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SUMMER AND WINTER VITAMIN D3 LEVELS IN SEVEN
PLATYRRHINE SPECIES HOUSED AT A BRITISH ZOO,
WITH REFERENCE TO NATURAL UVB LEVELS
Author(s): Rowena Killick, M.Sc., D. Zoo. Med., M.R.C.V.S., Richard Saunders,
B.V.Sc., D. Zoo. Med., M.R.C.V.S., and Sharon P. Redrobe, B. Vet. Med., D.
Zoo. Med., M.R.C.V.S.
Source: Journal of Zoo and Wildlife Medicine, 48(3):732-741.
Published By: American Association of Zoo Veterinarians
https://doi.org/10.1638/2016-0071.1
URL: http://www.bioone.org/doi/full/10.1638/2016-0071.1
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Journal of Zoo and Wildlife Medicine 48(3): 732–741, 2017
Copyright 2017 by American Association of Zoo Veterinarians
SUMMER AND WINTER VITAMIN D3 LEVELS IN SEVEN
PLATYRRHINE SPECIES HOUSED AT A BRITISH ZOO,
WITH REFERENCE TO NATURAL UVB LEVELS
Rowena Killick, M.Sc., D. Zoo. Med., M.R.C.V.S., Richard Saunders, B.V.Sc., D. Zoo. Med., M.R.C.V.S.,
and Sharon P. Redrobe, B. Vet. Med., D. Zoo. Med., M.R.C.V.S.
Abstract: Serum samples were collected from 24 platyrrhines of seven diurnal species housed with outdoor
access at Bristol Zoo Gardens (United Kingdom) to test 25-hydroxyvitamin D3 (25OHD3) levels as part of the
veterinary department’s preventative health care program. Samples were collected in August 2008 (summer) and
January 2009 (winter) to examine the effect of season on 25OHD3 levels. Dietary levels of vitamin D3 remained the
same throughout the study period and fell within the range of 2000–4000 IU/kg dry matter, in accordance with
current primate guidelines. Statistical analysis showed that there was no significant difference between the
platyrrhines’ summer 25OHD3 values (range, ,4.0–.150.0 lg/L) and winter 25OHD3 values (range, ,4.0–80.1
lg/L). However, ultraviolet B (UVB) measurements taken at the zoo during the study period confirmed that UVB
levels were significantly higher in summer (mean reading for 1200–1300 hours GMT time period, 153.8 lW/cm2)
compared with winter (mean reading for 1200–1300 hours GMT time period, 19.4 lW/cm2). The 25OHD3 levels
measured were generally found to be low compared with previously published values from healthy captive and
wild platyrrhines.
Key words: Callitrichid, Cebid, Cholecalciferol, Primate, UVB, Vitamin D.
INTRODUCTION
Although disorders of calcium metabolism
(historically known by terms such as metabolic
bone disease, rickets, and cage paralysis) have
been widely reported in captive primates of both
Old and New World species, New World primates
(platyrrhines) are more susceptible.7,15,17,18,22,29 This
is because most platyrrhine species show a
relative resistance to the active form of vitamin
D3 (1,25-dihydroxyvitamin D3), so they require
much higher levels of vitamin D3 to maintain
normal calcium levels.2,3,34,37 Several authors have
shown that platyrrhines can exhibit symptoms of
vitamin D deficiency despite circulating levels of
active vitamin D3 that would be consistent with
hypervitaminosis D in humans and Old World
primates (catarrhines).3,29,34,41
In the past, researchers have attributed the
1,25-dihydroxyvitamin D3 (1,25OHD3) resistance
to a reduced number of receptors in target organs,
but more recent studies have shown that platyr-
From the Department of Veterinary Services and
Conservation Medicine, Bristol Zoological Society, Bristol
Zoo Gardens, Clifton, Bristol BS8 3HA, United Kingdom
and the University of Bristol, Bristol, United Kingdom.
Present address (Killick, Saunders, Redrobe): School of
Veterinary Sciences, University of Bristol, Langford
House, Langford, Bristol BS40 5DU, United Kingdom.
Correspondence should be directed to Dr. Killick
(rkillick@bristolzoo.org.uk).
rhines exhibit an overexpression of a vitamin D
response element binding protein, which competes with the vitamin D receptor.3,8,35 The reason
for the development of the resistance in unknown.
Postulated theories include the following: an
adaptation to eating South American plant species (eg, Solanum glaucophyllum) that contain a
1,25OHD3 glycoside that causes hypercalcaemia,
a genetic mutation, or an adaptation to very high
levels of ultraviolet B (UVB) exposure in their
natural environment.2,19 The fact that nocturnal
owl monkey (Aotus) species are the only platyrrhines that do not appear to exhibit the resistance
lends weight to the latter theory.1,29
High levels of vitamin D3 can be provided for
platyrrhines in captivity by feeding commercial
New World primate pellets, by adding vitamin D3
supplements to the diet and/or by providing
access to natural and/or artificial UVB (wavelengths, 290–315 nm) radiation. Current primate
nutrition guidelines recommend providing dietary
vitamin D3 concentrations of 1000–3000 IU/kg
dry matter (DM) and exposure to natural or
artificial UVB radiation.10 Some authors have
reported that even dietary vitamin D3 levels
exceeding 3000 IU/kg DM did not prevent
diseases associated with impaired calcium metabolism in platyrrhines without the addition of
artificial UVB exposure.20,28
Access to UVB by exposure to natural, unfiltered sunlight is often recommended in husband-
732
KILLICK ET AL.—SEASONAL VITAMIN D3 LEVELS IN PLATYRRHINES
ry guidelines for captive primates such as callitrichids and squirrel monkeys (Saimiri spp.).6,39,40
However, because the amount of UV radiation
that reaches the earth’s surface diminishes as
distance from the equator increases, levels at
United Kingdom latitudes are not as high as
those found in regions closer to the equator,
including the natural habitats of platyrrhines,
even on some days in summer.5,20,24 This is
especially true during winter months (as mentioned in platyrrhine husbandry guidelines).39
Wild platyrrhines inhabit a range in Central and
South America ‘‘within 208 north and south of the
equator.’’8 The British zoo in which the current
study was carried out lies on latitude 518 north.21,30
It has been known for some time that people
living in the United Kingdom and other regions of
similar latitude in the northern hemisphere show
an increased incidence of vitamin D deficiency
compared with those living closer to the equator.23
Although several previously published studies
have included measurement of circulating vitamin
D3 levels in platyrrhines (Table 1), a study on
seasonal variation of vitamin D3 levels in captive
platyrrhines with outdoor access, with reference
to environmental UVB levels, has not been
published thus far.2,11–14,16,20,32–34,36,38,41 The purpose
of this study was to determine whether vitamin D3
levels in captive platyrrhines in the United
Kingdom vary between summer and winter, in
correlation with seasonal outdoor environmental
UVB levels, and therefore whether outdoor access
is actually beneficial in terms of provision of
natural UVB at latitudes as far north as the
United Kingdom.
MATERIALS AND METHODS
The same materials and methods were used as
for a similar study, run concurrently, on captive
lemurs, which has already been published.27
Twenty-four platyrrhines of seven diurnal species
housed at Bristol Zoo Gardens (Bristol, United
Kingdom) were anaesthetized for routine health
checks during August 2008 (summer) and January
2009 (winter) as part of the zoo veterinary
department’s preventative healthcare program.
The species were as follows: common squirrel
monkey (Saimiri sciureus), white-faced saki monkey (Pithecia pithecia), Goeldi’s monkey (Callimico
goeldii), Geoffroy’s marmoset (Callithrix geoffroyi),
golden lion tamarin (Leontopithecus rosalia), golden-headed lion tamarin (Leontopithecus chrysomelas), and black lion tamarin (Leontopithecus
chrysopygus). Further details of these platyrrhines
are given in Table 2. Each primate was manually
733
restrained and anaesthetized using isoflurane
(Isoflo, Abbott Animal Health, Maidenhead,
Berkshire SL6 4XE, United Kingdom), and
oxygen was administered via face mask for
induction and maintenance. Blood samples were
collected and placed into lithium heparin anticoagulant tubes and plain (no additive) tubes, and
blood smears were made.
Samples in the plain tubes were processed on
the day of collection as described previously.27
The serum samples were sent to Pinmoore
Animal Laboratory Services (PALS, Clotton,
Cheshire CW6 0EG, United Kingdom) for
25OHD3 testing by radioimmunoassay (RIA).
Plasma chemistry and hematology tests were
carried out on the heparinized blood samples
and blood smears, respectively, to check the
health status of the primates as described previously.27
During the health checks, the primates were
also given clinical examinations, and radiographs
were taken. All blood samples were taken prior to
other testing (eg, tuberculosis tests) and medicating to prevent any effect on the blood parameters
measured. Any primates diagnosed with a condition such as renal failure that would affect
calcium metabolism were excluded from the
study.
The platyrrhines were provided with diets
consisting of a mixture of commercial products
marketed for New World primates (manufactured
and supplied by Special Diets Services [SDS],
Witham, Essex CM8 3TH, United Kingdom),
plus a variety of fresh fruit and vegetables, and
in some cases dried fruit, nuts, seeds, and bread,
plus occasional boiled eggs. Calcium and vitamin
D3 supplements (Zolcal-D and/or Nutrobal, Vetark Professional, Winchester SO23 9XN, United
Kingdom) were added to the fresh produce. The
overall calcium content of the diets (DM) was
0.58–1.16%, with most in the region of 0.7%. The
overall dietary vitamin D3 content of the diets was
2000–4000 IU/kg DM. The diets fed remained the
same throughout the study period for each
species.
UVB measurements were taken by the authors
using a digital UV Meter (Solarmeter Model 6.2,
Solartech Inc., Glenside, Pennsylvania 19038,
USA), which measures UVB light (wavelengths
280–320 nm) in microWatts per cm2 (lW/cm2), as
described previously.27 The measurements were
taken on 12 days in summer (July and August
2008) and 13 days in winter (December 2008 and
January 2009) on the main (central) lawn of the
zoo at three time points. All the platyrrhine
Species
NG
NG
5.6–42.2a
32.8–204.1
12.4–16.5
NG
NG
104.8–137.1a
19.5 6 3.0a
43.3 6 18.3a
21.2 6 1.4a (SEM not SD)
126.5 (SD NG)
14.5 (SD NG)
474.0 6 96.0
15.0 6 1.5
121.2 6 33.3a
101.2–144.3a
NG
83 6 16.3a (SEM not SD)
Mexican mantled howler
monkey (Alouatta palliata
mexicana)13
Black-handed spider monkey
(Ateles geoffroyi)11
White-faced capuchin (Cebus
capucinus)14
Goeldi’s monkey (Callimico
goeldii)12
Common marmoset (Callithrix
jacchus)34
Common marmoset (C.
jacchus)34
Common marmoset (C.
jacchus)41
Common marmoset (C.
jacchus)41
Black-tufted marmoset
(Callithrix penicillata) 36
115.2 6 32.2a
NG
308.4 6 24.7a (SEM not SD)
Black-and-gold howler monkey
(Alouatta caraya)33
Black-tufted marmoset (C.
penicillata)36
NG
281.9 6 23.24a (SEM not SD)
NG
Black-and-gold howler monkey
(Alouatta caraya)33
,70.0
Platyrrhines (three species)20
NG
NG
134.0 6 23.8 (SEM not SD)
.210.0 (raw data not given)
Min–Max
Platyrrhines (three species)20
2
Mean 6 SD
25OHD3 (lg/L)
34
29
3
17
2
5
56
9
11
6
14
12
10
10
23
n
Laboratory; osteomalacia
observed
Primate research center, Brazil;
blood samples collected July–
August
Primate research center, Brazil;
blood samples collected July–
August
Laboratory; osteomalacia
observed
Laboratory
Zoo; history of decreased renal
function
Laboratory
Wild (free-ranging); Panama
Zoo
Wild (free-ranging) males;
northern Argentina;
November
Wild (free-ranging) females;
northern Argentina;
November
Wild (free-ranging); Mexico;
just before rainy season
Zoo; three of 10 had rickets
Zoo
Zoo
Comments
Summary of published serum values of 25OHD3 obtained from captive and wild platyrrhines of various species
Platyrrhines (four species)
Table 1.
Exposure to direct natural UV
early morning and late
afternoon
Free exposure to direct natural
UV throughout the day
NG
NG
NG
NG
NG
Unrestricted
None
Unrestricted
Unrestricted
Outdoor access 3 mo/yr; some
spp. given supplemental UV
10 h/day
Outdoor access 3 mo/yr; given
supplemental UV 10 h/day
for 6 months prior to testing
Outdoor access 3 mo/yr; no
supplemental UV given
Unrestricted
UV exposure
734
JOURNAL OF ZOO AND WILDLIFE MEDICINE
Max, maximum; Min, minimum; dNG, not given in reference paper; SD, standard deviation; SEM, standard error of mean.
a
Not specified as 25OHD3.
None
Laboratory; all had moderate
to severe colitis
11.0–560.0a
NG
24
None
Zoo
48.0–236.0a
NG
6
Unrestricted
Wild (free-ranging); Colombia
25.5–120.0a
76.4a (SD NG)
18
Unknown
Unknown
12–120
NG
8
NG
Emperor tamarin (Saguinus
imperator)20
Saddle-back tamarin (Saguinus
fuscicollis)16
Cotton-top tamarin32 (Saguinus
oedipus)
Cotton-top tamarin38 (S.
oedipus)
Cotton-top tamarin38 (S.
oedipus)
34.9 6 5.3 (SEM not SD)
Unknown
Outdoor access 3 mo/yr
No direct UV exposure
Primate research center, Brazil;
blood samples collected July–
August
Zoo; three of eight had rickets
21
35.1–72.5a
53.3 6 10.4a
Min–Max
Species
Black-tufted marmoset (C.
penicillata)36
Table 1.
Continued.
Mean 6 SD
25OHD3 (lg/L)
n
Comments
UV exposure
KILLICK ET AL.—SEASONAL VITAMIN D3 LEVELS IN PLATYRRHINES
735
enclosures were situated within 150 m of this
lawn. The only UVB radiation that the platyrrhines had access to was that from natural
sunlight in their outdoor enclosures, except for
the golden-headed lion tamarin, which had access
to artificial UVB sources (UV bulbs, manufacturer unknown, providing levels of 100–200 lW/cm2
UVB at the level of the shelf beneath them) in one
area of its indoor enclosure in winter. Generally,
the platyrrhines had free access to their outdoor
enclosures during the day, and the average period
keepers observed them spending outside during
daylight hours varied from about 6 hr/day in
summer (cebids and callitrichids) to 4 (cebids)
and 0–2 hr/day (callitrichids) during winter.
Statistical analyses were performed to determine whether there were any significant differences between the 25OHD3 results obtained in
summer and those obtained in winter. Analyses
were not performed at the individual species level
or for the different sexes due to the small numbers
involved. The laboratory’s detection range for
25OHD3 was 4.0–150.0 lg/L. For the purposes of
statistical analysis, the values that fell outside the
laboratory testing range were represented as
follows: ,4.0 lg/L was represented by 3.9 lg/L
and .150.0 lg/L was represented by 150.1 lg/L.
The UVB recordings taken on the main lawn
were tested for a statistically significant difference
between summer and winter.
Analyses were performed using the statistics
software package SPSS 16.0 for Windows (SPSS
Inc., Chicago, Illinois 60606, USA). Data were
checked for normality using normal probability
(Q-Q) plots.
Paired t-tests were used to analyze normally
distributed data, whereas data that were not
normally distributed and could not be transformed, due to a lack of exact values for some
individuals, were analyzed using the nonparametric equivalent Wilcoxon matched-pairs signed
rank test.31 Independent numerical observations
(UVB readings) that were not normally distributed even when transformed were analyzed using
the nonparametric Mann-Whitney U-test.31 Significance was accepted if P , 0.05.
RESULTS
None of the platyrrhines were diagnosed with
any problems that could affect calcium metabolism (eg, renal failure), so none were excluded
from the study. The number of platyrrhines that
were pregnant or lactating was the same in
summer and winter (Table 2). All seven of the
juvenile platyrrhines included in the study had
736
JOURNAL OF ZOO AND WILDLIFE MEDICINE
Table 2. Details of platyrrhines housed at Bristol Zoo Gardens and given health checks August 2008 (summer)
and January 2009 (winter)
Adults
(.2 years old)
Juveniles
(,2 years old)
Species
Male
Female
Male
Female
Total of
each species
Common squirrel monkey (Saimiri sciureus)
White-faced saki monkey (Pithecia pithecia)
Geoffroy’s marmoset (Callithrix geoffroyi)
Goeldi’s monkey (Callimico goeldii)
Golden lion tamarin (Leontopithecus rosalia)
Golden-headed lion tamarin (Leontopithecus chrysomelas)
Black lion tamarin (Leontopithecus chrysopygus)
0
1
2
1
1
0
1
5a
1b
2
1c
0
1
1
2
1
0
0
0
0
0
4
0
0
0
0
0
0
11
3
4
2
1
1
2
a
Two of the female squirrel monkeys were lactating in August 2008 and January 2009 and one other was lactating in January
2009 only.
b
The female saki monkey was lactating in August 2008 and was pregnant in January 2009.
c
The female Goeldi’s monkey was pregnant in August 2008.
open epiphyseal (growth) plates on radiography
in summer and winter.
Healed fracture sites were noted on the radiographs of three platyrrhines, but no recent
fractures were seen. None of the radiographs
showed evidence of clinical rickets or osteomalacia.
The 25OHD3 results are summarized for each
species for summer and winter in Table 3. The
summer values for two of the Geoffroy’s marmosets (C. geoffroyi) were higher than the laboratory’s detection range for 25OHD3 (ie, .150.0 lg/
L), whereas the winter value for one of the black
lion tamarins (L. chrysopygus) and both summer
and winter values for one of the saki monkeys (P.
pithecia) were lower than the laboratory’s detection range (ie, ,4.0 lg/L), so exact values were
not available for any of these results. Thus, it was
not possible to calculate a summer mean value for
the Geoffroy’s marmosets and the saki monkeys, a
winter mean value for the black lion tamarins and
saki monkeys, or a summer or winter mean value
for the group as a whole, so medians were used. It
can be seen from Table 3 that in three platyrrhine
species (white-faced saki monkey, Geoffroy’s
marmoset, and golden lion tamarin), the mean
and/or median 25OHD3 value was higher in
summer than in winter. However, in the other
four platyrrhine species (common squirrel monkey, Goeldi’s monkey, golden-headed lion tamarin, and black lion tamarin), it was lower in
summer than in winter. The median 25OHD3
value for the whole group was almost exactly the
same in summer and winter.
A summary of the UVB readings taken on the
main lawn of the United Kingdom zoo is shown in
Table 3. Summary of serum 25OHD3 values in platyrrhine species at a UK zoo in summer (August 2008) and
winter (January 2009)
Summer 25OHD3 (lg/L)
Species (sample size)
Mean 6 SD
Median
Min–max
Winter 25OHD3 (lg/L)
Mean 6 SD
Median
Min–max
Common squirrel monkey (11)
9.32 6 4.26
7.40
5.70–20.00
10.69 6 6.61
8.60
5.30–28.40
c
c
White-faced saki monkey (3)
8.90b ,4.00b–12.60
5.70b ,4.00b–7.70
Goeldi’s monkey (2)
12.40 6 1.98 12.40
11.00–13.80
18.80 6 7.78 18.80
13.30–24.30
c
Geoffroy’s marmoset (4)
150.05c
61.10–.150.00c 38.73 6 30.30 33.60
7.60–80.10
Golden lion tamarin (1)
51.50
51.50
51.50
31.60
31.60
31.60
Golden-headed lion tamarin (1)
20.60
20.60
20.60
22.80
22.80
22.80
c
Black lion tamarin (2)
8.50 6 6.08
8.50
4.20–12.80
26.90b ,4.00b–49.90
a
c
All platyrrhine species
11.00b,c ,4.00b–.150.00c
10.95b ,4.00b–80.10
combined (24)
Max, maximum; Min, minimum; SD, standard deviation.
a
One or more values lying above or below the laboratory values range so exact value unknown and therefore mean cannot be
calculated.
b
Median calculated using maximum possible value for value lying below laboratory range (ie, ,4.0 ¼ 3.9).
c
Median calculated using minimum possible value for value lying above laboratory range (ie, .150.00 ¼ 150.1).
737
KILLICK ET AL.—SEASONAL VITAMIN D3 LEVELS IN PLATYRRHINES
Table 4. Mean and median UVB readings (lW/cm2) taken on main lawn of a UK zoo in summer (July/August
2008) and winter (December 2008/January 2009)
Time period during which readings were taken (GMT)
Type of average and season
Mean summer UVB reading lW/cm (6SD) (12)
Mean winter UVB reading lW/cm2 (6SD) (13)a
Median summer UVB reading lW/cm2 (12)a
Median winter UVB reading lW/cm2 (13)a
2
a
0730–0830 hours
1200–1300 hours
1530–1630 hours
53.2 (620.4)
0.5 (60.5)
56.5
1.0
153.8 (674.1)
19.4 (66.4)
122.0
20.0
77.0 (631.5)
1.3 (61.4)
72.5
1.0
GMT, Greenwich Mean Time; SD, standard deviation.
a
Number of days on which readings were taken.
Table 4. In all cases, the mean and median
summer readings were higher than the mean and
median winter readings.
Statistical analyses
The 25OHD3 results were not normally distributed, and as mentioned above, not all of them
were exact values because some fell above the
upper limit of the laboratory testing range and
some fell below the lower limit, so parametric
tests could not be used. The allocation of a value
of 3.9 lg/L for results of ,4.0 lg/L and a value of
150.1 lg/L for results of .150.0 lg/L enabled
ranking of the values as accurately as possible for
the Wilcoxon signed rank test, representing them
as their highest and lowest possible value, respectively, to minimize bias (the difference between
summer and winter values was potentially underestimated but not overestimated using this method). The analysis showed that there was no
significant difference between 25OHD3 levels in
summer and winter for the group as a whole (P ¼
0.60). Statistical testing was not performed at the
species level due to the small sample sizes.
The UVB readings did not follow a normal
distribution even when transformed. For all three
time periods, a Mann-Whitney U-test showed that
the UVB readings from the main lawn in summer
were significantly higher than the UVB readings
in winter (P , 0.001 for all).
DISCUSSION
This study investigated circulating levels of
vitamin D3 in captive platyrrhines housed with
outdoor access at a United Kingdom zoo in
summer and winter, with reference to natural
environmental UVB levels at the zoo. The metabolite 25OHD3 (calcidiol), which was used as a
measure of circulating vitamin D3 in this study, is
considered the most reliable for assessing vitamin
D3 status in humans and most terrestrial vertebrates.10 25OHD3 has a half-life of about 3 wk, so
levels reflect intake and endogenous synthesis of
vitamin D3 over the preceding weeks or months.37
The sample size (24 animals) was limited by the
number of platyrrhines held by the zoo, and
funding only allowed for testing during two
seasons in one 12-mo period, so the results must
be interpreted with caution, but they indicate that
access to natural sunlight year-round in a United
Kingdom zoo may have little impact on circulating levels of vitamin D3 in platyrrhines. Although
there was variation between species, overall, no
statistically significant difference was found between summer and winter 25OHD3 levels in the
platyrrhine group, despite significantly higher
levels of natural UVB in sunlight being present
at the zoo in summer compared with winter.
The amount of dietary calcium and vitamin D3
provided to each platyrrhine species remained the
same year round and fell within the current
recommended ranges for primates (at least
0.55% calcium on a DM basis and 2000–4000 IU
vitamin D3/kg DM).10 Despite this, vitamin D3
levels among the platyrrhines were generally low
in both seasons compared with values from
healthy platyrrhines in previously published studies (Table 1).2,11,13,14,16,20,32–34,36,38,41 The actual vitamin D3 intake of the platyrrhines was not
measured, so it is possible that there was an
element of selective feeding from the diets
provided. Interestingly, in another northern European zoo, year-round outdoor access and dietary vitamin D3 levels greater than 3000 IU/kg
DM did not prevent ‘‘metabolic bone disease’’ in a
group of platyrrhines (pied tamarins, Saguinus
bicolor), and artificial UVB sources were required.28 However, in a study carried out at the
same United Kingdom zoo (Bristol) as the current
study, outdoor access provided sufficient UVB for
lemurs (Varecia rubra, Lemur catta, Eulemur mongoz and Hapalemur griseus alaotrensis) to have
elevated vitamin D3 levels in summer compared
with winter.27
738
JOURNAL OF ZOO AND WILDLIFE MEDICINE
Although sample numbers were small, it is still
useful to consider possible explanations for the
apparent fact that environmental UVB levels at
the United Kingdom zoo were sufficient to
promote increased vitamin D3 production in
summer in the lemurs but not in the platyrrhines.
The first possibility is that the environmental
UVB levels were not high enough even in summer
to stimulate pre–vitamin D3 production in the
platyrrhines due to an inherent requirement for
higher UVB levels. The second explanation is that
the actual UVB exposure of the two groups
(platyrrhines and lemurs) at the zoo was different
due to a discrepancy in levels of UVB reaching the
enclosures and differing behavior and outdoor
enclosure use between the two groups.
Given the well-known platyrrhine resistance to
vitamin D3 metabolites relative to other species, it
seems reasonable to suggest that platyrrhines
might have also developed a degree of resistance
to the stimulation of vitamin D3 synthesis by UVB
radiation.2,3,34 However, evidence for this has not
been reported previously, and an artificial UVB
source that provided levels of UVB within the
range detected in this study has been shown to
stimulate sufficient vitamin D3 production to
prevent metabolic bone disease in one platyrrhine
species (the pied tamarin).28 In addition, unlike
the other platyrrhines in the current study, the
four Geoffroy’s marmosets had much higher
circulating levels of 25OHD3 in summer than in
winter, but this could not be proven statistically
significant due to the small number of animals
involved. These observations suggest that species
differences in sensitivity to the effects of UVB
radiation may exist among platyrrhines and that
the platyrrhine species included in this study
other than Geoffroy’s marmosets may have a
degree of ‘‘UVB resistance.’’ Further studies are
required to investigate this.
The second possible explanation for the observation of raised vitamin D3 levels in summer
compared with winter in the lemurs, but not in the
platyrrhines, is that the platyrrhines were not
actually exposed to increased UVB levels in their
enclosures in summer due to enclosure design
and/or position, and/or behavioral enclosure use,
whereas the lemurs were. Preliminary UVB readings taken within the primate enclosures in
summer and winter suggested that both platyrrhines and lemurs were exposed to increased UVB
levels in summer compared with winter, but
further data collection is needed to confirm this.27
As UVB levels can vary significantly even within
one enclosure, depending on the presence of
foliage and other structures that absorb and
scatter UV radiation, and the actual UVB dose
received depends on where the primate positions
itself, further work should include more detailed
enclosure UVB readings in conjunction with
behavioral (enclosure use) observations.
As stated above, compared with published
values for healthy platyrrhines, the circulating
25OHD3 levels of platyrrhines at the United
Kingdom zoo were generally low in both seasons.2,11,13,14,16,20,32–34,36,38,41 There were no published
data available for comparison for the two individual cebid species (squirrel monkeys and saki
monkeys) tested at the United Kingdom zoo,
and few published data are available for comparison from other cebid species. However, the data
that were available from platyrrhine groups,
which included cebids, and from two studies on
howler monkeys, one study on spider monkeys,
and one on capuchins, suggested that the 25OH
D3 values in cebid species at the United Kingdom
zoo were generally low in both summer and
winter.2,11,13,14,20,33 From this limited comparison,
the possibility that the majority of cebids included
in the current study were subclinically vitamin D
deficient in both seasons cannot be ruled out.
The published 25OHD3 values available for
callitrichids were also not from the same species
as those included in this study, except for Goeldi’s
monkeys, and in their case the published values
included some from animals with decreased renal
function.12 Using the published values from
healthy callitrichids that were available (Table 1)
for comparison, the vitamin D3 levels in the
Goeldi’s monkeys and black lion tamarins in this
study appeared to be low in both summer and
winter, but the single golden lion tamarin appeared to have adequate vitamin D3 levHowever,
the
Geoffroy’s
els.16,20,32,34,36,38,41
marmoset results were more varied and quite
different to the other platyrrhine species, as
mentioned above. There are no published values
for 25OHD3 in Geoffroy’s marmosets, but there
are several for two other Callithrix species: the
common marmoset (C. jacchus) and the blacktufted marmoset (C. penicillata).34,36,41 Compared
with these values, all of the Geoffroy’s marmosets
in the current study had 25OHD3 values within
the range of healthy marmosets in summer, but
two had levels below this range in winter, and one
of these fell below the mean measured in the
common marmosets with osteomalacia and was
similar to 25OHD3 values obtained from Geoffroy’s marmosets with metabolic bone disease at
another United Kingdom zoo (0–15 nM; ¼0–37.44
KILLICK ET AL.—SEASONAL VITAMIN D3 LEVELS IN PLATYRRHINES
lg/L) (Chatterton, pers. comm.). These results
indicate that, despite the high vitamin D3 levels
detected in the Geoffroy’s marmosets in the
current study during the summer, at least one of
these marmosets may have been at risk of
developing clinical vitamin D deficiency during
the winter.
Interestingly, the golden-headed lion tamarin’s
25OHD3 values were bordering on low in both
summer and winter, compared with published
values for healthy animals of tamarin species (Table
1), despite the artificial UVB sources provided in
its indoor enclosure in winter.16,20,32,38 Although this
result must be interpreted with caution as it is only
from one individual and there are no published
25OHD3 values for this species, keepers reported
that this tamarin was rarely seen near the UV
lamps. This emphasizes the importance of ensuring
that artificial UVB sources are well positioned to
improve vitamin D3 levels in primates.
Although no clinical signs of vitamin D deficiency were seen in this study, subclinical vitamin
D deficiency could not be ruled out, based on
previously published data, so it would be advisable to continue to monitor these animals closely.
Subclinical vitamin D deficiency could lead to an
increased risk of clinical signs developing when
calcium demands are increased (eg, during pregnancy and lactation). Subclinical vitamin D deficiency is also likely to reduce breeding success,
through diminished fertility and a reduced ability
to maintain calcium levels sufficient for normal
fetal growth, although, subjectively, poor breeding success had not been noted in this group of
platyrrhines.37 In addition, in humans, vitamin D
deficiency has been linked with an increased risk
for developing a variety of diseases such as
neoplastic, autoimmune and cardiovascular conditions, and infectious diseases such as tuberculosis.9,25
The diets provided to the platyrrhines in this
study were shown to contain adequate levels of
vitamin D3 as per current primate nutrition
guidelines.10 However, a recent study showed that
in common marmosets (Callithrix jacchus) digestive efficiency may play a role in circulating
vitamin D3 levels, and, as previously mentioned,
some studies have found recommended dietary
levels insufficient for preventing calcium metabolism disorders in platyrrhine species without the
use of supplemental artificial UVB radiation.20,26,28
Outdoor access can provide captive platyrrhines with benefits other than exposure to
natural UVB radiation, including environmental
stimulation and enrichment, and in at least one
739
genus (lion tamarins, Leontopithecus spp.), maintenance of natural coat color.6 However, it does
carry potential increased risks, such as exposure
to lower temperatures than occur in native
environments, and therefore potentially increased
susceptibility to yersiniosis, as well as increased
risk of predation by wild predators.4 Some authors
recommend the use of UV-penetrable roofing
materials to allow exposure to natural UV (including UVB) radiation, and this certainly solves
the issue of exposure to low temperatures,
although these materials tend to be expensive.6
Given the results of this study, the authors
recommend caution in relying on natural environmental UV to boost vitamin D3 levels in
captive platyrrhines in the United Kingdom, and
by extension, other regions of a similar latitude in
northern Europe. If providing outdoor access
and/or exposure to natural UV radiation via
UV-penetrable enclosure roofing, it would be
advisable to measure UVB levels within the
enclosure(s), in conjunction with behavioral enclosure use studies of the platyrrhines and
circulating vitamin D3 levels, to ensure that this
is beneficial in terms of vitamin D provision. The
alternative would be to provide suitable artificial
UV lighting, in suitable position(s) within the
enclosure, but again, behavioral studies and
measurement of circulating vitamin D3 levels
would be needed to determine efficacy.
Acknowledgments: The authors thank current
and previous Bristol Zoo Gardens vet staff,
students, and primate keepers, in particular Kellie
Wyatt and Melanie Bacon. They also thank Jane
Murray, Adrian Sayers, Frances Baines, and
Pinmoore Animal Laboratory Services (PALS)
for help with this project. It would not have been
possible without financial support provided by
the Royal College of Veterinary Surgeons Trust
and the discounted 25OHD3 testing supplied by
PALS.
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Accepted for publication 9 March 2017
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