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7/27/2019 Milk Composition in Grey Headed Flying Fox
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C S I R O P U B L I S H I N G
Australian Journalof Zoology
Volume 45, 1997 CSIRO Australia 1997
A journal for the publication of the results of
original scientific research in all branches of zoology,
except the taxonomy of invertebrates
w w w . p u b l i s h . c s i r o . a u / j o u r n a l s / a j z
All enquiries and manuscripts should be directed to
Australian Journal of ZoologyCSIRO PUBLISHING
PO Box 1139 (150 Oxford St)
Collingwood Telephone: 61 3 9662 7622
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Australia Email: [email protected]
Published by CSIRO PUBLISHING
for CSIRO Australia and
the Australian Academy of Science
http://www.publish.csiro.au/journals/ajzhttp://www.publish.csiro.au/http://www.publish.csiro.au/http://www.publish.csiro.au/http://www.publish.csiro.au/journals/ajz7/27/2019 Milk Composition in Grey Headed Flying Fox
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Milk Composition in the Grey-headed Flying-fox,
Pteropus poliocephalus (Pteropodidae:Chiroptera)
Michael MesserA and Kerryn Parry-JonesB
ADepartment of Biochemistry, University of Sydney, NSW 2006, Australia.BSchool of Biological Science, University of New South Wales, Kensington, NSW 2033, Australia.
Abstract
Milk samples from 11 captive flying-foxes were collected at various times during lactation from 5 to 139
days post partum and analysed for protein, carbohydrate, total solids and ash. In addition, samples from 14
free-living animals, collected on a single occasion, were analysed. No significant changes in milkcomposition were observed during lactation in the captive bats except for a small increase in protein and a
small decrease in carbohydrate concentration late in lactation. The milk from captive bats contained less
protein and total solids than that from free-living animals (mean values: protein, 259 and 364%,
repectively; total solids, 111 and 127%, repectively) but there was no significant difference with repect to
the carbohydrate (613 and 644%, respectively). The fat content, estimated from the total solids by
difference, was low (19 and 22%, respectively) in both captive and free-living animals. The results are
compared with previously published values for milk composition in Chiroptera and are discussed in the
context of nursing behaviour and diet in captive and free-living flying-foxes.
Introduction
Although there is a considerable amount of information on the composition of the milk of a
large variety of mammalian species (Jenness and Sloan 1970; Oftedal and Iverson 1995),
relatively little is known concerning milk composition in bats (Kunz et al. 1995). For example,
there are over 60 species of Chiroptera in Australia (Strahan 1992) but none has until now beenstudied with respect to the composition of its milk.
The grey-headed flying-fox, Pteropus poliocephalus (Suborder Megachiroptera) is the largest
of eight species of fruit-eating bats found in Australia. Lactation usually begins in October and
continues for 34 months or even longer (Nelson 1965); the mothers generally have only a
single young. The bats are regarded as pests by many orchardists and lactating flying-foxes are
frequently shot (Parry-Jones 1996). Their orphaned young are sometimes rescued and have been
hand-reared on a variety of milk formulae whose composition is mostly based on trial-and-error.
Information on the composition of their milk should therefore be of assistance to hand-rearers as
well as provide comparative data that may increase our understanding of growth and
development in this species.
In this study we collected milk samples from both captive and free-living animals. All
samples were analysed for protein and carbohydrate. Samples from the free-living bats that were
sufficiently large were also analysed for total solids, as were pooled samples from captive bats.
Methods
Milk Collection
A total of 67 milk samples, each at least 100 mL in volume, was obtained from 11 captive bats at various
stages of lactation, from 5 to 139 days post partum, between early November 1995 and March 1996.
Milking was usually done once every 2 weeks between 1200 and 1400 hours. The milk was manually
expressed from one mammary gland and collected into microcapillary tubes while the mothers young was
attached to the nipple of the other gland. The lactating bats, whose ages ranged from 2 to 9 years, were
housed in a common enclosure measuring 18 21 73 m. Their diet consisted of chopped mixed fruit,
supplied ad libitum, and a ration, averaging 10 g per animal per day, of a supplement (Wombaroo Food
Australian Journal of Zoology, 1997, 45, 6573
10.1071/ZO96052 0004-959X/97/010065$05.00
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Products, Glen Osmond, SA) reportedly containing a minimum of 50% protein and 12% fat as well as
minerals and vitamins.
Milk samples from 14 free-living bats, caught with the aid of a harp trap (Tidemann and Loughland
1993), were obtained near Cabramatta, NSW, on 13 December 1995 between 0400 and 0600 hours. The
animals were milked, usually from both mammary glands, within 2 h of capture. Since very few of the
young were with their mothers their ages were unknown but if one assumes that most P. poliocephalus are
born in October (Nelson 1965; Parry-Jones 1987) then most of the young would have been between 40 and
70 days of age.
The milk samples were stored in 05-mL Eppendorf tubes for up to 4 months at 20C, prior to analysis.
Analytical
The milk samples were thawed, warmed to 37C and thoroughly mixed. For carbohydrate and protein
analysis, duplicate 10-mL aliquots were diluted to 200 mL with 10 mM NaOH. (We noted that when water
was used as the diluent, an insoluble precipitate tended to form, but this could be prevented by use of a
slightly alkaline solution. Control experiments with standards showed that 10 mM NaOH did not affect the
analysis of either carbohydrate or protein). Of the diluted milk, 10-mL aliquots were assayed for
carbohydrate by a modification (Messer and Green 1979) of the phenolsulphuric-acid method, with lactose
as a standard. Aliquots (10 mL) of the diluted milk were then assayed for protein by the dye-binding
(Coomassie Blue G-250) method (Bradford 1976) with bovine serum albumin as a standard. Since the dye-
binding method is dependent on the amino acid composition of the protein being analysed (Oftedal and
Iverson 1995), it was calibrated by Kjeldahl analysis (total nitrogen determination) of three separate 200-mL
aliquots of pooled milk obtained during early, mid and late lactation. The protein values obtained by the
Kjeldahl method were 134 05% higher than those obtained by the dye-binding method; all our values
were therefore adjusted accordingly, even though part of the difference would have been due to non-protein
nitrogen, which was not estimated. Oftedal and Jenness (1988) found that non-protein nitrogen accounted
for a fairly large proportion of the total nitrogen in the milk of equids and that the use of total nitrogen
assays to calculate crude protein overestimated the protein content by 0203 g per 100 g of equid milk. It is
possible, therefore, that our adjusted values for crude protein similarly overestimate the true protein content.
Total solids were determined by measuring the mass change, to the nearest 001 mg, after freeze-dryingto constant mass. Since most of the samples from the captive bats were too small for accurate determination
of total solids by this method, the determinations were done only on duplicate 200-mL aliquots of pooled
samples. Pooling was done by combining 50-mL aliquots from each of the individual milk samples. Those
samples from the free-living bats that were at least 250 mL in volume (10 of 14) were also analysed for total
solids, with duplicate 100-mL aliquots.
The ash of pooled milk samples (each 400 mL) from captive and free-living bats was determined by
incineration at 400C for 20 h.
Milk fat was estimated as the difference between total solids and the sum of protein, carbohydrate and
ash. Our estimates for fat are therefore subject to considerable error. If the values for protein were
overestimated (see above), those for fat would be underestimates. Attempts were made to dermine the fat
content by the creamatocrit method (Lucas et al. 1978) but it became apparent that the concentration of fat
was too low to permit reliable results by this method.
Statistical comparisons of the data for captive bats were made by a mixed model ANOVA (BMDP
Statistical Software, University Press of California, 1992) which controlled for individual contributions of
each bat and stage of lactation. Pairwise differences were determined by t-tests. Comparisons between thedata for free-living bats and those for captive bats during the same stage of lactation were made by
unpaired t-tests.
Results
Results of protein and carbohydrate analyses of 67 milk samples collected from 11 captive
flying-foxes at various times post partum are shown in Fig. 1. The data are summarised in Table
1, which lists the mean values for samples obtained from 5 to 50 days, from 51 to 99 days and
from 100 to 139 days post partum; these time intervals are arbitrarily designated as early, mid
and late lactation, respectively. There was no significant change in the protein or carbohydrate
content up to 99 days post partum (P > 005) but late in lactation there was a small but
significant increase in the protein content (P < 0008) and a decrease in the carbohydrate content
(P < 0001).
66 M. Messer and K. Parry-Jones
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67Milk Composition in Grey-Headed Flying-Foxes
1501005000
2
4
6
8
10
Protein
(%)
(a)
1501005000
2
4
6
8
10
Time post partum (days)
Carbohydrate
(%)
(b )
Fig. 1. Composition of milk of 11 captive grey-headed flying foxes with respect to (a) protein and (b)
carbohydrate from 5 to 139 days post partum. Each of the symbols used for the data points is specific to a
given animal.
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Total solids and ash content of pooled samples obtained during early, mid and late lactation
are also listed in Table 1, thus allowing estimation of the fat content (see Methods). The dataindicate that the milk of captive flying foxes is relatively dilute in terms of dry matter and
contains only about 2% fat.
Comparison of milk samples from 14 free-living bats with 13 samples from captive bats at
the same stage of lactation (4070 days post partum; Table 1) shows that their protein content is
significantly greater (P < 0001) but there is no significant difference with respect to
carbohydrate. Of the 14 samples from the free-living bats, 10 were also analysed for total solids;
the mean value obtained was higher than that for the milk of the captive bats but most of this
difference appears to be due to the higher protein content. The mean value for fat (22%) was
slightly higher than that for the milk from the captive bats but the results for milk fat were very
variable, ranging from 073 to 35%.
Discussion
The only previously published values for milk composition in Megachiroptera are limited toa single sample from the epauletted fruit bat, Epomophorus wahlbergi (Quicke et al. 1984). By
contrast, there have been several studies on milk composition in Microchiroptera, including an
extensive recent investigation on three insectivorous species (Kunz et al. 1995) (Table 2). With
two exceptions, the milk of Microchiroptera is more highly concentrated in terms of total solids
and energy density, and lower in carbohydrate, than that ofP. poliocephalus. The exceptions are
the long-nosed bat, Leptonycterus sanborni, which is a pollen and nectar feeder (Huibregtse
1966) and the Jamaican fruit bat, Artibeus jamaicensis, which, like P. poliocephalus, forages
primarily on fruit, blossoms and leaves (Parry-Jones and Augee 1991; Kunz and Diaz 1995). It
seems likely, therefore, that milk composition in bats is related to the maternal diet (see also
Kunz and Stern 1995). In other eutherian mammals, dilute milks, with a total solids content of
less than 20%, are mostly confined to herbivorous or frugivorous species and are rarely found in
carnivores or omnivores (Jenness and Sloan 1970; Oftedal and Iverson 1995).
68 M. Messer and K. Parry-Jones
Table 1. Milk composition in captive and free-livingPteropus poliocephalus
Fat, total solids and ash of the milk of captive animals were determined on pooled samples only. Fat was
estimated as the difference between total solids and the sum of protein, carbohydrate and ash. The values
in parentheses represent the number of individual samples analysed. Those within square brackets are the
number of samples from which equal aliquots were pooled. All percentages are expressed as weight
per volume; n.d., not determined. Values showing the same superscript are significantly different:
a = P < 0008; b = P < 0025; c, d = P < 0001
Days post partum Protein Carbohydrate Fat Total solids Ash Energy
(%) (%) (%) (%) (%) (kJ mL1)
(Mean s.d.)
Captive
550 252 054 622b 028 202 112 046 241
(15) (15) [15] [15] [15] [15]
5199 242a 048 628c 037 174 108 040 229
(31) (31) [31] [31] [31] [31]
100139 283a 057 590b,c 042 190 111 046 239
(21) (21) [21] [21] [21] [21]
4070 227d 053 626 033 n.d. n.d. n.d. n.d.
(13) (13)
Free-living
4070 (est.) 364d 064 644 037 216 086 127 075 062 274 030
(14) (14) (10) (10) [10] (10)
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Table 2. Milk composition in Chiroptera
Mean values based on the number of samples in parentheses: n.d., no data
Total solids Protein Carbohydrate Fat Ash EnergyA
(%) (%) (%) (%) (%) (kJ mL1)
Microchiroptera
Tadarida brasiliensisB (21) 365 769 336 258 n.d. 123
Myotis lucifugusB (3) 271 850 395 158 n.d. 875
Myotis veliferB (3) 324 107 438 199 n.d. 109
Myotis thysanodes (1) 405 121 34 179 16 104
Eptesicus fuscus (4) n.d. 617 252 164 n.d 837
Leptonycterus sanborni 121 (1) 437 (1) 539 (5) 171C
(1) 063 261Artibeus jamaicensis (21) 178 36 61 90 n.d. 532
Megachiroptera
Epomophorus wahlbergi (1) 120 42 40 35 n.d. 302
Pteropus poliocephalus
Captive 111 (3) 259 (67) 613 (67) 189C (3) 044 (3) 236
Free-living 127 (10) 364 (14) 644 (14) 216C (10) 062 (1) 274
AAll Energy densities were calculated with energy equivalents of 245, 165 and 381 kJ g1 for protein, carbohydrate and fat, respectively (Oftedal
sake of simplicity, it was assumed that all milk samples had a specific gravity of 100.BPeak lactation.CEstimated by difference (see Methods)DUnpublished data cited by Oftedal and Iverson (1995).
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Ben Shaul (1962) was perhaps the first to suggest a relationship between the composition of
the milk of different species and their nursing behaviour; species (e.g. primates) whose young
suckle frequently or on demand have dilute, low-fat milks whereas those whose young feed at
widely spaced intervals (e.g. pinnipeds) have concentrated milks with a high fat content (Jenness
and Sloan 1970; Kunz et al. 1995). P. poliocephalus give birth in spring and carry their young
on foraging flights during the first three weeks (Nelson 1965). The young remain permanently
attached to their mothers during this time and are able to suckle on demand. After three weeks of
age, in free-living animals, the young are found attached during the day, but during the night the
mothers leave them in the colony site. The mothers may return during the night to feed their
young (Ratcliffe 1931), who are unable to forage for themselves until they are about 3 months
old. In captive animals we observed a similar pattern with older young being attached to the
nipple throughout the day but only permitted the occasional feed during the night. The young of
P. poliocephalus can therefore be regarded as frequent feeders and the low total solids and fat
content of the milk of this species is consistent with Ben Shauls proposal. It should be noted,
however, that the sampling procedure used in the present study may not have been optimal. In
many species there is an increase in the concentration of milk fat during the course of milk
let-down (e.g. Atwood and Hartmann 1992) and therefore our samples may not have been
entirely representative of the milk ingested by the young during a normal feed. In future studies
it may be worth determining the effect of prior administration of oxytocin, since this would most
probably increase the size of the samples. Further, we did not investigate whether separating the
young from its mother for an extended period before milking would affect milk composition.
Kunz et al. (1995), who studied this in T. brasiliensis, found that milk samples collected after
46 hours of separation contained about 41% more fat than those obtained immediately after the
pre-dawn feeding period; protein and carbohydrate were unchanged. It is possible therefore, that
our values for milk fat are underestimates and that the milk is more concentrated than would
appear from Table 1. (An increase of 41% would have the effect of changing our values for fat
from about 2% to almost 3%).Kunz et al. (1995) noted significant increases in the fat and total solids content during
lactation in all three of the insectivorous species they studied, with the carbohydrate and protein
values remaining constant. In the present investigation, changes in milk composition were small
and appeared to be confined to protein and carbohydrate concentrations towards the end of
lactation. Studies on other megachiropterans and/or other frugivorous species should reveal
whether an increase in the milk fat and total solids content during lactation is found only in
insectivorous species of bats.
In the present study the milk of the free-living bats was very significantly higher in protein
than that of the captive animals. This difference may conceivably be due to diurnal variations in
milk composition since the milk from the free-living bats was obtained during the early morning
whereas the captive animals were milked in the afternoon. However, differences in milk
composition between free-living and captive animals have previously been noted in other
species. In bears (Jenness et al. 1972) the milk carbohydrate concentration was found to belower in free-living than in captive animals, whereas in ringtail possums (Munks et al. 1991) the
milk fat was higher but the protein was lower. Munks et al. (1991) have noted that the diet of
their captive animals contained more protein than that of the free-living ones and suggested that
this may have contributed to higher milk protein concentrations.
It is quite possible that the protein content of the diet of our lactating captive bats was less
than optimal. Lactation imposes a great metabolic demand on small animals and has to be met
by very significant increases in food consumption (Jenness 1974). Protein may be the limiting
factor in the diet of frugivorous bats (Thomas 1984; Steller 1986) and although our animals
received a protein supplement this was not provided ad libitum. The preferred foods of free-
living P. poliocephalus are the nectar and pollen from blossoms of the family Myrtaceae and of
the genus Banksia, as well as native figs (e.g. Ficus rubiginosa) and other native fruits, rather
than cultivated orchard fruits such as those supplied to our captive bats (Parry-Jones 1987;
70 M. Messer and K. Parry-Jones
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Parry-Jones and Augee 1991). In addition, their diet probably includes leaves and some insects
(Parry-Jones and Augee 1992; Parry-Jones 1993). Kunz and Diaz (1995) believe that folivory
may be quite common in species that feed largely on fruits that are low in protein while
Funakoshi et al. (1993) consider that insects form a small but nutritionally important component
of the diet of the warm-temperate fruit bat, Pteropus dasymallus dasymallus. Since pollen,
leaves and insects are higher in protein content than orchard fruits (Rasweiler 1977; Hume
1982), our free-living bats may have ingested more protein than the captive ones, which could
explain the difference in milk composition. Nevertheless, all the young of our captive animals
appeared to be healthy and gained weight steadily, their mean weight at 20 weeks post partum
being 531 g. Since there are no published values for growth rates in P. poliocephalus we were
not able to determine whether our captive young grew at the same rate as free-living animals.
Our results suggest that none of the commercial milk substitutes currently available is
entirely suitable for the hand-rearing of orphaned flying-foxes (Table 3). All these substitutes
contain more fat and some contain either more protein (e.g. Wombaroo and Biolac) or less
protein (e.g. Nan 1 or 2) than the milk ofP. poliocephalus. When one compares the composition
of the milk of free-living P. poliocephalus with that of other species (Jenness and Sloan 1970) it
appears that equid milk, which contains 12% fat, 1618% protein and 67% carbohydrate
(Oftedal and Jenness 1988), is the most similar. A milk substitute designed for foals,
supplemented with about 15% protein and 05% fat, might therefore be close to optimal for
suckling grey-headed flying-foxes.
Acknowledgements
We thank Dr Chris Tidemann for permitting us to milk the flying-foxes caught at his study
site in Cabramatta and Julie Spence for helping with the project on the site. We also thank the
Wambina Flying-fox Research Centre in Gosford for the use of their captive breeding colony.
We are indebted to Keith Newgrain (CSIRO Division of Wildlife and Ecology, Canberra) for
performing Kjeldahl (total N) estimations of three samples of milk and to Dr Thomas Kunz
(Department of Biology, Boston University, USA) for reviewing the initial manuscript of this
paper. We are most grateful to Dr Samir Samman (Human Nutrition Unit, University of
Sydney) for his assistance with the statistical analyses.
Table 3. Comparison of composition ofP. poliocephalus milk with that of some milk substitutes
Protein Carbohydrate Fat Energy
(%) (%) (%) (kJ L1)
P. poliocephalus milk
Captive 26 61 19 2360
Free-living 36 64 22 2740
Nan 1A 15 76 34 2729
Nan 2A 23 73 32 2743
DiVetelactB 30 50 37 2800
WombarooC 50 63 30 3200
Biolac for puppiesD 60 40 70 4797
ANestle Aust Ltd, GPO Box 4320, Sydney, NSW 2001.BSharpe Laboratories Pty Ltd, 3/12 Hope St, Ermington, NSW 2115.CWombaroo Food Products, PO Box 151, Glen Osmond, SA 5064.D
Biolac, 15 OShannassy St, Mount Pritchard, NSW 2170.
71Milk Composition in Grey-Headed Flying-Foxes
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73Milk Composition in Grey-Headed Flying-Foxes