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Comparison of gut proportions in four small-bodied Amazonian cebids.

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American Journal of Primatology 35139-142 (1995)
Comparison of Gut Proportions in Four Small-Bodied
Amazonian Cebids
STEPHEN F. FERRARI' AND M. APARECIDA LOPES'
Departments of 'Genetics and 2Biology,Universidade Federal do Pa&, Belem, Brazil
Gut proportions in four small-bodied Amazonian cebids (Callicebus caligatus, Callicebus moloch, Pithecia irrorata, and Saimiri madeirae) are reported and compared in the context of known differences in feeding ecology. The gastrointestinal tracts of both Callicebus and Pithecia were found
to be relatively undifferentiated, as expected from their predominantly
frugivorous diets. In Saimiri, the marked dominance of the small intestine
correlates with a highly insectivorous diet. o 1995 Wiley-Liss, Inc.
Key words: Cebidae, gut proportions, diet
INTRODUCTION
The morphology of the gastrointestinal tract in primates varies systematically
in relation to feeding ecology [Chivers & Hladik, 1980; Martin e t al., 1985; MacLarnon et al., 19871. In broad terms, the relative size of the small intestine correlates negatively with the proportion of structural carbohydrates in the diet and
positively with that of high quality items such as animal material and seeds.
Chivers and Hladik [1980] record the gut morphology of a number of wildcaught platyrrhines from Panama, but quantitative data on South American taxa
are limited [Ayres, 1986; MacLarnon et al., 1987; Ferrari et al., 19931, especially
in comparison with Old World primates. The present study reports on the gut
proportions of eight wild-caught monkeys from western Brazilian Amazonia. The
specimens represent three of the four smallest-bodied cebid genera, including one
(Callicebus) that has not been studied previously. Gut proportions observed in all
specimens were consistent with both those of related taxa [Fooden, 1964; Chivers
& Hladik, 1980; Ayres, 1986; Ferrari, submitted], and the data available on feeding ecology [Kinzey, 1981; Happel, 1982; Terborgh, 1983; Oliveira et al., 1985;
Setz, 1987; Boinski, 1989; Peres, 19931.
METHODS
The adult specimens analyzed here were collected during a survey in the
Brazilian states of Amazonas and Rond6nia [Ferrari & Lopes, 19921. Two male
Saimiri madeirae [sensu Thorington, 19851, a female Callicebus moloch, and a
male Pithecia irrorata were collected a t Lago dos Reis, Amazonas (7"32'S,
Received for publication November 16, 1993; revision received April 15, 1994
Address reprint requests to Stephen F. Ferrari, Department of Genetics, Universidade Federal do Para,
Caixa Postal 8607, 66.075-150 Belem-PA, Brazil.
0 1995 Wiley-Liss, Inc.
140 I Ferrari and Lopes
TABLE I. Body Size and Gut Dimensions of C. caligatus, C. moloch, P. irrorata,
and S . madeirae
Body
weight
Length of
small intestine/
colon (mm)
Specimen
(d
length
(mm)
Total gut
area (an2)
C . caligatus
C. moloch
Female
Male
Mean
P. irrorata
S . madeirae
Male 1
Male 2
Male 3
Female
Mean
880
296
9441324
352.5
1,020
860
940
1,580
290
284
287
332
1,0561521
1,1681540
1,1121530.5
1,44017 17
564.0
624.7
594.4
711.0
1,010
880
970
820
920
280
264
272
246
265.5
1,2731190
1,1601178
1,241/148
1,0381125
1,1781160.25
471.2
369.1
268.1
245.9
338.6
62"52'W), and a male C. moloch and two S . madeirae (1male, 1female) a t Calama,
RondBnia (8"03'S, 62"53'W). Callicebus caligatus is represented by a male from Rio
Ipixuna, Amazonas (7"31'S, 63"22'W).
All specimens were weighed and measured (bregma to ischium) prior to removal of the gastrointestinal tracts. Measurements of the length and surface area
of gut compartments were carried out 2 to 4 h after death, following Chivers and
Hladik [1980] and Ferrari et al. [1993], and double-checked to ensure accuracy.
Specimens (stuffed skins and skeletocs) were deposited at the Goeldi Museum in
Belem [see Ferrari & Lopes, 19921.
RESULTS
Body weights and lengths of the eight specimens ranged between 820-1,580 g
and 246-332 mm, respectively (Table I). While there is a n overall tendency for gut
area to increase with body size, there are only weak correlations with body weight
(Spearman rank: r, = 0.60, P > 0.05, N = 8) and length (r, = 0.59, P > 0.051, and
the small size of the samples prohibits meaningful comparisons a t the species level.
There are, nevertheless, some interesting contrasts between S. madeirae and the
remaining specimens, especially in colon length (Table I).
The contrasts between taxa are further emphasized in the data on gut proportions (Table 11).The gastrointestinal tracts of Callicebus and Pithecia are somewhat undifferentiated (coefficient of gut differentiation [CGD] of 0.89-1.131, values highly characteristic of primate frugivores [Chivers & Hladik, 19801. S.
madeirae exhibits a relatively huge small intestine, by contrast, and a high degree
of differentiation more typical of mammalian faunivores (CGD < 0.50). S. madezrue body size, gut area, and CGDs are in fact closely similar to those recorded for
other Saimiri species [Chivers & Hladik, 1980; Ayres, 19861.
DISCUSSI 0N
As for other squirrel monkey species, gut proportions observed in S. madeirae
are consistent with a highly insectivorous diet [see Terborgh, 1983; Boinski, i9891.
The evidence presented here also suggests that Saimiri is more specialized for
insectivory than the callitrichids Callithrix and Saguinus [see Ferrari et al., 19931.
This is supported by differences in the foraging behavior of syntopic Saimiri and
Gut Proportions in Small-Bodied Amazonian Cebids I 141
TABLE 11. Surface Area of Gut Compartments and Coefficient of Gut Differentiation of
SDecimexis Described in Table I
Surface area (cm’)
SDecimen
C. caligatus
C . moloch
Female
Male
Mean
P. irrorata
S . madeirae
Male 1
Male 2
Male 3
Female
Mean
Coefficient
of gut
differentiation
(CGD)“
Stomach
Small
intestine
Caecum
Colon
66.5
(18.9)b
165.3
(46.9)
61.3
(17.4)
59.4
(16.8)
1.13
42.7
74.5
58.6
(9.9)’
286.1
329.7
307.9
(51.8)
180.6
165.7
173.2
(29.1)
0.97
0.89
0.93
84.0
(11.8)b
335.1
(47.1)
54.5
54.8
54.7
(9.2)
74.0
(10.4)
217.9
(30.7)
1.12
73.8
55.3
39.7
21.0
47.4
(14.0)’
322.2
252.9
180.4
189.8
236.3
(69.8)
18.2
13.2
9.5
9.7
12.7
(3.7)
57.0
47.7
38.5
25.4
42.1
(12.5)
0.46
0.46
0.49
0.30
0.43
“CGD = surface area of stomach
19801.
+ caecum + colonlsurface area of small intestine [following Chivers & Hladik,
bPercentage of total gut area.
‘Mean value as a percentage of mean total gut area.
Saguinus in Peru [Terborgh, 1983; Terborgh & Stern, 19871, especially during the
dry season period of resource scarcity.
While they are known to feed on arthropods, both Callicebus and Pithecia are
primarily frugivores [Kinzey, 1981; Happel, 1982; Terborgh, 1983; Oliveira et al.,
1985; Setz, 1987; but see Peres, 19931, and this is reflected in their gut proportions.
Gut passage rates in Pithecia, nevertheless, suggest that the digestion of low quality resources, such as leaves, may be important [Milton, 19841. Both genera are
also highly similar to the fourth small-bodied cebid, Aotus [Chivers & Hladik,
19801, whose diet is basically frugivorous [Wright, 19813. Pithecia also appears to
be far more similar in gut proportions to Aotus and Callicebus than to other pitheciines, Cacajao and Chiropotes [Fooden, 1964; Ayres, 1986; Ferrari, submitted], a s
might be expected from differences in their degree of specialization for seed predation [Kinzey, 19921.
CONCLUSIONS
1. Gut proportions in wild-caught Saimiri madeirae were typical of highly
insectivorous primates, including other Saimiri species.
2. Gut proportions recorded for Callicebus moloch, Callicebus caligatus, and
Pithecia irrorata were both typical of relatively unspecialized frugivores and similar to those of the fourth small-bodied cebid. Aotus.
ACKNOWLEDGMENTS
Data collection was authorized by IBAMA (special license 1404/90-31) and
supported by the John D. and Catherine T. MacArthur Foundation. We thank
142 I Ferraii and Lopes
Dionisio Pimentel Neto, David C. Oren, Cazuza Junior, Katharine Milton, and
three anonymous reviewers.
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