Cross-fostering and short-term pouch young isolation in macropodoid marsupials: implications for conservation and species management

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SUMMARY
Cross-fostering is the rearing of young by a surrogate
mother of a different taxon. In marsupials this tech-
nique has been used to study lactation as well as
pouch young growth and development. Recently,
cross-fostering and short-term pouch young isola-
tion have been used by wildlife agencies and zoos to
increase female reproductive rates and fecundity,
and to manage the genetics of captive and wild ani-
mals as part of wider conservation and management
strategies for macropodoid marsupials. Data on
cross-fostering are now available for six potoroid and
13 macropodid species. Success of cross-fostering
studies between donor and foster species varies
widely from complete failure to an eight-fold increase
in the production of pouch young annually. Factors
implicated in successful cross-fostering include rela-
tive size of donor and surrogate females, size of pouch
young at weaning, differences in length of pouch life
between species and size differences between donor
young and those of the surrogate species at transfer.
Studies have shown that females regulate milk com-
position and production irrespective of pouch young
age, and that transfer of donor young to species with
more immature or advanced mammary glands will
result in a slowing or an acceleration of pouch young
growth and development, and affect the duration of
pouch life. Small pouch young tolerate short-term
isolation from the pouch at a range of temperatures,
provided high humidity is maintained throughout
the period of isolation. Maintenance of pouch young
at temperatures lower than those that occur in the
pouch (23°C compared with 37°C) during isolation
reduces the pouch young’s basal metabolic rate,
oxygen consumption and evaporative water loss and
thus improves survival rates of very small pouch
young. The success of these techniques in managing
population genetics and accelerating breeding in
donor species within the Macropodoidea are
enhanced by post-partum oestrus and mating after
the removal of pouch young, and the reactivation
and birth of the diapausing embryo. This chapter
reviews the available data on cross-fostering and
23 Cross-fostering and short-term
pouch young isolation in
macropodoid marsupials:
implications for conservation
and species management
D.A. Taggart, D.J. Schultz, T.P. Fletcher, J.A. Friend, I. Smith,
W.G. Breed and P.D. Temple-Smith
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264 Macropods: The Biology of Kangaroos, Wallabies and Rat-kangaroos
pouch young isolation in macropodoid marsupials,
and examines use of these techniques in the conser-
vation and management of species in this group.
INTRODUCTION
The development and application of assisted repro-
ductive technology in marsupials is a comparatively
new field and has only recently been applied to assist
in conservation of threatened species (Taggart et al.
2005; Schultz et al. 2006; Taggart and Smith, unpubl.
data; Taggart and Friend, unpubl. data). Although a
variety of reproductive technologies are being exam-
ined, the techniques which offer the most immediate
benefit to many marsupial species are those of pouch
young isolation and cross-fostering. Cross-fostering
is defined as the rearing of young by a surrogate
mother of a different taxon. In marsupials, this tech-
nique has the distinct advantage of being used as
early as day 1 of pouch life when the pouch young
weighs <1 g. When applied to marsupial conserva-
tion, the aim is to circumvent the period of lacta-
tional anoestrus or lactational quiescence from the
natural mother’s reproductive cycle, thus permitting
her to undergo a series of pregnancies with a mini-
mum of intervening lactation and thereby enhance
her reproductive rate and fecundity. Cross-fostering
was initially proposed and developed approximately
40 years ago by Merchant and Sharman (1966). At
that time they stressed the importance of cross-fos-
tering for the conservation of threatened marsupial
species, but despite their early successes in a variety
of macropodids (Merchant and Sharman 1966), few
studies (Johnson 1981) were published on this topic
until the late 1990s (Table 23.1). There is still little
information available on non-macropodoid species
(Caton 2005; Finlayson et al. 2008).
Short-term pouch young isolation is a technique
developed in marsupials to facilitate the collection of
milk samples from mothers with pouch young, sur-
gery on pouch young, or transport of young (Mer-
chant and Sharman 1966; Shield 1966; Messer and
Green 1979; Rose et al. 1998; Taggart et al. 2002).
Recently this procedure has been used in association
with cross-fostering for transporting small pouch
young between donor and surrogate mothers. For the
purposes of this discussion, it refers to the isolation of
small pouch young from the teat for up to 12 hours.
A controversial aspect of cross-fostering in macro-
podoids is the selection of surrogate taxa that will
ensure the most successful outcome. There are no
simple and effective guidelines or criteria to direct
the selection of the most appropriate surrogate taxon
for cross-fostering, or to help predict the optimum
time for pouch young transfer to maximise both
survival of young and female reproductive rate. This
chapter reviews the available data from the Macro-
podoidea, provides technical recommendations to
enhance the likelihood of cross-fostering and pouch
young isolation success and examines the potential
application of these techniques as tools for conserva-
tion and management in this group.
METHODS
Cross-fostering
Selecting a donor species
In order to achieve accelerated breeding, and thus
obtain the greatest conservation benefit from a cross-
fostering program, the donor species (the species
that is to be fostered) must display polyoestry and
ideally cycle for a considerable portion of the year, if
not year-round. Removal of the donor pouch young,
and therefore the sucking stimulus, ends the mother’s
period of lactational anoestrus or lactational quies-
cence (Tyndale-Biscoe et al. 1974; Tyndale-Biscoe
1979). In most species with embryonic diapause, this
acts to reinitiate development of the diapausing
embryo and a young is usually born within 20–40
days (Tyndale-Biscoe et al. 1974; Tyndale-Biscoe
1979; Tyndale-Biscoe and Renfree 1987). Even in
those species without diapause, pouch young removal
provides an opportunity for the female to cycle, mate
and give birth again within the same season (Finlay-
son et al. 2007, 2008).
Knowledge of the social organisation of the donor
species (solitary or gregarious), breeding require-
ments and behaviour (space, den requirements,
cover, diet etc.) and reproductive biology (time
between mating and birth, length of lactation, age at
sexual maturity) are relevant in maximising repro-
ductive success and influencing the determination of
the most appropriate surrogate species for the rear-
ing of donor young.
Selecting a potential surrogate species
The following factors appear to be important in
selecting a potential surrogate species for maximis-
ing the likelihood of a successful cross-fostering
program and maximising breeding and fostering
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Cross-fostering and short-term pouch young isolation in macropodoid marsupials 265
opportunities (Merchant and Sharman 1966; John-
son 1981; Jones et al. 2004; Taggart et al. 2005;
Schultz et al. 2006; Menzies et al. 2007). Most criteria
are self-explanatory:
1 quiet and tractable surrogate mothers of (roughly)
similar size to the donors (Merchant and Shar-
man 1966; Johnson 1981; Jones et al. 2004; Tag-
gart et al. 2005; Schultz et al. 2006; Menzies et al.
2007);
2 similar pouch life duration in donor and surro-
gate species (Merchant and Sharman 1966; John-
son 1981; Jones et al. 2004; Taggart et al. 2005;
Schultz et al. 2006; Menzies et al. 2007);
3 no major mismatch in milk contents or the time
each young receives critical milk components
(Menzies et al. 2007);
4 a close taxonomic relationship between donor
and foster species;
5 donor and foster species do not naturally occur
within the same region/environment;
6 foster species are gregarious, easy to maintain and
breed reliably in captivity (Merchant and Shar-
man 1966; Taggart et al. 2005).
Criterion 4 has been included as detailed studies
examining the success of cross-fostering between
distantly related macropodoids have yet to be under-
taken. Preliminary trials (Taggart, unpubl. data, n =
2) involving transfers of long-nosed potoroo
(Potorous tridactylus) pouch young to tammar wal-
laby (Macropus eugenii) surrogate mothers were
unsuccessful. It is therefore recommended that, until
more detailed studies have been undertaken and
there is available data to suggest otherwise, a close
taxonomic relationship between donor and surrogate
species will result in the greatest likelihood of cross-
fostering success.
When selecting a potential surrogate species it is
not recommended that a species be chosen if it occurs
in the same geographical region as the donor species
(criterion 5), as this may lead to problems with spe-
cies recognition upon reintroduction of foster-reared
animals. Although there is no evidence to support or
refute this idea, it would be wise to avoid any factor
that may negatively affect the breeding success of
foster-reared animals.
Pouch young transfer procedure
Pouch young removal
Hands should be cleaned in warm water without
soap before handling pouch young and kept moist
during fostering to prevent pouch young sticking to
hands when being handled (Taggart et al. 2005;
Schultz et al. 2006). Hand creams or any other sub-
stance that will leave hands perfumed or oily prior to
handling pouch young should be avoided.
To remove the pouch young in preparation for
transfer, the thumb and forefinger of one hand are
used to grasp the teat while those of the other hand
are positioned around the front of the young’s mouth
to prevent the head moving forward. The teat is then
gently and slowly removed from the mouth using
bouts of intermittent pressure and relaxation. This
procedure places minimal pressure on the head and
Table 23.1: Summary of cross-fostering and pouch young isolation studies in the Macropodoidae
Cross-fostering
Macropodids (M)/Potoroids (P)
Pouch young isolation
Macropodids (M)/Potoroids (P)
Published articles
Merchant and Sharman 1966 – M
Johnson 1981 – M
Bell and Close 1994 – M (abstract)
Smith 1998 – P
Taggart 2002 – M
Jones et al. 2004 – M
Taggart et al. 2005 – M
Waite et al. 2005 – M
Sterneberg 2005 – P
Schultz et al. 2006 – M
Menzies et al. 2007 – M
Honours theses
Collins 2002 – P
Menzies 2003 – M
O’Brien 2004 – M
Published articles
Bolliger and Pascoe 1953 – M
Renfree and Tyndale-Biscoe 1978 – M
Green et al. 1980 – M
Crowley et al. 1988 – P
Merchant et al. 1996 – M
Rose et al. 1998 – P
Taggart et al. 2002 – M
Honours theses
Collins 2002 – P
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266 Macropods: The Biology of Kangaroos, Wallabies and Rat-kangaroos
mouth of the pouch young. Rapid removal of the teat
from the young’s mouth can result in damage to the
buccal cavity and tearing of the pouch young’s
tongue. It is essential to confirm the presence and
size of the pouch young on the surrogate mother
prior to removal of the donor pouch young (Taggart
et al. 2005; Schultz et al. 2006).
Pouch young reattachment
A physical examination of the surrogate mother is
recommended before transferring any donor young.
Particular attention should be paid to the oral cavity
(to exclude the presence of disease) and pouch of the
potential surrogate mother. A healthy tooth–gum
margin and a clean moist pouch with no apparent
odour are essential to maximise the chances of suc-
cess (Schultz et al. 2006). Different methods of pouch
young reattachment have been used, including the
simple placing of the fostered young into the surro-
gate mother’s pouch and allowing the young to attach
to the teat unaided (Smith 1998; Collins 2002). The
end of a match stick (Merchant and Sharman 1966),
fine blunt-nosed forceps (Taggart 2002; Figs 23.1,
23.2) and the flexible plastic sheath of a hypodermic
needle (Sterneberg 2005) have been used to assist
attachment. Those three aids help the operator to
position the teat inside the foster young’s mouth
(Merchant and Sharman 1966; Taggart 2002; Tag-
gart et al. 2005; Sterneberg 2005).
If young are placed within the surrogate mother’s
pouch and not physically attached to a teat, anaesthe-
sia of the surrogate mother is not necessary (Smith
1998; Taggart Collins and Breed, unpubl.; Taggart
and Friend, unpubl.). Although this method of teat
attachment is not recommended for members of the
Macropodidae, it has been successful in potoroos
(long-nosed potoroo; Gilbert’s potoroo, Potorous gil-
bertii) and bettongs (northern bettong, Bettongia
tropica; brush-tailed bettong, B. penicillata) using
pouch young much less than 21 days old. Individuals
of these species have been found to readily attach to
the teat of their own mothers (Smith 1998; Taggart,
Collins and Breed, unpubl. data; Taggart and Friend,
unpubl.data) or surrogate mothers (Smith 1998; Tag-
gart, Collins and Breed, unpubl. data). This may be
due to the early development of the lateral margins of
the lips in this group (Hill and Hill 1955; Sharman
1962; Hughes and Hall 1988).
For direct physical attachment of small pouch
young to the teat in any species, chemical restraint
(sedation) is required (Merchant and Sharman 1966;
Taggart 2002; Sterneberg 2005; Taggart et al. 2005).
This ensures the surrogate mother is immobile while
physical attachment of the young is carried out.
Attachment is achieved by placing the tip of the teat
at the opening of the mouth of the pouch young and
gently pushing the teat into the young’s mouth (Figs
Figure 23.1: Attaching pouch young to teat.
Figure 23.2: Attachment of a brush-tailed rock-wallaby
pouch young to the teat of its tammar wallaby surrogate
mother.
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Cross-fostering and short-term pouch young isolation in macropodoid marsupials 267
23.1, 23.2; Merchant and Sharman 1966; Johnson
1981; Sterneberg 2005; Taggart 2002; Taggart et al.
2005). The use of fine blunt-nosed forceps in direct-
ing the teat into the mouth has proved useful (Tag-
gart 2002; Taggart et al. 2005).
Successful attachment of the young to the surro-
gate mother’s teat results in immediate suckling and
the procedure takes very little time to perform (Mer-
chant and Sharman 1966; Taggart et al. 2005). Mois-
tening the hands prevents the young from sticking to
the operator and facilitates the procedure (Schultz et
al. 2006). The surrogate mother is kept anaesthetised
for 15–20 minutes after the transfer and the foster
young should be periodically checked to ensure that
it remains attached to the teat. If it detaches, the pro-
cedure is repeated (Taggart et al. 2005; Schultz et al.
2006). Checking teat attachment should be rapid and
with limited artificial light. Shining strong artificial
light directly into the pouch and for prolonged peri-
ods is not recommended as it results in restlessness
(squirming) of the pouch young and increased
movement of the front legs, which may lead to disen-
gagement from the teat. Likewise, the raising and
separation of the outer pouch wall also causes
squirming and may result in dislodgment (Taggart et
al. 2005; Schultz et al. 2006). When pouch young
have been separated from the teat for more than two
hours, two or three drops of Hartmann’s Solution
(Baxter Healthcare Pty Ltd, Toongabbie, NSW)
placed at the entrance to the young’s mouth aids in
reducing dehydration (Taggart and Schultz, unpubl.
data). After successful attachment of the young to
the surrogate mother’s teat has been confirmed, the
surrogate mother can be returned to her enclosure
and the fostered pouch young allowed to grow and
develop in the pouch (Fig. 23.3) with as little interfer-
ence as possible from researchers and keeping staff.
SHORT-TERM (<10 HR) ISOLATION OF
VERY SMALL (1–40 G) POUCH
YOUNG
Preparing pouch young for short-term
isolation
Olive oil (Johnson 1981) and humilac (an oil-free
humectant; Taggart et al. 2005) have been used to help
maintain skin moisture of unfurred pouch young fol-
lowing removal from their mother’s pouch. In mild
weather or over short periods, this is not necessary.
Young are then generally wrapped in soft, smooth,
moistened porous cloth such as linen, medical cotton
swabs and/or surgical scarf material and transferred
to an incubator for the period of isolation.
Incubator characteristics
The type of incubator used to maintain isolated,
unfurred macropodoid pouch young depends on the
purpose of the study, the desired length of isolation
and the age of the young (Loh and Shield 1977; Rose
et al. 1998; Taggart et al. 2002). The function of an
incubator is to maintain young in an environment
with a stable temperature and humidity. Laboratory
studies that examined the onset of homeothermy
typically described the unfurred pouch young,
wrapped as outlined above, and placed within con-
tainers suspended within a water bath (Messer and
Green 1979; Green et al. 1980, 1988; Gemmel and
Johnson 1985).
Incubators used for the transport of pouch young
from one site to another should be light-weight and
portable (Figs 23.4, 23.5) and, if powered, run on a
12 V DC system (Taggart and Schultz, unpubl. data).
Figure 23.3: Cross-fostered brush-tailed rock-wallaby in
the pouch of its yellow-footed rock-wallaby surrogate
mother. Figure 23.4: Incubator design.
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268 Macropods: The Biology of Kangaroos, Wallabies and Rat-kangaroos
In the authors’ experience, power is generally only
required in hot conditions for maintenance of a
cooler environment for the pouch young. Careful
planning of pouch young movements can avoid these
conditions. If artificially heated, incubators should
be floor-heated. There should not be any convection
of warm air, as this dries the skin of the young and, in
severe cases, causes death (Taggart and Schultz,
unpubl. data). Small (17 × 12 × 9 cm) portable incu-
bators (Fig. 23.4b) can be warmed very effectively
using the body heat of the person involved in the
isolation (held under clothing against the skin) and
heat loss can be further minimised by placing the
incubator in a soft insulated cooler.
Supplementary feeding/fluids
Supplementary feeding of pouch young is not
required or advised if young are isolated from the
pouch for ≤10 hours. Depending upon the size of the
pouch young and the temperature and humidity of
the environment inside the incubator or holding
container, there may be a need to supplement the
young with fluids (Taggart et al. 2002). Larger
unfurred young, or those maintained in warmer
conditions, are more likely to require a fluid supple-
ment. A drop of Hartmann’s Solution placed on the
lips will generally be accepted without any side effects
(Taggart and Schultz, unpubl. data).
OBSERVATIONS/DISCUSSION
Cross-fostering
Survival of cross-fostered young
Cross-fostering studies have been carried out with six
potoroid and 13 macropodid species, with a total of
30 different crosses trialled (six potoroid and 21
macropodid; Tables 23.2 and 23.3). Survival of cross-
fostered pouch young, to either the end of the experi-
ment or permanent pouch exit, varied from 0–100%
between species pairings. Most studies examined
fostering within members of the families Macropodi-
dae or Potoroidae; four of nine crosses in the Potoroi-
dae and 14 of 21 crosses in the Macropodidae resulted
in survival rates of cross-fostered young in excess of
75%. One study, however, performed crosses between
a potoroid (long-nosed potoroo) and macropodid
species (tammar wallaby); neither (n = 2) was suc-
cessful (Taggart, unpubl. data). Failure of these pouch
young to survive may have been due to milk incom-
patibilities or to problems with teat size or pouch size,
or all of them. Further studies are required to explore
the limits of this technique across families.
Differences in cross-fostering success rates
between various interspecific crosses and different
studies are hard to interpret. Differences between
studies in the age and size of the donor young at fos-
tering, the age and size of the donor and foster
mother’s own young at fostering, the length of time
cross-fostered young were allowed to remain on the
teat of their surrogate mother and sample sizes (Table
23.1) make comparisons difficult. Despite these chal-
lenges, the studies clearly show that young from one
macropodoid species can be successfully reared to
independence by the female of another and, if an
appropriate foster species is available, the survival
rates of fostered young can equal or better (Smith
1998; Schultz et al. 2006) those of young reared on
their natural mother (Tables 23.2 and 23.3).
Timing/age of donor young at transfer
In marsupials, pouch young from day 1 of pouch life
(<1 g) to 80% of the period of lactation, when the
pouch young had already developed some body hair
(Merchant and Sharman 1966; Taggart et al. 2005),
have been successfully cross-fostered. Although most
studies have not shown a period during lactation
when cross-fostering is more likely to succeed (Mer-
chant and Sharman 1966) there do appear to be some
advantages, especially in endangered species, in
transferring young early in pouch life. Unless the
researcher is very experienced, the use of pouch
young <1.5 g for cross-fostering is not recommended
because of physical constraints associated with han-
dling and reattaching tiny young. Likewise, leaving
young on their mothers until late in pouch life is not
ideal as this lengthens the period of lactation of the
Figure 23.5: Rock-wallaby pouch young in incubator.
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Cross-fostering and short-term pouch young isolation in macropodoid marsupials 269
donor female, increases the birth interval and reduces
the donor female’s reproductive rate and production
of additional pouch young. Interestingly, a recent
study of growth and survival of tammar wallaby
young cross-fostered to parma wallabies (Macropus
parma) reported an increased weaning success when
Table 23.2: Cross-fostering studies of potoroid pouch young detailing survival rates of surrogate-reared young to the end
of experimentation or permanent pouch exit
Donor Surrogate n % survival Reference
Po. tridactylus B. penicillata 7 43 Collins 2002
Po. tridactylus B. lesueur 2 100 Taggart, unpubl. data
Po. tridactylus M. eugenii 2 0 Taggart, unpubl. data
Po. tridactylus B. gaimardi 7 86 Sterneberg 2005
Po. gilbertii Po. tridactylus 5 60 Taggart, Hill and Friend, unpubl.
data
B. gaimardi Po. tridactylus 7 29 Sterneberg 2005
B. penicillata Po. tridactylus 10 40 Collins 2002
B. lesueur Po. tridactylus 2 100 Taggart, unpubl. data
B. tropica B. penicillata 11 82 Smith 1998
Table 23.3: Cross-fostering studies of macropodid pouch young detailing survival rates of surrogate reared young to the
end of experimentation or permanent pouch exit
Donor Surrogate n % survival Reference
M. eugenii (KI) M. rufus 2 0 Merchant and Sharman 1966
M. eugenii (KI) T. billardierii 6 20 O’Brien 2004
M. eugenii (KI) M. parma 4 100 Menzies et al. 2007
M. eugenii (ML) M. eugenii (KI) 87 78 Taggart and Smith, unpubl. data
M. rufus W. bicolor 1 100 Merchant and Sharman 1966
M. rufus M. giganteus 1 100 Merchant and Sharman 1966
M. parryi M. agilis 9 77 Johnson 1981
M. parma M. eugenii (KI) 8 25 Menzies et al. 2007
M. giganteus M. rufus 4 100 Merchant and Sharman 1966
M. rufogriseus M. rufus 1 0 Merchant and Sharman 1966
T. billardierii M. eugenii (KI) 8 66 O’Brien 2004
L. conspicillatus Pe. inornata 2 100 Johnson 1981
O. fraenata Pe. inornata 1 100 Johnson 1981
W. bicolor M. rufus 5 80 Merchant and Sharman 1966
W. bicolor M. agilis 2 100 Johnson 1981
Pe. penicillata M. eugenii (KI) 15+ 83 Taggart et al. 2005; Schultz et al.
2006
Pe. penicillata Pe. xanthopus 20+ 82 Taggart et al. 2005; Schultz et al.
2006
Pe. xanthopus M. eugenii (KI) 14 71 Schultz and Taggart, unpubl. data
Pe. xanthopus M. rufus 2 0 Merchant and Sharman 1966
Pe. lateralis M. eugenii (KI) 2 100 Jones et al. 2004
Pe. lateralis Pe. xanthopus 15 87 Taggart and Smith, unpubl. data
ML = mainland; KI = Kangaroo Island.
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270 Macropods: The Biology of Kangaroos, Wallabies and Rat-kangaroos
young were transferred after day 30 of pouch life
compared with those transferred before day 15
(Menzies et al. 2007).
When cross-fostering of brush-tailed rock-wal-
laby (Petrogale penicillata) pouch young was delayed
until young were between day 40 and day 70 of age
there was a significant mortality of donor pouch
young ‘prior to transfer’. No pouch young mortality
was observed in donor females, however, when young
were cross-fostered between eight and 20 days of age
(Schultz et al. 2006). Schultz et al. (2006) showed
that this pouch young mortality prior to transfer
resulted from a behavioural abnormality in some
mothers (ejection of the pouch young) that was not
linked to cross-fostering. While the cause of pouch
young losses could not be identified and it was not
known if these losses were accidental or caused by
hidden stressors influencing maternal behaviour, the
timing of losses appeared to coincide with an increase
in the activity of the young and/or in the mother’s
awareness of the presence of its young (Schultz et al.
2006). It is still unknown why the foster mothers
were less accident-prone or less sensitive to the
increased movement of the pouch young. A suggested
starting-point for cross-fostering of pouch young
from an untested species is for the donor young to be
between days 10–20 post-partum, or 2–10 g in weight
(Merchant and Sharman 1966; Taggart and Schultz,
pers. obs.).
Age and weight of pouch young of
donor and surrogate mothers: effects on
survival of cross-fostered young
Most cross-fostering studies suggest that synchrony
in the age of the pouch young transferred and that of
the young removed is an important factor influenc-
ing the success of fostering. However, the data from
fostering studies do not fully support this. Merchant
and Sharman (1966) showed that six of 10 fostered
young had retarded growth or died when the fostered
young was older than the young removed from the
surrogate mother. This contrasts with the findings of
Johnson (1981), in whose study five pouch young
transferred to surrogate mothers with younger pouch
young survived and developed normally. Likewise,
cross-fostering studies using long-nosed potoroos
and Tasmanian bettongs (Bettongia gaimardi)
(Sterneberg 2005) showed that age differences at
transfer did not appear to influence mortality rates,
although sample size in this study was small.
These studies highlight the age difference between
the young being fostered but give no clear guidance
on the effects of weight differences (Merchant and
Sharman 1966; Johnson 1981; Smith 1998) between
the donor and foster mother’s own young. In studies
of brush-tailed rock-wallabies, 13 of 16 pouch young
that were 0–50% lighter at the time of transfer than
the young they were replacing, survived and grew to
independence, whereas two pouch young 5% and
68% heavier than the young of the surrogate species
did not survive (Taggart et al. 2005). The differences
in weight between the young of donor and surrogate
mothers relate directly to the volume and perhaps
composition of milk the young has been consuming
and thus may be an indicator of the suitability of
potential surrogate mothers as hosts for foster young.
Cross-fostering is more likely to be successful if the
pouch young being transferred is of similar or slightly
smaller size/weight than the young of the foster spe-
cies, thus increasing the likelihood that sufficient
milk of appropriate composition is available for the
fostered pouch young (Taggart et al. 2005). Studies
on other macropodid species (Johnson 1981; Bell and
Close 1994) suggest that this difference may become
less critical when the transferred young are older/
larger (>40 g). Ideally, preference should be given to
fostering donor young that are similar in size or
slightly larger than young from a surrogate mother.
Cross-fostering studies in black-footed rock-walla-
bies (Petrogale lateralis) used donor young weighing
between 20% less and 10% more than the surrogate
mother’s own pouch young. Success rates to weaning
in this study were 87% of young transferred (Taggart
and Smith, unpubl. data; Table 23.3). Age and weight
of pouch young of selected surrogate mothers are,
however, not the only factors to consider when select-
ing an appropriate surrogate female.
Effects of fostering on growth and
development
Growth rate, development and pouch life
Various effects of cross-fostering on growth and
length of pouch life of transfer pouch young have been
reported, from slowed growth and extended pouch
life to accelerated growth and shortened pouch life
(Table 23.4). In general, the data show that the growth
rate and pouch life of foster-reared young approached
that of their surrogate species after transfer, although
there were exceptions. For example, although the
pouch life of young agile wallabies (Macropus agilis) is
090901 Macropods 1pp.indd 270 17/09/09 11:41:45

Cross-fostering and short-term pouch young isolation in macropodoid marsupials 271
Table 23.4: Growth and pouch life of macropodoid young on mothers and surrogate mothers
Donor
species
Surrogate
species
Pouch life
(donor)
Pouch life
(surrogate)
No. of
surrogate
young (n)
Pouch life
(surrogate
young)
Effect of
fostering on
pouch life of
donor
Effect of fostering
on growth/
development of
donor Key reference
M. eugenii T. billardierii 250–260 200 6 - - Accelerated O’Brien 2004
T. billardierii M. eugenii 200 250–260 8 - - Slow O’Brien 2004
M. parryi M. agilis 259–281 207–237 5 266–381 Normal Normal Johnson 1981
M. parryi M. agilis 259–281 207–237 2 - Increased Slowed Johnson 1981
M. eugenii M. pama 250–260 212 4 - - Normal Menzies et al. 2007
M. parma M. eugenii 212 250–260 10 270 Increased Slowed Menzies et al. 2007
M. rufus M. rufogriseus 235 (229–253) 270 1 - - Normal Merchant and Sharman 1966
M. eugenii M. rufus 250–260 235 (229–253) 1 ~178 Decreased Normal Merchant and Sharman 1966
M. giganteus M. rufus 319 (283–330) 235 (229–253) 1 - - Normal Merchant and Sharman 1966
M. giganteus M. rufus 319 (283–330) 235 (229–253) 1 374 Increased Normal Merchant and Sharman 1966
Pe. lateralis M. eugenii 180–200 250–260 2 - - Slow Jones et al. 2004
W. bicolor M. agilis 256 (210–260) 207–237 2 ~197 and
~204
Acc ? Johnson 1981
W. bicolor M. rufus 256 (210–260) 235 (229–253) 2 267 Normal Accelerated Merchant and Sharman 1966
Pe. xanthopus M. rufus 190–200 235 (229–253) 1 ~181 Normal Normal Merchant and Sharman 1966
Pe. penicillata Pe. xanthopus 190–230 190–200 180–210 Normal Accelerated Taggart et al. 2005
Pe. penicillata M. eugenii 190–230 250–260 255 Increased Slow Taggart et al 2005
L. conspicillatus Pe. inornata 140–162 204 2 205 and 234 Increased Normal Johnson 1981
Po. tridactylus B. gaimardi 130 109 7 - - Accelerated Sterneberg 2005
B. gaimardi Po. tridactylus 109 130 7 - - Slow Sterneberg 2005
B. tropica B. penicillata 100–109 90–100 9 104 Normal Normal Smith 1998
090901 Macropods 1pp.indd 271 17/09/09 11:41:45

272 Macropods: The Biology of Kangaroos, Wallabies and Rat-kangaroos
shorter than that of whiptail wallabies (M. parryi), the
duration of pouch life of whiptail wallaby young
increased when they were cross-fostered to agile wal-
labies (Johnson 1981). Similarly, the growth rate of an
eastern grey kangaroo (M. giganteus) young trans-
ferred to a red kangaroo (M. rufus) was normal,
although pouch life in red kangaroos is some 70–80
days shorter than that of eastern grey kangaroos (Mer-
chant and Sharman 1966).
Retarded growth has been noted in some species
following cross-fostering. For example, two of seven
young whiptail wallabies cross-fostered to agile walla-
bies had extended pouch lives, yet all survived to
weaning (Johnson 1981). Spectacled hare-wallabies
(Lagorchestes conspicillatus) transferred to unadorned
rock-wallabies (Petrogale inornata) grew at normal
rates but remained in the pouch for significantly
longer periods (n = 2; Johnson 1981). In 2004, O’Brien
reported that all eight Tasmanian pademelon (Thyl-
ogale billardierii) pouch young cross-fostered to
tammar wallaby surrogates showed retarded growth,
including head length, weight and pes length, com-
pared to controls. Ten parma wallaby young trans-
ferred to tammar wallaby (Menzies et al. 2007) showed
a similar pattern of slowed growth. Developmental
milestones including eyes opening, eruption of vibris-
sae and pigmentation of nails and skin also occurred
later in lactation in both cross-fostering studies
(O’Brien 2004; Menzies et al. 2007). In contrast,
swamp wallaby (Wallabia bicolor) pouch young trans-
ferred to red kangaroos (Merchant and Sharman
1966), and brush-tailed rock-wallaby young trans-
ferred to yellow-footed rock-wallabies (Petrogale xan-
thopus) grew at accelerated rates (head length and
weight) (Taggart et al. 2005). In a study of cross-foster-
ing between long-nosed potoroos and Tasmanian bet-
tongs, undernourishment due to inappropriate milk
quality or quantity, or both, led to delayed growth and
development while transfers of pouch young to surro-
gate mothers with more advanced milk generally
enhanced growth and development (Sterneberg 2005).
Time to weaning, milk composition/timing of
milk components
In some species the time of weaning of foster young
was similar to that of the surrogate species’ natural
young, particularly when young of species with short
pouch lives were transferred into the pouches of a
foster species that normally carried young for longer
periods. Young of the brush-tailed rock-wallaby, for
example, were weaned significantly later when reared
on tammar wallaby surrogate mothers than when
reared in the pouches of donor mothers or yellow-
footed rock-wallaby surrogate mothers (Taggart et al.
2005). In other species, such as the parma wallaby
(Menzies et al. 2007), weaning of fostered animals
(~365 days) occurred significantly later than in both
the donor (300 days) and the foster species (tammar
wallaby [270–300]; Murphy and Smith 1970). Like-
wise, Merchant and Sharman (1966) reported that a
young eastern grey kangaroo reared on a red kanga-
roo surrogate mother continued to be suckled for
over 550 days even though weaning in red kangaroo
young usually occurs around 360 days. They con-
cluded that, by continuing to demand milk, the foster
young imposed on the red kangaroo surrogate
mother a condition like that normally found in east-
ern grey kangaroos, which usually wean young
around 540 days (Kirkpatrick 1965).
Onset of sexual maturity
In cross-fostering studies of the long-nosed potoroo
and Tasmanian bettong, reduced adult size and
delayed onset of puberty in foster-reared animals
compared to controls was rare (Sterneberg 2005). In
contrast, Menzies et al. (2007) observed, from a small
sample size of foster-reared female parma wallaby
and tammar wallaby young, that the production of
first pouch young occurred later than was typical for
either species. However, Merchant and Sharman
(1966) reported that a swamp wallaby young reared
on a red kangaroo surrogate mother showed acceler-
ated growth and early sexual maturity.
Gastrointestinal maturation
Waite et al. (2005) examined the effects on gastroin-
testinal maturation in tammar wallabies of providing
younger pouch young with older-stage milk. They
reported a significant increase in pouch young weight
when donor young were supplied with older-stage
milk, possibly due to higher concentrations of lipid in
milk from the more advanced mammary glands.
However, no difference was found in stomach or small
intestine development between young reared on the
appropriate milk for age and those reared on milk for
more advanced pouch young (Waite et al. 2005).
Observations on the behaviour of
surrogate mothers and fostered animals
Surrogate mothers readily accepted cross-fostered
pouch young at least for short periods, during which
growth occurred, regardless of species differences
090901 Macropods 1pp.indd 272 17/09/09 11:41:45

Cross-fostering and short-term pouch young isolation in macropodoid marsupials 273
and differences in lengths of pouch life between spe-
cies (Merchant and Sharman 1966; Johnson 1981;
Smith 1998; Sterneberg 2005; Taggart et al. 2005;
Schultz et al. 2006; Menzies et al. 2007). In addition,
although the calls of donor and foster species are
often quite different (Sterneberg 2005), surrogate
mothers show normal maternal responses to the calls
of their foster young if they became lost after pouch
emergence or when separated in captivity (Merchant
and Sharman 1966; Sterneberg 2005). Cross-fostered
long-nosed potoroo young were able to recognise the
calls of their surrogate mothers and both surrogate
mother and fostered young showed increased vigi-
lance when young left the pouch (Sterneberg 2005).
Sterneberg (2005) reported that young cross-fostered
potoroos and bettongs initially imitated the preferred
locomotion of their surrogate mother (i.e. bipedal
locomotion for bettongs and a quadrupedal locomo-
tion for potoroos) before their species-specific loco-
motion began to dominate. Heightened aggression
was observed when integrating bettongs reared in
potoroo pouches with mother-reared bettongs:
potoroo-reared male bettongs became the target of
agonistic behaviour from adult females (Sterneberg
2005). This appeared to be due to the more solitary
life-style of the mother-reared bettongs compared
with those reared in potoroo pouches.
In contrast, from the time of pouch exit, young
brush-tailed rock-wallabies foster-reared on tammar
wallabies showed normal donor species behavioural
traits, with young at foot using trees, rocks, hollows
and other high vantage points when basking or
moving between locations while their tammar wal-
laby surrogate mothers remained terrestrial (Taggart
et al. 2005) Young foster-reared brush-tailed rock-
wallabies also readily mixed with, and chose to den
close to, members of their own species following
separation from their surrogate mothers immedi-
ately after weaning. Den sites included caves, tree
overhangs and rabbit burrows (Taggart 2002; Tag-
gart et al. 2005; Taggart, unpubl. data).
Results from all studies indicate that, at sexual
maturity, reproductive behaviour was normal for all
cross-fostered animals for which data are available.
These animals recognised and mated with their own
species and, in the case of females, gave birth to and
nursed their own young (swamp wallaby, Merchant
and Sharman 1966; Johnson 1981; northern bettong,
Smith 1998; brush-tailed rock-wallaby, Taggart 2002;
Taggart et al. 2005; long-footed potoroo and Tasma-
nian bettong, Sterneberg 2005; brush-tailed
rock-wallaby and yellow-footed rock-wallaby, Schultz
et al. 2006; tammar wallaby and parma wallaby,
Menzies et al. 2007).
Effects of pouch young removal for
fostering on donor female reproductive
rate
The effects of pouch young removal on the reproduc-
tive rate of donor females can be dramatic. In some
individuals, up to eight-fold increases in female
reproductive rate have been observed (Table 23.5;
Smith 1998; Taggart et al. 2005; Schultz et al. 2006).
In the brush-tailed rock-wallaby, Schultz et al. (2006)
reported a reduction in the birth interval in some
females from ≥250 days to only 40 days where pouch
young averaging just eight to 14 days old and weigh-
ing ~2 g were removed. The authors described one
female that gave birth to 26 young in six seasons and
another that produced 19 young in only four seasons.
This is markedly higher than the life-time reproduc-
tive output of a normal female brush-tailed rock-
wallaby, which is probably around four young and
very unlikely to exceed seven young (Jarman and
Bayne 1997; Hazlitt et al. 2006; Wynd et al. 2006,;
Taggart, Reside and Martin, unpubl. data).
In the northern bettong, Smith (1998) found that
transfer of young at 21 days of age to brush-tailed bet-
tongs resulted in the birth of northern bettong off-
spring (which survived to weaning) at intervals of
about 40 days (Smith 1998). This suggests, since all
potoroid species are capable of breeding year-round,
that cross-fostering could increase the production of
young from the norm of two to three per year to as
many as nine, an increment of about 300%. In addi-
tion to the benefit of a greater success rate of brush-
tailed bettong surrogate mothers rearing northern
bettong pouch young to weaning than their natural
mothers (Smith 1998), this provides a very effective
means of enhancing breeding and recruitment. A
critical element in the success of this procedure and
maintenance of the high production rates is for the
breeding program to have suitable numbers of appro-
priate surrogate mothers, for the continued successful
breeding of both donor and foster species.
Recommendations for maximising cross-
fostering success and production of
pouch young
Based on available data (Merchant and Sharman
1966; Johnson 1981; Smith 1998; Jones et al. 2004;
Taggart et al. 2005; Schultz et al. 2006) the following
090901 Macropods 1pp.indd 273 17/09/09 11:41:45

274 Macropods: The Biology of Kangaroos, Wallabies and Rat-kangaroos
recommendations are made to ensure maximum
cross-fostering success:
1 that the size (weight and head length) of the
pouch young to be fostered is similar to, or slightly
smaller than, that of the young removed from the
surrogate mother’s pouch (Jones et al. 2004; Tag-
gart et al. 2005; Schultz et al. 2006);
2 that the selected surrogate mother has a pouch
young of similar age to that of the intended foster
young (Merchant and Sharman 1966; Johnson
1981; Smith 1998; Jones et al. 2004);
3 that teat size (particularly diameter) is similar
between donor and surrogate mothers at the time
of pouch young transfer (Merchant and Sharman
1966; Sterneberg 2005; Taggart, unpubl. data);
4 that cross-fostering is done early in pouch life
when the young weighs 2–5 g;
5 that handling of surrogate mothers with cross-
fostered pouch young is kept to a minimum, espe-
cially in the second half of pouch life.
SHORT-TERM ISOLATION STUDIES IN
SMALL POUCH YOUNG
Temperature regulation in small
unfurred pouch young
At birth and during most of pouch life marsupial
young are ectothermic, obtaining heat directly from
the environment (Reynolds 1952; Shield 1966;
Gemmel and Johnson 1985; Rose et al. 1998). In the
tammar wallaby, as in other marsupials studied,
pouch temperature equates roughly with the rectal
temperature of the mother (~37°C) (Reynolds 1952;
Bartholomew 1956; Gemmel and Johnson 1985).
Early development of pouch young therefore gener-
ally occurs at a relatively constant temperature simi-
lar to the mother’s body temperature. As development
proceeds, macropodoid pouch young gradually
increase their metabolic heat production, to adult
levels by the time of pouch exit (Loh and Shield 1977;
Rose et al. 1998).
Pouch young isolation studies in the
Macropodoidea
Young of two potoroid and 11 macropodid species
have been isolated from the pouch at a range of ages
from one to 25 weeks and for various lengths of time
from 30 minutes to 30 hours (Table 23.6). Most of the
available data come from studies that examine
changes in the composition of milk during develop-
ment (Table 23.6; Shield 1966; Renfree and Tyndale-
Biscoe 1978; Messer and Green 1979; Green et al.
1980, 1988; Gemmel and Johnson 1985; Merchant et
al. 1996; Rose et al. 1998; Taggart et al. 2002). Suc-
cessful short-term pouch young isolation has been
reported at temperatures ranging from <4ºC to 35ºC
with all studies indicating that humidity was main-
tained at high levels (>90% RH) during the period of
isolation from the pouch (Renfree and Tyndale-Bis-
coe 1978; Gemmel and Johnson 1985; Rose et al.
1998; Taggart et al. 2002). Differences between the
success rates of pouch young isolation at higher tem-
peratures (≥30°C) may be explained by differences in
study design, supplementation of young with fluids
and/or pouch young age/size at the time of isolation
Table 23.5: Effects of cross-fostering on female reproductive rate in threatened macropodoid taxa
Threatened donor
taxon Surrogate taxon
Donor female
reproductive rate
PY survival to
weaning (%) Reference
Pe. penicillata Pe. xanthopus
2–8-fold ↑
82 Taggart et al. 2005;
Schultz et al. 2006
M. eugenii
2–3-fold ↑
83 Taggart et al. 2005;
Schultz et al. 2006
M. eugenii (ML) M. eugenii (KI)
2–3-fold ↑
78 Taggart and Smith,
unpubl. data
B. tropica B. penicillata
2–9-fold ↑
82 Smith 1998
Pe. lateralis Pe. xanthopus
>2-fold ↑
87 Taggart and Smith,
unpubl. data
Pe. lateralis M. eugenii
2–3-fold ↑
100 Jones et al. 2004
Po. gilbertii Po. tridactylus ? 75 Taggart and Friend,
unpubl. data
ML = mainland; KI = Kangaroo Island.
090901 Macropods 1pp.indd 274 17/09/09 11:41:45

Cross-fostering and short-term pouch young isolation in macropodoid marsupials 275
(Taggart et al. 2002). Data indicate that, as their size
increases, survival of pouch young after isolation
from the teat at higher temperatures and possibly for
longer periods also increases (Green et al. 1988; Mer-
chant et al. 1996; Taggart et al. 2002). This is probably
related to differences in the surface area to body mass
ratio between small and larger pouch young, and
thus differences in rates of evaporative water loss.
The tolerance of ectothermic pouch young to tem-
porary cooling during the first half of pouch life and
their ability to recover and grow normally is well
documented (Renfree and Tyndale-Biscoe 1978;
Rose et al. 1998; Taggart et al. 2002). The success of
pouch young isolation studies at lower temperatures
is likely to be due to a combination of factors includ-
ing lowered heart and metabolic rate, reduced evapo-
rative water loss at lower temperatures, and slowing
of the dehydration rate of the pouch young (Loh and
Shield 1977; Rose et al. 1998; Taggart et al. 2002). A
reduction by ~50% in the metabolic rate and heart
rate of pouch young held at ~23°C has been reported
(Bartholomew 1956; Loh and Shield 1977; Renfree
and Tyndale Biscoe 1978; Rose et al. 1998; Shield
1966). All tammar wallaby and brush-tailed rock-
wallaby pouch young, including one that weighed
only 0.4 g, held at 23°C survived a six-hour isolation
period from the pouch; when returned, they survived
and developed normally (Taggart et al. 2002). The
temporary lowering of metabolic rate for both small
and large pouch young prevents excessive depletion
of energy reserves while isolated from the teat (Loh
and Shield 1977). In addition, as small unfurred
pouch young are poikilothermic, lower ambient tem-
peratures result in lower body temperatures and
lower oxygen consumption rates (Bartholomew
1956; Loh and Shield 1977, Rose et al. 1998).
Recommendations for maximising pouch
young survival after short-term isolation
Based on available data (Shield 1966; Renfree and
Tyndale-Biscoe 1978; Messer and Green 1979; Green
et al. 1980, 1988; Johnson 1981; Gemmel and John-
son 1985; Merchant et al. 1996; Rose et al. 1998; Tag-
gart et al. 2002) and assuming small unfurred pouch
young have been prepared and isolated as described,
the following recommendations should maximise
pouch young survival after short-term isolation:
1 all unfurred pouch young should be isolated at
high humidity (>90% RH);
2 very small, unfurred pouch young should be iso-
lated at temperatures around 20–25º C;
3 isolation of very small, unfurred pouch young
should not exceed six to eight hours without sup-
plementary fluids and, if data for that species is not
available, without further research on that species.
IMPLICATIONS FOR CONSERVATION
AND SPECIES MANAGEMENT
The use of procedures to maintain macropodoid
young in isolation from the pouch for short periods,
Table 23.6: Short-term pouch young isolation studies using small macropodoid marsupial young
Species
PY age
(weeks)
Isolation
temperature
(ºC)
Isolation
humidity
(%RH)
Hours
isolated Survival References
Po. tridactylus 1–25 23–35 Humid (>95) 3–5; 10 Y Crowley et al. 1988
B. gaimardi 1–25 22–35 >95 3–5 Y Rose et al. 1998
Pe. penicillata 1–23 23–30 >95 6–13 Y (20–25ºC) Taggart et al. 2002
Pe. xanthopus 4–10 23–25 >95 6–8 Y (20–25ºC) Schultz and Taggart,
unpubl. data
Pe. lateralis 2–8 20–25 >95 5.5–9 Y (20–25ºC) Taggart and Smith,
unpubl. data
Pe. assimilis 10–22.5 Humid Y Merchant et al. 1996
M. eugenii 4–32 <4–35 >95 0.5; 3–8 Y Renfree and Tyndale-
Biscoe 1978; Green et al.
1980; Taggart et al. 2002
M. rufus 14+ ? Humid 3 Y Lemon and Baker 1967
S. brachyurus 1.2–25 20–40 Humid 9 Y Shield 1966
090901 Macropods 1pp.indd 275 17/09/09 11:41:45

276 Macropods: The Biology of Kangaroos, Wallabies and Rat-kangaroos
in combination with cross-fostering techniques
(Merchant and Sharman 1966; Smith 1998; Taggart
et al. 2002) gives conservationists a powerful tool for
accelerating breeding in endangered species. Assum-
ing suitable foster species are available, the tech-
niques described here eliminate the need to bring
wild-caught adults into captivity for genetic or
breeding purposes. This has the advantage of not
compromising the long-term reproductive capacity
of threatened small populations in the wild and
avoids the associated stressors that can potentially
reduce the reproductive output in captivity of wild-
born and raised adults. The techniques provide an
effective means of more safely moving animals, and
their genes, between captive institutions to assist
breeding and conservation objectives (Taggart and
Schultz, unpubl. data) and eliminate welfare issues
associated with bringing wild adults into captivity
(Taggart et al. 2002).
Merchant and Sharman (1966) were the first to
use this technique to transfer (transfer conditions
unknown) a 78-day-old swamp wallaby, approxi-
mately 75 g (Bellamy 1992), from a mother shot in
the field to a red kangaroo surrogate mother 177 km
away. The pouch young was reared to independence.
Based on their observations, Merchant and Sharman
(1966) suggested that ‘transfer of young of rare spe-
cies to the pouches of common species of marsupials
appeared to be a feasible method of increasing the
numbers of rare species in captivity’. The combina-
tion of cross-fostering and pouch young isolation
techniques has been used successfully to transfer
pouch young as small as 1 g up to 1000 km to estab-
lish captive breeding colonies and/or supplement
genetics in captive colonies of black-footed rock-
wallaby, brush-tailed rock-wallaby, yellow-footed
rock-wallaby and Gilbert’s potoroo (Taggart, Smith,
Schultz and Friend, unpubl. data).
Embryonic diapause in macropodoid species
(Tyndale-Biscoe 1979; Tyndale-Biscoe and Renfree
1987) is an important but not essential factor in the
success of cross-fostering for captive breeding and
conservation. In species displaying embryonic dia-
pause, pouch young removal causes cessation of lacta-
tion and reactivation and birth of the diapausing
embryo. The capacity of most female macropodoids
to rapidly enter a new cycle of post-partum oestrus
and mating, to generate a new diapausing embryo,
enhances the success of this procedure with captive
and wild polyoestrous females. Removal of pouch
young reduces birth intervals in macropodoid marsu-
pials and significantly increases the number of pouch
young available for cross-fostering. In this way pouch
young removal, short-term isolation from the pouch
and fostering not only benefit captive breeding pro-
grams but can be used to accelerate the production of
young by females of endangered species in the wild.
Based on these studies, we suggest that the number
of pouch young produced by females of many macro-
podoid species could be readily increased from one
to as many as four to eight young per female annually
depending upon the species and the frequency of
cycling. Application of this technique could have a
dramatic effect on animal numbers within a rela-
tively short period, so maintaining a genetically
diverse captive breeding group would therefore be a
high priority.
CONCLUSIONS
The greatest current threat to many endangered
macropodoid species is the small size and fragmenta-
tion of remaining populations. Small populations are
highly vulnerable to local catastrophes, predation,
inbreeding and the loss of genetic variation by genetic
drift, and without an active program of intervention
their continued decline is likely. As breeding in many
of these species is slow, recovery of their populations
through natural recruitment alone, even with signifi-
cant protection and environmental manipulation,
will likewise be slow. Cross-fostering and pouch
young isolation techniques provide a means of rapidly
and effectively alleviating the threat of small and
declining population size without drastically affect-
ing remaining wild populations. They also offer a
subtle way of diversifying the genetic make-up of
remnant isolated wild or captive populations. Thus,
these techniques have major implications as tools for
conservation and management of these species and
endangered species from other marsupial groups
(Caton 2005; Foster et al. 2006; Finlayson et al. 2008).
REFERENCES
Bartholomew GA 1956. Temperature regulation in the
macropod marsupial, Setonix brachyurus. Phys. Zool.
29: 26–40.
Bell JN and Close RL 1994. Fostering rock-wallaby pouch
young: a method of accelerated production of young
(abstract). National Rock-wallaby Symposium, p. 12.
Oraparinna, South Australia.
090901 Macropods 1pp.indd 276 17/09/09 11:41:45

Cross-fostering and short-term pouch young isolation in macropodoid marsupials 277
Bellamy T 1992. Urban Wildlife. University of Sydney
Press, Sydney.
Bolliger A and Pascoe JV 1953. Composition of kangaroo
milk (wallaroo, Macropus robustus). Aust. J. Sci. 15:
215–217.
Caton W 2005. The real deal, the good stuff. Mother’s
milk: you can’t beat it! Thylacinus 29: 2–4.
Collins M 2002. Cross-fostering and pouch isolation
studies in the Potoroidae. BSc Hons thesis. University
of Adelaide, Australia.
Crowley HM, Woodward DR and Rose RW 1988. Changes
in milk composition during lactation in the potoroo,
Potorous tridactylus (Marsupialia: Potoroinae). Aust. J.
Biol. Sci. 41: 289–296.
Finlayson GR, Taggart DA, Shimmin GA, White CR,
Dibben R, Steele V, Paris M and Temple-Smith PD
2007. Pouch young removal and return to oestrus in
wild southern hairy-nosed wombats (Lasiorhinus
latifrons). Anim. Reprod. Sci. 100: 216–222.
Finlayson G, Taggart DA, Steele VR, Shimmin GA and
Temple-Smith PD 2008. The application of intra-
species fostering techniques to the southern hairy-
nosed wombat, Lasiorhinus latifrons. Pacif. Conserv.
Biol. 13: 259–263.
Foster WK, Bradley AJ, Caton W and Taggart DA 2006.
Comparison of growth and development of the
red-tailed phascogale (Phascogale calura) in three
captive colonies. Aust. J. Zool. 54: 343–352.
Gemmel RT and Johnson G 1985. The development of
thermoregulation and the emergence from the pouch
of the marsupial bandicoot Isoodon macrourus.
Physiol. Zool. 58: 299–302.
Green B, Newgrain K and Merchant J 1980. Changes in
milk composition during late lactation in the tammar
wallaby (Macropus eugenii). Aust. J. Biol. Sci.33:
35–42.
Green B, Merchant J and Newgrain K 1988. Milk
consumption and energetics of growth in pouch
young of the tammar wallaby, Macropus eugenii. Aust.
J. Zool. 36: 217–227.
Hazlitt SL, Sigg DP, Eldridge MDB and Goldizen AW
2006. Restricted mating dispersal and strong breeding
group structure in a mid-sized marsupial mammal
(Petrogale penicillata). Mol. Ecol. 15: 2997–3007.
Hill JP and Hill WCO 1955. The growth stages of pouch
young of the native cat (Dasyurus viverrinus) together
with observations on the anatomy of the newborn
young. Trans. Zool. Soc. Lond. 28: 348–453.
Hughes RL and Hall LS 1988. Structural adaptations of
the newborn marsupial. In The Developing Marsupial:
Models for Biomedical Research. (Eds CH Tyndale-
Biscoe and PA Janssens) pp. 8–27. Springer-Verlag,
Berlin.
Jarman PJ and Bayne P 1997. Behavioural ecology of
Petrogale penicillata in relation to conservation. Aust.
Mammal. 19: 219–228.
Johnson PM 1981. The rearing of marsupial pouch young
by foster mothers of different species. Int. Zoo
Yearbook 21: 173–176.
Jones M, Taggart DA and Temple-Smith PD 2004. Age
determination and growth in wild Petrogale lateralis
pearsoni and captive Petrogale lateralis ‘MacDonnell
Ranges race’. Aust. J. Zool. 52: 447–461.
Kirkpatrick TH 1965. Studies of Macropodidae in
Queensland. III. Reproduction in the grey kangaroo
(Macropus major) in southern Queensland. Qld J. Agr.
Anim. Sci. 22: 319–328.
Lemon M and Baker S 1967. Changes in milk composition
of the red kangaroo, Megaleia rufa (Desmarest), during
lactation. Aust. J. Exp. Biol. Med. Sci. 45: 213–219.
Loh TT and Shield J 1977. Temperature regulation and
oxygen consumption in the developing macropod
marsupial, Setonix brachyurus. J. Physiol. 269:
677–686.
Menzies BR, Shaw G, Fletcher TP and Renfree MB 2007.
Perturbed growth and development in marsupial
young after reciprocal cross-fostering between species.
Reprod. Fertil. Dev. 19: 976–983.
Merchant JC and Sharman GB 1966. Observations on the
attachment of marsupial pouch young to the teats and
on rearing of pouch young by foster-mothers of the
same or different species. Aust. J. Zool. 14: 593–609.
Merchant JC, Marsh H, Spencer P and Death G 1996.
Milk composition and production in free-living allied
rock-wallabies, Petrogale assimilis. Aust. J. Zool. 44:
659–674.
Messer M and Green B 1979. Milk carbohydrates of
marsupials. II. Quantitative and qualitative changes in
milk carbohydrates during lactation in the tammar
wallaby (Macropus eugenii). Aust. J. Biol. Sci. 32:
519–531.
Murphy CR and Smith JR 1970. Age estimation of pouch
young and juvenile Kangaroo Island wallabies. Trans.
Roy. Soc. South Aust. 94: 15–20.
O’Brien N 2004. Cross-fostering and its effects on the
growth and development of pademelon (Thylogale
billardierii) and tammar wallaby (Macropus eugenii)
pouch young. BSc Hons thesis. University of
Melbourne, Australia.
Renfree MB and Tyndale-Biscoe CH 1978. Manipulation
of marsupial embryos and pouch young. In Methods in
Mammalian Reproduction. (Ed. JC Daniel) pp.
307–331. Academic Press, London.
Reynolds HC 1952. Studies on reproduction in the
opossum (Didelphis marsupialis virginiana). Uni. Calif.
Pub. 52: 223–283.
Rose RW, Kuswanti N and Colquhoun EQ 1998.
Development of endothermy in a Tasmanian
marsupial, Bettongia gaimardi and its response to cold
and noradrenaline. J. Comp. Physiol. 168: 359–363.
Schultz D, Whitehead P and Taggart DA 2006. Review of
surrogacy program for endangered Victorian
brush-tailed rock wallaby (Petrogale penicillata) with
special reference to animal husbandry and veterinary
considerations. J. Zoo. Wildl. Med. 37: 33–39.
Sharman GB 1962. The initiation and maintenance of
lactation in the marsupial Trichosurus vulpecula. J.
Endocrin. 25: 375–385.
090901 Macropods 1pp.indd 277 17/09/09 11:41:45

278 Macropods: The Biology of Kangaroos, Wallabies and Rat-kangaroos
Shield J 1966. Oxygen consumption during pouch
development of the macropod marsupial Setonix
brachyurus. J. Physiol. 187: 257–270.
Smith MJ 1998. Establishment of a captive colony of
Bettongia tropicia (Marsupialia: Potoroidae) by
cross-fostering; and observations on reproduction. J.
Zool. Lond. 244: 43–50.
Sterneberg B 2005. The pouch advantage: cross-fostering
for the conservation of rat kangaroos. B.I.F. Futura 20:
245–253.
Taggart DA 2002. Use of pouch young removal and cross
fostering techniques to accelerate breeding and
recruitment in the threatened brush-tailed rock wallaby,
Petrogale penicillata. ANZCCART News 15: 7–9.
Taggart DA, Shimmin GA, Underwood G and Phillips K
2002. Survival of very small macropod pouch young
following short-term isolation from the pouch at
various environmental temperatures. Animal Conserv.
5: 275–282.
Taggart DA, Schultz DJ, White C, Whitehead PJ,
Underwood G and Phillips K 2005. Cross-fostering,
growth and reproductive studies in the brush-tailed
rock wallaby, Petrogale penicillata (Marsupialia:
Macropodidae): efforts to accelerate breeding in a
threatened marsupial species. Aust. J. Zool. 53: 1–11.
Tyndale-Biscoe CH 1979. Hormonal control of embryonic
diapause and reactivation in the tammar wallaby. In
Maternal Recognition of Pregnancy. Ciba Foundation
Symposium 64 (new series) pp. 173–190. Excerpta
Medica, Amsterdam.
Tyndale-Biscoe CH and Renfree MB 1987. Reproductive
Physiology of Marsupials. Cambridge University Press,
Cambridge.
Tyndale-Biscoe CH, Hearn JP and Renfree MB 1974.
Control of reproduction in macropodoid marsupials.
J. Endocrinol. 63: 589–614.
Waite R, Giraud A, Old J, Howlett M, Shaw G, Nicholas K
and Familari M 2005. Cross-fostering in Macropus
eugenii leads to increased weight but not accelerated
gastrointestinal maturation. J. Exp. Zoo. 303(A):
331–344.
Wynd NA, Sigg DP, Pople AR, Hazlitt SL and Goldizen
AW 2006. Factors affecting female reproductive
success and the survival of pouch young in the
threatened brush-tailed rock-wallaby, Petrogale
penicillata. Aust. J. Zool. 54: 61–70.
090901 Macropods 1pp.indd 278 17/09/09 11:41:46