2003 2010 2003 2010 2003 2010 2007 2010 2003 2010
Primate pellet1
Trio Munch1
Leaf eater primate pellet1
Terrier biscuit2
Brown rice
Bread
Seed mix3
Dried fruit mix3
Egg
24
50
30
5
95
3
24
16
54
30
50
30
6
70
58
24
16
54
11
25
30
10
40
10
10
160
33
40
30
11
170
40
20
56
12
20
20
2
36
30
16
25
35
30
38
4
9
70
30
35
Fruit (apple, banana etc) 320 285 341 263 290 374
Green leafy veg
Starchy root veg
Other vegetables
293
82
23
450
363
363
402
91
50
450
363
363
45
29
52
475
75
100
71
54
51
156
156
156
118
106
87
325
325
325
49
138
55
338
150
394
1Mazuri Zoo Foods, Witham, Essex, UK.
2Winalot mixer, Purina, Horley, Surrey, UK.
3Seed mix was 5% peanuts, 95% sunower seed by weight; dried fruit mix was approximately equal weights of raisins and sultanas.
Journal of Zoo and Aquarium Research 1(2) 2013 75
Diet reviews for monkeys
the provisioned weight to calculate weight of each food type
consumed. Data were collected on a group basis and divided by
the number of individuals to give a mean intake per individual.
Following dietary changes food intake was recalculated as above.
Nutrient analysis and composion
To minimise me and cost, standard nutrient values given in
Zootrion (Zootrion™, version 2.6) were used for most food
items. Where these were not available food samples were
subjected to laboratory analysis by an external laboratory
(Eurons, Wolverhampton). Mean daily intake of each food type
per individual was entered into Zootrion and a full diet analysis
performed. Readily digesble carbohydrate (sugars and starch)
was esmated by calculaon: 100% dry maer minus crude
protein, crude fat, NDF and ash.
Recommended dietary changes
Following nutrient analysis of exisng diets, some changes were
recommended based on available informaon in the literature for
the species, any issues in the group and recommended nutrient
requirements (NRC 2003). Dietary changes evolved over a period
of years starng with the removal of all fruit, then bread and eggs
and lastly sunower seeds. For some species the commercial
pellets used were changed to increase bre content. Fruit and
dried fruit were replaced with vegetables. Vegetables were
divided into three types: Group A, ‘green leafy’, such as cabbage,
leuce, spinach; Group B, ‘other’, such as celery, cucumber, peas,
peppers, fennel; and Group C, ‘starchy root’, such as carrots,
beetroot, swede, sweet potato. To make diet preparaon easier
the total amount of each vegetable group was stated rather than
each parcular type of vegetable.
Results
Dietary intake
Prior to the review process, most of the monkeys were fed a
similar diet of commercial pellets, fruit and vegetables, a seed
mix (peanuts and sunower seed), a dried fruit mix (raisins and
sultanas), bread and eggs (Table 2). Very lile food was le uneaten
by any species, so the amounts of provisioned food are similar to
those actually consumed in most cases. During the diet review
process all fruit and dried fruit was removed from the diets. Bread
was included in the original diets because it had tradionally been
donated free by local supermarkets when nearing its sell-by date.
However, this had stopped and it was now being purchased at
a much higher cost than providing similar grain-based nutrients
via pelleted feeds; bread was therefore removed. The seed and
dried fruit mixes were considered important to provide a hard-to-
nd scaer feed and promote foraging behaviour but are high in
energy and sugar. These were replaced with alternave dry feeds;
terrier biscuit and cooked brown rice. Most species were switched
from primate pellet to leaf eater primate pellet to further increase
bre levels.
Nutrient composion
By 2010 the diets of all six species were higher in protein, with
increases of 3–47% compared with their 2003 diet (Table 3). Fibre
levels were also higher, with NDF increasing by 36–77%. Esmated
levels of readily digesble carbohydrate decreased by 6–14%. With
the excepon of the two colobus species, fat levels also decreased
substanally, largely due to the removal of sunower seeds from
the diets.
Dental health
Following dietary adjustments the frequency of dental treatment
required decreased rapidly (Fig. 1). Between 1998 and 2003 there
were 17 instances of treatment for dental problems including gum
disease, gingivis, tartar build up, the removal of several teeth
and even one euthanasia due to extremely poor dental condion.
These involved 12 dierent individual monkeys, all but one of which
were Abyssinian colobus (Fig. 1). Following the inial changes to
the diet to reduce sugar levels, the frequency of dental treatment
Table 3. Nutrient composion of the diets as consumed by six species of monkey at Paignton Zoo Environmental Park prior to (2003) and following diet
reviews (2010). Highly digesble carbohydrate esmated by calculaon (Dry maer – protein – fat – NDF – ash). ME = metabolisable energy.
Nutrient
Abyssinian
colobus
King
colobus
Diana
monkey
Hamadryas
baboon
Spider
monkey
Sulawesi crested
black macaque
2003 2010 2003 2010 2003 2010 2003 2010 2007 2010 2003 2010
Dry maer (g)
Crude protein (%)
Crude fat (%)
NDF (%)
ADF (%)
Ca (%)
P (%)
Highly digesble carbohydrate (%)
ME (kJ per day)
283
11.7
3.9
12.6
8.1
0.44
0.39
68.1
3765
296
16.4
2.6
17.2
11.2
0.48
0.43
58.4
3850
282
15.9
6.2
9.7
6.2
0.67
0.57
63.2
3680
296
16.4
2.6
17.2
11.2
0.48
0.43
58.4
3850
146
19.8
13.4
11.5
7.6
0.46
0.55
51.2
2385
169
21.2
6.3
17.9
12.3
0.75
0.50
48.5
2300
324
18.9
10.1
11.2
6.1
1.20
0.80
52.4
5650
295
21.7
5.5
15.8
10.6
1.5
0.90
48.3
4730
194
16.9
10.3
10.5
7.1
0.90
0.72
55.8
3180
258
18.4
2.7
17.6
11.5
0.57
0.44
55.8
3430
222
12.9
12.2
11.9
8.4
0.48
0.43
58.8
3600
269
19.0
3.4
18.2
11.7
0.60
0.44
53.3
3390
Figure 1. Frequency of dental issues idened or treatment required for
six species of primate at Paignton Zoo Environmental Park before and
aer the iniaon of diet improvements to reduce dietary sugar (March
2003).
Journal of Zoo and Aquarium Research 1(2) 2013 76
Plowman
declined markedly, to the extent that veterinary intervenon
specically for dental treatment has not been necessary since
2004. Dental health connues to be monitored opportuniscally
when monkeys are restrained for other reasons and is generally
very good.
Body weights
In order to monitor the eects of diet reviews over this period,
keepers on the secon began to train the animals to staon
on weighing scales and have since been able to obtain body
weights on a regular basis for most individuals. The diet changes
implemented resulted in gradual but sustained weight loss of some
overweight individuals within a group, whilst others maintained
stable healthy weights. This was parcularly noceable in the
Diana monkey group, where the overweight adult male decreased
in weight from 12.0 kg in October 2007 (immediately aer the rst
diet changes were made) to 9.2 kg in early 2010, and appeared
to be stable at this weight prior to his departure to another zoo
in late 2010 (Fig. 2). A similar eect was also seen in the Sulawesi
crested black macaques, where three overweight individuals also
showed slow, sustained weight loss whilst other members of the
group maintained steady weights throughout. These were the
adult male (from 17.0 kg to 14.5 kg) and two adult females, both
9.0 kg before diet changes and now 7.5 kg and 6.9 kg. These three
individuals also now appear to be at a stable weight.
Faecal quality
Faeces was not formally monitored, but anecdotally keepers
report that for all species, with the excepon of Sulawesi crested
black macaques, it has generally improved in consistency with far
fewer instances of loose faeces. The Sulawesi crested macaques
sll have frequent diarrhoea that does not appear to be related to
diet and to date remains unexplained despite extensive veterinary
invesgaon.
Diet costs
The cost of the 2003 diet for each species was calculated using
2010 prices for each ingredient and compared with the cost of the
current diet (Table 4). The 2010 diets are substanally cheaper than
the 2003 diets for all species. For the total number of individuals
held in 2010 these reducons in cost represent an overall saving
of £9717 per year as a result of using the 2010 diets rather than
the 2003 diets.
Discussion
The diet review process in the Monkey Heights secon started in
2003 and has resulted in changes to most of the medium-sized
monkey diets such that they now all receive a very similar diet that
is higher in bre and protein and lower in readily digesble sugars
and starch than previously. During the review process, low bre and
Figure 2. Body weights of a group
of Diana monkeys at Paignton Zoo
Environmental Park following a diet
review that prompted a change from a
fruit-based to a vegetable-based diet.
The removal of all fruit occurred in April
2007; other changes were completed in
September 2007 immediately before the
rst weights were obtained.
Table 4. Cost comparisons of the diets fed in 2003 and 2010 to six species of monkey at Paignton Zoo Environmental Park; all costs based on 2010 prices
(UK £ sterling).
Abyssinian
colobus King colobus Diana monkey
Hamadryas
baboon Spider monkey
Sulawesi crested
black macaque
Cost per monkey per year
2003 diet 441 453 291 359 331 362
2010 diet 296 296 162 222 241 267
Group size in 2010 2 3 4 50 5 12
Total annual cost
2003 diet 882 1359 1164 17950 1655 4344
2010 diet 592 888 648 11100 1205 3204
Journal of Zoo and Aquarium Research 1(2) 2013 77
Diet reviews for monkeys
high sugar in largely fruit-based diets was concluded to be the most
likely cause of a variety of issues of concern. All fruit was therefore
removed from the diets and the amount of vegetables increased.
However, some vegetables, parcularly starchy root vegetables
also contain high levels of readily digesble carbohydrate (e.g.
Clauss et al. 2010). In order to prevent overfeeding of these
vegetables types, the ‘three veg group’ system was devised. These
three groups are green, leafy vegetables (e.g. cabbage, spinach,
leuce), starchy root vegetables (e.g. carrots, swede, squashes)
and others (e.g. peas, onions, fennel). The total weight of each
group is specied but keepers are free to use any vegetable type
within the group to make up that weight. This, along with the
fact that diets across the secon are now so similar, has reduced
preparaon me.
In addion, because we have replaced relavely expensive
fresh and dried fruit with cheaper vegetables, and increased scope
for exibility to take advantage of seasonally cheap produce and
special oers, we have made substanal costs savings, esmated
to be on average £129 per year per monkey, resulng in an overall
saving of nearly £10,000 per year.
Although it has increased since 2003, the bre content of the
2010 diets is sll not as high as that found in items consumed by
free-living monkeys (typically over 50% NDF; Oedal and Allen
1996). However, the dietary analysis presented here does not
include browse, which is very high in bre and provided to most of
the target species on a regular basis.
The main impetus for beginning diet reviews on this secon
was poor dental health of the colobus monkeys, which had
necessitated 17 instances of restraint and anaesthec for
treatment within the previous ve years. The removal of sugary
fruit from their diet had an almost immediate eect, drascally
reducing the need for treatment. Since 2003 there has only been
one case in which an individual of the species concerned has been
specically restrained for a dental condion. The vast majority
of dental issues aected the Abyssinian colobus monkeys so we
would expect fewer instances now we have fewer individuals in
the collecon. However, unl about 2007 the numbers of animals
was sll similar to the situaon pre-2003, so there was a genuine
reducon in treatment rate, at least from 2004–2007.
An unexpected result of the dietary changes was weight loss
of overweight individuals within a group, whilst other animals in
that group maintained healthy weights. This was achieved without
taking steps to limit food intake of parcular individuals, such as
separang them at feeding mes. These overweight individuals
are the more dominant animals in the group and so are able to
select and consume much more than their fair share of their
preferred food items (Smith et al. 1989). When the diet included
many highly desirable, sweet items, this ability to select preferred
items and prevent access for other group members presumably
resulted in an over-consumpon of high energy items. It appears
that when these highly preferred items were removed from the
diet, there was much less movaon for the dominant animals to
monopolise certain food types, and thus they no longer consumed
more than their fair share of the group diet. Within the macaque
group, the most subordinate individual is now the heaviest adult
female, possibly due to higher voluntary energy intake in response
to the chronic stress of being subordinate (Wilson et al. 2008).
During the process of diet review for the monkeys only very
minimal human resistance to changing the diets was encountered,
mostly towards the inial removal of all fruit. Possible factors
liming resistance to change could include the gradual nature
of the changes over a period of me. It was also benecial that
support for review and change was generated across all relevant
departments early on in the process through collaborave and
consensus-building meengs, where keepers were the main
drivers in determining priories for dietary review.
Conclusions
A connual process of diet review and adjustment for all medium
sized monkeys over several years has resulted in less expensive
diets that beer meet the nutrional needs of the animals. The
most signicant change made to the diets was the removal of all
fruit, including dried fruit, in order to reduce the levels of readily
available energy and parcularly sugar in the diets.
Acknowledgements
I would like to thank all the keepers involved in the diet evaluaons
discussed in this paper, parcularly Andrew Fry and Nicky Jago who
assisted in compiling informaon from keeper diaries over the last seven
years.
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