American Journal of Primatology 40:99-130 (1996)

RESEARCH ARTICLES

Perinatal Life History Traits in New World Monkeys

WALTER CARL HARTWIG
Department of Anthropology, University of California, Berkeley, California

Gestation length, neonatal and maternal body weight, and neonatal and
adult brain weight data were collected for New World monkeys in an
attempt to establish typical patterns of perinatal life history. This study
attempts to illuminate the most accurate values from the available data,
which suggest that gestation length and prenatal growth rate are broadly
conserved in relation to maternal size in New World monkeys. Exceptions
to the patterns evident in the data point to derivations in life history
strategies. In particular, this study suggests that the extended gestation
length of callitrichines is a function of minimum viable neonate size and
not exclusively energy minimization associated with simultaneous lacta-
tion. Cebus is shown to undergo more postnatal brain growth relative to
other New World monkeys, but not as much as previously believed. AZ-
ouatta is shown to be relatively small brained at birth as well as in adult-
hood. Saimiri is shown to present the most unusual package of perinatal
life history traits, in which precocial neonates are gestated for a relatively
long time and a t a slightly faster growth rate than is typical for New World
monkeys. o 1996 Wiley-Liss, Inc.

Key words: PZutyrrhini, ontogeny, neonate, growth and development

INTRODUCTION
The biology and behavior of adult animals are best understood in the context
of the overall life history of the species. This premise has been a major focus of
evolutionary biology in the last 10 years [Harvey & Clutton-Brock, 1985; Stearns,
1992; Charnov, 1993; Roff, 19921. The importance of perinatal and postnatal
growth patterns for understanding primate life history is now well established
[Harvey et al., 1987; Pereira & Fairbanks, 1993; Leigh, 1994al. Comparative stud-
ies of life history patterns for major primate radiations, however, have yet to be
undertaken.
This study analyzes the available data on five basic life history variables that
can be measured cross-sectionally. Such an analysis is necessary because the ex-
isting data for New World monkeys are inconsistent within taxonomic groups, and
because a baseline pattern of perinatal life history is a useful foundation for lon-
gitudinal studies that address ontogeny more empirically. Examining the rela-

Received for publication June 1, 1995; revision accepted February 10, 1996.
Address reprint requests to Walter Carl Hartwig, Department of Anthropology, University of California,
Berkeley, CA 94720.

0 1996 Wiley-Liss, Inc.

100 / Hartwig
tionship among variables such as gestation length, brain size, and neonatal
and adult body size is a first step toward understanding how New World mon-
keys grow in response to different ecological constraints [Ross, 1991; Martin,
19921.
Understanding postnatal ontogeny requires longitudinal data and a sensitive
measure of growth rate during various life cycle phases [Janson & van Schaik,
19931. Such data speak more directly to interpreting life history as adaptation.
When compared across the entire radiation of New World monkeys, however, cross-
sectional variables can produce a profile of typical perinatal growth. Species that
depart from this pattern can then be studied more effectively because the context
of their departure is known. Despite the magnitude of body size difference between
the largest and smallest New World monkeys, perinatal life history traits are
conservatively expressed. Genera that emerge as outliers on bivariate regressions
of these traits are the same genera that appear to display distinctive behavioral
repertoires and ecological risk aversion strategies.
The general hypotheses examined in this study can be summarized as follows.
1. Prenatal growth rate and gestation length are tightly correlated with ma-
ternal body size. This null hypothesis for prenatal growth is tested by bivariate
comparisons of gestation length, maternal body weight, and neonatal body weight.
The hypothesis can also be effectively falsified if interspecific variation in prenatal
growth rate exceeds the point a t which correlations among the above variables are
significant.
2. Callitrichines depart from other New World monkeys only in number of
offspring and not in an adaptive scheduling of prenatal growth. This hypothesis is
an alternative explanation of the mechanism of twinning rather than of the evo-
lutionary reasons for its occurrence [Leutenegger, 1980; Ford, 1980; Sussman &
Kinzey, 1984; Ross, 1991; Martin, 19921. It is tested by comparing data for cal-
litrichine singletons (rather than total litter mass) to data for noncallitrichines.
Without discounting the many correlated energetic demands of twinning [Tardif et
al., 1993; Tardif, 19941, this hypothesis is examined in order to place the values for
gestation length, neonatal size, and prenatal growth rate in callitrichines in the
context of size-based expectations for anthropoid primates.
3. Prenatal growth rate or neonatal brain or body size departures from the
platyrrhine baseline reflect unusual behavioral ontogenies or ecological con-
straints in the same species. This hypothesis is tested by regressing a basic mea-
sure of prenatal growth rate, neonatal body weight, and neonatal brain weight on
adult body weight, then by evaluating life history differences in light of available
field data on behavioral ecology. At the current stage of awareness of these aspects
of New World monkey natural history, this process is more exploratory than de-
monstrative.

MATERIALS AND METHODS

Data for this study were collected from the literature, captive breeding colo-
nies, zoos, and primate research centers. The data judged most reliable for each
variable are reported in a summary table (Table I). It is important to note that the
summary data represent my assessment of reliability. For this reason, a more
comprehensive table of reported values for each genus, regardless of reliability, is
included (see Appendix). In general, data from literature sources in which indi-
vidual data were published [e.g., Manocha, 19791 were judged more reliable than
data from literature sources in which only summary means were reported [e.g.,
Harvey et al., 19871. Data from primary studies of life history [e.g., Elias, 19771
 NWM Life History Traits I 101
were considered more reliable than data reported in the context of more general
studies [e.g., Eisenberg, 19811.
It is important to note that for callitrichine genera, the weight values reported
are for singletons in cases of live twin births. Obviously, any consideration of life
history adaptations and energy management strategies in marmosets and tama-
rins must account for twinning. Because the questions under direct examination
relate to offspring viability, and relative neonatal brain and body size (not com-
bined litter weight or brain size), the standard chosen here is singleton data.
Where litter weight and maternal energetic load are considered, callitrichine data
are accounted for accordingly.

Gestation Length
Gestation length has been reported as a variety of measures including inter-
birth interval, time since last copulation, time since controlled date of conception,
and hormone profile analysis. In this study quantified measures (hormone assays)
were considered more reliable than observational data, but quantified measures of
gestation length are available for only a few genera [Hearn, 1983; Ziegler et al.,
1987, 1990b; Carroll et al., 1990; Missler et al., 19921. Reliable estimates of ges-
tation length are lacking for larger-bodied New World monkeys in particular, an
absence of data that clearly affects interpretations of the typical gestation length-
body size relationship.

Neonatal Body Weight

Neonatal body weight data have been reported for 12 of the 16 New World
monkey genera (Table I). Neonatal body weight data are lacking for the three
genera of pitheciines (Pithecia, Chiropotes, and Cmujuo) and for the rare woolly
spider monkey (Brachyteles). Some studies report sample size, range, and even
individual neonatal weights [Elias, 1977; Manocha, 1979; Mason et al., unpub-
lished (for CuZZicebus)l, and were given highest priority. In cases of two different
means of equal priority reported for the same species, a composite mean was
calculated. Data derived from infants more than 24 hr after birth were given least
priority.

Adult Body Weight

Determining the most accurate adult body weights for a given species is very
difficult [Ford & Davis, 1992; Leigh, 1994b; Peres, 19941. Because the neonatal
data used in this study were obtained entirely from captive populations, captive
adult body weights were given priority. Within that dataset, weights derived from
the actual mothers of the neonates used in this study were given the highest
priority [Elias, 1977; Manocha, 1979; Mason et al., unpublished (for Cullicebus)].
Data on captive adult female body weights from Leigh [1994b] or on mixed wild
and captive females from Ford and Davis [19921were used in other cases. In some
cases the data in Table I reflect a composite mean of the most reliable sources.

Neonatal Brain Weight

Neonatal brain weight is the least reported variable of the study. Circum-
stances under which reliable neonatal brain weights can be obtained are rare.
Data used in this study come primarily from Sacher and Staffeldt [19741 and
Harvey et al. [19871. Well controlled studies on Cebus [Elias, 19771 and Suimiri
[Elias, 1977; Manocha, 19791 provided the most reliable data for these genera.
102 I Hartwig
TABLE I. Summary Perinatal Life History Data
Gestation Neonatal Adult Neonatal Adult Relative
length body body brain brain neonatal
Genus species (days)" weight (g)b weight (g) weight (g) weight ( g ) size
Callitrichines
Cebuella 131 16 128 4.2 0.125
Callithrix 144 31.5 352 4.0 7.9 0.089
Saguinus
fuscicollis 149 39 419 9.3 0.093
geofftoyi 145 41 493 10.5 0.083
labiutus 44 465 0.095
midas 140 39 432 10.4 0.090
nigricollis 140 44 450 8.9 0.098
oedipus 184 38 534 4.9 9.0 0.071
Callimico 150 47 463 5.8 10.8 0.102
Leontopithecus 128 57 659 12.9 0.086
Noncallitrichines
Aotus 133 97 1,000 10.1 18.2 0.097
Callicebus 79.3 1,112 0.071
Saimiri
boliviensis 155 102 800 0.128
sciureus" 153 1 l O f ; 113m 617 14.6f; 15.5m 23.3f; 25.3m 0.181
sciureus 153 105f; 114m 675 14.0f; 13.8m 24.lf; 29.0m 0.168
Cebus
albifrons 162 228f; 238m 2,060 32.6f; 34.4m 66.8 f 0.113
apella 155 238 3,190 73 0.075
capucinus 230 2,900 29 0.079
Pithecia 153 1,515 31.7
Chiropotes 2,555
Cacajao 3,057
Alouatta
palliatu 186 398 6,095 55.1 0.065
seniculus 191 5,600 30.8 57.9
villosa 187 480 6,000 0.080
Lagothrix 215 413 5,750 79.2 0.072
Ateles
fusciceps 229 7,995 114.7
geofioyi 229 466 8,000 64 110.9 0.058
paniscus 480 7,410 109.9 0.065
Brachvteles 9.450
"Data for atelines are from Eisenberg [19771, Glander [19801, and Crockett and Sekulic t19821 for Alouotta,
Eisenberg [1973] for Ateles, and from Logsdon (unpublished) for Lagothrirr. Hormonally derived unpublished
data on Pithecia were provided by Anne Savage. Cebus data are from Hayes et al. [19721 for C . albifrvns, and
Nagle and Denari [19831 for C. apella. Controlled date of conception data for Saimiri sciureus are from Stolzen-
berg et al. [1979], and for Aotus from Hunter et al. 119791. Hormonally determined data for Callithrirr were taken
from Hearn [1983] and for Saguinus fuscieollk from Heistermann and Hodges [19951. Other Saguinus species
data were determined from modal occurrence or from the only studies available [Wolfe et al., 1972, for S .
nigricollis; Epple, 1970, for S . geoffroyil. Leontopithecus data were taken from multiple observations of the
captive colony at the National Zoological Park [Kleiman, 1977,1978; Hoage, 1978; Wilson, 19781. The pygmy
marmoset (Cebuella)gestation length is the mean of hormonally collected samples by Ziegler et al. t1990aI. The
Callimico figure is the modal occurrence in the hormonally collected sample of Carroll et al. [19901.
bAlounttupalliatudata were averaged from Harvey et al. [19871 and Lee et al. [19911. The estimate for Alouatta
uillosa is from the only published study [Leutenegger, 19701. The estimate for Ateks geoffrsvi is an average of
Leutenegger [1970] and Lee et al. [1991], and for A. pankcus is from the only published study [Gensch, 19651.
Lagothrirr neonatal weight values considered most reliable are from a long-term captive study (Logsdon, un-
published). Cebus albifrons data are from Elias [19771, and C. apella data are from Nagle and Denari [19831. The
two values for S . sciumlrs are from Elias [19771 and Manocha [19791, respectively. The Callicebus data are
courtesy of W.A.Mason. The CdlithTir average is from Heger and Neubert t19881. Saguinus data were calcu-
lated as composite means for species represented by numerous studies (S. nigricollis, S. oedipus), or taken
directly from single primary studies [Leutenegger, 1973, for S. midas].Leontopithecus and Cebuella data were
taken from the summaries in Hershkovitz [19771, and the Cdlimico estimate was averaged from all available
studies because no single study seemed most reliable.
'Neonatal data are taken from Elias [19771 in the upper row and Manocha [19791 in the lower row.
 NWM Life History Traits / 103
Adult Brain Weight
Adult brain weight data are available for 12 of the 16 New World monkey
genera. For this variable the pitheciines are represented by a mean for Pitheciu
reported by Harvey et al. [19871. Missing genera include Brachyteles, Cacajcw,
Chiropotes, and Callicebus. With the exception of Cebus and Saimiri, all data used
in this study derive from Sacher and Staffeldt [19741 or Harvey et al. [19871.

Relative Neonatal Size

This index was calculated by dividing the neonatal body weight mean value by
the adult body weight mean value in Table I, and represents the most general
quantification of neonatal size. It is important to note that for callitrichine genera,
this value is calculated as that for singletons only. This is done primarily to facil-
itate comparison across New World monkey genera, and in no way is it intended to
minimize consideration of the unusual load carried by these genera of small-bodied
anthropoids.

RESULTS AND DISCUSSION

Gestation Length
Most New World monkey species have a gestation length between 130 and 160
days, or roughly 4.5-5.5 months (Table I). An abrupt transition from this range to
a range of 6-7.5 months separates nonatelines from atelines. The longest gestation
lengths reported, for Ateles [Eisenberg, 1973; Harvey et al., 19871 and Lagothrix
(Logsdon, unpublished), are observational rather than empirically determined,
and thus the strict gestation lengths may actually be shorter.
The lower limit for gestation length applies not to the smallest-bodied genus,
Cebuella, but rather to the golden lion tamarin, Leontopithecus [Kleiman, 1977;
Hoage, 1978; Eisenberg, 19811. Three genera of different body size ranges (Ce-
buella, Leontopithecus, Aotus) have gestation lengths reliably measured to be
around 130 days. While it is true that some of the shortest gestation lengths are
those of the marmosets and tamarins, Martin [19921 has argued convincingly that
callitrichines would have much shorter gestation lengths if they matched predic-
tions of a broad comparison across placental mammals. Their relatively long ges-
tations are almost certainly related to their unique habit of twinning. An alter-
native explanation is that callitrichine gestation lengths may represent a
minimum threshold for anthropoids regardless of body size, since these genera are
the smallest anthropoids and likely underwent an evolutionary reduction in body
size; moreover, although they are the only anthropoids to habitually twin, they do
not give birth to unusually altricial neonates (Table I) [see also Ross, 19911. These
interpretations are considered in greater detail below.
Gestation length ranges within genera vary typically less than 10 days, as
reflected by the data of well controlled studies [Hunter et al., 1979; Hearn, 1983;
Carroll et al., 1990; Ziegler et al., 1987, 1990a,bl. The two exceptions are Saimiri
and Saguinus. A reliable range of 17 days (141-158) has been reported for the
squirrel monkey [Goss et al., 1968; Kerber et al., 1977; Stolzenberg et al., 19791.
Boinski [19871 has suggested that squirrel monkeys synchronize birthing in the
wild as a strategy to reduce predation risk by maximizing the number of new
offspring in the group. The large range of days reported for captive colonies may
reflect a measure of flexibility in the timing of parturition for this genus. An
alternative explanation may be that birth synchrony in squirrel monkeys may
function to safeguard infants from infanticide, as has been suggested recently for
104 I Hartwig
ringtailed lemurs [Pereira, 1991; Pereira & Weiss, 19911. Similarities between
ringtailed lemurs and squirrel monkeys in relation to factors argued to play a role
in infanticide include strictly seasonal reproduction and the tendency of females
with infants to react aggressively to male proximity (M. Pereira, personal com-
munication).
The large range evident in Saguinus is interspecific. One species, Saguinus
oedipus, appears to have a relatively very long gestation length of 184 days [Zieg-
ler et al., 19871.This is more than 30 days longer than the reliable figures reported
for other Saguinus species (Table I), but was measured in a tightly controlled
hormonal study and thus is considered very reliable in the present analysis. Re-
ported interbirth intervals are routinely longer than this period, and thus indi-
rectly support such a long period of gestation [French, 1983; Baker & Woods, 1992;
Tardif et al., 19931. Reported neonatal body weights for this species are not un-
usually high for New World monkeys in general or Saguinus in particular (Ap-
pendix). The weights of the neonates in the Ziegler et al. El9871 study were not
reported.
This unusually long gestation length is not easily explained in light of the data
for other New World monkey species. Cotton-top tamarins are the only callitri-
chines outside of South America. It is tempting to suggest that ecological con-
straints imposed by a more seasonal habitat than their tropical congeners in turn
impose a narrow window of optimal birthing time on a semiannual basis. In this
scenario, the extended gestation length would be the result of retaining the cal-
litrichine pattern of rapid postpartum conception combined with the external in-
fluence of seasonal decline in food resources. Neonates thus undergo an extended
lag phase of intrauterine growth [Martin, 19921, or develop at a constant but
relatively slower rate, until food resources are sufficient to support the offspring
and nursing mother. At this time, however, such unusual ecological constraints
have not been identified in summaries of S . oedipus behavioral ecology [Snowdon
& Soini, 1988; Garber, 19931.
Is Gestation Length Driven by Phylogeny or Correlated to Body Size?
Maternal body size is clearly correlated to gestation length in New World
monkeys (Figs. 1,2), as in other placental mammals. A reduced major axis regres-
sion of these data yields slope and r-values consistent with those derived by Martin
and MacLarnon [1985, 19881 for placental mammals in general. Martin [1992]
cited a slope of 0.11 as typical for an order of placental mammals. The data con-
sidered most reliable here for all New World monkeys (Fig. 1)yield a slope of 0.12.
Martin [1992] did not calculate an r-value for all New World monkeys, arguing
instead that callitrichines and noncallitrichines form two natural clusters of very
different correlations. Martin’s 119921 r-value for noncallitrichines, which he con-
sidered to show good correlation between gestation length and adult female body
weight, was 0.82, P < 0.001, slope = 0.16. The data considered in this study to be
most reliable for the same genera yield r = 0.86, P < 0.001, slope = 0.15. The
results when all New World monkey genera are included are not significantly
different: r = 0.83, P < 0.001, slope = 0.12, but it is clear that callitrichines are
transposed above what would be expected from a noncallitrichine regression (Fig.
1).The correlation between gestation length and maternal body weight in New
World monkeys is at least as strong as that calculated for ordinal groups of pla-
cental mammals.
Phylogeny must also be considered as a factor in gestation length, either as a
determinant or a measure of inertia. Closely related New World monkey genera do
have similar gestation lengths, but they are also similar in body size in most cases,
 NWM Life History Traits / 105
250 I I I I I

A A

-a0, 200
M
C X
s
-
c
C
.-0
m
150
6

100
4 5 6 I 8 9 10

Maternal Body Weight

Fig. 1. Regression of gestation length on log mean adult female body weight. Each symbol represents species
means as reported in Table I. Gestation length is not logged in order to facilitate comparison to other studies.
The regression ellipse* is through all noncallitrichines. The reduced major axis slope value (0.15)and r-value
(0.86) are similar to those reported by Martin [19921 for noncallitrichines. Note that Saimiri is scaled with
callitrichines and appears to have a relatively long gestation length. The symbols used in Figures 1-7 are as
follows: Q Cebuella; 0Aotus; 0 Callithrix; 0 Cebus; 0 Callimico;
-h- Saimiri; A Ateles; 4 Callicebus; -Lagothrix; A Leontopithecus.
+ Pithecia; X Saguinus; - Alouatta;

*The ellipse in all figures is a graphic device to illustrate how uniformly the data scale with reference to the
best-fit reduced major axis regression line. In each case the ellipse is calculated as the smallest ellipse that
encloses 75% of the data space; a long, narrow ellipse reflects the strongest correlations, while a short, wide
ellipse reflects a weaker correlation.

thus confounding attempts to isolate cause and effect. Saimiri and Cebus, two
genera of radically different body size but potentially close evolutionary relation-
ship, have similar gestation lengths (Table I). Because the data for Cebus are not
out of line with other larger and smaller noncallitrichines (Fig. l), and because a
good argument can be made for extended gestation length in Saimiri [Hartwig,
19951, it is unlikely that phylogeny is driving the pattern of similar gestation
lengths in these two genera.
The best test of relationship among phylogeny, body size, and gestation length
would be in the closely related pitheciines, in which the largest genus (Cacajao)is
twice the size of the smallest genus (Pithecia) and the phylogenetic affinities are
undisputed. Unfortunately, no data on gestation length are available for Cacajao
or Chiropotes. Gestation length in Pithecia (153 days; A. Savage, personal commu-
nication) is similar to that in Cebus, which in turn is similar in body size to
Cacajao, and conforms to the expectations of a regression through non-callitrichine
New World monkeys (Fig. 1)and anthropoid primates [Martin, 19921. Thus, pend-
ing more exact measures of gestation in the larger-bodied New World monkeys, it
appears that gestation length is most closely correlated to maternal body size,
particularly among non-callitrichines.
A weak but significant correlation pertains to gestation length and neonatal
106 / Hartwig
250 I I I I

-
-5
.d
200
M
E
2
s
.-c
0
d
*
150
Q
v1

I I I I
100
2 3 4 5 6 I
Neonatal Body Weight

Fig. 2. Regression of gestation length on log neonatal body weight, demonstrating a general but weak corre-
lation (1.2 = 0.55,SE = 19.2, P < 0.005).Symbols represent species means as reported in Table I. The gestation
length values for Lagothrir and Ateles are estimates rather than controlled observations. If‘ they and the
outlying Saguinw oedipus are removed from the regression, the correlation improves to P = 0.68, SE = 9.8,
P < 0.001.

body size (Fig. 2). This correlation improves when the observational data on Ateles
and Lugothrix are removed from the calculation of regression statistics. However,
there is enough variation among genera similar in size to warrant a more detailed
explanation of how gestation length scales with neonatal weight.
Callitrichine Prenatal Development: Suspended Fetal Growth or
Neonatal Size Constraint?
Even though correlation coefficients in New World monkey genera between
gestation length and adult female body weight are similar with or without cal-
litrichines, a good case can be made that callitrichines depart from a “typical”
platyrrhine pattern. Martin [19921 demonstrated this by calculating a low r-value
of 0.27 for callitrichine genera; the callitrichine data used here yield a similarly
low r-value of 0.32. A graph of the pattern in non-callitrichines (Fig. 1)illustrates
that all callitrichines except Leontopithecus have longer gestations than would be
predicted from a regression through noncallitrichine New World monkeys. While
this is certainly related to their unique habit of twinning, data on prenatal growth
[Chambers & Hewn, 1985; Moore et al., 1985; Jaquish et al., 19951 and relative
neonatal size suggest that other factors may be influencing gestation length. Two
interpretations of their scaling seem acceptable for the data now available. One is
Martin’s [19921 interpretation of suspended fetal growth. An alternative interpre-
tation is that callitrichine gestation length is at a minimum anthropoid threshold
for prenatal development of a viable single offspring.
Martin [1992] argued that suspended fetal growth (an extended postimplan-
tation lag phase) is an accommodation to the energetic demands of lactation that
 NWM Life History Traits / 107
accompany postpartum conception and normal implantation in callitrichines. This
is based on the observations that Callithrix conceives very shortly postpartum,
implants the embryo in a typical manner [Hearn, 1980, 1983; Moore et al., 1985;
Smith et al., 19871, then seems to extend the lag phase prior to the onset of fetal
development [Chambers & Hearn, 1985; Jaquish et al., 19951 until the energetic
demands of lactation subside [but see French, 1983; Ziegler et al., 199Oc; Tardif,
19941.
Controlled studies of common marmoset prenatal growth generally support
this interpretation. According to Chambers and Hearn [1985:5571, “the lengthen-
ing of the embryonic period in the marmoset is primarily a post-implantation
phenomenon.’’ Chambers and Hearn [1985:5571 also note that “half-way through
pregnancy . . . the marmoset lags considerably behind the growth achieved by
other species, and it is not until nearly three-quarters of pregnancy is completed
, . .that the percentages become similar.” Jaquish et al. [19951 have corroborated
this recently in the first study of longitudinal prenatal growth in Callithrix. Evi-
dence of delayed growth is as early as the appearance of the primitive streak,
which appears later in absolute days than is the case for macaques, baboons, and
humans. However, as noted by Chambers and Hearn [19851, differences in time
scale of development between platyrrhines and catarrhines can be evaluated only
when other platyrrhine genera are studied in detail.
Chambers and Hearn [1985] conclude that prenatal growth in Callithrix is
“behind schedule” from day 10 to day 60, or from immediately postimplantation to
near the end of embryonic development [Phillips, 1976; Oerke et al., 19951. Moore
et al. [19851 attribute the relatively slow progress of postimplantation growth to
the unusually massive proliferation of trophoblast and the unusual condition of a
common chorion with fused trophoblasts in which both embryos develop.
The conclusion that marmosets delay embryonic development as a strategy to
minimize energy while simultaneously nursing two offspring is well reasoned [Zieg-
ler et al., 199Oc; Tardif, 19941, but the mechanism of an extended lag phase fol-
lowed by resumption of normal fetal growth may be more complicated than what
actually happens. The duration of prenatal growth simply might be longer. It may
be that extra time in utero is a less complicated mechanism for these smallest
anthropoids to deliver twins, each singleton of which must be viable, while en-
cumbered with nursing the previous litter. Growth continues throughout gesta-
tion, but at two different rates prior to and following fetal development. The slower
rate is attributed to the energetic cost of developing a complex haemochorial pla-
centa, rather than or in addition to energetic suppression imposed by simultaneous
lactation. The extra length of callitrichine gestation is attributed to the need to
bring each neonate to a hypothetical minimum neural and somatic threshold of
viability for anthropoids. The degree to which callitrichine gestation appears to be
long compared to other New World monkeys may be exacerbated by an evolution-
ary reduction in callitrichine adult body size.
The above discussion does not explain why Leontopithecus, a callitrichine
which twins, maintains a gestation length typical for anthropoids while Callimico,
a genus with definite affinities to callitrichines, has a “callitrichine-like”gestation
length but gives birth only to singletons. With regard to Callimico, Martin [1992]
suggested that the advent of twinning in marmosets and tamarins followed their
evolutionary separation from Callimico, and that Callimico manages a high max-
imum intrinsic rate of population increase by lowering its age at first breeding
rather than by twinning. Thus, its relatively long gestation length is explained as
an energy-minimizing strategy while the lack of twinning is explained by lower
age at first breeding as an alternative route to increased reproductive output in a
108 I Hartwig
radiation of small-bodied anthropoids subject to unpredictable environments (edge
and secondary forests) [ROSS,19911. In this study Callimico mimics callitrichines in
all perinatal life history traits except for twinning, which indirectly suggests that
the relative length of gestation in callitrichines may be a default result of evolu-
tionary reduction in body size followed by further modifications necessary to sup-
port twinning.
The lion tamarin (Leontopithecus) has the shortest reliably measured gesta-
tion length among anthropoids, but it is not relatively short for noncallitrichines
(Fig. 1) based on its body size. In all other respects, the known reproductive biology
of Leontopithecus is similar to other callitrichines. This suggests that either Le-
ontopithecus has overcome the energetic demands that determine the gestation
length-body size relationship in other callitrichines, or that its location on the
regression is due to some other cause. Martin [19921 suggested that Leontopithecus
simply lacks the extended lag phase of growth suspension inferred for the other
callitrichines. Dietz et al. [19941 argued that lion tamarin reproductive biology is
subject to dry season constraints that select for two litters in a 7-9 month annual
window. Another relevant issue to measures of gestation length is the argument
that Leontopithecus has undergone an increase in body size subsequent to the body
size reduction coincident with the callitrichine radiation [Rosenberger, 1979;
Rosenberger & Coimbra-Filho, 19841.
Data from long-term studies in the wild indicate that lion tamarin births occur
most frequently during peak times of resource availability [Dietz et al., 19941.
Females which gave birth to two litters per year did so at the onset and end of the
wet season, such that at least 1 month of wet season and one transitional month
followed birth. Interbirth interval in two litterlyear females was very short be-
tween early and late wet season births, but averaged 141 days across the dry
season interval. However, the frequency of two litter seasons (17 cases out of 114
observations) was not as high as would be expected for a trait as fixed as gestation
length. Dietz et al. [19941 have clearly demonstrated that the timing of reproduc-
tion in Leontopithecus is tied to resource availability [Coimbra-Filho & Maia,
19791, but additional evolutionary factors may be affecting the relationship of
gestation length to body size.
Based on cranial and dental morphology, Leontopithecus may have undergone
an increase in body size subsequent to the body size reduction that characterizes
the callitrichine subfamily [Rosenberger, 1979; Rosenberger & Coimbra-Filho,
19841. Leontopithecus may in fact have an absolute gestation length typical for the
marmosets to which it has been linked as a sister taxon, but a body size that
transposes it along the size axis so that it appears to fall within a typical noncal-
litrichine regression for gestation length on body size (Fig. 1). Thus, its gestation
length may be a function of seasonal influences on maximizing reproductive out-
put, and further as a result of an independent increase in body size. This body size
increase may itself be a result of selective pressures or opportunities particular to
their Atlantic coastal forest habitat.
Individual Leontopithecus neonates are not relatively small (Table I), even
when the largest mean weight [Leigh, 1994131 for adult females is used in the
calculation. Relatively small neonates compared to other callitrichines would be
predicted from their short gestation length according to the above explanation for
callitrichines in general. Leontopithecus neonates may be of “typical” size because
Martin’s [19921 interpretation that they lack a post-implantation lag phase is true,
or because lion tamarins have crossed a crucial body size threshold for which
twinning does not present as substantial an energetic burden. A body size thresh-
old of approximately 600 g may be enough to sustain a large litter mass after a
 NWM Life History Traits / 109
“typically anthropoid” gestation length and without the need to slow the rate or
extend the duration of prenatal growth.
If this is a valid explanation for Leontopithecus, it is reasonable to wonder why
Saimiri, a genus a t virtually the same weight and which habitually births single-
tons, does not have the same gestation length. In fact, Saimiri has a relatively long
gestation length according to the anthropoid regressions of Martin [19921and this
study (Fig. 1). Squirrel monkey gestation lengths are nearly a month longer than
those of a noncallitrichine of slightly larger body size (Aotus) and are similar to
those reported for genera more than twice its body size (Pithecia, Cebus; see Table
I). This longer gestation period results in a relatively very heavy neonate with one
of the highest cranial widtldpelvic inlet ratios of any anthropoid (Fig. 3) [see also
Goss et al., 1968; Leutenegger, 1970, 1973, 1982; Hartwig, 1995; Ridley, 19951.
The morphological consequences of such a derived prenatal development pat-
tern include obstetric complications [Leutenegger, 19821, a relatively dolichoceph-
alic neurocranium, and eyes very closely approximated to midline resulting in a
fenestrated interorbital septum [Hartwig, 19951. Calculations of relative neonatal
size in Saimiri may also reflect an evolutionary reduction in body size in the
squirrel monkey, which has been argued on the basis of other morphological traits
[Rosenberger, 19921. The behavioral and ecological correlates of relatively preco-
cia1 neonates in this genus are discussed below [see also Boinski, 1987; Boinski &
Fragaszy, 1989; Hartwig, 19951.
Neonatal Body and Brain Size
New World monkey neonatal size is a function more of maternal body size than
of gestation length or the phenomenon of twinning (Figs. 2, 3). The data summa-
rized in Table I, as well as the Appendix data considered most reliable, indicate
that New World monkey neonates are typically 9-10% of maternal body weight
(Fig. 3b). With increasing adult body size (e.g., Ateles, Lagothrix, Alouatta), this
percentage drops to 7%,which is consistent with the trend for mammals in general.
The clear exception to this tight regression is Saimiri, in which an individual
neonate is typically 17% as heavy as the mother carrying it (Table I).
The data collected for this study indicate that callitrichine singletons of nor-
mal twin births are not relatively small compared to other platyrrhine neonates.
Ross [19911 and Martin [19921 have argued that they are relatively small in a
haplorhine-wide comparison. A critical parameter here is offspring viability, a
threshold that must be met by each singleton regardless of a single, twin, or triplet
birth. A strong correlation of individual neonatal body weight and maternal body
weight [r2 = 0.95, SE = 0.24, P < 0.0011 demonstrates that single callitrichine
neonates are as heavy as would be predicted from other New World monkeys (Fig.
3). Maternal neglect of even slightly altricial offspring, particularly in callitri-
chines [Rothe, 1973,1977; Cicmanec & Campbell, 1977; Beck et al., 19821, suggests
that neonates cannot afford to be relatively small.
The perinatal life history of the squirrel monkey may be relevant to under-
standing neonatal size and gestation length in callitrichines. Saimiri neonates are
typically 17%of maternal body weight, a figure comparable to the 18%calculation
for callitrichine litter mass for a typical twin birth (see Table I). Gestation length
in Saimiri (153 days) is similar in absolute and relative measures to that in cal-
litrichines (Fig. l),with the exception of Leontopithecus and Saguinus oedipus.
This suggests, but does not confirm, that regardless of hypothesized rates of de-
velopment, a 140-150 day gestation is necessary to produce either one very pre-
cocial neonate or viable twins in anthropoids with body weights less than 700 g.
Neural development is a critical component of primate perinatal life history
110 I Hartwig

I 7

Y
G
M
.3

5 -
h
'c)
0
c9
4

J
cd
4 -
0
0
z
3 -

2 ' I I I I I
4 5 6 I 8 9 10

Maternal Body Weight

0.20

9)
N

-
.4

0.15
d
c)
16
C
3
z
Y
9) 61 1

-2
.-
0.10
2 1

t l l l l l l l l l l l
0.05

Fig. 3. Regression of log neonatal body weight on log captive adult female body weight. Callitrichine data are
for singletons fmm normal twin births. a: Symbols represent species mean values as reported in Table I and the
Appendix. The correlation is strong (9= 0.96,SE = 0.19,P < 0.001)and the regression ellipse demonstrates
that Suirniri neonates are relatively large for a given maternal body weight [Leutennegger, 1973, 1980;
Hartwig, 19951.This regression is converted to a ratio and expressed as a box plot (b),where the dependent
variable represents neonatal weight as a percentage of maternal weight. Most genera cluster around lo%, aa
reflected in Table I. The value for Suimiri is statistically significantly higher than that for other New World
monkeys.
 NWM Life History Traits / 111
[Harvey & Clutton Brock, 1985; Brizzee & Dunlap, 1986; Stephan et al., 1986;
Martin, 19903. It has been hypothesized to determine gestation length [Sacher &
Staffeldt, 19741, life span [Allman et al., 19931, and the potential repertoire of
learned behavior [Elias, 1977; but see Fragaszy, 19903. As demonstrated above,
relative neonatal size is a conservative feature across New World monkeys. To the
extent that neural growth is a dominant component of prenatal development, it is
also expressed conservatively in New World monkeys (Figs. 4,5). The exceptions
are the same genera for which adult relative brain size is unusual: Saimiri, Cebus,
and Alouutta.
Neural development in Saimiri has been reviewed from structural and behav-
ioral perspectives by several authors [Bauchot & Stephan, 1969; Hemmer, 1971;
Elias, 1977; Kaack et al., 1979; Manocha, 1979; Bauchot & Manocha, 1981; Leu-
tenegger, 1982; Stephan et al., 1986; Boinski & Fragaszy, 1989; Pucciarelli et al.,
1990; Corner & Richtsmeier, 1992; Hartwig, 19931. Most studies suggest that
Saimiri has a relatively large brain, but differ in how this is measured and how
they rank Saimiri against other New World monkeys. The data used here (Fig. 4)
represent one interpretation of the most reliable New World monkey brain weights
and body weights, and indicate that Saimiri adults have relatively large brains.
Cebus adults also emerge as having relatively large brains, while Alouutta
adults, which are larger in body size than Cebus, have absolutely smaller brains
(Table I). These three genera present different patterns of perinatal brain growth,
and it may be the case that these differences can be mapped logically onto their
differing niche positions. Cebus, Saimiri, and Alouutta all fall along or very close
to the regression of neonatal brain size on adult brain size (Fig. 5a), suggesting
that adult relative brain sizes are largely determined at birth. Of the three, only
Cebus appears to have a slightly larger adult brain than would be predicted from
the regression. Figure 5b further demonstrates that squirrel monkey neonates are
large brained and large bodied. Alouattu, on the other hand, exhibits a relatively
low neonatal brain weight for its neonatal body weight, which is the very same
condition expressed in adults.
The percentage of terminal brain weight that develops postnatally rather than
prenatally can be used to further examine the differences between Cebus and
Saimiri neonatal brain size [Elias, 1977; Fragaszy, 19901. The available data for
New World monkeys suggest a typical pattern for six genera, and two different
patterns for Saimiri and Cebus (Fig. 6).
The two different estimates of relative postnatal brain growth for Saimiri are
derived from the raw data of Manocha [19791 and Elias [19771, studies which are
both considered very reliable. The average of these, or roughly 0.43, is a reasonable
estimate of the percent of postnatal brain growth in Saimiri. This value is in the
low range of what is typical for New World monkeys (Fig. 6b), and indicates that
57%,or more than half, of squirrel monkey adult brain size is determined at birth.
The data for Cebus also come from two sources but are not equally reliable. The
data from Sacher and Staffeldt [1974] yield a postnatal brain growth estimate of
0.60, while the more reliable data from Elias [19771 yield an estimate of 0.51. The
difference is significant given the distribution in Figure 6 and in light of previous
analyses [Harvey et al., 1987; Fragaszy, 1990; Fedigan & Rose, 19951 that use the
higher estimate and not that derived by Elias [19771. The value of 0.51 preferred
here would still place Cebus as having the most postnatal brain growth, but would
considerably narrow the range of values for New World monkeys.
Cebus and Saimiri are thus two New World monkeys with relatively large
brains but different underlying neural development patterns. Attempts to corre-
late these physical maturation differences with behavioral maturation differences
112 I Hartwig
5 I I I I I

I I I I I
1
4 5 6 7 8 9 10
Maternal B o d y Weight

5 1 I I I I

a&

4
*
0
M

s
.I

c
.- 3
cf
-
Y

a
W
4
2

fi
b
I I I I I
1
4 5 6 7 8 9 10

Maternal B o d y Weight
Fig. 4. Regression of log adult brain weight on log captive adult female body weight. Symbols represent species
means as reported in Table I. a: When all species are considered, P = 0.92, SE = 0.30,P < 0.001; Saimiri and
Cebus appear to have relatively heavy brains for their body weight, while Alouatta appears to fall below the
regression ellipse. b: Symbols represent species means as reported for the most reliable data in the Appendix.
The ellipse is calculated by excluding Sairnzri, Cebus, and Alouattu (3 = 0.98, SE = 0.16,P < 0.001) to
graphically emphasize how they differ from other New World monkeys.
 NWM Life History Traits / 113
5 I I I

4
2M
.-
sc
.-
-
m
2 3
Q
Y
cd
c
0

2 2
0
X

I I I

1 2 3 4 5

Adult Brain Weight

5 I I I I

M
4
200
.-
s
F
.I

-2
m
Q
Y
3

Q
c
0

2 2

0
I I I I
1
2 3 4 5 6 I
Neonatal Body Weight

Fig. 5. a: Regression of log neonatal brain weight on log adult brain weight, with a scaling coenicient of
isometry (0.995; 1.2 = 0.99, SE = O.ll,P < 0.001). Symbols represent species means as reported in the Appendix.
Note the relative position of Cebw,which has an absolutely larger brain than Alounttn, and thus appears to be
transposed horizontally in the regression. When this is compared to Figure 4,it is clear that relative postnatal
brain growth in Cebus is greater than that for other New World monkeys. b Regression of log neonatal brain
weight on log neonatal body weight (3= 0.94, SE = 0.23,P < 0.001).Note the position of Sairniri, whose
neonates are heavier, and have larger brains, than those of Aotw. Aotw adult body weights average 40% more,
and brain weights 20% less, than those in the squirrel monkey. The position of Sazrniri reflects the relatively
heavy nature of their neonates compared to other New World monkeys (Fig. 3), and thus their apparent
conformation to the overall NWM regression. Note also the position of Alountta, in which neonates reflect the
same pattern of relatively small brains as seen in adults.
 . #P
114 I Hartwig
c,
c,

B3.
In

s
z
Postnatal Brain Growth

I
z

0
0
I

x
&=
0
E
I

x
9)
s

1
1
z
Postnatal Brain Growth

I
z I

I
I
I
1
z
I

I
1 c

-
Culliinico

Cebus

Sairniri
Cullithrir

Saguinus
Aloiturra

Aleles
Aotus

Fig. 6. a: Regression of the postnatal brain growth estimate (see text) on log captive adult female body weight.
Symbol8 represent species means 88 reported in the Appendix. The high value for Saimiri is derived h m
Manoeha L19791. and the low value from Elias [19771. The high value for Cebus is derived from Sacher and
Staffeldt [1974], and the low value from Elias 119771. b: A box plot of the postnatal brain growth estimate by
genus, in the form of species means. Only Aluuatta is represented by more than two estimates. For the other
genera, the line within the box represents the mean of two estimates.
 NWM Life History Traits / 115
[Elias, 1977; Fragaszy, 1990; Watts, 1990; Fedigan & Rose, 19951 agree that ca-
puchin monkeys display a delayed or longer postnatal period of musculoskeletal,
motor, and “learned behavior” development. These same studies differ, however, in
the degree to which they attribute this difference to the relative amount of post-
natal brain growth. Elias [19771 favored a more direct attribution in part, perhaps,
because her data for squirrel monkeys indicated very little postnatal brain growth.
Fragaszy [19901 accepted the most divergent estimates of postnatal brain growth
for Cebus and Suimiri but argued that neonatal brain size was not a good predictor
of neonatal behavioral capacity because the unit of measure cannot account for
how different subdivisions of the brain develop. Fedigan and Rose [1995] attribute
the relatively long interbirth interval in Cebus to time necessary to nurture off-
spring undergoing extensive postnatal brain growth.
A progressive interpretation of the interaction between brain size and behav-
ioral complexity in Suimiri is less clear [Goss et al., 1968; Kaplan, 1974, 1977;
Kaack et al., 19791. Squirrel monkeys appear to acquire motor, behavioral, and
foraging skills relatively quickly [Boinski & Fragaszy, 19891. It could be argued
that its behavioral repertoire is more limited than that of Cebus, and that this is
a result of its more limited potential for postnatal brain growth [Hartwig, 19951
coupled with its abbreviated maturation to foraging independence [Janson & van
Schaik, 19933. However, Suimiri exhibits a very large relative brain size for New
World monkeys. The implications of this are varied but not mutually exclusive: (1.)
A general measure of brain volume or size is truly a poor indicator of primate
“ecological intelligence” [Fragaszy, 19901. (2.) Various measures of behavioral so-
phistication are too subjective to be compared to more objective size and growth
relationships. (3.) The calculation of relative brain size in Suimiri is in large part
a result of body size reduction rather than neural expansion [Rosenberger, 19921.
While the inherent problems of size measurements and behavioral assessments are
irresolvable, increased attention to combining theoretical and methodological ap-
proaches may ultimately register the most likely impression of platyrrhine peri-
natal growth and adaptive radiation.

Prenatal Growth Rate

The final general hypothesis to be examined in this study is the scaling of
prenatal growth rates and their relationship to external selection pressures. A
strict calculation of fetal growth rate is the difference between neonatal weight
(W,) and the weight of the incipient fetus (Wi, postembryogenesis), divided by the
difference between total gestation length (GI and pre-embryogenesis gestation
length (Gf):
fetal growth rate (FGR) = (W, - Wi)/(G - Gf).
This calculation is impossible for most genera because Gf and Wi (albeit negligible)
are not known. The result is that various measures of FGR are not calculated
uniformly [Brizzee & Dunlap, 1986; Ross, 19911. Therefore, following Ross [1991],
a more basic measure of prenatal growth rate is used here, calculated as WJG
(Table 11).
Prenatal growth rate in New World monkeys is tightly correlated to maternal
body weight (Fig. 7). This is not surprising, given the tight correlation between
neonatal weight and maternal weight (Fig. 3). The effect of gestation length on
prenatal growth rate is to elevate genera with shorter gestation lengths (Aotus,
Leontopithecus, Alouuttu), and depress genera with heavy neonates (Suimiri) or
longer gestation lengths (Suguinus oedipus, Ateles). The correlation would be even
116 I Hartwig
TABLE 11. Prenatal Growth Rates*
Taxon This study Ross, 1991 Harvey et al., 1987 Misc.
Callitrichines
Cebuella 0.12 0.23 0.12 0.10"
Callithrix jacchus 0.22 0.38 0.19 0.22b
0.24'
Saguinus oedipus 0.21 0.50 0.30
Saguinus fuscicollis 0.26 0.27
Saguinus midas 0.28 0.28
Saguinus geofiyi 0.28
Callimico 0.31 0.33 0.32 0.29d
Leontopithecus 0.44 0.78 0.42 0.48"
Noncallitrichines
Aotus 0.73 0.73 0.74 0.70'
Saimiri sciureus 0.73 0.56 1.15k 0.67=
1.6h
Cebus albifrons 1.44 1.51
Cebus apella 1.54 1.55 1.55 1.28'
1.54
Alouatta palliata 2.14 2.84 2.57
Lagothrix 1.92 2.02 2.00
Ateles geofioyi 2.03 1.89 1.86
*Prenatal growth rate is calculated as neonatal weight/gestation length. The data from Ross [1991] are from the
same calculation; all other figures were determined from the data reported in those studies.
"Soini [19881.
"Epple [19701.
"Sacherand Staffeldt [19741.
dChristen [19681.
"Hoage [19781.
Qixson [19831.
gJarosz et al. [19771.
"Brizzee and Dunlap [1986; derived from a subset of data in Manocha, 19791.
'Leutenneger [19731.
JNagle and Denari [19831.
kBased on a reported neonatal body weight of 195 g.

stronger if the actual gestation lengths in Ateles and Lagothrix are shorter than
the published estimates, and if the discrepancy between neonatal size and gesta-
tion length in Saguinus oedipus is excluded. Assuming that prenatal growth rate
as calculated here is comparable to fetal growth rate, the data support the hypoth-
esis that fetal growth rate is a conservative life history phenomenon in New World
monkeys.
Regardless of how prenatal growth rate is ultimately calculated for the miss-
ing genera in Figure 7 , Saimiri stands out as having a relatively high prenatal
growth rate. Thus, it appears that several interrelated aspects of perinatal life
history have evolved toward greater neonatal precociality in this genus: an ex-
tended gestation period, a relatively high rate of fetal growth during that period,
and relatively large-bodied and large-brained neonates.

CONCLUSIONS
1. Perinatal life history traits in New World monkeys are poorly understood
because the relevant data have been reported under varying standards of control
and accuracy. Some of the most robust data, moreover, have not been cited in the
most referenced treatments of anthropoid life history.
 NWM Life History Traits I 117

1 I I I I

1 I I I 1

4 5 6 7 8 9 10
Maternal Body Weight

Fig. 7. Regression of log prenatal growth rate on log captive adult female body weight (9= 0.91, SE = 0.29,
P < 0,001).Symbols represent species means as reported in Table I and calculated in Table 11; data for callitri-
chines reflect relative size of singletons from normal twin births. These data are static measures of a dynamic
phenomenon, but do indicate, at a general level, that the rate of fetal growth is scaled to maternal body size.

2. Perinatal life history traits are conservatively expressed across species

when evaluated as a function of maternal body size.
3. Due to large litter size, small maternal size, complex placentation, and often
simultaneous lactation, early phases of callitrichine prenatal development may be
inevitably, rather than adaptively, delayed. Within callitrichines, Suguinus oedi-
pus has a uniquely long gestation length of 184 days, the reasons for which are not
yet understood.
4. Perinatal life history traits in Suimiri all point toward precocial prenatal
development and slightly more limited postnatal growth. Gestation length is ex-
tended, neonates are relatively large bodied and large brained, and prenatal
growth rate is slightly faster than for other New World monkeys.
5. Postnatal brain growth in Cebus is more extensive than is that in other New
World monkeys, but is probably less extensive than previously believed. Differ-
ences in behavioral development between squirrel and capuchin monkeys associ-
ated with these differences in neurological development merit further study.
6. Prenatal development in Alouattu mimics postnatal development to the
extent that neonates have relatively small brain weights. More precise data on
perinatal life history traits in large-bodied New World monkeys are needed.

ACKNOWLEDGMENTS
Alfie Rosenberger, Suzette Tardif, John Hearn, John Fleagle, Steve Leigh, and
Karen Strier provided very useful advice in the course of this study. Helpful com-
ments were provided by Anthony Rylands, John Ballou, Anne Savage, Sue Boin-
ski, William Mason, and Toni Ziegler. Michael Pereira offered detailed and very
118 / Hartwig
constructive criticisms of the manuscript. Tahalia Barrett and Sabrina Lewis as-
sisted with data collection. Unpublished data for Callicebus were provided by D.J.
Mayeaux, W.A. Mason, and S.P. Mendoza. Unpublished data for Lagothrix were
provided by Silvia Logsdon. This work was completed while the author was a
vostdoctoral research associate in the Department of Anatomy, State University
bf New York a t Stony Brook.
REFERENCES
Allman, J.; McLaughlin, T.; Hakeem, A. Brizzee, K.R.; Dunlap, W.P. Growth. Pp.
Brain weight and life-span in primate me- 363-413 in PRIMATE BIOLOGY, VOL-
cies. PRGCEEDINGS OF -THE NA- UME 3: REPRODUCTION AND DEVEL-
TIONAL ACADEMY OF SCIENCES USA OPMENT. W.R. Dukelow; J. Erwin, eds.
90~118-122. 1993. New York, Alan R. Liss, Inc., 1986.
Ardita, G. Checklist of the data on the ges- Carroll, J.B.; Abbott,-D.H.; George, L.M.;
tation length of primates. JOURNAL OF Hindle, J.E.; Martin, R.D. Urinary endo-
HUMAN EVOLUTION 5~213-222,1976. crine monitoring of the ovarian cycle and
Baker, A.J.; Woods, F. Reproduction of the pregnancy in Geoldi's monkey (Callimico
emperor tamarin (Saguinus imperator) in geoldii).JOURNAL OF REPRODUCTION
captivity, with comparisons to cotton-top AND FERTILITY 89149-161,1990.
and golden lion tamarins. AMERICAN Chambers, P.L.; Hearn, J.P. Embryonic, foe-
JOURNAL OF PRIMATOLOGY 26~1-10, tal and placental development in the com-
1992. mon marmoset (Callithrizjacchus).JOUR-
Bauchot, R.; Stephan, H. Encephalisation et NAL OF ZOOLOGY, LONDON [A] 207:
le niveau evolutif chez les simiens. MAM- 545-561.
MALIA 33:225-275,1969. Charnov, E.L. LIFE HISTORY INVARI-
Bauchot, R.; Manocha, S.L. La croissance en- ANTS. Oxford, Oxford University Press,
cephalique chez Saimiri sciureus [Simiens, 1993.
Cebides]. MAMMALIA 45:251-255, 1981. Chartin, J.; Petter, F. Reproduction et e1-
Beck, B.B.; Anderson, D.; Ogden, J.; Rett- Bvage en captivitk du oustiti. MAMMALIA
berg, B.; Brejla, C.; Scola, R.; Warneke, M. 24:153-155, 1960.
Breeding the Goeldi's monkey Callimico Chase, J.E.; Cooper, R.W. Saguinus nigricol-
goeldii at Brookfield Zoo, Chicago. INTER- lis: Physical growth and dental eruption
NATIONAL ZOOLOGICAL YEARBOOK in a small population of captive-born in-
22:106-114, 1982. dividuals. AMERICAN JOURNAL OF
Beischer, D.E.; Furry, D.E. Saimiri sciureus PHYSICAL ANTHROPOLOGY 30:111-
as an experimental animal. ANATOMI- 116,1969.
CAL RECORD 148:615-624,1964. Christen, A. Fortpflanzungsbiologie und
Boinski, S. Birth synchrony in squirrel mon- Verhalten bei Cebuellapygmaea und Tam-
keys (Saimiri oerstedi). A strategy to re- arin tamurin. ZEITSCHRIFT FUR
duce neonatal predation. BEHAVIORAL TIERPSYCHOLOGIE 14:5,1974.
ECOLOGY AND SOCIOBIOLOGY 21: Cicmanec, J.C.; Campbell, A.K. Breeding
393-400,1987. the owl monkey [Aotus trivirgatus] in a
Boinski, S.; Fragaszy, D.M. The ontogeny of laboratory environment. LABORATORY
foraging in squirrel monkeys, Saimiri oer- ANIMAL SCIENCE 27512-517, 1977.
stedi. ANIMAL BEHAVIOR 37:415-428, Coimbra-Filho, A.F.; Maia, A. 0 process0 de
1989. muda de p6los em Leontopithecus r. rosalia
Bowden, D.; Winter, P.; Ploog, D. Pregnancy (Linnaeus, 1766) (Callitrichidae, Pri-
and delivery behavior in the squirrel mon- mates). REVISTA BRASILEIRO DE BIO-
key [Saimiri sciureus] and other primates. LOGIA 39:83-93,1979.
FOLIA PRIMATOLOGICA 5:l-42,1967. Coimbra-Filho, A.F.; Pissinatti, A.; Rylands,
Brand, H.M. Urinary oestrogen excretion in A.B. Breeding muriquis Brachyteles arach-
the female cotton-topped tamarin (Sagui- noides in captivity: The experience of the
nus oedipus oedipus). JOURNAL OF RE- Rio de Janeiro Primate Center (CPRJ-
PRODUCTION AND FERTILITY 62:467- FEEMA). DODO 29:66-77,1993.
473,1981. Corner, B.D.; Richtsmeier, J.T. Cranial
Brand, H.M.; Martin, R.D. The relationship growth in the squirrel monkey (Saimiri
between female urinary estrogen excretion sciureus): A quantitative analysis using
and mating behavior in cotton-topped tam- three dimensional coordinate data. AMER-
arins, Saguinus oedipus oedipus. INTER- ICAN JOURNAL OF PHYSICAL AN-
NATIONAL JOURNAL OF PRIMATOL- THROPOLOGY 87:67-82,1992.
OGY 4:275-290,1983. Crockett, C.M.; Sekulic, R. Gestation length

in red howler monkeys. AMERICAN
JOURNAL OF PRIMATOLOGY 3~291-
294,1982.
Dietz, J.M.; Baker, A.J.; Miglioretti, D. Sea-
sonal variation in reproduction, juvenile
growth, and adult body mass in golden lion
tamarins (Leontopithecus rosaliu). AMER-
ICAN JOURNAL OF PRIMATOLOGY 34:
115-132,1994.
Dixson, A.F. The owl monkey (Aotus triuirg-
atus). Pp. 29-114 in REPRODUCTION IN
NEW WORLD PRIMATES. J.P. Hearn, ed.
Lancaster, MTP Press, 1983.
Dixson, A.F.; Martin, R.D.; Bonney, R.C.;
Fleming, D. Reproductive biology of the
owl monkey, Aotus triuirgatus griseimem-
bra. Pp. 61-68 in NON-HUMAN PRI-
MATE MODELS FOR STUDY OF HU-
MAN REPRODUCTION. Satellite Symp.
7th Congr. Int. Primatol. Soc., Bangalore,
1980.
Dukelow, W.R. The squirrel monkey (Sai-
miri sciureus). Pp. 181-216 in REPRO-
DUCTION IN NEW WORLD PRIMATES.
J.P. Hearn, ed. Lancaster, MTP Press,
1983.
Eisenberg, J.F. Reproduction in two species
of spider monkeys, Ateles fusciceps and
Ateles geofioyi. JOURNAL OF MAM-
MALOGY 541955-957, 1973.
Eisenberg, J.F. Comparative ecology and re-
production of New World monkeys. Pp.
13-21 in THE BIOLOGY AND CONSER-
VATION OF THE CALLITRICHIDAE.
D.G. Kleiman, ed. Washington, Smithso-
nian Institution Press, 1977.
Eisenberg, J.F. THE MAMMALIAN RADI-
ATIONS: AN ANALYSIS OF TRENDS IN
EVOLUTION, ADAPTATION, AND BE-
HAVIOR. Chicago, University of Chicago
Press, 1981.
Elias, M. Relative maturity and growth of
Cebus and squirrel monkeys at birth and
during infancy. DEVELOPMENTAL PSY-
CHOBIOLOGY 10:519-528,1977.
Elliott, M.W.; Sehgal, P.K.; Chalifoux, L.V.
Management and breeding of Aotus tri-
uirgatus. LABORATORY ANIMAL SCI-
ENCE 26:1037-1040,1976.
Epple, G. Maintenance, breeding and devel-
opment of marmoset monkeys (Callithri-
cidae) in captivity. FOLIA PRIMATOLOG-
ICA 12:56-76, 1970.
Epple, G.; Katz, Y. The saddle back tamarin
and other tamarins. Pp. 115-148 in RE-
PRODUCTION IN NEW WORLD PRI-
MATES. J.P. Hearn, ed. Lancaster, MTP
Press, 1983.
Fedigan, L.M.; Rose, L.M. Interbirth inter-
val variation in three sympatric species of
New World monkey. AMERICAN JOUR-
NAL OF PRIMATOLOGY 37:9-24,1995.
Fleagle, J.G.; Samonds, K.W. Physical
NWM Life History Traits I 119
growth of Cebus monkeys (Cebus albifrons)
during the first year of life. GROWTH 39:
35-53,1975. -
Ford, S.M. Callitrichids as phyletic dwarfs
and the d a c e of the Callitrichidae in
Platyrrhiii. PRIMATES 21:31-43, 1980.
Ford, S.M.; Davis, L.C. Systematics and
body size: Implications for feeding adapta-
tions in New World monkeys. AMERICAN
JOURNAL OF PHYSICAL ANTHROPOL-
OGY 88:415-468,1992.
Fragaszy, D.M. Early behavioral develop-
ment in capuchins (Cebus). FOLIA PRI-
MATOLOGICA 54:119-128,1990.
French, J.A. Lactation and fertility: An ex-
amination of nursing and interbirth inter-
vals in cotton-top tamarins (Saguinus 0.
oedipus). FOLIA PRIMATOLOGICA 40:
276-282,1983.
Garber. P.A. Feeding ecolom and behaviour
of the genus Sa&inus.u@p. 273-295 in
MARMOSETS AND TAMARJNS: SYS-
TEMATICS. ECOLOGY AND BEHAV- ~~~~ ~
IOUR. A.B.' Rylands, ed. Oxford, Oxford
University Press, 1993.
Gengozian, N.; Batson, J.S.; Smith, T.A.
Breeding of tamarins (Saguinus spp.) in
the laboratory. Pp. 207-213 in THE BIOL-
OGY AND CONSERVATION OF THE
CALLITRICHIDAE. D.G. Kleiman, ed.
Washington, Smithsonian Institution
Press, 1977.
Gensch, W. Birth and rearing of a black-
faced spider monkey, Ateles paniscus chu-
m e k Humboldt, at Dresden Zoo. INTER-
NATIONAL ZOO YEARBOOK 5:110,
1965.
Glander, K.E. Reproduction and population
growth in free-ranging mantled howling
monkeys. AMERICAN JOURNAL OF
PHYSICAL ANTHROPOLOGY 53:25-36,
1980.
Goss, C.M.; Popejoy, L.T.; Fusiler, J.L.;
Smith, T.M. Observations on the relation-
ship between embryological development,
time of conception, and gestation. Pp. 171-
192 in THE SQUIRREL MONKEY. L.A.
Rosenblum; R.W. Cooper, eds. New York,
Academic Press, 1968.
Hall, R.D.; Hodgen, G.D. Pregnancy diagno-
sis in owl monkeys (Aotus triuirgatus):
Evaluation of the haemagglutination inhi-
bition test for urinary chorionic gonadotro-
phin. LABORATORY ANIMAL SCIENCE
29~345-348, 1979.
Hampton, S.H.; Hampton, J.H. Detection of
reproductive cycles and pregnancy in tam-
arins (Suguinus spp.).Pp.193-206 in THE
BIOLOGY AND CONSERVATION OF
THE CALLITRICHIDAE. D.G. Kleiman,
ed. Washington, Smithsonian Institution
Press, 1977.
Hartwig, W.C. COMPARATIVE MOR-
120 / Hartwig
PHOLOGY, ONTOGENY AND ALLOME- Hill, K. Life history theory and evolutionary
TRY OF THE PLATYRRHINE CRA- anthropology. EVOLUTIONARY AN-
NIUM. Unpublished Ph.D. dissertation, THROPOLOGY 2:78-88,1993.
University of California, Berkeley, 1993. Hopf, S. Notes on pregnancy, delivery and
Hartwig, W.C. The effects of life history on infant survival in captive squirrel mon-
the squirrel monkey (PZatyrrhini: Saimiri) keys. PRIMATES 8323-332,1967.
cranium. AMERICAN JOURNAL OF Hrdlicka, A. Weight of the brain and of the
PHYSICAL ANTHROPOLOGY 97:435- internal organs in American monkeys.
449,1995. AMERICAN JOURNAL OF PHYSICAL
Harvey, P.; Clutton-Brock, T.H. Life history ANTHROPOLOGY 8:201-211,1925.
variation in Drimates. EVOLUTION 39: Hunter, A.J.; Martin, R.D.; Dixson, A.F.;
559-581, 198k Rudder, B.C.C. Gestation and inter-birth
Harvey, P.; Martin, R.D.; Clutton-Brock, intervals in the owl monkey (Aotus triuirg-
T.H. Life histories in comparative per- atus grisseimembra). FOLIA PRIMATO-
spective. Pp. 181-196 in PRIMATE SOCI- LOGICA 31:165-175, 1979.
ETIES. B.B. Smuts; D.L. Cheney; R.M. Janson, C.H.; Boinski, S. Morphological and
Seyfarth; R.W. Wrangham; and T.T. Stru- behavioral adaptations for foraging in gen-
shaker, eds. Chicago, University of Chi- eralist primates: The case of the cebines.
cago Press, 1987. AMERICAN JOURNAL OF PHYSICAL
Hayes, K.C.; Faye, G.; Roach, G. Breeding ANTHROPOLOGY 88:483-498,1992.
New World monkeys in a laboratory envi- Janson, C.H.; van Schaik, C. Ecological risk
ronment. Pp. 122-129 in BREEDING PRI- aversion in juvenile primates: Slow and
MATES. W.I.B. Beveridge, ed. Basel, steady wins the race. Pp.57-76 in JUVE-
Karger, 1972. NILE PRIMATES LIFE HISTORY, DE-
Hearn, J.P. The endocrinology of reproduc- VELOPMENT AND BEHAVIOR. M.E.
tion in the common marmoset, Callithrix Pereira; L.A. Fairbanks, eds. New York,
jacchus. Pp. 163-171 in THE BIOLOGY Oxford University Press, 1993.
AND CONSERVATION OF THE CAL- Jaquish, C.E.; Toal, R.L.; Tardif, S.D.; Car-
LITRICHIDAE. D.G. Kleiman, ed. Wash- son, R.L. Use of ultrasound to monitor pre-
ington, Smithsonian Institution Press, natal growth and development in the com-
1977. mon marmoset (Callithrix jacchus).
Hearn, J.P. Endocrinology and timing of im- AMERICAN JOURNAL OF PRIMATOL-
plantation in the marmoset monkey, Cal- OGY 36:259-275, 1995.
lithrix jacchus. PROGRESS IN REPRO- Jarosz, S.J.; Kuehl, T.J.; Dukelow, W.R.
DUCTIVE BIOLOGY 71262-269,1980. Vaginal cytology, induced ovulation and
Hearn, J.P. The common marmoset (Cal- gestation in the squirrel monkey (Saimiri
lithrk jacchus). Pp. 181-216 in REPRO- sciureus). BIOLOGY OF REPRODUC-
DUCTION IN NEW WORLD PRIMATES. TION 16:97,1977.
J.P. Hearn, ed. Lancaster, MTP Press, Jungers, W.L.; Fleagle, J.G. Postnatal
1983. growth allometry of the extremeties in Ce-
Heger, W.; Neubert, D. Maintenance and bus albifrons and Cebus apella: A longitu-
breeding of Callithrix jacchus in a colony in dinal and comparative study. AMERICAN
Berlin. Pp. 53-63 in NON-HUMAN PRI- JOURNAL OF PHYSICAL ANTHROPOL-
MATES-DEVELOPMENTAL BIOLOGY OGY 53:471-478, 1980.
AND TOXICOLOGY. D. Neubert, H J . Jurke, M.H.; Pryce, C.R.; Dobeli, M.; Martin,
Merker; A.G. Hendricx, eds. Wien, Ueber- R.D. Non-invasive detection and monitor-
reuter Wissenschaft, 1988. ing of pregnancy and the postpartum pe-
Heistermann, M.; Hodges, J.K. Endocrine riod in Goeldi’s monkey (Callirnico goeldii)
monitoring of the ovarian cycle and preg- using urinary pregnediol-3a-glucuronide.
nancy in the saddle-back tamarin (Sagui- AMERICAN JOURNAL OF PRIMATOL-
nus fuscicollis) by measurement of steroid OGY 34~319-331,1994.
conjugates in urine. AMERICAN JOUR- Kaack, B.; Walter, L.; Brizze, K.R. The
NAL OF PRIMATOLOGY 35:117-127, growth and development of the squirrel
1995. monkey (Saimiri sciureus). GROWTH 43:
Hemmer, B. Beitrag zur Erfassung der pro- 116-135, 1979.
gressionen Cephalisation bei Primaten. Kaplan, J. Growth and behavior of surro-
PROCEEDINGS OF THE 3RD INTERNA- gate-reared squirrel monkeys. DEVELOP-
TIONAL CONGRESS OF PRIMATOL- MENTAL PSYCHOBIOLOGY 7:7-13,
OGY 2~99-107,1971. 1974.
Hershkovitz, P. LIVING NEW WORLD Kaplan, J. Breeding and rearing squirrel
MONKEYS, VOLUME 1, WITH AN IN- monkeys, (Saimiri sciureus) in captivity.
TRODUCTION TO THE PRIMATES. Chi- LABORATORY ANIMAL SCIENCE 27:
cago, University of Chicago Press, 1977. 557,1977.

Kerber, W.T.; Conaway, C.H.; Moore-Smith,
D. The duration of gestation in the squirrel
monkey (Saimiri sciureus). LABORA-
TORY ANIMAL SCIENCE 27~700-702,
1977.
Kleiman, D.G. Characteristics of reproduc-
tion and sociosexual interactions in pairs of
lion tamarins (Leontopithecusrosalia) dur-
ing the reproductive cycle. Pp. 181-190 in
THE BIOLOGY AND CONSERVATION
OF-THE CALLITRICHIDAE. D.G. Klei-
man, ed. Washington, Smithsonian Insti-
tution Press, 1977.
Lee, P.C.; Majluf, P.; Gordon, I.J. Growth,
weaning and maternal investment from a
comparative perspective. JOURNAL OF
ZOOLOGY [LONDON] 225:99-114.1991.
Leigh, S.R. Growing up to be a primate.
EVOLUTIONARY ANTHROPOLOGY 3:
~ PRIMATOLOGY 21:285-298,1992.
106-108,1994a.
Leigh, S.R. Relations between captive and
noncaptive weights in anthropoid pri-
mates. ZOO BIOLOGY 13:21-43, 1994b.
Leutenegger, W. Beziehungen zwischen der
Neugeborenengrosse und dem Sexualdi-
morphismus am Becken bei simischen Pri-
maten. FOLIA PRIMATOLOGICA 12:
224-235,1970.
Leutenegger, W. Maternal-fetal weight re-
lationships in primates. FOLIA PRIMA-
TOLOGICA 201280-293,1973.
Leutenegger, W. Monogamy in callitrichids:
A consequence of phyletic dwarfism? IN-
TERNATIONAL JOURNAL OF PRIMA-
TOLOGY 1195-98,1980.
Leutenegger, W. Encephalization and ob-
stetrics in primates with particular refer-
ence to human evolution. Pp. 85-95 in
PRIMATE BRAIN EVOLUTION, METH-
ODS AND CONCEPTS. E. Armstrong; D.
Falk, eds. New York, Plenum, 1982.
Long, J.O.; Cooper, R.W. Physical growth
and dental eruption in captive-bred squir-
rel monkeys, Saimiri sciureus (Letica, Co-
lombia). Pp. 193-206 in THE SQUIRREL
MONKEY. L.A. Rosenblum; R.W. Cooper,
eds. New York, Academic Press, 1968.
Lorenz, R. von; Heinemann, H. Beitrag zur
morphologie und korperlichen jugen-
dentwicklung des springtamarin Callirnico
goeldii (Thomas, 1904). FOLIA PRIMATO-
LOGICA 611-27,1967.
Malaga, C.A.; Weller, R.E.; Buschbom, R.L.
Twinning in the karyotype I night monkey
(Aotus nancymui). JOURNAL OF MEDI-
CAL PRIMATOLOGY 20:370-372,1991.
Manocha, S.L. Physical growth and brain
development of captive-bred male and fe-
male squirrel monkeys, Saimiri sciureus.
EXPERIENTIA 35~96-98,1979.
Martin, R.D. PRIMATE ORIGINS AND EV-
OLUTION. Princeton, Princeton Univer-
sity Press, 1990.
NWM Life History Traits I 121
Martin, R.D. Goeldi and the dwarfs: The ev-
olutionary biology of the small New World
monkeys. JOURNAL OF HUMAN EVO-
LUTION 22:367-393, 1992.
Martin, R.D.; MacLarnon, A.M. Gestation
period, neonatal size and maternal invest-
ment in placental mammals. NATURE
313:220-223,1985.
Martin, R.D.; MacLarnon, A.M. Compara-
tive quantitative studies of growth and re-
production. SYMPOSIUM OF THE ZOO-
LOGICAL SOCIETY OF LONDON 60:39-
80, 1988.
Missler, M.; Wolff, J.R.; Rothe, H.; Heger,
W.; Merker, HA.; Treiber, A.; Scheid, R.;
Crook, G.A. Developmental biology of the
common marmoset: Proposal for a “postna-
tal staging.” JOURNAL OF MEDICAL
Mitchell, S.K.;Jones, S.M. Diagnosis of
pregnancy in marmosets (Callithrijc jac-
ehus). LABORATORY ANIMALS 9:49-
56, 1975.
Moore, H.D.M.; Gems, S.; Hearn, J.P. Early
implantation stages in the marmoset mon-
key (Callithrijc jacchus). AMERICAN
JOURNAL OF ANATOMY 172:265-278,
1985.
Nagle, C.A.; Denari, J.H. The Cebus monkey
(Cebus upella). Pp. 39-68 in REPRODUC-
TION IN NEW WORLD PRIMATES.
Hearn, J.P., ed. Lancaster, MTP Press,
1983.
Oerke, A.-K.; Einspanier, A.; Hodges, J.K.
Detection of pregnancy and monitoring
patterns of uterine and fetal growth in the
marmoset monkey (Callithrijcjacchus) by
real-time ultrasonography. AMERICAN
JOURNAL OF PRIMATOLOGY 36:l-13,
1995.
Pereira, M.E. Asynchrony within estrous
synchrony among ringailed lemurs (Pri-
mates: Lemuridae). PHYSIOLOGY AND
BEHAVIOR 49:47-52,1991.
Pereira, M.E.; Weiss, M.L. Female mate
choice, male migration, and the threat of
infanticide in ringtailed lemurs. BEHAV-
IORAL ECOLOGY AND SOCIOBIOL-
OGY 28~141-152,1991.
Pereira, M.E.; Fairbanks, L., eds. JUVE-
NILE PRIMATES: LIFE HISTORY, DE-
VELOPMENT AND BEHAVIOR. New
York, Oxford University Press, 1993.
Peres, C.A. Notes on the primates of the
JuruA River, Western Brazilian Ammonia.
FOLIA PRIMATOLOGICA 61:97-103,
1993.
Peres, C.A. Which are the largest New
World monkeys? JOURNAL OF HUMAN
EVOLUTION 26:245-249, 1994.
Phillips, I.R. The embryology of the common
marmoset (Callithrix jacchus). AD-
VANCES IN ANATOMY, EMBRYOL-
122 I Hartwig
OGY, AND CELL BIOLOGY 52:l-46, sition of the squirrel monkey (Suimiri sci-
1976. ureus). GROWTH 44:271-286,1980.
Ploog, D.; Hopf, S.; Winter, P. Ontogenese Sacher, G.A.; Staffeldt, E.F. Relation of ges-
des Verhaltens von TotenkopfAffen tation time to brain weight for placental
(Suimiri sciureus). PSYCHOLOGISCHE mammals: Implications for the theory of
FORSCHUNG 3l:l-41,1967. vertebrate growth. AMERICAN NATU-
Pucciarelli, H.M.; Dressino, V.; Niveiro, RALIST 108593-615,1974.
M.H. Changes in skull components of the Schmidt, U. Untersuchungen zur visuellen
squirrel monkey evoked by growth and nu- Raumorientierung bei TotenkoDfMen
trition: An experimental study. AMERI- (Suimiri sciureii). ZEISCHRW~ FUR
CAN JOURNAL OF PHYSICAL AN- VERGLEICHEND PHYSIOLOGIE 60
THROPOLOGY 81:535-544,1990. 176-208.1968.
Rabb, G.B.; Rowell, J.E. Notes on reproduc- Shoemaker, A.H. Notes on the reproductive
tion in captive marmosets. JOURNAL OF biology of the white-faced saki (Pithecia
MAMMALOGY 41:401,1959. pithecia) in captivity. INTERNATIONAL
Rasmussen, K.M.; Ausman, L.M.; Hayes, ZOO YEARBOOK 22:124-126,1980.
K.C. Vital statistics from a laboratory Smith, C.A.; Moore, H.D.M.; Hearn, J.P. The
breeding colony of squirrel monkeys ultrastructure of early implantation in the
(Suimiri sciureus). LABORATORY ANI- marmoset monkey (Cullithrix jucchus).
MAL SCIENCE 30:99,1980. ANATOMY AND EMBRYOLOGY 175:
Ridley, M. Pelvic sexual dimorphism and 399-410,1987.
relative neonatal brain size really are re- Snowdon, C.T.; Soini, P. The tamarins. ge-
lated. AMERICAN JOURNAL OF PHYS- nus SGuinus. Pp.223-298 in ECOLOGY
ICAL ANTHROPOLOGY 97:197-200, AND BEHAVIOR OF NEOTROPICAL
1995. PRIMATES, VOLUME 2. R.A. Mitter-
Roff, D.A. THE EVOLUTION OF LIFE HIS- meier; A.B. Rylands; A. Coimbra-Filho;
TORY: THEORY AND ANALYSIS. New G.A.B. Fonseca, eds. Washington, DC,
York, Chapman and Hall, 1992. World Wildlife Fund, 1988.
Rosenberger, A.L. PHYLOGENY, EVOLU- Soini, P. The pygmy marmoset, genus Ce-
TION, AND CLASSIFICATION OF THE buellu. Pp.79-129 in ECOLOGY AND BE-
NEW WORLD MONKEYS (PLATYR- HAVIOR OF NEOTROPICAL PRI-
RHINI, PRIMATES). Unpublished Ph.D. MATES, VOLUME 2. R.A. Mittermeier;
dissertation, New York, City University of A.B. Rylands; A. Coimbra-Filho; G.A.B.
New York, 1979. Fonseca, eds. Washington, DC, World
Rosenberger, A.L. Evolution of feeding Wildlife Fund, 1988.
niches in New World monkeys. AMERI- Stearns, S.C. THE EVOLUTION OF LIFE
CAN JOURNAL OF PHYSICAL AN- HISTORIES. Oxford, Oxford University
THROPOLOGY 88525-562,1992. Press, 1992.
Rosenberger, A.L.; Coimbra-Filho, A.F. Stephan, H.; Baron, G.; Frahm, H.D. Com-
Morphology, taxonomy status and &hi- parative size of brains and brain com-
ties of the lion tamarins, Leontopithecus ponents. Pp. 1-38 in COMPARATIVE
(Callitrichinae, Cebidae). FOLIA PRIMA- PRIMATE BIOLOGY, VOLUME 4: NEU-
TOLOGICA 42~149-179,1984. ROSCIENCES. Steklis, H.D.; Erwin, J.,
Ross, C. Life history-patterns of New World eds. New York, Alan R. Liss, Inc., 1986.
monkeys. INTERNATIONAL JOURNAL Stevenson, M.F. Birth and perinatal behav-
OF PRIMATOLOGY 12:481-502,1991. ior in family groups of the common marmo-
Rothe, H. Beobachtungen zur Geburt beim set (Cullithrix jacchus jucchus), compared
Weissbushaffen (Cullithrix jucchus Er- to other primates. JOURNAL OF HUMAN
xleben, 1777). PRIMATES 19:257-285, EVOLUTION 5:365-381,1976.
1973. Stolzenberg, S.J.; Jones, D.C.L.; Kaplan,
Rothe, H. Further observations on the deliv- J.N.; Barth, R.A.; Hodgen, G.D.; Madan,
ery behaviour of the common marmoset S.M. Studies with timed-pregnant squirrel
(Cullithrix jacchus). ZEITSCHRIFT FUR monkeys (Suimiri sciureus). JOURNAL
SAUGERTIERKUNDE 39:135-142,1974. OF MEDICAL PRIMATOLOGY 8:29,
Rothe, H. Parturition and related behavior 1979.
in Cullithrix iacchus (Ceboidea. Callitri- Strier, K.B. Reproducfto de Brachyteles
chidae). Pp. i93-206 in THE BIOLOGY urachnoides (Primates, Cebidae). Pp. 163-
AND CONSERVATION OF THE CAL- 176 in A PRIMATOLOGIA NO BRASIL,
LITRICHIDAE. Kleiman. D.G.. ed. Wash- VOLUME 2.de Mello, M.T., ed. Rio de Ja-
ington, Smithsonian Institution Press, neiro, Sociedade Brasileira de Primatolo-
1977. gia, 1986.
Russo, A.R. ; Ausman, L.M.; Gallina, D.L. ; Sussman, R.W.; Kinzey, W.G. The ecological
Hegsted, D.M. Developmental body compo- role of the Callitrichidae: A review.

AMERICAN JOURNAL OF PHYSICAL
ANTHROPOLOGY 64~419-449,1984.
Tardif, S.D. Relative energetic cost of infant
care in small-bodied neotropical primates
and its relation to infant-care patterns.
AMERICAN JOURNAL OF PRIMATOL-
OGY 34:133-143, 1994.
Tardif, S.D.; Harrison, M.L.; Simek, M.A.
Communal infant care in marmosets and
tamarins: Relation to energetics, ecology,
and social organization. Pp. 220-234 in
MARMOSETS AND TAMARINS. Ry-
lands, A.B., ed. Oxford. Oxford University
Press, 1993.
Ulmer, F.A. Gestation of the lion marmoset.
JOURNAL OF MAMMALOGY 42:253-
254,1961.
Watts, E.S. A comparative study of neonatal
skeletal development in Cebus and other
primates. FOLIA PRIMATOLOGICA 54:
217-224,1990.
Wilen, R.; Naftolin, F. Pubertal age, weight,
and weight gain in individual female New
World monkeys (Cebus albifrons). PRI-
MATES 19:769-774,1978.
Williams, L. Breeding Humboldt's woolly
monkey (Lagothrix lagotrich) at Murray-
ton Woolly Monkey Sanctuary. INTERNA-
TIONAL ZOO YEARBOOK 7~86-89,
1967.
Wilson, C.G. Gestation and reproduction in
golden lion tamarins. Pp.191-192 in THE
BIOLOGY AND CONSERVATION OF
THE CALLITRICHIDAE. Kleiman, D.G.,
ed. Washington, Smithsonian Institution
Press, 1977.
Wolfe, L.G.; Ogden, J.D.; Deinhardt, J.B.;
Fisher, L; Deinhardt, F. Breeding and
hand-rearing marmosets for viral oncogen-
NWM Life History Traits / 123
esis studies. Pp. 145-157 in BREEDING
PRIMATES. Beveridee. - , W.I.B.. ed. Basel.
Karger, 1972.
Wolfe, L.G.; Deinhardt, F.; Ogden, J.D.; Ad-
a m ~ .M.R.: Fisher. L.E. ReDroduction of
wild-caught and laboratory born marmoset
species used in biomedical research (Sagu-
inus sp., Callithrix jacchus). LABORA-
TORY ANIMAL SCIENCE 26:802,1975.
Ziegler, T.E.; Bridson, W.E.; Snowdon, C.T.;
Eman, S. Urinary gonadotropin and es-
trogen excretion during the postpartum
estrus, conception, and pregnancy in the
cotton-top tamarin (Saguinusoedipus oedi-
P U S ) .AMERICAN JOURNAL OF PRIMA-
TOLOGY 12:127-140, 1987.
Ziegler, T.E.; Snowdon, C.T.; Warneke, M.
Postpartum ovulation and conception in
Goeldi's monkey, Callimico goeldii. FOLIA
PRIMATOLOGICA 52206-210,1989.
Ziegler, T.E.; Snowdon, C.T.; Bridson, W.E.
Reproductive performance and excretion of
urinary estrogens and gonadotropins in the
female pygmy marmoset (Cebuella pyg-
m a ) . AMERICAN JOURNAL OF PRI-
MATOLOGY 22:191-203,1990a.
Ziegler, T.E.; Snowdon, C.T.; Warneke, T.E.;
Bridson, W.E. Urinary excretion of oes-
trone conjugates and gonadotrophins
during pregnancy in the Goeldi's monkey
(Callimico goeldii). JOURNAL OF RE-
PRODUCTION AND FERTILITY 89:163-
168,1990b.
Ziegler, T.E.; Widowski, T.M.; Larson, M.L.;
Snowdon, C.T. Nursing does affect the du-
ration of post partum to ovulation interval
in cotton-top tamarins (Saguinus oedipus).
JOURNAL OF REPRODUCTION AND
FERTILITY 90563-570,1990~.
124 I Hartwig
APPENDIX Genera Arranged Alphabetically*
Gestation Neonatal Adultbody Neo Adult Re1
length body w t weight brain brain neo
source Species (days) (9) (a) wt (e) wt (El size
Alouatla
Leutenegger, 1970 A . uillosa 480 6,000(est)
Sacher & SMeldt,
1974 139 440 7,670 30.8 54 0.06
Ardito, 1976 180-194 440
Ardito, 1976 A . seniculus 139
Eisenberg, 1977 A . uillosa 180-194
Glander, 1980 A . palliata 186 c. 6.000
Crockett & Sekulic,
1982 A . seniculus 1M-194
Harvey et al., 1987 A. camya 5,700 56.7
A. palliatu 187 480 5,700 30.8 55.1
A . seniculus 6,400 57.9
Lee et al., 1991 A. palliata 318 fj,000
Ford & Davis, 1992 mixed 5,572
A . camya 3,800-5410
x = 4,800
A . palliata 3,100-7.600
x = 6,095
A . seniculus 4,200-7,000
x = 5,600
Leigh, 1994b A . camya 5,539
Fedigan & Rose, 1995 A . palliatu 5,700(f)
Aotus
Elliott et al., 1976 A. triuirgatus 148-159* 71-113 715-1,120d
x = 91.9 x = 878
Cicmanec & Campbell,
1977 120-140b
Hall & Hodgen, 1979 126 0.09
Hunter et al., 1979 133'
Dixson et al., 1980 133*
Dixson, 1983 13Ea 90-105
Harvey et al., 1987 133 98 1,000 10.1 18.2 0.1
Lee et al., 1991 98 1,000
Malaga et al., 1991 120-159
Ross, 1991 97 724
Ford & Davis, 1992 567-1,208
x = 945
Peres, 1993 87 1,057k 132
Leigh, 1994b 1,000
Ateles
Gensch, 1965 A . paniscus 480
Leutenegger, 1970 A. geofroyi 512 7,600
Eisenberg, 1973 A. fusciceps 226-232
A . geofroyi 226-232
Sacher & Staffeldt,
1974 A . dariensis 140 407 9,100 58 114 0.04
A . geofroyi 140 512 7,640 64 109 0.07
Ardito, 1976 A . paniscus 139
Harvey et al., 1987 A . belzebuth 5,800 106.6
A . fusciceps 226 9,100 114.7
A. geofroyi 229 426 5,800 64.0 110.9
A. paniscus 480 5,800 109.9
Lee et al., 1991 A . geofroyi 426 8,400
A . paniscus 480 7,700
Ford & Davis, 1992 mixed 8,214
A . belzebuth 5,824-10,400
x = 8,112
A . fusciceps 6,590-9,400
x = 7,995
A. geofroyi 6,000-10,000
x = 8,000
A. paniscus 6,500-11,000
x = 8,750
Leigh, 1994b A . geofroyi 6,458
(continued)
 NWM Life History Traits / 125
APPENDIX Genera Arranged Alphabetically* (Continued)
Gestation Neonatal Adult body Neo Adult Re1
length body w t weight brain brain neo
Source Species (days) (9) ig) wt ig) wt (9) size
Fedigan & Rose, 1995 A.geofiyi 6,750
Brachytules
Strier, 1986 210-260 est
Ford & Davis, 1992 6,900-12.000
x = 9,450
Cacajan
Ford & Davis, 1992 2,740-3,550
x = 3,057
Callicebus
Ross, 1991 C . moloch 100 1,004
79.3, n
Mason et al., unpub. C . moloch = 27 1,112 (n = 19)
SE =
3.05
Ford & Davis, 1992 C . moloch 700-1,266
x = 983
Leigh, 1994b C. moloch 1,241
Callimico
Lorenz & Heinemann,
1967 C. goeldii 149-165a 59.8 445-481
Christen, 1968 133-140' 35-45 472 0.08
Leutenegger, 1973 154 40
Ardito, 1975 149-154 40
Harvey et al., 1987 154 48.6 530 5.8 10.8 0.09
Ziegler et al., 199Ob 144-157'
x = 148.8
Carmll et al., 1990 150-160
145; 155'
Ross, 1991 51 582
Ford & Davis, 1992 410-5558
x = 492
Jurke et al., 1994 147-157'
151.5
Leigh, 1994b 621
Callithrix
Lucae Hume, 1927 [in
Hershkovitz, 19771 138-170 21-38
x = 30.3
Chartin & Petter, 1960 150 21.3
Christen, 1968 140' 25-30 220 average 0.12
28.0
Leutenegger, 1970 mean 262 mean
Epple, 1970 140-150' 29.3-34.7
117-173 27.5
x = 137 29.3
Rothe, 1974 14Cih
Sacher & Staffeldt,
1974 145 35.3 220 3.7 7.8 0.16
Mitchell & Jones, 1975 135-140h
Rothe, 1975 150-156b 30.0
Phillips, 1976 150
Ardito, 1976 140-150
117-156
140-146
160-173
Stevenson, 1976 144 27.5
Rothe, 1977 144 27.5
150-155b
Hearn, 1977 148 k 4.7
Hershkovitz, 1977 117-173 30 316
Chambers & Hearn,
1979 144
Hearn, 1983 144k2
141-146'
126 I Hartwig
APPENDIX Genera Arranged Alphabetically*(Continued)
Gestation Neonatal Adultbody Neo Adult Re1
length bodywt weight brain brain neo
Source Species (days) (g) (g) wt(g) wt@) size
Harvey et al., 1987 148 28 290 4.4 7.9 0.1
Heger & Neubert, 1988 143 avg 26-36
x =
31.47
Ross, 1991 C . jacchus 27 287
C. argentata 35 353
Missler et al., 1992 142.4'
141-144b
Ford & Davis, 1992 C. argentata 236-404
x = 320
C . humemlifer 240-380
x = 310
C .jaechus 125-617
x = 371'
Leigh, 1994b C . jacchus 352
Cebuella
Christen, 1968 C. p y g m a 133-140 16; 14-16 136 0.1
Leutenegger, 1973 145 16 0.13
Ardito, 1976 140-150
Hershkovitz, 1977
(summary of many
reports) 137-142 16,s 107 wild
141 avg
119 avg
124 avg
117 avg
108 avg
116 avg
128 avg
138 avg
133 avg
Harvey et al., 1987 136 16 140 4.2 0.11
Soini, 1988 137-138 13-15 121.8
Ziegler et al., 1990a 129-134'
Ross, 1991 15 79
Ford & Davis, 1992 112-155
x = 128
Leigh, 1994b 156
Cebus
Hayes et al., 1972 Capella + 162 234 0.10
C . albifrons
Leutenegger, 1973 180 230 0.1
Sacher & Staffeldt,
1974 180 250 3.700 29 73 0.07
Fleagle & Samonds,
1975 C . albifrons 222.1 f
250.7 m
Ardito, 1976 180
Eli=, 1977 C. albitivns 227.7 f 1,840-2,280 32.6 66.8f
237.5 m x = 2,060 34.4
Wilen & NaFtolin, 1978 C. albifrons 226
Jungers & Fleagle,
1980 C. albifrons 225.9 f
247.6 m
C. apella 214.0 f
243.2 m
Harvey et al., 1987 C . albifrons 234 2,600 82
C. apella 160 248 2,100
C. capueinus 230 2,700 29
Ross, 1991 C. albifrom 234 2,067
C . apella 240 2,201
C. capueinus 230 2,578
Nagle & Denari, 1983 155 2 7 238 0.10
(continued)
 NWM Life History Traits I 127
APPENDIX Genera Arranged Alphabetically* (Continued)
Gestation Neonatal Adultbody Neo Adult Re1
length body wt weight brain brain neo
Source Species (days) (g) (g) wt (9) wt (g) size
Ford & Davis, 1992 C . albifmns 1,400-2,228
x = 1,814
C . apella 1,370-3.400
x = 2,385
C . capucinus 2.610-4,090
x = 3,350
C . olimeous 1,589-3,200
x = 2,395
Leigh, 1994b C . apella 3,190
Fedigan BE Rose, 1995 C. capucinus 2,280 (0
Chimpotes
Ford & Davis, 1992 1,900-3,300
x = 2,555
Logothrir
Williams, 1967 225 450
Leutenegger, 1973 450 5,400
Ardito, 1976 250
Harvey et al., 1987 225 450 5,800 79.2 0.08
Ford & Davis, 1992 5,000-6,500
x = 5,750
Leigh, 1994b 5,770k
Logedon, unpub. 215 310-530
x = 413
Leontopithecus
Rabb & Rowell, 1959 L.msalin 134b
Ulmer, 1961 132-134h
133b
Lorenz & Heinemann,
1967 133
132-137
Christen, 1968 140-168 33-35 483 0.07
Epple, 1970 540
Ardita, 1976 132-134
Hershkovitz, 1977 57 583 0.10
Kleiman, 1977 128h
Wilson, 1977 136Bb
Hoage, 1978 128 61
Wilson, 1978 125-132
Kleiman, 1978 125-132
Eisenberg, 1981 128 61 0.11
Harvey et al., 1987 129 53.6 550 12.9 0.1
Roes. 1991 50 559
Ford & Davis, 1992 361-794
x = 578
Dietz et al., 1994 598'
Leigh, 1994b 659
Pithecia
Leutenegger, 1973 163
Eisenberg, 1977 163
Shoemaker, 1982 148
Harvey et al., 1987 163 1,400 31.7
Ford & Davis, 1992 779-2,250
x = 1.515
Savage, pers. comm. 153'
Saguinus
Hrdlicka, 1925 42.6 482 0.29
43.5 494
44.5 472
46.5 487
Christen, 1968 S.oedipus 154 35-40 510
Chase & Cooper, 1969 S.nigricollis 33.8-56.8 435
x = 43.5
37.9-50.1 491
128 / Hartwig
APPENDIX Genera Arranged Alphabetically*(Continued)
Gestation Neonatal Adult body Neo Adult Re1
length body wt weight brain brain neo
Source Species (days) (g) (g) wt (p.1 wt (a) size
x = 44.7
32.0-48.1 467
x = 42.4
24.0-45.0 491
x = 36
48.4 436
45.7 450
35.3 458
47.5 469
43.3 505
44.0 477
Epple, 1970 S. geoffroyi 140-150 41
Hamptan & Hampton,
1977 S. oedipus 36 (24-45)
Wolfe et al., 1972 S. nigricollis 140 43.5 419 0.1
140-168 30.1-46.0 432
x = 37.9
Leutenegger, 1973 S. midas 140 39 510 0.08
S.oedipus 140 40
Wolfe et al., 1975 S. fuscicollis 30-53 314-375
x = 39
S. nigricollis 34-57 447
x = 43.5
33.2-52.8 480
x = 42.1
Ardito, 1976 s. fuscicollis 134-170
S . nigricollis 132-134
S . oedipus 140-150
Gengozian et al., 1977 140-150
Hershkovitz. 1977 S. fwcicollis 146-170
S. miah 140-168
S . oedipus 122-153 453-567 10.6
summary 43 450
Brand, 1981 S . oedipus 153-166
Eisenberg, 1981 S. midas 140 39,40 0.08
Brand & Martin, 1983 S . oedipus 170-172
Epple & Katz, 1983 S . oedipus 150
Ziegler et al., 1987 S . oedipus 182-185'
Harvey et al., 1987 S. midm 127 36 530 10.4 0.07
S. nigricollis 43.5 460 8.9
S. oedipus 145 43.2 510 4.9 9.0
S . fuscicollis 149 40 370 9.3
S. geoffmyi 50 510 10.5
Ross, 1991 S. midas 40 558
S . nigricollis 44 350
S . oedipus 44 425
s. fuscicollis 40 350
S . labintus 44 520
Baker & Woods, 1992 S. impemtor 154b
Heistermam &
Hodges, 1995 s. fuscicollis 149.3'
Ford & Davis, 1992 S . midas 272-600
x = 432
S . nigricollis 458-505
x = 482
S. oedipus 244-510
x = 377
s. fuscicollis 327-535
x = 403
S. geoficyi 448-640
x=544
S. labiatus 380-550
x = 465
Leigh, 1994b s. fuscicollis 419
S. geofroyi 493
(continued)
 NWM Life History Traits / 129
APPENDIX Genera Arranged Alphabetically*(Continued)
Gestation Neonatal Adultbody Neo Adult Re1
length bcdywt weight brain brain neo
Source Species (days) (g) (g) wt (g) w t (g) size
S . impemtor 525
S . oedipus 534
Saimiri
Beischer & Furry, 1964 S.sciureus 167 * 2 530.5 18.5
471.1 22.8
721.2 23.3
603.0 14.3
785.2 21.6
929.5 21.6
742.5 26.9
583.0 22.8
688.0 20.6
580.0 21.1
Hopf, 1967 87;155 0.12
Bowden et al., 1967 175 84 590
Christen, 1968 175-182 84 590
Leutenegger, 1973 157 84
Mito,1976 152-168
165
168-172
168-182
175
180
Elias, 1977 female 110.0 590-744 14.6 23.3
male 112.9 910-1,070 15.5 25.3
Jarosz et al., 1977 S. boliviensis 155 102 0.15
Kerber et al., 1977 141-154'
Manocha, 1979 105.0 620-710 13.13
96.2 13.05
118.1 13.84
102.0 13.57
114.0 14.56
124.5 14.56
119.5 13.99
120.0 14.11
117.5 14.22
110.0 13.99
91.8 13.95
114.5 14.01
97.0 12.04
117.2 14.32
112.5 13.98
118.5 16.00
91.6 14.96
96.3 12.80
107.7 14.41
Stolzenberg et al., 1979 141-158 100
x = 152.5
Russo et al., 1980 116.3 m
108.2 f
Dukelow, 1983 137-170 0.13
x = 150
Harvey et al., 1987 170 95 580 24.4
Ross, 1991 95 699
Ford & Davis, 1992 S . boliuiensis 700-900
x = 800
S . sciureus 327-810
x = 569m
Leigh, 1994b 668

*Species names are listed when specified by the authors. Gestation length is assumed to be from observation of
last copulation unlesa otherwise specified. The use of a single mean figure or a range and mean follows the usage
of the authors in question. Neonatal body weight ranges follow those reported by the authors. Data for
(continued)
130 / Hartwig
individuals are reproduced here as they were originally reported. The figures reported in the adult body weight
column are means for the sample reported by the authors. In most cases this mean includes males and females,
and is presented here as a record of the information the authors used.The graphs in this study were generated
from captive adult female body weights as reported by Ford and Davis [19921and Leigh [1994bJ. Ford and Davis
[1992]figures were compiled from their Tables 1 and 3. Ford and Davis [19921 did not calculate a mean for
captive adult females, 80 the mean figure reported here is their mean for wild and captive females as reported
in their Table 3.The range is the composite range of values for female weights as reported in their Table 2.Peres
[19931data are on wildcaptured individuals; weights reported are the wild-caught weights of adults from the
same population.
*Observation.
bInterbirth interval.
"Controlled date of conception.
%I = 14.
eEstimate.
Qormonally determined.
%ales and females.
hObservationa1 data.
'This value is considerably higher than the overall mean (307)reported by Ford and Davis [1992:Table 31 for
the species.
Jn = 13.
'Mean for wild females.
'Wild weights, but based on large sample (n = 185)measured throughout the year.
mThisunusually low mean is driven by the low weights of the range aa reported by Bauchot and Stephan [19691.