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Clinical Biochemistry and Hematology of the Elusive Sun-Tailed Monkey (Cercopithecus solatus) in Gabon Inaugural Data From the Only Semifree Ranging Colony in the World.

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American Journal of Primatology 74:236–246 (2012)
RESEARCH ARTICLE
Clinical Biochemistry and Hematology of the Elusive Sun-Tailed Monkey
(Cercopithecus solatus) in Gabon: Inaugural Data From the Only Semifree
Ranging Colony in the World
PEGGY MOTSCH1∗ , JEAN-PAUL GONZALEZ1 , AND DELPHINE VERRIER1,2
‘Primatologie et Santé’, Unité de Recherche en Ecologie et Santé, Centre International de Recherches Médicales de
Franceville (CIRMF), Franceville, Gabon
2 Centre de Primatologie, CIRMF, Franceville, Gabon
1 Equipe
Clinical blood biochemistry and hematology are valuable tools to evaluate health and welfare in many
animal species. In order to document the general biology of one of the most poorly known nonhuman
primate species, and contribute to its conservation, the clinical blood biochemistry and hematology of
the sun-tailed monkey (Cercopithecus solatus Harrisson) was investigated in its range of endemicity
in Gabon. Data derived from 26 years of clinical monitoring of the only semicaptive colony of this
species in the world, housed at CIRMF (Franceville, Gabon), were analyzed in order to establish reference values of age–sex classes. Consistent with previous reports in other primate species, age and sex
significantly affected a number of biochemical and hematological parameters in C. solatus. Hematological analyses demonstrated significant differences in red blood cells, hemoglobin (HB), and hematocrit
(HT), with males showing significantly greater values than females. In contrast, neutrophil counts
were greater in females. An ontogenetic effect was detected for HB, HT, eosinophil, and monocyte
counts, while lymphocytes significantly decreased with age. Biochemical analyses also showed significant differences, with females displaying greater cholesterol and alanine aminotransferase levels.
Increase in levels of blood urea and aspartate aminotransferase coupled with decrease in albumin in
old individuals suggested declining kidney, liver, and muscle functions with age. Interspecific comparisons were conducted and the effects of the unique semifree-ranging setting on the validity and
value of the results presented are discussed. The reference values established will be useful in further
ecological, parasitological, and virological studies of the sun-tailed monkey. Am. J. Primatol. 74:236–246,
2012.
C 2012 Wiley Periodicals, Inc.
Key words: Cercopithecus; clinical chemistry; guenons; hematology; reference values; semifreeranging population
INTRODUCTION
Growing concern is being raised about the health
of nonhuman primates worldwide [Boesch, 2008;
Gillespie et al., 2008; Walsh, 2008]. Indeed, in the
past decades, some endangered great ape populations have been pushed to the brink of extinction
by infectious diseases such as Ebola [Walsh et al.,
2003] and severe respiratory syndromes [Kondgen
et al., 2008; Leendertz et al., 2004]. In addition, nonhuman primates are increasingly threatened by both
a number of diseases and the constant expansion of
human activities into their home ranges [Gillespie
et al., 2008]. Furthermore, due to their phylogenetic
proximity and the increasing frequency of encounters with human populations, nonhuman primates
represent a major source of pathogens that threaten
human health [Keele et al., 2006; Rayner et al., 2011;
Wolfe et al., 2005]. Documenting health, diseases,
C 2012 Wiley Periodicals, Inc.
and threats in nonhuman primates has, therefore,
become a priority.
Establishing baseline biologic data is an essential step for the assessment of animal health,
for the diagnosis of pathologies, for comprehending
the physiological alterations induced by pathogens,
stress and/or contaminants, and ultimately, for monitoring responses to translocations, therapy, or experimental treatments [Hambleton et al., 1979; Jain,
∗ Correspondence to: Peggy Motsch, CIRMF, BP 769 Franceville,
Gabon. E-mail: p.motsch@yahoo.fr
Received 04 July 2011; revised 19 October 2011; revision accepted 16 November 2011
DOI 10.1002/ajp.21993
Published online in Wiley Online Library (wileyonlinelibrary.
com).
Blood Parameters of Sun-Tailed Monkeys / 237
1986]. Clinical blood biochemistry and hematology,
for instance, are valuable tools to evaluate health
and welfare, and detect different metabolic disorders
and diseases in many animal species [Jain, 1986], in
particular, those for whom thorough clinical investigations cannot be easily conducted (e.g. wildlife)
[De Thoisy et al., 2001]. The extent to which such
parameters are useful for either clinical or research
use depends, however, upon the availability of reference ranges.
Reference blood biochemistry and hematology
data are available for a number of nonhuman primate species that have been extensively used in laboratory research, including rhesus and cynomolgus
macaques [Andrade et al., 2004], African green monkeys [Liddie et al., 2010], squirrel monkeys [Andrade
et al., 2004; Ausman et al., 1976], and chimpanzees
[Howell et al., 2003]. Except for these species, data
remain often anecdotic, mostly because of the great
difficulty in capturing and sampling free-ranging
nonhuman primates. It is, however, important to
document the clinical biology of these animals in
order to contribute to both their conservation and
the global effort on wildlife diseases epidemiological
survey.
The sun-tailed monkey (Cercopithecus solatus
Harrisson) is one of the most poorly known nonhuman primate species. Due to its very cryptic nature, this guenon species was only first described
in 1984 [Harrison, 1988]. It is endemic to a restricted forest area in Gabon [Brugiere et al., 1998;
Gautier et al., 1992], although its precise distribution area is still debated [Coad et al., 2010; Motsch
et al., 2011]. Most of the current knowledge concerning C. solatus is derived from the only captive colony of this species in the world, which is
housed in a semifree-ranging rainforest enclosure at
the Centre International de Recherches Médicales
de Franceville (CIRMF), Gabon. Previous studies
have described social and foraging behaviors, as
well as social organization in the CIRMF sun-tailed
monkeys [Charpentier et al., 2008; Peignot et al.,
2000].
The aim of the present study was to report blood
biochemical and hematological parameters obtained
from the long-term monitoring of the CIRMF suntailed monkey colony and establish reference values of age–sex classes. In addition to contributing
to the general description of the biology of this elusive species, such information will be useful in future
studies of the colony linking animal health condition with sociality, reproductive performances, and
infectious status. For comparison purposes, we also
present data on blood biochemistry and hematology
in two mustached guenons (C. cephus) and two hybrid guenons (C. cephus × C. nictitans) that live sympatrically within the CIRMF semifree-ranging rain
forest enclosure.
MATERIALS AND METHODS
All procedures involved in the present study
were approved by the Animal Care Committee of
the Game and Wildlife Department of Libreville,
Gabon (permit #01029). They complied with the
current laws of the Gabonese Republic and relevant international guidelines. Animals were handled under the supervision of trained veterinarians, in accordance with standard operating procedures at CIRMF, as well as in accordance with
the American Society of Primatologists (ASP) Principles for the Ethical Treatment of Non Human
Primates.
Study Animals and Sampling Procedures
The CIRMF sun-tailed monkey colony was established between 1984 and 1998, with the introduction of five wild-born individuals (two males (M) and
three females (F), aged from 1 to 2 years) into a 0.5ha forested enclosure. The age of the founders was
estimated from dental eruption patterns. Between
1989 and 2011, 35 infants (19 M, 16 F) were born
into the colony that numbered an average of 11.3 ±
SD 4.2 individuals. Population size was 16 (7 M, 9 F)
as of 2011. All individuals are identified by a unique
code tattooed on the internal face of the thigh to
allow for at-distance recognition. Furthermore, two
female hybrid guenons (C. cephus × C. nictitans)
have been living sympatrically with the sun-tailed
monkeys since the 1990s, and two additional wildborn mustached guenons (one immature male and
one adult female, kept as pets by local people), were
also released into the semifree-ranging enclosure in
2005 and 2010, respectively. Animals forage freely
in the forested enclosure (feeding on leaves, fruits,
roots, bark, seeds, stems, and insects) [P. Motsch,
personal observations; Peignot et al., 2000] and are
supplemented with bananas, wild fruits, and soyabased homemade cake spread in a fenced feeding
area twice a day. Water is available ad libitum.
A long-term monitoring program of this colony
has been conducted since its creation. Presence,
births, and deaths are recorded and individuals are
captured annually for veterinary health checks. At
these occasions, animals are captured in the fenced
feeding area and anaesthetized by blowpipe intramuscular injections of ketamine (10 mg/kg body
weight). They are then transferred to the CIRMF Primate Center for medical examination and sampling.
Blood samples (representing <7% of total blood volume) are taken from the femoral vein in both EDTAtreated tubes and tubes containing no anticoagulant. After completion of the physical, animals are
returned to the fenced feeding area and monitored
until full recovery from anesthesia prior to being released into the enclosure.
Am. J. Primatol.
238 / Motsch et al.
TABLE I. Hematological and Biochemical Parameters Tested
Parameters
Platelet count
White blood cell
Red blood cells
Haemoglobin
Hematocrit
Mean corpuscular volume
Mean corpuscular
haemoglobin
Mean corpuscular
haemoglobin concentration
Neutrophils
Eosinophils
Basophils
Lymphocytes
Monocytes
Absolute neutrophils
Absolute eosinophils
Absolute basophils
Absolute lymphocytes
Absolute monocytes
Albumin
Calcium
Cholesterol
Creatinine
Glucose
Triglycerides
Total protein
Urea
Gamma
glutamyltranspeptidase
Total birulin
Direct birulin
Alkanine phosphatase
Aspartate aminotransferase
Alanine aminotransferase
Abbreviation
Units
WBC
RBC
HB
HT
VGM
TCM
109 /l
109 /l
1012 /l
g/dl
%
Fl
pg
CCM
g/dl
%Neutro
%Eosino
%Baso
%Lympho
%Mono
Neutro
Eosino
Baso
Lympho
Mono
GGT
%
%
%
%
%
109 /l (cells)
109 /l (cells)
109 /l (cells)
109 /l (cells)
109 /l (cells)
μmol/l
mmol/l
mmol/l
μmol/l
mmol/l
g/l
g/l
mmol/l
U/l
AP
ASAT
ALAT
μmol/l
μmol/l
U/l
U/l
U/l
Hematological and Clinical Chemistry
Analyses
All analyses were conducted at the Laboratoire
d’Analyses Médicales (LAM) of the CIRMF. The
quality of the analyses is subject to in-house control,
and LAM is also affiliated with the French national
quality control scheme.
Hematological parameters (Table I) were determined from fresh EDTA-treated blood using
commercial kits (diluents, cleaner, lysing solution, Eosino FIX, and Basolyse II; Laboratory
HORIBA ABX Diagnostics, Tokyo, Japan) on an ABX
PENTRA C+ auto-analyzer (Laboratory HORIBA
ABX Diagnostics). Blood biochemical parameters
(Table I) were determined from fresh serum using
commercial kits (BIOLAB kits, Laboratory Roche
PESSIMEDICAL, Fontenay-sous-Bois, France and
BIOMERIEUX kits, Laboratory MEDILAB, Mèze,
France) on a HITACHI 902 automatic analyzer (Laboratory MEDIM EQUIP, Mèze, France).
Am. J. Primatol.
Data Analyses
A total of 162 hematological profiles and 145
serum biochemical profiles obtained from 32 individuals (15 females and 17 males; 1 to 20 observations per individual) from 1985 to 2010 were used.
Only data from healthy individuals were included in
the present study. Data were classified into four age
groups: (1) immature individuals (IM; 0 to 4 years of
age); (2) adolescent males (SUB for subadults; aged
from 4 to 7 years); (3) adults (AD; females aged >4
years and mature males aged >7 years); and (4) old
individuals (OL; >12 years of age).
Statistical analyses were performed using
SPSS® (version 17.0 for Windows; SPSS, Chicago,
IL). The Kolmogorov–Smirnov test was used to determine whether the data were normally distributed,
and an F-test was used to confirm homogeneity of
variances. Linear mixed models were used to analyze
data with a repeated-measure pattern [Littell et al.,
1998]. Individuals were used as random effect, and
the age at the time of capture as ranks for repeated
measures. Gender and age class were included as
factors to test for sex, age, and sex × age interaction
effects by mixed analysis of variance (ANOVA). For
each mixed-model analysis, the covariance structure
was examined, and the best fit selected based on lowest Schwarz’s Bayesian criterion. Sidak adjustments
were performed to allow for multiple pairwise comparisons. Values are reported as means, and results
were considered significantly different at P < 0.05.
RESULTS
Hematology
The hematological values obtained for each age
group and for the entire C. solatus CIRMF population are presented in Table II, while age and sex
differences are summarized in Table III. Platelets,
red blood cells (RBC), hemoglobin (HB), hematocrit
(HT), and neutrophils (%) were influenced by sex
(P < 0.05 in all cases; Table III). Males displayed
significantly greater levels of RBC, HB and HT,
and lower platelets and neutrophils (%), as compared to females (Table IV). Age also had a significant effect on some hematological parameters (Table III). In both sexes, immature individuals had
significantly lower eosinophils (%) and monocytes
(%), and greater lymphocytes (%) than the other
age classes (P < 0.05 in all cases). Old individuals showed significantly reduced lymphocytes (%) as
compared to adolescent males and adults but greater
eosinophils (%) than adolescents (P < 0.05 in all
cases). In males, immature individuals had significantly lower RBC, HB, HT, and mean corpuscular
haemoglobin (TCM), and greater platelets than the
other age classes (P < 0.05 in all cases), while old
individuals showed significantly greater neutrophils
(%) (P < 0.05). In females, immature individuals had
72
72
72
72
72
72
72
72
72
72
72
72
72
72
72
72
72
72
476.6
8.8
5.3
11.8
36.9
71.3
22.3
31.4
46.2
1.9
0.2
41.0
9.9
3.9
0.2
0.00
2.1
0.5
104.1
4.2
0.7
1.2
4.4
3.7
2.1
3.0
18.7
2.5
0.4
20.3
12.7
2.3
0.3
0.03
0.9
0.6
SD
357.0–659.0
5.0–20.0
4.0–7.0
10.0–15.0
31.0–45.0
65.0–77.0
18.0–25.0
24.0–35.0
19.0–73.0
0.0–7.0
0.0–1.0
12.0–74.0
0.0–41.0
1.5–9.5
0.0–0.8
0.00–0.08
0.6–3.8
0.0–2.0
95% CIs
21
21
21
21
21
21
21
21
21
21
21
21
21
21
21
21
21
21
470.3
6.5
5.7
13.6
41.8
73.4
23.7
32.2
45.4
2.2
0.2
40.2
11.2
4.2
0.2
0.02
3.9
0.5
N Mean
128.7
1.7
0.9
2.6
7.3
3.6
0.7
1.6
20.2
2.2
0.4
19.5
14.5
3.5
0.3
0.05
2.5
0.8
SD
308.0–657.0
4.0–10.0
4.0–7.0
11.0–18.0
34.0–53.0
66.0–79.0
22.0–25.0
29.0–34.0
19.0–76.0
0.0–7.0
0.0–1.0
11.0–77.0
1.0–42.0
1.1–9.9
0.0–0.7
0.0–0.1
1.0–8.4
0.0–2.8
95% CIs
Adolescent males
47
47
47
47
47
47
47
47
47
47
47
47
47
47
47
47
47
47
404.4
6.6
5.4
12.7
39.0
74.2
23.7
31.8
55.8
2.2
0.1
34.2
7.7
3.6
0.3
0.03
1.1
1.2
N Mean
87.7
2.6
0.8
2.5
6.8
4.9
2.3
3.2
16.3
3.0
0.4
16.1
9.8
1.7
0.2
0.04
0.8
1.3
SD
95% CIs
256.0–541.0
3.0–13.0
4.0–7.0
10.0–17.0
31.0–52.0
66.0–82.0
19.0–27.0
25.0–37.0
28.0–80.0
0.0–8.0
0.0–1.0
6.0–60.0
0.0–40.0
1.7–7.9
0.1–0.8
0.0–0.1
0.2–3.1
0.1–3.7
Adults
15
15
15
15
15
15
15
15
15
15
15
15
15
15
15
15
15
15
167.4
2.1
1.3
2.3
7.3
5.0
2.7
3.6
17.8
1.4
0.5
13.5
14.9
1.9
0.2
0.04
0.7
0.9
SD
232.0–833.0
3.0–10.0
3.0–8.0
10.0–17.0
30.0–53.0
66.0–82.0
17.0–27.0
23.0–35.0
29.0–84.0
3.0–8.0
0.0–1.0
5.0–53.0
1.0–46.0
1.3–7.1
0.0–0.4
0.0–0.1
1.4–4.1
0.0–2.8
95% CIs
Old adults
440.8
6.3
5.6
12.8
38.3
73.4
23.5
31.9
58.0
4.9
0.5
19.1
17.9
3.3
0.2
0.02
2.5
0.6
N Mean
Hematological values are presented as means with sample size (N), standard deviation (SD), and 95% confidence intervals (95% CIs).
Platelets
WBC
RBC
HB
HT
VGM
TCMH
CCMH
%Neutro
%Eosino
%Baso
%Lympho
%Mono
Neutro
Eosino
Baso
Lympho
Mono
Parameters N Mean
Immature
TABLE II. Hematological Parameters in Cercopithecus solatus With Age-Specific Reference Values
155
155
155
155
155
155
155
155
155
155
155
155
155
155
155
155
155
155
446.0
7.6
5.4
12.4
38.3
72.6
23.1
31.7
50.9
2.3
0.2
35.8
10.3
3.9
0.2
0.02
2.9
0.6
N Mean
118.0
3.5
0.8
2.1
6.1
4.4
2.3
3.0
18.5
2.7
0.4
19.2
12.6
2.9
0.3
0.04
2.1
0.8
SD
95% CIs
281.0–640.0
4.0–14.0
4.0–7.0
10.0–17.0
31.0–52.0
66.0–79.0
19.0–27.0
25.0–35.0
19.0–80.0
0.0–8.0
0.0–1.0
7.0–68.0
0.0–42.0
1.1–8.8
0.0–0.6
0.0–0.1
0.6–7.6
0.0–2.8
All ages
Blood Parameters of Sun-Tailed Monkeys / 239
Am. J. Primatol.
240 / Motsch et al.
TABLE III. Influence of Sex and Age on Hematological and Blood Biochemical Parameters in Cercopithecus
solatus
Statistics
N
F
df
Psex
Page
Page × sex
Sex effect
Age or age × sex effect
Platelets
WBC
RBC
HB
HT
VGM
TCMH
CCMH
%Neutro
155
155
155
155
155
155
155
155
155
693.57
31,880.44
3,208.42
4,040.09
3,884.59
13,788.22
5,084.80
6,453.35
11,251.56
1,27
1,20
1,30
1,31
1,31
1,14
1,21
1,17
1,27
0.039
0.155
0.000
0.000
0.000
0.158
0.074
0.273
0.048
0.004
0.000
0.112
0.001
0.030
0.132
0.068
0.857
0.848
0.010
0.021
0.033
0.000
0.000
0.077
0.037
0.452
0.035
F>M
n.s.
F<M
F<M
F<M
n.s.
n.s.
n.s.
F>M
%Eosino
%Lympho
%Mono
Albumin
Calcium
Cholesterol
Creatinine
Glucose
Triglyceride
Total protein
Urea
GGT
AP
Total birulin
Direct birulin
ASAT
ALAT
155
155
155
138
138
138
138
138
138
138
138
138
138
138
138
138
138
121.49
5,386.79
333.23
161.96
1,213.49
547.42
248.16
221.09
363.13
563.26
96.28
1,644.35
62.70
859.09
352.90
250.33
3,643.48
1,33
1,26
1,31
1,27
1,43
1,21
1,30
1,35
1,102
1,24
1,20
1,21
1,18
1,28
1,23
1,27
1,21
0.887
0.267
0.442
0.830
0.833
0.042
0.499
0.761
0.916
0.793
0.399
0.355
0.399
0.413
0.480
0.767
0.018
0.001
0.000
0.000
0.000
0.795
0.515
0.002
0.191
0.548
0.336
0.009
0.819
0.065
0.784
0.187
0.024
0.051
0.293
0.216
0.520
0.830
0.447
0.077
0.419
0.477
0.455
0.392
0.072
0.313
0.131
0.136
0.114
0.493
0.114
n.s.
n.s.
n.s.
n.s.
n.s.
F>M
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
F>M
IM>SU>AD>OL in M
IM>(AD & OL) in F
OL>(AD, IM & SU) in M
(AD & OL)>(SU & IM) in M
IM<(SU, AD& OL) in M
n.s.
IM<(SU, AD & OL) in M
n.s.
(AD & IM)>OL in F; OL>
(AD, SU & IM) in M
IM<(AD &OL) and SU<OL
IM>AD>OL and SU>OL
IM<(AD &OL)
OL<(IM, SU &AD)
n.s.
n.s.
AD>(IM &OL) and SU>(IM &OL)
n.s.
n.s.
n.s.
OL>AD
n.s.
n.s.
n.s.
n.s.
OL>(AD &SU)
IM>OL
Parameters
Mixed ANOVAs with individuals included as random effect and the age at the time of capture as ranks for repeated measures were used to account for
the repeated measure pattern of the data. Gender and age class were included as factors to test for sex, age, and age × sex interaction effects. Results
were considered statistically significant at P < 0.05.
F, females; M, males; IM, immature individuals; SU, adolescent males; AD, adults; OL, old individuals; n.s., not significant (P > 0.05). Significant results
are in bold (P < 0.05).
TABLE IV. Summary of the Hematological and Biochemical Parameters Showing Statistically Significant Differences Between the Sexes (P < 0.05) in Cercopithecus solatus
Females
Males
Parameters
N
Mean
SD
95% CIs
N
Mean
SD
95% CIs
Platelets
RBC
HB
HT
% Neutro
Cholesterol
ALAT
68
68
68
68
68
63
63
456.1
5.0
11.1
34.8
56.3
3.1
69.0
108.1
0.8
1.0
3.1
16.0
0.8
47.4
274.0–833.0
3.4–8.0
9.0–13.0
27.0–43.0
17.0–87.0
1.8–6.4
16.0–225.0
87
87
87
87
87
75
75
436.5
5.7
13.4
41.2
46.7
2.8
52.5
127.2
0.7
2.2
6.4
19.4
1.0
32.1
230.0–774.0
4.1–7.3
9.5–19.1
30.0–54.0
15.0–84.0
1.5–6.9
9.0–152.0
Values are presented as means with sample size (N), standard deviation (SD), and 95% confidence intervals (95% CIs).
significantly greater white blood cells than the other
age classes (P < 0.05), while old individuals exhibited significantly lower neutrophils (%) (P < 0.05).
Blood Chemistry
The biochemical values obtained for each age
group and for the entire C. solatus population are
Am. J. Primatol.
presented in Table V, while age and sex differences
are summarized in Table III. Sex had a significant effect on cholesterol and alanine aminotransferase (ALAT) only (values presented in Table IV),
with females displaying greater circulating concentrations than males (P < 0.05 in both cases; Table
III). Creatinine was elevated in adults and adolescent males, urea, and aspartate aminotransferase
230.0–771.0
2.0–3.5
1.9–6.1
49.0–133.0
2.2–7.1
0.3–2.5
31.0–72.0
1.5–10.0
33.0–410.0
84.0–1,427.0
2.4–25.0
0.6–14.0
32.0–176.0
24.0–152.0
95% CIs
21
21
21
21
21
21
21
21
21
21
21
21
21
21
557.4
2.3
2.5
122.0
4.7
0.8
63.1
3.2
138.7
480.9
14.6
5.9
69.7
49.9
181.8
0.2
0.5
48.4
1.7
0.4
10.7
2.0
89.6
381.4
8.9
3.8
36.9
29.7
N Mean SD
220.0–752.0
1.9–2.5
1.5–3.5
65.0–220.0
3.2–7.7
0.2–1.9
39.0–76.0
1.0–9.1
38.0–292.0
63.0–1,316.0
4.1–32.2
1.8–13.0
29.0–146.0
17.0–87.0
95% CIs
Adolescent males
46
46
46
46
46
46
46
46
46
46
46
46
46
46
548.9
2.4
3.0
109.6
3.9
1.0
64.3
2.8
164.5
388.4
11.8
3.3
81.3
61.3
159.8
0.3
0.9
46.0
1.9
0.7
9.4
1.8
175.3
281.2
7.2
2.7
37.8
40.4
N Mean SD
95% CIs
224.0–764.0
1.8–2.7
1.8–4.6
51.0–168.0
0.6–7.6
0.5–3.2
43.0–76.0
0.9–6.9
59.0–481.0
76.0–801.0
3.2–23.7
0.5–8.0
34.0–139.0
21.0–149.0
Adults
15
15
15
15
15
15
15
15
15
15
15
15
15
15
389.3
2.4
2.6
72.7
3.0
1.2
53.1
4.6
162.8
434.9
10.5
5.2
129.8
55.8
162.5
0.6
0.7
25.4
1.1
1.4
10.6
2.8
148.5
432.3
6.8
4.8
76.6
62.1
187.0–656.0
1.8–4.0
1.7–4.0
46.0–129.0
0.4–4.0
0.2–4.7
40.0–72.0
1.3–9.2
48.0–554.0
56.0–1,605.0
3.4–22.0
1.3–15.0
41.0–313.0
10.0–225.0
95% CIs
Old Adults
N Mean SD
Blood biochemical values are presented as means with sample size (N), standard deviation (SD), and 95% confidence intervals (95% CIs).
182.0
0.5
1.1
27.1
1.4
0.6
13.7
2.4
156.6
452.1
7.4
4.4
46.6
37.4
56
56
56
56
56
56
56
56
56
56
56
56
56
56
Albumin
Calcium
Cholesterol
Creatinine
Glucose
Triglyceride
Total protein
Urea
GGT
AP
Total birulin
Direct birulin
ASAT
ALAT
557.7
2.5
3.1
84.6
4.1
1.1
58.2
4.0
178.2
688.2
12.0
5.4
93.6
64.4
N Mean SD
Parameters
Immature
TABLE V. Blood Biochemical Parameters in Cercopithecus solatus With Age-Specific Reference Values
138
138
138
138
138
138
138
138
138
138
138
138
138
138
536.3
2.4
2.9
97.2
3.9
1.0
60.4
3.6
166.1
535.0
12.2
4.8
89.8
60.2
178.9
0.4
0.9
40.9
1.6
0.7
12.2
2.3
153.0
411.1
7.5
4.0
49.1
40.6
N Mean SD
95% CIs
218.0–761.0
1.9–2.8
1.8–4.6
50.0–167.0
0.8–7.1
0.3–2.5
40.0–76.0
1.0–9.1
48.0–410.0
72.0–1,316.0
3.3–25.0
0.7–13.0
32.0–172.0
18.0–152.0
All ages
Blood Parameters of Sun-Tailed Monkeys / 241
Am. J. Primatol.
242 / Motsch et al.
Fig. 1. Hematological reference values for the sun-tailed monkeys, mustached guenons, and guenon hybrids of the CIRMF colony as
compared to other primate species. SOL, sun-tailed monkeys; CEP, mustached guenons; HYB, guenon hybrids (present study); AGM,
African green monkeys [Liddie et al., 2010]; MAC, bonnet macaques [Pierre et al., 2011]; LEM, red ruffed lemurs [Dutton et al., 2008];
CPZ, chimpanzees [Loeb, 1986]; GOR, gorillas [Loeb, 1986]; HUM, humans [Kratz et al., 2004]. Vertical bars represent mean and 2×
standard deviation (SD) for high and low range.
(ASAT) in old individuals (P < 0.05 in all cases; Table III). Old individuals also exhibited lower albumin
levels than the other age classes, and lower ALAT
than their immature counterparts (P < 0.05 in both
cases).
Interspecific Comparisons
The biochemical and hematological values obtained for the mustached guenons and the hybrid
guenons are presented in Figures 1 and 2.
Am. J. Primatol.
DISCUSSION
The main purpose of the present study was to establish reference values for biochemical and hematological parameters in the sun-tailed monkey, one of
the most poorly known nonhuman primate species,
within its geographical range in Gabon. Complementary data on two sympatric guenon species are also
provided for comparison purposes.
The results show that age and sex significantly
affect a number of biochemical and hematological
parameters in the study species, contributing to individual variation. Many of our findings converge
Blood Parameters of Sun-Tailed Monkeys / 243
Fig. 2. Blood chemical reference values for the sun-tailed monkeys, mustached guenons, and guenon hybrids of the CIRMF colony as
compared to other primate species. SOL, sun-tailed monkeys; CEP, mustached guenons; HYB, guenon hybrids (present study); AGM,
African green monkeys [Hambleton et al., 1979; Liddie et al., 2010]; MAC, bonnet macaques [Pierre et al., 2011]; LEM, red ruffed
lemurs [Dutton et al., 2008]; CPZ, chimpanzees [Hambleton et al., 1979; Herdon and Tigges, 2001; Loeb, 1986]; GOR, gorillas [Loeb,
1986]; HUM, humans [Kratz et al., 2004]. Vertical bars represent mean and 2× standard deviation (SD) for high and low range.
Am. J. Primatol.
244 / Motsch et al.
with the patterns of gender- and age-related differences reported in other primate species. For instance, hematological analyses demonstrated significant differences in RBC, HB, and HT, with males
showing greater values than females. This is consistent with previous reports in African green monkeys (Chlorocebus sabaeus) [Kagira et al., 2007],
cynomolgus macaques (Macaca fascicularis) [Andrade et al., 2004; Schuurman and Smith, 2005],
bonnet macaques (M. radiata) [Pierre et al., 2011],
tonkean macaques (M. tonkeana) [Thierry et al.,
2000], tufted capuchin monkeys (Cebus apella) [Samonds et al., 1974], owl monkeys (Aotus azarai infulatus) [Takeshita et al., 2011], mandrills (Mandrillus
sphinx) [Setchell et al., 2006], chimpanzees (Pan
troglodytes) [Loeb, 1986], and humans (Homo sapiens) [Kratz et al., 2004]. Differences in hormonal status and muscular mass between genders, as well as
menstrual blood loss, have been proposed as explanatory factors [Dacie and Lewis, 1984; Jain, 1986].
In contrast, neutrophil counts were greater in females, as previously reported in African green monkeys [Liddie et al., 2010], mandrills [Setchell et al.,
2006], and hamadryas baboons (Papio hamadryas)
[Harewood et al., 1999; Havill et al., 2003] but
not in macaques [Andrade et al., 2004] and humans [Kratz et al., 2004]. Such sex differences in
white blood cell counts have been attributed to the
level of female sexual promiscuity [Anderson et al.,
2004; Nunn, 2002]. Females also displayed greater
cholesterol than males, as previously reported in red
ruffed lemurs (Varecia rubraga) [Dutton et al., 2008]
and African green monkeys [Liddie et al., 2010],
and greater ALAT levels, which has been elsewhere
attributed to greater levels of parasitic infections
rather than sex-related differences [Monteiro et al.,
2009; Takeshita et al., 2011].
Age also markedly affected biochemical and
hematological parameters. For instance, we detected
an ontogenetic effect for HB and HT increasing with
age in males, as well as eosinophil and monocyte
relative counts in both sexes. In contrast, lymphocytes significantly decreased with age. These results
are consistent with a previous report on mandrills
[Setchell et al., 2006]. Furthermore, the increase in
blood urea in old individuals may suggest a declining kidney function as commonly described in elderly
humans [Tietz et al., 1992] and aging chimpanzees
[Videan et al., 2008]. Increase in ASAT coupled with
decrease in albumin in old individuals may also suggest a decrease in liver function with age, as reported in rhesus macaques, chimpanzees, and humans [Smucny et al., 2001; Tietz et al., 1992; Videan
et al., 2008]. In addition to indicating a loss of liver
function, the significant decrease in albumin may
also indicate a decrease in muscle strength [Schalk
et al., 2005].
Although most hematological and biochemical
parameters were broadly consistent with previous
Am. J. Primatol.
reports in a number of primate species (Figs 1 & 2), as
well as most of the trends in sex- and age-related differences, some parameters measured in the present
study tended to be outside the reference value ranges
commonly reported for other species. Lymphocyte
counts were particularly low in the CIRMF mustached and hybrid guenons (18–20% vs. 35–45%),
and monocyte counts relatively elevated in both suntailed monkeys (10%) and the two other guenon
species (16–18% vs. 5%) in comparison to other selected primates (Fig. 1). In addition, the present
study reported elevated values for blood creatinine,
total bilirubin and ASAT, and reduced blood urea as
compared to other primate species (Fig. 2). Whether
this reflects actual interspecies differences is hard
to determine. For instance, stress response is one
of the processes that can decrease lymphocytes and
increase monocyte counts [Davis et al., 2008]. The
semifree-ranging conditions and relatively low level
of habituation to humans at the CIRMF Cercopithecus colony could be responsible for a greater level of
stress during manipulation as compared to captive
and zoo populations of primates. Maintained physical activity and natural foraging within the forest
enclosure could also account for the differences observed in blood metabolites.
Several studies have discussed the effect of captivity on biological parameters in wildlife. A comparison between captive and free-ranging red ruffed
lemurs showed differences associated with physiological state, hydration, and diet between the two
populations [Dutton et al., 2008]. In particular, the
lower hematocrit, plasma concentrations of total proteins, albumin, and cholesterol found in the freeranging cohort have been interpreted as a consequence of the lower protein, and trace mineraldeficient diet in wild animals. In contrast, levels of
ASAT, ALAT, and triglycerides were lower in captive
ruffed lemurs. Similarly, Liddie et al. [2010] showed
that captivity increases a number of biological parameters in African green monkeys (total proteins,
albumin, total bilirubin, alkaline phosphatase, phosphorus, and sodium) depending on the time spent in
captivity, while RBC and platelets fluctuate over the
course of captivity. Correspondingly, Kagira et al.
[2007] highlighted the need for a long adaptation
period and individual baseline measures before experimental use in nonhuman primates.
However, obtaining blood samples from wild
nonhuman primates can prove extremely challenging, as well as ethically questionable. Indeed, nonhuman primates very often inhabit inaccessible areas, display cryptic behaviors, and prove difficult to
follow and/or habituate in the wild. This is particularly true in the case of the sun-tailed monkey that
was first described only 27 years ago due to the difficulty to observe it in its habitat [Brugière and Gautier, 1999; Harrison, 1988]. In addition, wild animals
may experience greater individual variation in the
Blood Parameters of Sun-Tailed Monkeys / 245
factors that influence biological parameters of significance (due, for instance, to greater energetic demands, less balanced diets, more variation in food
intake, and exposure to a potentially wider array
of parasites and pathogens) [Nunn, 2002], and thus
the establishment of reference values may require
a much larger sample size. In homogeneous captive
cohorts kept in controlled conditions and of known
medical history, interindividual variation is likely to
be less substantial.
In the present study, the fact that the CIRMF
sun-tailed monkeys are kept within their geographical range, in a semifree-ranging setting, where they
move and forage freely might reduce the effects
linked to environmental conditions such as climate
and artificial housing, as well as the diet-related
bias. This unique setting might indeed represent
an ideal compromise between natural free-ranging
populations that are difficult to study, and captive
colonies, which preclude any investigation on natural processes. Hence, data emanating from this
colony, including the clinical biochemistry and hematology data presented here, will be useful in the further ecological, parasitological, and virological studies to be conducted in both CIRMF and free-ranging
populations of sun-tailed monkeys in Gabon.
ACKNOWLEDGMENTS
The authors thank the past and present staff
of the CIRMF Primate Center and the Laboratoire
d’Analyses Médicales for technical assistance, as
well as Simon Childs and Guillaume Le Flohic for
improving the English. The CIRMF is financed by
the Gabonese government, TOTAL Gabon, and the
Ministère Français des Affaires Etrangères et Européennes (M.A.E.E.). P.M., J.-P.G., and D.V. were
funded by the French Cooperation, French Embassy,
Gabon.
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