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Are Kirindy sifaka capital or income breeders It depends.

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American Journal of Primatology 67:365–369 (2005)
Are Kirindy Sifaka Capital or Income Breeders? It Depends
Department of Biological Anthropology and Anatomy, Duke University, Durham,
North Carolina
Department of Sociobiology and Anthropology, University of Göttingen, Göttingen,
Department of Behavioral Ecology and Sociobiology, German Primate Center, Göttingen,
The capital and income breeding framework has only recently been used
to explain variation in female reproductive strategies in primates. The
application of this framework to primates and other mammals with long
reproductive cycles has not been consistent. We evaluated data on
Verreaux’s sifaka (Propithecus verreauxi verreauxi) in the Kirindy Forest
of western Madagascar to determine whether they are capital or income
breeders. We found that Verreaux’s sifaka can be classified as either
capital or income breeders, depending on how these concepts are
operationalized. These conflicting findings highlight why the capital/
income framework is currently problematic and must be standardized
if it is to be a useful framework for primatologists. Am. J. Primatol.
67:365–369, 2005.
r 2005 Wiley-Liss, Inc.
Key words: life history; Propithecus; female reproductive strategies
Studies of life history often examine the relationship between resource
availability and reproduction. The allocation of resources to somatic and
reproductive investment is typically viewed as antagonistic. When animals live
in a seasonal environment, this trade-off between survival and reproduction can
be particularly pronounced. How females manage the consequences of the
fluctuation of food availability can have important implications for their
reproductive success.
One framework that has been used to explain primate reproductive strategies
in this context is the distinction between capital and income breeding [e.g., Gould
et al., 2003; Richard et al., 2000, 2002]. Drent and Daan [1980] originally
introduced this dichotomy to describe avian reproductive tactics. Most studies,
however, refer to the revised definitions suggested by life-history theorists:
Contract grant sponsor: Wenner-Gren Foundation; Contract grant sponsor: Leakey Foundation;
Contract grant sponsor: NSF; Contract grant sponsor: DFG.
Correspondence to: Rebecca J. Lewis, Department of Anthropology, University of Texas at Austin,
1 University Station C3200, Austin, TX 78712. E-mail:
Received 22 November 2004; revised 17 February 2005; revision accepted 31 March 2005
DOI 10.1002/ajp.20190
Published online in Wiley InterScience (
2005 Wiley-Liss, Inc.
366 / Lewis and Kappeler
‘‘capital breeders’’ build their resources (e.g., body fat, food caches, etc.) and store
them for times of reproduction, whereas ‘‘income breeders’’ use current food
intake (rather than any stored sources of fat or food caches) to determine
offspring production [Jönsson, 1997; Stearns, 1989, 1992]. In birds, this
framework has been used to ascertain whether increased food intake will allow
a female to increase her clutch size. However, primates and other large mammals
generally give birth to singletons. The framework is thus applied to mammals
such that interspecific variation in patterns of body mass fluctuation may depend
on the reproductive strategy of the species. For instance, whereas a capital
breeder that stores energy endogenously is expected to have the highest body
mass just prior to reproduction, the body mass of an income breeder is not
expected to fluctuate as much.
One difficulty with applying the capital/income breeding framework to
mammals is that the definition of the term ‘‘reproduction’’ is not clear. In animals
with a short reproductive cycle such as birds, ‘‘reproduction’’ can refer to the
entire cycle of conception through weaning. However, in most primates and other
large mammals, reproduction lasts for a longer period of time. The entire cycle of
reproduction (conception, gestation, birth, lactation, and weaning) in these
species can take a year or more to complete. Determining which stage in the
reproductive cycle should be considered reproduction makes it difficult to apply
the capital/income framework in primates, and has led to different interpretations of the same strategy in sympatric lemurs. For example, Richard and
colleagues [2000, 2002] suggested the fact that sifakas (Propithecus verreauxi)
give birth during the lean season, and wean during periods of high food
availability is evidence of a capital breeding strategy. On the other hand, Gould
and colleagues [2003] interpreted ‘‘reproduction’’ to mean lactation and weaning.
Thus, they stated that ‘‘yring-tailed lemurs at Beza Mahafaly may be ‘income
breeders’ rather than ‘capital breeders,’ i.e., females do not strongly rely upon
resources such as fat stores during reproduction; rather they use maximum
resources obtained from the environment when in the process of gestation and
lactation [Stearns, 1992; Jönsson, 1997]. Ring-tailed lemurs lactate and wean
infants during the wet season, a time of maximal food availability [Sauther et al.,
1999].’’ [Gould et al., 2003, p 190]. Thus, Gould and colleagues [2003] asserted
that ringtailed lemurs (Lemur catta) are income breeders because, like the
sympatric sifaka, they time lactation and weaning with the period of high food
availability. Rather than promoting one definition of ‘‘reproduction,’’ in this
paper we explore the consequences of the different definitions, using another
lemur example.
The capital/income breeding concept is particularly problematic because the
long reproductive cycle of many primates and other mammals may span very
different environmental conditions. It is therefore difficult to develop predictions
based on the capital/income breeding framework for primates that live in seasonal
environments. Furthermore, dividing primates and other mammals with long
reproductive cycles into capital and income breeders may not be very useful
except for some extreme cases, such as certain pinnipeds [Boyd, 2000; Jönsson,
1997] and black bears [cf., Harlow et al., 2002]. Rather than assuming that all
large mammals are capital breeders (Festa-Bianchet et al., 1998), modifying the
framework [cf., Brockman & van Schaik, in press] or applying another framework
may prove to be more useful for understanding how female primates and other
mammals coordinate reproduction with fluctuating food resources.
Verreaux’s sifaka (Propithecus verreauxi verreauxi) are folivorous lemurs
found in the southwest of Madagascar. Their reproductive cycle lasts approxi-
Am. J. Primatol. DOI 10.1002/ajp
Kirindy Sifaka Life History / 367
mately 1 year. Richard and colleagues [2000] found that the body mass of
Verreaux’s sifaka fluctuates with the seasons at Beza Mahafaly Special Reserve in
the southwest of Madagascar, and suggested that Verreaux’s sifaka are capital
breeders. They based this assertion on data from hundreds of sifaka captured over
16 years. Forty-seven of these individuals had been captured more than one time
over the course of 12 years. Richard and colleagues [2000, 2002] suggested that
Verreaux’s sifaka are capital breeders because they time reproduction so that
births occur during the lean season (which suggests that they rely on fat stores for
part of lactation), and weaning occurs during the periods of the highest food
Verreaux’s sifaka are also found in Kirindy Forest, a dry, deciduous forest in
western Madagascar, approximately 500 km north of Beza Mahafaly. Lewis and
Kappeler [in press] combined phenological data with both long-term demographic
data and an intense 18-month study of the seasonal influences on the fluctuations
of sifaka body mass and condition. They found that Verreaux’s sifaka time
conception to coincide with the period of high or declining food supply so that the
most energetically demanding phase of the reproductive cycle, mid/late-lactation,
coincides with the annual peak in food abundance [cf., van Schaik & van
Noordwijk, 1985]. However, they did not evaluate the hypothesis that Verreaux’s
sifaka at Kirindy are capital breeders, as was proposed by Richard et al. [2000] for
the Beza Mahafaly Verreaux’s sifaka.
In this paper, we use the results presented in Lewis and Kappeler [in press]
to 1) evaluate which strategy is used by the Verreaux’s sifaka in Kirindy, and 2)
highlight why the capital/income framework is currently problematic. Lewis and
Kappeler [in press] found that both male and female Verreaux’s sifaka at Kirindy
exhibit significant losses in body mass and body fat during the dry season.
The sifaka mated when food availability was high and declining, gave birth during
the lean season, and timed the most costly phase of lactation to coincide with
the period of increased food availability. Females that were better able to
maintain good condition during the mating season were more likely to give birth
and successfully wean an infant. These results are consistent with the findings for
the Beza Mahafaly population [cf., Richard et al., 2000, 2002].
If ‘‘reproduction’’ in Jönsson’s [1997] review is defined as conception, then
the results of the Lewis and Kappeler [in press] study would support the
conclusion that Verreaux’s sifaka are capital breeders, as concluded by Richard
and colleagues [2000, 2002]. Capital breeders must build sufficient resources
before they reproduce [Jönsson, 1997; Stearns, 1989]. The Kirindy sifakas mate at
the end of the peak in food availability, after the females have had a chance to
recover from the difficult dry season. Females are less likely to successfully
reproduce if during the mating season they have not achieved a certain body mass
threshold (i.e., they have not achieved a certain level of fat stores). They then give
birth and lactate during the periods of lowest food availability, and wean their
infants during the following wet season of high food availability. Pereira [1993]
suggested that lemurs have evolved a system whereby females can help their
infants grow large enough and store enough energy so that the infants are able to
reduce their metabolic rate during the dry season. In fact, sifaka infant growth
not only stalls during the dry season, but generally becomes negative, with
Am. J. Primatol. DOI 10.1002/ajp
368 / Lewis and Kappeler
infants losing as much as 10% of their body mass from late April to September
(Kappeler and Lewis, unpublished data).
If, on the other hand, ‘‘reproduction’’ is interpreted to mean the most costly
part of lactation [cf., Gould et al., 2003], then the sifaka in the Lewis and Kappeler
[in press] study are more likely to be considered income breeders because they
time mid- to late- lactation with the probable increase in food availability.
Females (and males) experience an increase in body mass and subscapular body
fat at the very end of the dry season, the second half of lactation. Capital breeders
would be expected to build up fat stores before lactation and rely on them during
lactation; in sifaka, however, body fat is lowest around the periods of birth and
early lactation, and then begins to rise during the second half of lactation. This
finding by Lewis and Kappeler [in press] suggests that sifaka use the steadily
increasing income from food for direct conversion to energy for lactation.
Furthermore, if reproduction influences body mass, as suggested for capital
breeders by Pettorelli et al. [2002], then sifaka females would be expected to have
a lower body mass after they had successfully reared an infant to at least 9
months (i.e., reproduction is expected to have a significant cost in female body
mass). Contrary to the capital breeding hypothesis, and in support of the income
breeding hypothesis, there is no significant relationship between reproduction
and subsequent body mass [Lewis & Kappeler, in press].
The application of the concepts of capital and income breeding to large, longlived mammals has not been consistent [e.g., Boyd, 2000; Festa-Bianchet et al.,
1998; Gould et al., 2003; Pettorelli et al., 2002; Richard et al., 2000, 2002]. The
example of Verreaux’s sifaka discussed above demonstrates that depending upon
how ‘‘reproduction’’ is defined, one species may legitimately be described as both
a capital and an income breeder. Table I demonstrates how the different
measures used by researchers to determine capital or income strategy can lead to
TABLE I. Verreaux’s Sifaka Reproductive Strategy Varies Depending Upon the Definition of
‘‘Reproduction’’ as Well as Which Measure is Used
Suggested strategy if
‘‘reproduction’’ refers to
Body mass fluctuates seasonally
Body fat fluctuates seasonallya
Body mass highest just after mating seasonb
Body fat highest during mating seasonb
Body mass lowest just after early lactationb
Body fat lowest during early lactationb
Mid-/Late-lactation during increasing food availabilityb
Weaning during period of high food availabilityc
Body mass during mating season influences reproductiond
Reproduction influences body masse
cf. Jönsson [1997].
Predictions that follow from Jönsson [1997] depending upon how ‘‘reproduction’’ is operationalized.
Richard et al. [2000, 2002] and Gould et al. [2003] make contrasting predictions.
Boyd [2000].
Festa-Bianchet et al. [1998].
Am. J. Primatol. DOI 10.1002/ajp
Kirindy Sifaka Life History / 369
very different results in Verreaux’s sifaka. The interpretation of whether
Verreaux’s sifakas are capital or income breeders depends on how ‘‘reproduction’’
is defined, and how capital and income breeding are operationalized.
Given these conflicting results, it is currently difficult to evaluate whether
Verreaux’s sifakas are capital or income breeders. The capital/income breeding
model must be standardized before it can successfully and consistently be applied
to mammals with reproductive cycles of approximately 1 year or longer. While the
capital and income breeding model [Jönsson, 1997; Stearns, 1989] may be useful
for explaining reproductive strategies in some organisms, the model can only be
applied with limited success in most primates until the operational definition of
‘‘reproduction’’ is clarified and standardized. Given the ambiguities of the capital/
income model, we recommend caution in using this model.
This manuscript benefited from discussions with C. van Schaik, D. Brockman, D. Overdorff, K. Glander, K. Smith, and M. Munger, and comments from
A. Richard, S. Pochron, and three anonymous reviewers. This research was
funded by dissertation grants to R.J.L. from the Wenner-Gren and Leakey
foundations. This material is based on work supported by a National Science
Foundation dissertation improvement grant (no. 0002570) to R.J.L., and financial
support from the DFG to P.M.K.
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