J Comp Physiol B (2011) 181:423–435
DOI 10.1007/s00360-010-0521-7ORIGINAL PAPER
Is tissue maturation necessary for Xight? Changes in body
composition during postnatal development in the big brown bat
Wendy R. Hood · Olav T. Oftedal · Thomas H. Kunz
Received: 2 May 2010 / Revised: 13 September 2010 / Accepted: 22 September 2010 / Published online: 3 November 2010
© Springer-Verlag 2010
Abstract Patterns of oVspring development reXect the
availability of energy and nutrients, limitations on an indi-
vidual’s capacity to use available resources, and tradeoVs
between the use of nutrients to support current metabolic
demands and tissue growth. To determine if the long period
of oVspring dependency in bats is associated with the need
for an advanced state of tissue maturation prior to Xight, we
examined body composition during postnatal growth in the
big brown bat, Eptesicus fuscus. Despite their large size at
birth (22% of maternal mass), newborn bats are relatively
immature, containing 82% body water in fat-free mass.
However, the total body water content of newborn bat pups
decreases to near-adult levels in advance of weaning, while
concentrations of total body fat and protein exceed adult
values. In contrast to many other mammals, postnatal
growth of bat pups was characterized by relatively stable
concentrations of calcium and phosphorus, but declining
concentrations of magnesium. These levels remained stable
or rebounded in late postnatal development. This casts
doubt on the hypothesis that low rates of mineral transfer
necessitate an extended lactation period in bats. However,
our Wnding of near-adult body composition at weaning is
consistent with the hypothesis that extended lactation in
bats is necessary for the young to achieve suYcient tissue
maturity to undertake the active Xight necessary for inde-
pendent feeding. In this respect, bats diVer from most other
mammals but resemble birds that must engage in active
Xight to achieve nutritional independence.
Keywords Body composition · Calcium · Chiroptera ·
Eptesicus fuscus · Flight · Postnatal development
Introduction
Patterns of tissue maturation can provide insight into con-
straints on postnatal development such as availability of
energy and nutrients, limitations on an individual’s capacity
to use available resources, and tradeoVs at the tissue or cel-
lular level (Ricklefs 1979a; Ricklefs et al. 1998). This
should be particularly true during periods of maximal
growth, when tissue demand for structural materials is high.
Both poor nutrition and very high levels of activity can
redirect energetic substrates from muscle growth to catabolic
activity, reducing rates of tissue development (Ricklefs
1979a; Ricklefs et al. 1998).
In most mammals, nourishment is provided solely by the
mother in the form of milk (Clutton-Brock 1991). Mammalian
Communicated by I.D. Hume.
Electronic supplementary material The online version of this
article (doi:10.1007/s00360-010-0521-7) contains supplementary
material, which is available to authorized users.
W. R. Hood · T. H. Kunz
Center for Ecology and Conservation Biology,
Department of Biology, Boston University,
Boston, MA 02215, USA
O. T. Oftedal
National Zoological Park, Smithsonian Institution,
Washington, DC 20008, USA
Present Address:
W. R. Hood (&)
Department of Biological Sciences, Auburn University,
101 Life Sciences Building, Auburn, AL 36849, USA
e-mail: wrhood@auburn.edu
Present Address:
O. T. Oftedal
Smithsonian Environmental Research Center,
Edgewater, MD 21037, USA123

424 J Comp Physiol B (2011) 181:423–435milk is highly digestible and acts as an immediate buVer to
Xuctuations in food supply. There is considerable interest in
how species-speciWc milk composition relates to the nutri-
tional needs of the young, as well as to nutritional con-
straints on the mother (Oftedal 1984, 2000; Oftedal et al.
1993a). The quality of milk to some degree depends on
maternal condition. Milk composition and more notably
milk yield can vary with nutritional status of the mother
(Doreau et al. 1992; Hood et al. 2009; Rasmussen and War-
man 1983; Warman and Rasmussen 1983). Thus, changes
in tissue and body composition of young during the postna-
tal growth period may reXect a trade-oV between develop-
mental processes, maintenance requirements of developing
tissues, and the supply of nutrients available to the mother.
Because of their volant mode of locomotion and pro-
longed period of dependency, bats are a particularly inter-
esting group in which the transfer of nutrients from mothers
to oVspring through milk can be studied. Young bats do not
become nutritionally independent until they have achieved
about 70% of adult mass: nearly twice the average relative
mass (37%) of terrestrial species at weaning (Barclay 1994,
1995; Case 1978; Kunz 1987; Kunz and Hood 2000; Kurta
and Kunz 1987; Millar 1977). Because aerial insectivorous
species typically consume a low-calcium diet, it has been
postulated that low-calcium intake by mothers may con-
strain mineral deposition and thus the relative rates of skel-
etal maturation in dependent oVspring (Barclay 1994, 1995;
Studier and Sevick 1992), yet there is little direct evidence
to suggest that mineral intake in bats is suboptimal. For
example, Booher (2008) found no diVerence in the length
of forearm or body mass of litters born to big brown bats
(Eptesicus fuscus) fed a diet that mimicked the low-calcium
intake of free-ranging bats versus bats supplemented with
10£ more calcium. Booher and Hood (2010) further exam-
ined the body composition of these young and found no
diVerences between the low- and high-calcium groups.
Based on the calcium content of the feces collected from
these animals, it was apparent that supplemented animals
did not absorb greater amounts of calcium than is typically
obtained from their normal insect diet (Booher and Hood
2010).
Alternatively, the long period of dependency in bats
may reXect a need for an advanced state of tissue matura-
tion, and particularly maturation of bone, prior to under-
taking sustained Xight. Survival at independence depends
on the ability of juvenile bats to forage eVectively.
Because the relative strain on the distal elements of the
skeleton is greater for Xying bats than species using other
forms of locomotion (Swartz and Middleton 2008), insec-
tivorous bats that must capture food on the wing may need
to approach or achieve tissue maturity before nutritional
independence (Papadimitriou et al. 1996; Swartz et al.
1992).
We studied the development of suckling big brown bats
(Eptesicus fuscus), an obligate, aerial-feeding insectivore
(Kurta and Baker 1990). Our goal was to test the hypothesis
that the extended period of suckling in bats yields a high
level of tissue maturation and mineral deposition prior to
nutritional independence from milk. Chemical maturity is
achieved when the concentrations of nutrients in the body
reach adult values (Moulton 1923). Because chemical
maturity reXects the developmental state of the tissues, the
chemical composition of the body can be used as an aggre-
gate indicator of tissue maturation. For this investigation,
we characterized changes in total body macronutrient and
macromineral composition of bat pups from birth until
weaning, and compared our results with data on adult
females (Hood et al. 2006). We assessed the prediction that
prolonged suckling in bats is associated with an advanced
level of tissue maturation by comparing our Wndings with
published data on body composition in non-volant mam-
mals and birds at nutritional independence.
Methods
Big brown bat pups were collected with their mothers from
two maternity colonies located in Hollis and Milford, New
Hampshire, USA (42°74N 71°59W, 42°83N 71°68W,
respectively) during June and July 1999. All samples were
collected during the 5-week suckling period. At weekly
intervals, up to ten pups and their mothers were collected
from each colony between 0600 and 0900 h. Animals were
transported to Boston University where they were main-
tained in incubators at 30°C (within the zone of thermoneu-
trality for this species; Stack 1985). Pups were housed with
mothers (allowing them to be suckled by their mothers
overnight) and then separated the following morning for at
least 2 h prior to being killed, ensuring that the young had
minimal gastrointestinal contents. Bats were humanely
killed by prolonged exposure to gaseous chloroform (Gan-
non et al. 2007). Body composition analyses and care of the
mothers is described elsewhere (Hood et al. 2006). All pups
were weighed (§0.01 g), and lengths of forearm
(§0.1 mm) and total epiphyseal gap (§0.05 mm; forth right
metacarpal-phalangeal epiphysis; Kunz and Anthony 1982)
were measured post-mortem. These measurements were
used to estimate the age of pups (Burnett and Kunz 1982;
Hood et al. 2002). In 4 years of studying big brown bats in
Massachusetts and New Hampshire (1996, 1997, 1998 and
1999), we found no evidence that litter size deviated from
two (W.R. Hood, personal observation). Estimates of pup
age were slightly more accurate when accounting for the
relative age of the mother (Hood et al. 2002), but in the
present study we did not know the identity of all mothers.
Thus, maternal age was not considered as a variable in123