close

Вход

Забыли?

вход по аккаунту

?

Effect of life history on the squirrel monkey (Platyrrhini Saimiri) cranium.

код для вставкиСкачать
AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 97:435-449 (1995)
Effect of Life History on the Squirrel Monkey
(Platyrrhini, Saimiri) Cranium
WALTER CARL HARTWIG
Z)epartmen.t of AnatomicaE Sciences, State University of New York, Stony
Brook, New York 11794
KEY WORDS
Saimiri, Orbit, Ontogeny, New World monkeys,
Predation
ABSTRACT
Among primates, squirrel monkeys uniquely possess an interorbital fenestra, in which the midline bony orbitosphenoid septum is largely
absent and the soft tissues of the orbits are separated only by a thin membrane. Neural development may contribute t o the approximation of the orbits
to the midline in Saimiri, insofar as other platyrrhines with relatively large
brains also have relatively narrow interorbital spaces compared to their near
relatives. In Saimiri the narrow spacing of the orbits is further exacerbated
by intense predation pressure on infants that may select for precocial neonates. The result is a large-headed neonate that is subject to unusual parturition constraints. These parturition constraints apply to the size and dolichocephalic shape of the squirrel monkey head in general, and to the relatively
large eyes and approximated orbits in particular. The unique interorbital
condition in Saimiri is an example of the effects of life history on skeletal
morphology. o 1995 Wiley-Liss, Inc.
Stereoscopic vision requires overlapping
visual fields. This is accentuated by convergent orbits, and among mammals a decreased emphasis on olfaction has resulted
in relatively closely apposed orbits in primates, particularly anthropoid primates.
The squirrel monkey interorbital fenestra
(Fig. 1) is unique among primates and is
a rare, but not unknown, condition among
mammals (Haines, 1950). Hershkovitz
(1977) argued that thinning of the interorbital septum is typical of small New World
monkeys such as Saguinus, and that the condition in Saimiri was not a discrete character but rather an extreme expression along
a morphological continuum. Maier (1983)observed that the fenestra develops postnatally, presumably due t o secondary resorption of the septum by the closely apposed
musculature of the eye bulbs. This study
suggests that the unique approximation of
the eyes to the midline results from the large
relative brain size of squirrel monkeys and
the precocial nature of their prenatal devel0 1995 WILEY-LISS, INC.
opment. Cranial traits such as relative dolichocephaly and closely apposed orbits are
most likely the result of the need to pass a
precocial neonate, which already has a large
neurocranium, through the transverse diameter of the birth canal.
BACKGROUND
Schultz (1940, 1960) published the first
comparative, quantitative analysis of relative orbit and eye size in primates. In comparisons across major primate radiations,
Schultz (1940) correctly noted that larger
primates have relatively smaller orbits, and
he explicitly noted that orbit size and eye
size are not correlated in large-bodied animals; a measure of the bony orbit should not
substitute for an estimation of eye bulb size
Received June 30, 1994; accepted March 22, 1995.
Address reprint requests to Waiter Carl Hartwig, Department
of Anthropology, George Washington University, Washington,
DC 20052.
2 -
*
*
I
..
H
Saimiri
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
R
~
15.
16.
b
GENUS
Fig. 1. a: Oblique anterior view of Saimiri cranium, showing the fenestrated interorbital septum,
which is lined by membrane during life. b: Box plots of interorbital breadth in New World monkeys.
Saimiri (far right) has a narrower interorbital breadth than all modern anthropoids. Each box and
whiskers represents 95% of the sample. Asterisks represent outliers. See Table 1 for genus codes.
SQUIRREL MONKEY LIFE HISTORY
in these groups. He did not, however, compare orbit size to a measure of overall cranial
size, nor did he explore interspecific relationships within a radiation such as New
World monkeys.
Biegert (1963) laid further theoretical
groundwork and suggested that the potential for midline approximation of the orbits
was driven by the size of the intervening
nasal capsule. Maier (1993) has recently advanced this work in primates and demonstrated that the ossified parts of the nasal
capsule become the ethmoid bone and thus
do not directly contribute to the formation
of the interorbital septum, which is primarily an aspect of the orbitosphenoid (Maier,
1983).Considered broadly, primates with decreased reliance on olfaction develop smaller
nasal capsules and thus express a relative
narrowing of the interorbital space. It should
be pointed out that there is nothing unusual
about the food-processing habits or diet of
the squirrel monkey that would suggest that
the interorbital fenestra is due to a biomechanical advantage.
Specific discussions of the interorbital fenestra in squirrel monkeys essentially began
when a fossil cranium of Dolichocebus, a
New World monkey from the Oligocene of
Argentina, was fully prepared and appeared
to exhibit a homologous interorbital fenestra
(Rosenberger, 1979a; Hershkovitz, 1979).
Rosenberger (1979a) suggested that the
functional significance of the fenestra was
dubious, but neither he nor Hershkovitz
(1977, 1979) explained why the intriguing
morphology might exist.
The most detailed anatomical treatment
of the unusual interorbital morphology in
Saimiri is that of Maier (19831, who studied
an ontogenetic series of prenatal through
adult specimens. He demonstrated that the
interorbital septum does ossify, as evidenced
by fetal (Starck, 1960) and young postnatal
specimens with intact septa. The fenestration is an epigenetic phenomenon of steady
secondary resorption caused by the apposition of the relatively large eye bulbs and
their attendant musculature. In reference to
what is driving this phenomenon in squirrel
monkeys, Maier (1983) cited Cartmill’s
(1972) explanation that orbital convergence
is primarily connected with predatory hab-
437
its, but he also recognized that Saimiri was
not the only New World monkey that foraged
for insects via visual predation. He concluded that a reduction in the posterior nasal
capsule (Biegert, 1963;Maier, 1980), a characteristic of more encephalized primates
(Maier, 19931, also contributed to the condition of secondary fenestration. This study
agrees with Maier’s (1983) ontogenetic description of the fenestra, and attempts t o
explain its development in a bio-behavioral context.
Two hypotheses are considered here. As
noted by Cartmill (19721, increased orbital
convergence results in enhanced depth perception a t close range, but a t the expense of
depth perception at long range. Increased
convergence could lead to closer orbital approximation to the midline. Because squirrel
monkeys practice manual capture of insects
as a foraging behavior, a structural modification of the orbits that enhanced their ability
to resolve objects in three dimensions a t
close range would certainly be a selective
advantage. This possibility is evaluated here
in the context of laboratory studies of the
squirrel monkey visual system.
An alternative hypothesis is based on cranial morphometric data of other New World
monkeys and a consideration of squirrel
monkey life history. It is hypothesized that
the uniquely narrowed interorbital space
and fenestrated interorbital septum are
due t o growth constraints on the orbits imposed by a relatively large neurocranium
and the precocial condition of squirrel monkey neonates. This hypothesis predicts that
the relative sizes of the braincase and the
bony orbits will be large compared t o the
birth canal, and requires that a condition
of squirrel monkey life history explain the
precocial nature of their prenatal development.
MATERIALS AND METHODS
Morphometric data were collected on over
1,000 New World monkey crania (Table 1)
as part of a larger study (Hartwig, 1993).
These data were examined in order to determine if cranial size features were related to
orbital spacing across platyrrhines in general. Such comparison is facilitated by bivar-
438
W.C. HARTWIG
TABLE 1. Samwle size and distribution of ulatvrrhines used for moruhometric analysis'
Taxon
Alouatta
Aotus
Ateles
Brachyteles
Cacajao
Callicebus
Callimico
Callithrix
Cebuella
Cebus
Chil-opotes
Lagothrix
Leontopithecus
Pithecia
Saguinus
Saiiniri
Total
'N
=
N
M
F
28
133
110
4
44
125
10
56
11
110
15
78
13
41
145
174
1,097
12
45
40
2
22
63
16
81
68
2
21
49
4
20
8
43
8
35
3
13
64
65
500
number of individuals; M = males; F = females; S
5
32
3
66
7
43
9
25
75
108
557
=
subadults; Code
iate regressions of cranial dimensions on a n
estimate of size. The measurement of body
size used in the following allometric regressions is a surrogate derived from a composite
of three cranial measurements (total cranial
length, basion-prosthion, opisthocranionprosthion), which was determined to have
the best fit to a sample of 165 adult individuals across 14 genera for which known wildshot body weights were available. Reduced
major-axis regression of this composite
against the known body weights yielded a
slope value of 0.991 and a loss value of 0.181;
least squares regression on the same data
yielded a n r2 value of .977 and a standard
error of .047 (Hartwig, 1993). I t is recognized
that a morphometric composite will not represent size equally effectively for each genus.
The composite used here represents the closest match to known individual, wild-shot
body weights in the dataset, and was determined from numerous iterations of measurement combinations.
Neurocranium size is likewise estimated
from a composite of linear dimensions of the
neurocranium (maximum neurocranial
length, breadth, and height, postorbital constriction and biasterionic breadth). This
composite represents a reasonable surrogate
for cranial capacity as determined by filling
the braincase with sintered glass beads
(Martin, 1990), though here it is termed neurocranial size to avoid confusion with the
concept of cranial capacity as determined by
=
S
Code
2
20
17
2
6
5
1
1
2
28
2
5
1
5
15
16
128
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
numerical genus code for Figure l b .
brain weights. Other measurements used
are defined in Table 2.
Any explanation of a time-transgressive
phenomenon such as the evolution of a n unusual morphological character state cannot
be entirely deductive. The following analysis
uses analogies to cause and effect relationships in cranial development in New World
monkeys to interpret the most likely circumstances that have resulted in the squirrel
monkey interorbital fenestra. These circumstances involve intrinsic mechanisms such
a s the effect of relative brain size on the
positioning of the bony orbits, and extrinsic
mechanisms such as the size of the head
relative to the birth canal. These extrinsic
factors are mediated by aspects of squirrel
monkey life history that can be observed but
not directly tested. The results of the morphometric analysis are presented below, followed by a consideration of how those results
satisfy the predictions of the observed life
history causal mechanisms.
RESULTS
Orbital dimensions in
New World monkeys
Various measurements of the bony orbit
were observed in the sixteen genera of New
World monkeys in order to place the interorbital spacing of Saimiri in a comparative
context. As demonstrated in Figure l b ,
squirrel monkeys have a uniquely narrow
SQUIRREL MONKEY LIFE HISTORY
439
TABLE 2. Measurements used in this study
Variable
Definition
Neurocranial size
Body size surrogate
Biorbital breadth
Interorbital breadth
Palate length
(Maximum length, width, height of neuroeranium + biasterionic breadth
maximum postorbital constriction)/5
(Total skull length + basion-nasion + basion-opisthocranion)/3
Maximum breadth measured along outer margin of bony orbit
Dacryon-dacryon
Orale-alveolon
interorbital breadth. Within New World
monkeys, however, the uakari monkey (Cacajao) appears to have a relatively narrow
interorbital breadth, to the extent that its
absolute measurement is in the range of
platyrrhines of much smaller body size (Aotus, callitrichines). Because Cacajao belongs
to the Pitheciinae, a well-defined subfamily
of very closely related New World monkey
genera (Kinzey, 1992; Schneider et al.,
1993),a more detailed look at orbital spacing
in this group may serve as a case study for
changes in orbital positioning in the context
of a known phylogeny.
Orbital spacing in pitheciine
New World monkeys
The crania of pitheciine genera (Pithecia,
Chiropotes, and Cacajo) are remarkably similar t o one another except for key features
of the neurocranium and orbit, for which Cacajao is considered to represent the derived
condition (Hershkovitz, 1977; Rosenberger,
1992; Hartwig, 1993). Pitheciines are characterized by a distinctive masticatory morphology (Rosenberger, 1992) reflecting an
unusual and highly specialized diet common
to all three genera (Kinzey, 1992). These
morphological traits include parallel postcanine toothrows, large, projecting canines,
and procumbent upper incisors. In the upper
face and braincase, however, the differences
between Pithecia and Cacajao are distinct
(Fig. 2a; Chiropotes, which is similar to Cacajao in most aspects of cranial morphology,
is excluded in the following comparisons due
to small sample size). Orbit width is relatively greater than would be expected in the
larger cranium of Cacajao, but biorbital
breadth is interspecifically scaled with Pithecia (Fig. 2b-e). As expected, then, interorbital breadth is absolutely, and thus, relatively, narrower in Cacajao.
Neurocranial differences are illustrated
+
through a composite measure of neurocranial size, which clearly demonstrates the relatively large neurocranium of Cacajao when
compared to Pithecia (Fig. 3a). Uakaries
have larger neurocrania than would be expected for a pitheciine of their overall cranial
size. Across all platyrrhines, pitheciines as
a subfamily express a typical range of values
for neurocranial size (Fig. 3b). The fact that
a relative increase in neurocranial size is
correlated with a relative decrease in interorbital breadth among these closely related
genera supports the hypothesis that the relatively large neurocranial size of Saimiri is
responsible for its relatively closely spaced
orbits. This extends a general trend in anthropoids in which increased relative temporal and frontal lobe size results in a repositioning of the orbital cavity inferior and
medial to the anterior and middle cranial
fossae (Rosenberger, 1985).According to Ravosa (1991, p. 389), “this places greater constraints on the position of the anthropoid
orbit, which necessarily becomes more fully
integrated with morphological variation in
the basicranium.”
Implications for Saimiri
The data for Pithecia and Cacajao suggest
that neural development may influence ultimate orbital positioning in other New World
monkeys. Neural development in Sairniri
has been reviewed from structural and behavioral perspectives by several authors
(Bauchot and Stephan, 1969;Hemmer, 1971;
Elias, 1977; Kaack et al., 1979; Manocha,
1979; Rosenberger, 1979b; Bauchot and Manocha, 1981; Leutenegger, 1982; Stephan et
al., 1986; Harvey et al., 1987; Boinski and
Fragaszy, 1989; Martin, 1990; Pucciarelli
et al., 1990; Corner and Richtsmeier, 1992).
Most studies suggest that Saimiri has a relatively capacious neurocranium, but differ in
how this is measured and how they rank
a
1 cm
1 cm
Cucujao
Pifheciu
3.90
3 82
3.58
30
b
I
I
3s
40
350
--L--
4s
SU
-
I
I
412
424
448
460
SIZE
Body size (from cranial composite)
0 50
I
436
~
,
1
1
I
412
424
436
448
0,
Q
2
e
-2
!s
045
.s
040
*
E
035
0
e
0
030
2
m
0 25
5
d
Cacajao
21
400
14
Pithecia
e
Fig. 2
1
4.60
SIZE
441
SQUIRREL MONKEY LIFE HISTORY
Saimiri against other New World monkeys.
Clearly, the estimation and implications of
relative brain size are fundamental problems in evolutionary biology. While recognizing these problems, the objective here is to
assess the possible relationship between size
of the neurocranium and approximation of
the bony orbits in New World monkeys.
I n a regression of mean values for brain
weight on body weight in twelve New World
monkey genera, Saimiri appears to have a
relatively large brain compared to other genera (Fig. 4;Table 3). When more recent body
weight estimates and data from Elias (1977)
are used, Saimiri and Cebus both appear to
have relatively large brains (Fig. 4b). Body
weight estimates for the larger New World
monkeys are currently in dispute (Peres,
19941, and figures used as mean body
weights differ markedly across studies, as
do exactly what aspects of the brain are retained for weighing.
When Martin's (1990) modulus equation
for inferring cranial capacity from linear
craniometric data is applied to the present
dataset (Table l),Saimiri stands out as a
platyrrhine with a relatively large neurocranium (Fig. 3b). In the absence of a perfect
measurement of relatively neurocranial size,
data derived from measuring museum skeletal material do reliably demonstrate that
Saimiri has a relatively large neurocranium
among New World monkeys. Short of asserting that it has the relatively largest neurocranium, the morphometric data presented here are at least consistent with
published studies of brain and body weight
means (Bauchot and Stephan, 1969; Elias,
1977; Manocha, 1979; Stephan et al., 1986;
Fig. 2. Comparisons of orbital size and spacing in
Pithecia and Cacajao (a).For biorbital breadth (b),neither Pithecia nor Cacajao has a n unusual distribution
compared to other New World monkeys or to each other
(c) in log-log regressions against a body-size surrogate.
Rather, the observation that Cacajao has relatively
larger orbits is reflected in measurements of size-corrected interorbital breadth (d) and single orbit breadth
(e). Both absolutely and relatively (d; P < .Ol), Cucujao
has narrower interorbital breadth than Pithecia. Ellipses represent 90% of the sample. Figure 2a was drawn
by Luci Betti-Nash.
-
42
41
I
I
I
~
.-N
0
Y)
~
E 40
I
e
5
2
~
39
38 -
31
L
~
412
I
1
424
436
L.J
4.48
460
Body size (from cranial composite)
44
~
40 0
p!
a
1,
2
I+
36
-
2
2
2
32
~
35
40
45
50
Body size (from cranial composite)
Fig. 3. Log-log regression ofneurocranial size, a composite measurement representing cranial capacity in Pithecia and Cucujuo (see Table 2). Unlike measurements
of the face, Cucujuo has a relatively larger neurocranium
than would he expected from extending the ontogenetic
scaling of Pithecia (a). In order to verify that Pithecia
is not unusually small-brained, thus defeating the comparison, a broad interspecific regression is shown (b),
in which only Saimiri appears to have a relatively large
neurocranium. Ellipses represent 90% of the sample.
Harvey e t al., 1987; Martin, 1990; see Table 3).
Relative neurocranial size is thus associated with orbital approximation in Saimiri
and it fits a pattern established i n uakari
monkeys. The interorbital distance in Saim-
442
W.C. KARTWIG
iri, however, is absolutely narrow for anthro-
I
I
poid primates, while its degree of relative
brain size is not similarly extreme. Therefore, while large relative brain size may explain the baseline condition of interorbital
spacing in Saimiri, other mechanisms probably underlie the extreme degree to which
the orbits are approximated and the interorbital fenestra is manifested.
I
I
C
+
*
R
x
DISCUSSION
Orbital approximation and vision in the
squirrel monkey
0
*
Improvedvisual performance would be the
I
I
I
I
most direct, adaptive, selectionist explana5
6
I
8
4
9
Mean body weight I (g)
tion for the unusual squirrel monkey interor- a
I
I
I
bital morphology. Orbital approximation to
the midline, however, would not contribute
to enhanced stereoscopy or visual acuity. If
00
squirrel monkeys displayed a n unusual level
of visual performance, the size and disposic
tion of their eye bulbs may be explained as c
+
a consequence or artifact of such a condition. .eo
D
*
Data generated by studies of the squirrel
0
monkey visual system are particularly relevant to the hypothesis that enhanced visual c
x
performance may be a n underlying cause of
0
5 2
its closely approximated orbits.
I
In electrophysiological comparisons with
*
macaques, squirrel monkeys present similar
central visual field capacities (Doty et al.,
1 -1
I
I
9
19641, which may indicate that they are ca4
5
6
I
8
pable of resolving a finer retinal image given b
Mean body weight I1 (g)
their smaller eye diameter and total extent
Cebuella
0Aofirs
of unilateral striate cortex (Cowey and Ellis,
0
Cuiliihrk
0Cebzu
1967, 1969). The same studies, however,
Cuiiimico
Pirhecia
measure mean visual acuity in rhesus macaques as superior to that in squirrel monkeys, who moreover demonstrate poorer peSuimin
Aides
ripheral, parafoveal, and foveal acuity (Rolls
Cullicebus
- Lagofhrrr
and Cowey, 1970). Another study (Ordy and
Samorajski, 1968) ranked the thresholds at
Fig. 4. Log-log regressions of species brain and body
which separate objects could be discrimi- weight means in-selected New World monkey genera,
nated in Saimiri, Callithrix, Lemur, and Tu- from Stephan et al. (1986) and Ford and Davis (1992). a:
Data are taken directly from Stephan et al. (19861, and
paia a s comparable to one another and to demonstrate
that Saimiri has a relatively large brain
values for catarrhines, including humans. weight for a given mean body weight. This regression
To the extent that depth perception can be largely matches that derived morphometrically in Figure
measured in laboratory primates, the 3. Due to differences in reported mean body weights, rethreshold for depth discrimination in squir- vised body weight means reported by Ford and Davis
and data from Elias (1977) are compared to the
rel monkeys appears to be the same as that (1992)
Stephan et al. (1986) brain weight data in b. In this refor humans (Schmidt, 1968; Jacobs, 1985). gression Sairniri and Cebus clearly display relatively
The possibility that depth perception in large brains. See Table 3 for raw data and species names.
I
~
D
0
L
I
+
a
;I
443
SQUIRREL MONKEY LIFE HISTORY
TABLE 3. Brain and body weights in selected ptatyrrhine genera'
Taxon
Cebuetta pygmaea
Callithrir jacchus
Saguinus oedipus
Catlimico goetdii
Saimiri sciureus'
Saimiri sciureus3
Aotus triuirgatus
Callicebus rnoloch
Pithecia monachus
Cebus albifrons
Cebus a t b i f r o d
Lagothrix tagotricha
Alouatta senicutus
Ateles geoffroyi
Brain
weight (g)
4.15
7.60
10.00
11.00
24.12
23.30
17.10
19.00
35.00
71.00
66.8
101.00
52.00
108.00
Body
weight I (g)
Body
weight I1 (g)
Ratio I
(brain wtbody wt I)
Ratio I1
(brain wthody wt 11)
123
257
420
389
675
667
934
920
2,348
2,265
2,060
7,695
6,767
7,704
,035
.027
.026
,034
,030
.024
120
280
380
480
660
830
900
1,500
3,100
-
5,200
6,400
8,000
,023
.028
,037
,036
,035
,018
,021
,015
,031
,032
,013
,008
.014
,021
,021
,023
,023
,019
.008
,013
'Brain weight and body weight I from Stephan et al. (19861, body weight I1 from Ford and Davis (19921, except as specified.
zBrain weight data for 8 females from Manocha (1979).
3Brain weight and body weight data from Elias (1977).
Saimiri is qualitatively different from depth
perception in other primates still exists, but
laboratory measures of vision have failed to
demonstrate this to date. Indeed, laboratory
studies of the squirrel monkey indicate no
unusual functional or performance features
of the visual cortex, depth perception, or visual acuity (Allman and McGuinness, 1986).
Saimiri ontogeny and behavioral ecology
Field studies on Saimiri and other New
World monkeys indicate that squirrel monkeys occupy a niche subject to unpredictable
food supply and distribution ("erborgh,
1983), and to intense predation pressure
(Boinski, 1987a). These conditions factor
prominently in a life-history model of ecological risk aversion strategies that affect maturation patterns in primates (Janson and van
Schaik, 1993).Aspects of squirrel monkey behavioral ecology suggest that growth trajectories resulting in precocial neonates may be
advantageous. The following section details
prenatal and postnatal neural growth trajectories in squirrel monkeys in the context of
their life history and behavioral ecology.
Ontogeny
Squirrel monkeys appear to have a relatively long gestation period compared to
other New World monkeys and to many Old
World monkeys. The mean gestation length
of 170 days for Saimiri is greater than that
for all New World monkeys except the large-
bodied atelines, and is comparable to the
range of 162-187 days reported for the Old
World monkey genera Macaca, Cercocebus,
Papio, Cercopithecus, Nasalis, and Presbytis
(Ardito, 1976; Brizzee and Dunlap, 1986;
Harvey e t al., 1987). It should be noted that
a wide range of gestation lengths in captive
squirrel monkeys has been reported (Boinski, 1987a), and one study that controlled for
precise date of conception reported gestation
lengths in the 145-155 day range (Kerber
et al,. 1977). Gestation length in Aotus,
which is slightly larger than Saimiri (Table
31,is 133days, as would be predicted from a
regression for anthropoid primates (Martin,
1992). The preponderance of published data,
whether measured in captive animals or estimated in the wild, however, suggests relatively long gestation lengths in Saimiri (see
compiled data in Brizzee and Dunlap, 1986).
It seems that selection for relatively precocia1 neonates via extended gestation plays a
role in determining neonatal size in Saimiri.
The large size of the Saimiri neurocranium a t birth and its apparently rapid maturation after birth are unusual features for
New World monkeys. Most New World monkeys display isometric ontogenetic scaling
between sub-adults and adults for neurocranial size. This relationship does not obtain for squirrel monkeys (Fig. 5 ) . At birth,
female squirrel monkey brains are fully 62%
of adult brain weight (Elias, 1977; see also
Manocha, 1979), whereas in Cebus neonatal
W.C. HARTWIG
444
3.90
I
I
I
I
3.82
Sub-adult
6)
.A
N
m
F0
3.74
s
.r(
E
f!
0
s
3.66
2
0
0
3.58
3.50
3.6
I
I
I
I
3.7
3.8
3.9
4.0
4.1
Body size (from cranial composite)
Fig. 5. Log-log regression of neurocranium size on a composite measure of body size in subadult and
adult Sairniri, illustrating the early onset of adult neurocranium size in squirrel monkeys.
brain weight is less than 50% adult size
(Elias, 1977). These studies also indicate
that there is negligible brain weight increase
in squirrel monkeys beyond 60 days postnatally, while in Cebus brain growth rate is
slower and the duration of growth is much
longer (Elias, 1977;Manocha, 1979;Bauchot
and Manocha, 1981; Harvey et al., 1987).
The obstetric complicationsof giving birth
to a precocially large-brained neonate may
play a role in its unusual, arguably compromised, interorbital morphology. Among anthropoids, Saimiri neonates have the largest
neurocranial breadth dimensions as a percentage of transverse diameter of the female
pelvic inlet (Leutenegger, 1982). Likewise,
neonate neurocranial length is substantially
greater (136%)than is the corresponding sagittal dimension of the pelvic inlet.
Leutenegger (1982) suggested that during
birth non-human primates may pass
through the pelvic inlet in a “face-first”orientation, such that the head is extremely
dorsiflexed and cranial height rather than
cranial length must pass through the sagittal dimension of the pelvic inlet. Once past
the pelvic inlet, the head “relaxes”to assume
a typical delivery position of vertex distal,
occiput posterior, in reference to the nonhuman primate pelvic outlet. One study described the presentation of two normal squirrel monkey births in captivity in this manner
(Bowden et al., 1967).
A reorientation of the neonatal cranium
can mitigate stress on the sagittal axis of
the pelvic inlet during birth, but no simultaneous repositioning in order to relieve the
other pelvic inlet diameters is possible.
Thus, the transverse axis of the pelvic inlet
is still subject to the passage of the breadth
of the neonatal cranium. A compromise between pelvic inlet transverse diameter and
445
SQUIRREL MONKEY LIFE HISTORY
a neonate with a relatively large brain may
be the relatively dolichocephalic shape of the
Saimiri neurocranium, in which cranial
breadth is minimized. The Saimiri brain is
relatively larger than the brain of like-sized
Aotus and Callicebus, but is packaged in a
relatively longer, rather than relatively
longer and wider, neurocranium (Hartwig,
1993). It is suggested here that extreme orbital approximation in the squirrel monkey
is a function of the need to package the orbits
of a relatively large neonate in a transverse
dimension that is constrained by the size of
the pelvic inlet.
Data on biorbital breadth in neonatal
squirrel monkeys are not available. Data collected by Leutenegger (1973, 1982) and
Schultz (1940, 1960) demonstrate that the
neurocranium of squirrel monkey neonates
is in general quite large compared to the
birth canal, and that adult squirrel monkeys
have relatively capacious orbits and relatively voluminous eye bulbs compared to
other anthropoids. Given that squirrel monkeys are precocial at birth as demonstrated
by cranial morphometric and body weight
data, it is safe to hypothesize that the relationship between biorbital width and neurocranial width in neonates is not radically
different from that expressed in the subadults measured for this study.
These data for subadults (Fig. 6) indicate
that the biorbital breadth dimension in
squirrel monkeys does increase postnatally
in a typical pattern of ontogenetic scaling.
That is, at birth, biorbital breadth in the
squirrel monkey is slightly smaller than is
neurocranial breadth, t o a degree that is relatively smaller than is the condition in
adults. This observation satisfies the expectations of a hypothesis of parturition constraints. If the extremely narrow interorbital space in squirrel monkeys is a result
of the limits imposed by the transverse diameter of the birth canal, then neonatal biorbital breadth would be expected to be narrower than the canal rather than narrower
than the neurocranium, which can be deformed to a more narrow dimension during birth.
Leutenegger (1982) reported that the
squirrel monkey neonatal neurocranium
was 121%wider than the transverse diame-
1
'
06l-
I
1
a
2.
Subadult
3.60- 1
Adult
I
I
I
I
352 -
5
W
m
a
m
*
*
Adult
344 -
.-
336 -
328 -
320
34
b
I
I
I
I
I
I
I
35
36
31
38
39
40
41
42
Body size (from cranial composite)
Fig. 6. Biorbital breadth in subadult squirrel monkeys is relatively more narrow compared to neurocranial
breadth than is the condition in adults (a).Expansion of
biorbital breadth ontogenitically is depicted in b. These
comparisons suggest that neonatal biorbital breadth is
on the order of 25-30% more narrow than is neonatal
neurocranial breadth, which itself is reported to be 121%
the size of the transverse diameter of the pelvic canal
through which it must pass (Leutenegger, 1982).
ter of the birth canal, thus necessitating its
inward deformation during birth. Figure 6
indicates that biorbital breadth in subadult
(and, by inference, neonatal) squirrel monkeys is roughly 25% narrower than neurocranial breadth. This value is almost identical with the minimal difference required if
446
W.C. HARTWIG
the orbits are t o pass through the birth canal
without deforming.
It should be noted that these conditions do
not apply to neonates of the only nocturnal
anthropoid, Aotus, which are typically
platyrrhine in relative body size, brain size,
and altriciality (Harvey et al., 1987).Aotus
neonates are absolutely smaller than Saimiri neonates, whileAotus adults are, on average, absolutely larger than Saimiri adults.
Aotus adults display greatly enlarged orbits
but not unusually narrow interorbital
breadths (Fig. lb). Thus, despite having
greatly enlarged orbits as part of their adaptation to nocturnality, night monkeys do not
exhibit an interorbital fenestra. This is most
likely due to lateral expansion of the orbital
margin enabled by more relative postnatal
growth and by the absence of any spatial
constraint during parturition.
Behavioral ecology
Independent studies have indicated that
Saimiri neonates have a relatively large
brain and are born in a relatively precocial
state after a relatively long gestation. These
measurable characteristics of the reproductive biology of the squirrel monkey may be
explained through their behavioral ecology
and natural history.
Terborgh (1983) described the Saimiri
populations of Cocha Cashu, Peru, as temporary patch specialists who exploit ephemeral
resources described as unpredictable in location, of fluctuating abundance, and generally found and eaten by single individuals
(Boinski and Fragaszy, 1989). Their social
organization seems to be one in which every
individual forages for itself within a large
group assembly that lacks hierarchy or
unity. Squirrel monkey infants appear to forage independently at a relatively early age.
In their field study in Costa Rica, Boinski
and Fragaszy (1989) reported that squirrel
monkeys foraged successfully at 7 weeks of
age, first attempted to capture mobile prey
at 11weeks, and were weaned by 16 weeks.
Moreover, they observed very little social influence on foraging behavior and no food provisioning of infants by mothers or other troop
members. Elias (1977) found that captive
squirrel monkeys achieved locomotor and
manipulative skills far earlier than did captive capuchins of similar chronological ages.
The seasonal timing of foraging independence is also relevant here. Boinski (1987a)
reported that squirrel monkey births at her
field site were extremely synchronous within
troops, and occurred such that infants matured t o foraging independence at a time
when arthropod and fruitlflower abundance
reached annual highs (see also Coe and Rosenblum, 1978). Relative resource abundance is likely the primary influence on birth
synchrony in Saimiri, but Boinski (1987a)
noted an important secondary influence, intense predation by raptors, that more directly relates to infant size and precociality.
She noted that predation attempts by raptors were targeted almost exclusively at infants. Squirrel monkey infants are carried
dorsally, and thus are particularly susceptible to predation by aerial strike. Relatively
larger infants, as products of extended gestation, would be less obvious prey choices for
smaller predacious birds, and would stand
a better chance of surviving attacks by larger
raptors (Janson and van Schaik, 1993;Boinski, personal communication).
Given the combination of the low density
and patchy distribution of resources in squirrel monkey habitats (Boinski, 1987b;Janson
and Boinski, 1992), the “every individual for
itself‘ foraging behavior (Terborgh, 19831,
seasonal fluctuations in food availability
(Boinski, 19891,and early onset of infant foraging independence (Boinski and Fragaszy,
19891, a developmentally precocial neonate
would seem to be a logical component of
Saimiri behavioral ecology and adaptation.
The differential survival of precocial neonates during periods of intense infant predation pressure may further influence the reproductive biology of wild squirrel monkeys
(Boinski, 1987a).
The extended gestation and rapid maturation during an abbreviated infancy (Elias,
1977) follow the Janson and van Schaik
(1993) model of ecological risk aversion. The
Janson and van Schaik (1993) model argues
that juvenile growth will be slowed in group
living species subject to conditions of intense
predation pressure and intraspecific competition for resources. Because risk of predation is greater at the periphery of a group,
447
SQUIRREL MONKEY LIFE HISTORY
juveniles will tend to stay in the more protective center, where intraspecific competition
for resources is greatest. According to the
model, juvenile growth is adjusted to a
slower rate in order to lower metabolic needs
to a level that can be met by the inefficient
foraging techniques of juveniles competing
with adult conspecifics. It is suggested here
that the period of infancy in squirrel monkeys is the period in which the risk of predation is most critical, and any mechanisms
that reduced the duration of this period
would be selectively advantageous. Squirrel
monkeys appear to reduce this period via a
combination of extended gestation and early
onset of juvenility, at which time squirrel
monkeys are already competent foragers
and virtually full-sized. It is within this biobehavioral continuum that the unusual interorbital fenestra is explained most effectively.
SUMMARY
Ontogenetically, the sequence of events
leading to the unusual interorbital morphology in Saimiri would seem to involve:
a fetal brain that is relatively large at
birth (Harvey et al., 1987);
a developing eye that is relatively larger
in Saimiri adults than in all diurnal anthropoids (Schultz, 1940; Biegert, 1963);
obstetric constraints imposed by a relatively large natal neurocranium (Leutenegger, 1982) that are partially absorbed
by the dolichocephalic neurocranial contour and closely apposed orbits of the
Saimiri cranium; and
secondary resorption of the interorbital
septum postnatally due to approximation
of the eye bulbs and attendant musculature to the midline (Maier, 1983).
The preponderance of data suggest that
squirrel monkey infants must be able to forage independently at a very young age, presumably to survive intraspecific competition
for food and to reduce risk of predation during the dependent infancy period when they
are carried dorsally. These pressures are incompatible with a primate life history strategy in which infants mature slowly and are
a sustained energy cost to their mothers in
terms of “typical” primate lactation and ma-
ternal transport patterns. It would appear
that squirrel monkeys enter the growth period ofjuvenility, here considered to be equivalent to the onset of foraging independence,
as soon a s possible. The large but loosely
knit squirrel monkey troops would seem to
exist for the benefit of group defense, though
clearly at the aggravation of intraspecific
competition for food resources. To this extent
squirrel monkeys conform to the ecological
risk aversion model of Janson and van
Schaik (19931, though with particular reference to the infancy, rather than juvenile,
phase of life history.
CONCLUSIONS
Enhanced stereoscopy does not appear to
be a cause or effect of close approximation of
the eyes in the squirrel monkey. Its uniquely
closely apposed orbits result proximately
from the effects of having a relatively large
brain and reaching a precocial state of development prenatally. These effects intersect
with obstetric constraints imposed by the
absolute limits of the pelvic inlet. Compromise of midline interorbital breadth and
bony interorbital separation of the eyes reflects the potential of the midline craniofacia1 complex to absorb such growth outcomes. Ultimately, this derived perinatal
growth trajectory results from survival
pressures imposed by a niche in which a
small-bodied primate exploits unpredictable, widely dispersed food resources and is
subject to intense predation pressure.
ACKNOWLEDGMENTS
Alfred L. Rosenberger first encouraged me
to consider life history aspects of Saimiri
before attempting to explain its unusual cranial morphology. Conversations with him
and John Fleagle have greatly improved my
understanding of New World monkey natural history and my appreciation for a developmental approach to comparative anatomy.
Their comments and those of two anonymous
reviewers greatly improved the manuscript.
Steve Leigh, Sue Boinski, Katie Milton, and
Matt Ravosa also provided useful suggestions. For access to specimens under their
care I thank Bruce Patterson of the Field
Museum of Natural History, RDE MacPhee
448
W.C. HARTWIG
Elias MF (1977)Relative maturity of Cebus and squirrel
monkeys at birth and during infancy. Dev. Psychohiol. 10:519-528.
Falk D (1979) Cladistic analysis of New World monkey
sulcal patterns: Methodological implications for primate brain studies. J . Hum. Evol. 8:637-645.
Ford SM, and Davis LC (1992) Systematics and body
LITERATURE CITED
size: Implications for feeding adaptations in New
Allman J, and McGuinness E (1986) Visual cortex in
World monkeys. Am. J . Phys. Anthropol. 88:415-468.
primates. In HD Steklis, and J Erwin (eds.): Compara- Haines RW (1950)The interorbital septum in mammals.
tive Primate Biology, Volume 4: Neurosciences. New
J . Linnaean SOC.London 41585407.
York Alan R. Liss, Inc., pp. 279-326.
Hartwig WC (1993) Comparative Morphology, Ontogeny
Ardito G (1976) Checklist of the data on the gestation
and Allometry of the Platyrrhine Cranium. Unpublength of primates. J . Hum. Evol. 5:213-222.
lished Ph.D. dissertation. Berkeley: University of CalBauchot R, and Manocha SL (1981) La croissance enifornia.
cephalique chez Saimiri sciureus (Simiens, Cebides). Harvey P, Martin RD, and Clutton-Brock TH (1987) Life
Mammalia 45:251-255.
histories in comparative perspective. In BB Smuts,
Bauchot R, and Stephan H (1969) Encephalisation et le
DL Cheney, RM Seyfarth, RW Wrangham, and TT
niveau evolutif chez les simiens. Mammalia
Struhsaker (eds.) Primate Societies. Chicago: Univer33:225-275.
sity of Chicago Press, pp. 181-196.
Biegert J (1963) The evaluation of characteristics of the
Hemmer B (1971)Beitrag zur Erfassung der progressioskull, hands and feet for primary taxonomy. In Washnen Cephalisation bei Primaten. Proc. 3rd Int. Congr.
burn SL (ed.): Classification and Human Evolution.
Primatol. 2:99-107.
Chicago: Aldine, pp. 116-145.
Hershkovitz P (1977) Living New World Monkeys, VolBoinski S (1987a) Birth synchrony in squirrel monkeys
ume 1,with a n Introduction to the Primates. Chicago:
(Saimiri oerstedi). A strategy to reduce neonatal predUniversity of Chicago Press.
ation. Behav. Ecol. Sociobiol. 21:393-400.
Hershkovitz P (1979) Supposed squirrel monkey affniBoinski S (1987b) Habitat use by squirrel monkeys
ties of the late Oligocene Dolichocebus gainanensis.
(Saimiri oerstedi) in Costa Rica. Folia Primatol.
Nature 298:201-202.
49:151-167.
Jacobs GH (1985) Visual system of the squirrel monkey.
Boinski S (1989) The positional behavior and substrate
In LA Rosenblum, and CL Coe (eds.): Handbook of
use of squirrel monkeys: Ecological implications. J.
Squirrel Monkey Research. New York Plenum Press,
Hum. Evol. 18:659-678.
pp. 271-293.
Boinski S, and Fragaszy DM (1989) The ontogeny of
foraging in squirrel monkeys, Saimiri oerstedi. Anim. Janson CH, and Boinski S (1992) Morphological and
behavioral adaptations for foraging in generalist priBehav. 37:415-428.
mates: The case of the cebines. Am. J . Phys. AnthroBowden D, Winter P, Ploog D (1967) Pregnancy and
pol. 88:483-498.
delivery behavior in the squirrel monkey (Saimiri sciJanson CH, and van Schaik C (1993) Ecological
ureus) and other primates. Folia Primatol. 5:l-42.
risk aversion in juvenile primates: Slow and steady
Brizzee KP, and Dunlap WP (1986) Growth. In WR Duwins the race. In ME Pereira and LA Fairbanks (eds.):
kelow, and J Erwin (eds.):Comparative Primate BiolJuvenile Primates: Life History, Development, and
ogy, Volume 3: Reproduction and Development. New
Behavior. New York: Oxford University Press, pp.
York: Alan R. Liss, Inc., pp. 363413.
57-76.
Cartmill M (1972) Arboreal adaptations and the origin
ofthe order Primates. In Tuttle R (ed.): The Functional Kaack B, Walter L, and Brizze KR (1979) The growth
and development of the squirrel monkey (Saimiri sciand Evolutionary History of Primates. Chicago: Alureus). Growth 43; 116-135.
dine, pp. 97-122.
Coe CL, and Rosenblum LA (1978) Annual reproductive Kerber WT, Conaway CH, and Moore-Smith D (1977)
The duration of gestation in the squirrel monkey
strategy of the squirrel monkey (Saimiri sciureus).
(Saimiri sciureusj. Lab. Anim. Sci. 27:700-702.
Folia Primatol. 29:19-42.
Corner BD, and Richtsmeier J T (1992)Cranial growth in Kinzey WG (1992) Dietary and dental adaptations in
the Pitheciinae. Am. J.Phys. Anthropol. 88r499-514.
the squirrel monkey (Saimiri sciureus):A quantitative
Leutenegger W (1973) Maternal-fetal weight relationanalysis using three dimensional coordinate data. Am.
ships in primates. Folia Primatol. 20:280-293.
J . Phys. Anthropol. 87167-82.
Leutenegger W (1982) Encephalization and obstetrics
Cowey A, and Ellis CM (1967)Visual acuity of the rhesus
in primates with particular reference to human evoluand squirrel monkeys. J . Comp. Physiol. Psychol.
tion. In E Armstrong, and D Falk (eds.):Primate Brain
64~80-84.
Evolution, Methods and Concepts. New York: Plenum
Cowey A, and Ellis CM (1969) The cortical representaPress, pp. 85-95.
tion of the retina in the squirrel and rhesus monkeys
and its relation to visual acuity. Exp. Neurol. Maier W (1980) Nasal structures in Old and New World
24:374-385.
primates. In R Ciochon, andAB Chiarelli (eds.):EvoluDoty RW, Kimura DS, and Mogenson GJ (1964) Photitionary Biology of the New World Monkeys and Contically and electrically elicited responses in the central
nental Drift. New York: Plenum Press, pp. 219-241.
visual system of the squirrel monkey. Exp. Neurol. Maier W (1983) Morphology
.
-. of the interorbital region
- of
IOr19-51.
Saimiri sciureus. Folia Primatol. 41:277-303.
of the American Museum of Natural History,
Richard W. Thorington of the National Museum of Natural History, and their respective staffs.
SQUIRREL MONKEY LIFE HISTORY
Maier W (1993) Zur evolutiven und funktionellen Morphologie des Gesichtsschadels der Primaten. Z. Morphol. Anthropol. 79:279-299.
Manocha SL (1979) Physical growth and brain development of captive-bred male and female squirrel monkeys, Saimiri sciureus. Experientia 35:96-98.
Martin RD (1990) Primate Origins and Evolution.
Princeton: Princeton University Press.
Martin RD (1992) Goeldi and the dwarfs: The evolutionary biology of the small New World monkeys. J . Hum.
Evol. 22t367-393.
Ordy J, and Samorajski T (1968)Visual acuity and ERGCFF in relation to morphologic organization of the
retina among diurnal and nocturnal primates. Vision
Res. 8:1205-1225.
Peres CA (1994) Which are the largest New World monkeys? J . Hum. Evol. 26245-250.
Pucciarelli HM, Dressino V, and Niveiro MH (1990)
Changes in skull components of the squirrel monkey
evoked by growth and nutrition: An experimental
study. Am. J. Phys. Anthropol. 81.535-544.
Ravosa MJ (1991) Interspecific perspective on mechanical and non-mechanical models of primate circumorbital morphology. Am. J. Phys. Anthropol. 86:369-398.
Rolls ET, and Cowey A (1970) Topography of the retina
and striate cortex and its relationship to visual acuity
in rhesus monkeys and squirrel monkeys. Exp. Brain
Res. 1Ot298-310.
Rosenberger AL (1979a) Cranial anatomy and implications of Dolichocebus, a late Oligocene ceboid primate.
Nature 279:416-417.
Rosenberger AL (197913) Phylogeny, Evolution and Classification of the New World Monkeys (Platyrrhini, Primates). Unpublished Ph.D. dissertation. New York:
City University of New York.
449
Rosenberger AL (1985) In support of the NecrolemurTarsier hypothesis. Folia Primatol. 45:179-194.
Rosenberger AL (1992) Evolution of feeding niches in
New World monkeys. Am. J. Phys. Anthropol.
88525-562.
Schmidt U (1968) Untersuchungen zur visuellen Raumorientierung bei TotenkopfAffen (Saimiri sciureus). 2.
Vergleich. Physiol. 60:176-208.
Schneider H, Schneider MPC, Sapaio I, Harada ML,
Stanhope M, Czelusniak J , and Goodman M (1993)
Molecular phylogeny of the New World monkeys
(Platyrrhini, Primates). Mol. Phylogenet. Evol.
2225-242.
Schultz AH (1940) The size of the orbit and of the eye
in primates. Am. J. Phys. Anthropol. 26:389-408.
Schultz AH (1960) Age changes and variability in the
skull and teeth of the Central American monkeys
Alouatta, Cebus and Ateles. Proc. Zool. SOC.London
133~337-390.
Starck D (1960) Das Cranium eines Schimpansenfetus
(Pan troglodytes [Blumenbach 17991) von 71mm
SchStlg., nebst Bemerkungen uber die Korperform
von Schimpansenfeten. Gegenbaurs Morphol. Jahrb.
lOOt559-647.
Stephan H, Baron G, and Frahm HD (1986) Comparative size of brains and brain components. In HD
Steklis, and J Erwin (eds.):Comparative Primate Biology, Volume 4: Neurosciences. New York Alan R. Liss,
Inc., pp. 1-38.
Terborgh J (1983) Five New World Primates: A Study
in Comparative Ecology. Princeton: Princeton University Press.
Документ
Категория
Без категории
Просмотров
1
Размер файла
1 121 Кб
Теги
effect, monkey, saimiri, platyrrhine, history, squirrel, life, cranium
1/--страниц
Пожаловаться на содержимое документа