|
| |
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
First published online March 30, 2006
Journal of Experimental Biology 209, 1535-1547 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02137
Forage fibre digestion, rates of feed passage and gut fill in juvenile and adult red kangaroos Macropus rufus Desmarest: why body size matters
School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, NSW 2052, Australia
* Author for correspondence at present address: Institute of Wildlife Research, School of Biological Sciences, A08 University of Sydney, NSW 2006, Australia (e-mail: a.munn{at}unswalumni.com)
Accepted 31 January 2006
 |
Summary |
|---|
 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
50% lower on the oaten hay. In contrast, solute
and particle MRTs in the mature females were not significantly affected by
diet; they maintained DM intakes by increasing DM gut fill from 264±24
g on chopped lucerne to 427±26 g DM on chopped oaten hay. Clearly, the
mature female kangaroos did not maximise gut fill on the high-quality forage,
presumably as a consequence of their proportionally lower energy requirements
compared with still-growing juveniles. Overall, we have provided the first
mechanistic link between the physiological constraints faced by juvenile red
kangaroos in relation to their drought-related mortalities, rainfall and
forage quality.
Key words: herbivore, kangaroo, juvenile mortality, fibre digestion, gut fill
|
Introduction |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
). The population
dynamics of red kangaroos appear tightly linked with environmental factors,
mediated largely through juvenile survival and recruitment
(Bayliss, 1987;
Shepherd, 1987). Similar
patterns are seen in a number of other large mammalian herbivores
(Owen-Smith, 1990;
Clutton-Brock et al., 1992;
Sæther, 1997;
Gaillard et al., 1998;
Gaillard et al., 2000;
Owen-Smith et al., 2005).
Juvenile mortalities in large herbivores are usually low during favourable
environmental conditions, but typically very high under poor conditions (e.g.
Forchhammer et al., 2001;
Clutton-Brock et al., 1992).
Juvenile survival therefore is a major limiting factor for many large
herbivores, irrespective of climate/habitat (e.g. temperate vs
tropical; forest vs grassland) or of the proximate causes of
mortality (e.g. predation, disease, malnutrition)
(Sæther, 1997;
Gaillard et al., 1998;
Gaillard et al., 2000). This
also appears to be the case for the large kangaroos in Australia
(Dawson, 1995).
In arid and semi-arid Australia, rainfall is the most notable environmental
factor affecting kangaroo populations
(Newsome et al., 1967;
Bayliss, 1985a;
Bayliss, 1985b;
Robertson, 1986;
Shepherd, 1987;
Caughley et al., 1985;
Cairns and Grigg, 1993;
Dawson, 1995;
McCullough and McCullough,
2000). Rainfall has a strong influence on cohort survivorship and
population age-structure (Robertson,
1986). Juvenile mortality is typically high during drought
(Dawson, 1995;
McCullough and McCullough,
2000) and only after several rain periods does juvenile survival
improve, leading to significant population recruitment
(Newsome et al., 1967;
Robertson, 1986;
Dawson, 1995). The mechanism
by which rainfall affects juvenile survival has not been defined, but recent
work suggests that both diet quantity and diet quality are important
(Moss and Croft, 1999;
Munn and Dawson, 2003a;
Munn and Dawson, 2003b;
Munn et al., in press).
Adult red kangaroos are able to utilise fibrous vegetation by fermentative
digestion in a large colon-like forestomach (Forbes and Tribe, 1965;
Hume, 1974). Primarily
grass-eaters, red kangaroos prefer young, green vegetation low in fibre (i.e.
the structural carbohydrates cellulose and hemicellulose and also
lignin/cutin) and high in nitrogen and easily digestible cell contents
(Chippendale, 1968;
Griffiths and Barker, 1966;
Dawson et al., 1975;
Ellis et al., 1977). During
wet seasons, red kangaroos may also consume significant quantities of young
forbs (non-woody dicots) (Dawson and
Ellis, 1994). However, during dry seasons fresh plant growth is
quickly eaten out and mature, fibrous grasses predominate
(Bailey et al., 1971;
Barker, 1987). Increasing fibre
content is a major factor reducing the digestibility of most grasses
(Burton et al., 1964;
Terry and Tilley, 1964;
Short et al., 1974;
Ballard et al., 1990). During
dry seasons, fibrous grasses provide up to 90% of the adult red kangaroo diet
(Dawson and Ellis, 1994),
though the extent to which smaller, juvenile red kangaroos can utilise fibrous
forage is uncertain. Moreover, during prolonged or severe drought, red
kangaroo mothers usually cease lactating
(Frith and Sharman,
1964; Newsome,
1964a; Newsome,
1964b), making dependent young solely reliant on available
forage.
Like all marsupials, red kangaroos are extremely underdeveloped at birth,
weighing just 0.8 g. They spend their first 6 months of life within a large
well-developed pouch, a characteristic of macropodid marsupials
(Frith and Sharman, 1964;
Sharman et al., 1964). By
230–250 days, they permanently exit the mother's pouch, becoming a
`young-at-foot' (mass 4-5 kg). Young-at-foot (YAF) kangaroos continue to
suckle from their mother, accessing the same teat they used during pouch life.
Forage intake at this stage increases markedly and red kangaroos are fully
weaned at around one year (mass 10–12 kg)
(Sharman et al., 1964;
Dawson, 1995). It is this
age/size class, from permanent-pouch-exit (i.e. YAF) until shortly after
weaning, that red kangaroos appear most vulnerable to dry conditions
(Shepherd, 1987;
Dawson, 1995;
McCullough and McCullough,
2000), when mainly fibrous vegetation is available
(Dawson and Ellis, 1994).
Generally, the digestion of fibrous forage is less efficient among small
herbivores (Parra, 1978;
Demment and Van Soest, 1985;
Illius and Gordon, 1992;
Cork, 1994). Smaller animals
have higher mass-specific metabolic rates than larger species, but also
smaller absolute gut sizes and necessarily faster rates of food passage
(Mould and Robbins, 1982;
Demment and Van Soest, 1985;
Illius and Gordon, 1992).
Compared with larger animals, material ingested by smaller herbivores is
exposed to microbial action for a shorter period, thereby reducing digestive
efficiency (i.e. nutrient extracted per unit feed ingested). Furthermore,
metabolic rate in mammals scales with a body-mass exponent of less than 1,
often 0.75 (Kleiber, 1975;
Schmidt-Nielsen, 1984;
Hayssen and Lacy, 1985), but
gut size scales with a body-mass exponent equal to one
(Demment and Van Soest, 1985).
Therefore, compared with larger species, smaller herbivores have lower gut
capacities relative to their metabolic energy requirements
(`metabolic-gut-capacity'). The minimum body size predicted for effective
fibre digestion by foregut fermenting herbivores is 9–15 kg
(Parra, 1978;
Demment and Van Soest, 1985).
This is close to the weaning body mass of young kangaroos
(Dawson, 1995). In addition to
the potential constraints of small gut size and high mass-specific metabolism,
juvenile animals are also faced with additional costs associated with growth.
These costs can be substantial (Munn and
Dawson, 2003a; Munn and
Dawson, 2003b), further limiting the potential for young kangaroos
to utilise high-fibre forage (Munn et al.,
in press). Here we further explore the impact of fibrous forage on
digestive capabilities of YAF, weaned and mature red female kangaroos. In
particular we compare the ability of juvenile and adult kangaroos to ingest
and digest forages with markedly different fibre contents (neutral- and
acid-detergent fibre) in relation to body size, rates of food passage and dry
matter gut fill.
|
Materials and methods |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
)
and treated for parasites (internal and external) using Ivermectin (0.2 mg
kg–1; Large Animal Ivomec, Merck, Sharpe and Dohme,
Granville, Australia). The young kangaroos were reared in artificial pouches
(Williams and Williams, 1999)
until they reached the age of permanent-pouch-exit, about 250 days
(Sharman et al., 1964). Five
weeks prior to experimentation the animals were transferred to our laboratory
animal house and maintained in pens (430 cm x120 cm x250 cm) under
a 12 h:12 h L:D cycle. The now YAF kangaroos were weighed at the beginning of
each week (±0.05 kg). Rabbit Pellets (Gordon's Specialty Stock Feeds,
Yanderra, Australia), Kangaroo Cubes (Doust and Rabbidge, Forbes, Australia),
a lucerne/wheat bran mix (Kensington Produce, Sydney, Australia) and water
were available ad libitum. This diet was supplemented with
Digestelact (Digestelact Low Lactose, Sharpe Laboratories, Sydney), a
low-lactose milk powder commonly used for hand-rearing orphaned marsupials
(Williams and Williams, 1999),
made to full strength (125 g 900 ml–1 H2O). During
non-experimental periods a daily supplement of 100 ml of Digestelact was
offered to the YAF. Milk intakes by red kangaroo young have not been reported,
but on this intake of Digestelact, plus forage and pellets, the YAF red
kangaroos maintained growth rates comparable to those reported by Sharman et
al. and Frith and Calaby (Sharman et al.,
1964; Frith and Calaby,
1969).
Milk was withheld from the YAF according to the diet treatments described
below. Milk intake was reduced over time until it was eliminated at normal
weaning age, 360 days. During the rearing process, juveniles were exposed
to fresh grass and soil, and to the faeces of adult red kangaroos, to
facilitate infection by the microbes needed for the proper functioning of the
kangaroo forestomach.
Feeding trials were carried out when the average age (± standard error of the mean; s.e.m.) of the YAF was 302±6 days and their average body mass was 6.4±0.2 kg. Trials were repeated using the same animals after they had been fully weaned and were, on average, 394±7 days and 10.9±0.3 kg body mass.
Adults
Six tame non-lactating adult female red kangaroos from a captive colony
were maintained under housing conditions identical to those of the juveniles.
Kangaroo Cubes, the lucerne/wheat bran mix and water were available ad
libitum. Five of the adult females were known to be at least 5 years old;
the other was 4 years old. Average body mass of the adult females during the
experiments was 25.8±1.6 kg.
Diets and feeding regimens
Two forages of different fibre levels were used. Chopped lucerne (alfalfa,
Medicago sativa) hay was considered high-quality forage, being
comparatively low in neutral-detergent fibre and high in nitrogen (N). Chopped
oaten (Avena sativa) hay was considered poor-quality forage, being
higher in fibre and low in N content (Table
1). The N and fibre contents of the chopped oaten hay were similar
to that of grasses foraged by red kangaroos during a severe drought in arid
rangeland of western NSW (Bailey et al.,
1971). Apparent dry matter digestibility of lucerne and oaten hays
by adult red kangaroos was 55% and 45%, respectively
(McIntosh, 1966;
Hume, 1974). Some animals
initially refused the chopped oaten hay. Subsequently, the diet was always
lightly sprayed (<5% v/w) with unsweetened apple juice (Golden Circle,
Sydney, Australia) to increase palatability. The contribution of the juice to
energy and nitrogen intakes was assessed as negligible.
|
In preliminary trials, YAF red kangaroos offered only chopped oaten hay
(i.e. without a milk supplement) eventually did not eat. This treatment was
therefore omitted from the main trials. Only by using a milk supplement (80 ml
day–1 of full-strength Digestelact) were we able to assess
the YAF capabilities when fed chopped oaten hay. Milk was offered at 09:00 h
and 18:00 h at 40 ml per feed and was always completely consumed. This level
of milk intake was used to mimic that likely to be available to YAF red
kangaroos exposed to harsh environmental conditions. The importance of the
milk supplement to forage digestion by YAF red kangaroos was described by Munn
and Dawson (Munn and Dawson,
2003a).
Diet order was established by randomly allocating three YAF to a starting
diet of chopped lucerne or oaten hay (with milk). The YAF were then assigned a
fixed regimen of lucerne, followed by chopped oaten hay with milk or vice
versa. After weaning, feeding trials were repeated using the same
animals, maintaining the diet order initially established. Importantly, weaned
red kangaroos did not receive any milk supplement. Similarly, three adult
females were randomly assigned to a starting diet of chopped lucerne followed
by oaten hay, the order being reversed for the other three adults. This fixed,
counter-balanced design was used to minimise carry-over affects caused by diet
order or animal age (Zar,
1999).
Experimental procedure
Feeding trials were conducted in a temperature-controlled room (25°C)
on a 12 h:12 h L:D cycle, with lights on at 06:00 h. Adult and juvenile
kangaroos were housed individually in metabolism cages (1245 mmx960 mm
x 1670 mm) with mesh floors. Faeces and urine passed to a collection
tray beneath each cage. Collection trays consisted of a fine wire mesh on
which faeces and any spilt feed were trapped, allowing urine to flow to the
tray bottom where it drained continuously into polyethylene volumetric flasks.
Food and water containers were attached to the outside of each cage to
minimise feed spillage. Food and water containers and waste collection trays
were cleaned daily with demineralised water. During the preliminary and
feeding trials herbage was offered to the kangaroos at twice the previous
day's level of voluntary intake.
YAF and weaned kangaroos were allowed 5 days to acclimate to their metabolism cage before a preliminary trial commenced. Preliminary trials were conducted for at least 5 days or until food intake was stable, after which time a 5-day feeding trial commenced. During each trial, food refusals and faeces were collected quantitatively and bulked over the 5 days and stored frozen. YAF and weaned kangaroos were weighed (±0.05 kg) at the same time each day throughout the preliminary and feeding trials. At the end of each trial, animals received their usual diet (i.e. water, kangaroo cubes, rabbit pellets, lucerne/bran mix) ad libitum for at least 10 days; YAF also received 100 ml Digestelact day–1.
Adult red kangaroos were allowed at least 10 days to acclimate to their experimental diet and metabolism cage (i.e. preliminary trial). After food intake had stabilised a 5-day feeding trial commenced. Adult kangaroos were weighed (±0.05 kg) at the beginning of the preliminary and experimental trials and again at the end of the experimental trial. After each experimental trial adults received their usual diet (water, kangaroo cubes, lucerne/bran mix) ad libitum for at least 10 days.
Analysis of samples
Samples of food offered, together with all food refused and all faeces were
collected daily and stored frozen. Foodstuffs and faeces were later thawed and
sub-samples (20% wet mass) were prepared for analysis by air-drying in a
forced convection oven at 50°C
(Robertson and Van Soest,
1981) for 48 h. Further sub-samples were dried at 90°C for a
further 24 h, but there was no change in DM contents. Dried samples were
ground through a 1 mm mesh in a Wiley Mill (Arthur Thomas Co., Scientific
Apparatus, Philadelphia, USA). Ash contents of dried, ground foodstuffs
(including Digestelact milk powder) and faeces were determined in duplicate by
dry-ashing 0.5 g samples at 550°C overnight in a Thermolyne Muffle Furnace
(Model 62700; Dubuque, Iowa, USA). Organic matter content of foods and faeces
were calculated as DM – ash content.
Neutral-detergent fibre (NDF; largely cellulose, hemicellulose and
lignin/cutin), acid-detergent fibre (ADF; largely cellulose and lignin/cutin)
and lignin/cutin contents of feeds were determined in duplicate from 0.5 g
samples using a sequential filter-bag technique and an ANKOM Fibre Analyser
(Model 220, ANKOM Technology Corp., Fairport New York, USA). The reagents and
general procedures used were as described by Van Soest et al.
(Van Soest et al., 1991).
Prior to neutral-detergent digestion, samples were treated with 1 ml of heat
stable 
-amylase (Sigma A – 3306; Sigma Aldrich Pty Ltd, Sydney)
for 80 min to remove starch (Van Soest et
al., 1991). Sodium sulphite and decalin were removed from the
neutral-detergent procedure (Robertson and
Van Soest, 1981; Van Soest et
al., 1991). This sequential filter-bag technique ensured no
unintentional loss of sample throughout. Soluble cell contents (DM–NDF),
and contents of hemicellulose (NDF–ADF) and cellulose
(ADF–lignin/cutin) in foods and faeces were determined by
difference.
Energy contents of dried ground foodstuffs were determined by combusting duplicate sub-samples of 0.7 g in a ballistic bomb calorimeter (Gallenkamp, Model CB-375; Gallenkamp and Co. Ltd, UK), using a benzoic acid standard for calibration every 25 samples. The total nitrogen content of foodstuffs was determined in duplicate by total combustion of approximately 0.2 g samples in a Leco CHN-1000 elemental analyser (Leco Inc. St Joseph, Michigan, USA).
Food intake and apparent digestibility
Some kangaroos showed considerable diet selection during the feeding
trials. Intake of dietary components (e.g. DM) was therefore calculated as:
 | (1) |
 | (2) |
).
Food passage and mean retention times
The rate of passage of solutes and particles through the gastrointestinal
tract of kangaroos was measured using two inert markers. The solute marker
used was cobalt-ethylene diaminetetraacetic acid (Co-EDTA), prepared according
to Udén et al. (Udén et al.,
1980). Particles were marked with chromium mordanted to cell walls
(Cr-CW) according to Udén et al.
(Udén et al., 1980);
mordanting renders particles indigestible. Cell walls were prepared from
chopped lucerne hay (dried at 50°C and ground through a 1 mm mesh) by the
neutral detergent method (Robertson and
Van Soest, 1981; Van Soest et
al., 1991) and wet-sieved through a series of Endicott (London,
England) screens. Particles that passed through a 1-mm screen but were trapped
on a 600 µm screen were retained for mordanting.
Doses of Co-EDTA and Cr-CW were mixed, lightly sprayed with unsweetened apple juice and offered to the YAF, weaned and adult red kangaroos on day 2 of each feeding trial at 11:00 h. Some adults initially refused the marked food, which was subsequently spread on one half of a slice of 3-day-old fruit bread (Buttercup Bakeries, Moorebank, NSW, Australia), which was readily consumed. YAF and weaned kangaroos were offered 1.0 g Cr-CW and 0.5 g Co-EDTA. Adults were offered 2.0 g Cr-CW and 1.0 g Co-EDTA. Six mature female and juvenile kangaroos were offered the marked dose during each feeding trial, but only five animals from each age class completely consumed the marked foods on each occasion. In these cases, marked feeds were consumed within 5 min, and thus were considered a pulse dose. Exact doses, however, were unknown because a small amount of marker often remained in the bowl, and some was lost with spilt saliva. After dosing, faeces were collected from the YAF and weaned kangaroos at 4 h intervals for 24 h, followed by 6 h intervals for 24 h, then 8 h intervals for 24 h and 12 h intervals for a further 24 h (total 96 h). After dosing, faecal samples were collected from the adult kangaroos at 6 h intervals for 48 h, then 8 h intervals for 24 h and 12 h intervals for a further 24 h (total 96 h).
Faecal samples were analysed for Co and Cr concentration using an
Inductively Coupled Plasma Optical Emission Spectrometer (ICP OES, Optima
3000DV, Perkin Elmer, CT USA). Dry faecal samples (0.5 g) were prepared
for ICP analysis according to Mambrini
(Mambrini, 1990), but see also
Caton et al. (Caton et al.,
1996). Samples were dry-ashed overnight at 550°C in a
Thermolyne Muffle Furnace (Model 62700; Dubuque, Iowa, USA). Ash residue was
then boiled for 3 min in 10 ml of 2% HNO3 containing 2 g
l–1 CaCl (matrix solution). After boiling, solution and
residue were completely transferred to 25 ml volumetric flasks, allowed to
cool and made up to the mark with the matrix solution. The resultant solutions
were allowed to stand for 24 h before the supernatant was carefully drawn off
for analysis. Standards for ICP were prepared using Co-EDTA and Cr-dichromate
dissolved in the matrix solution.
Mean retention times (MRT) for solute and particle markers through the
entire gastrointestinal tract (Warner,
1981) were calculated according to Blaxter et al.
(Blaxter et al., 1956):
 | (3) |
).
An index of total gastrointestinal DM content (i.e. dry gut fill) was
calculated from faecal output, particle MRT and apparent dry matter
digestibility (Holleman and White,
1989). Indigestible fill (VN; g DM) was
calculated as:
 | (4) |
 | (5) |
).
Statistical analysis
Although the method of choice for statistical comparisons was analysis of
covariance (ANCOVA) with body mass as the covariate, the YAF and the weaned
kangaroos were the same animals, and hence the data sets were not independent.
Also, it was not logistically feasible to include greater numbers of such
large animals in the study. These constraints meant that the use of ANCOVA
resulted in overly complex comparisons with small numbers of replicates and
limited statistical power. Instead, repeated-measures analysis of variance
(RM-ANOVA) was used to compare within and between group data from YAF, weaned
and adult red kangaroos. As noted, non-independence of the YAF and weaned
kangaroos prevented their combined analysis with adult data
(Zar, 1999). Therefore, YAF
and weaned kangaroos were compared using two-way RM-ANOVA with two levels of
within-group factors (diet and age). YAF and weaned data were then compared
separately to those of adult red kangaroos using two-way RM-ANOVA. Statistical
outcomes for the within-YAF, within-weaned and within-adult kangaroo data were
the same across all between-group comparisons (e.g. outcomes for within-YAF
data were the same when YAF were compared to weaned or adult kangaroos). For
this reason results are presented as if they were one data set, even though
they were tested independently.
Data on intake and output are presented as g day–1, or as
g kg–0.75 day–1 for comparison with other
studies. The most appropriate exponent for intra-specific comparisons often
differs from 0.75 (Hume,
1999), but there were insufficient data to establish this
relationship in this study. Therefore we used a body-mass exponent of 0.75,
which was shown (Hayssen and Lacy,
1985) to be the most appropriate for comparisons of basal
metabolic rate among marsupials.
Assumptions for ANOVA were tested using the Kolmogorov–Smirnov test
for normality (=0.05) and Levene's test for homogeneity of variances
(=0.05). To achieve normality and or homogeneity, log (+1)
transformations were applied to the following data sets: DMI (g
day–1; YAF vs adults), digestible DMI (g
day–1; YAF vs weaned, YAF vs adults),
organic matter intake (OMI; g day–1; YAF vs adults)
and digestible OMI (g day–1; YAF vs weaned, YAF
vs adults), gut fill (g DM) (YAF vs weaned). Some data sets,
however, could not be normalised and were compared using a Friedman's test (a
non-parametric ANOVA for repeated measures)
(Zar, 1999). Data sets
compared using Friedman's test included: apparent digestibility (%) of DM,
organic matter (OM), soluble cell contents (YAF vs adult, YAF
vs weaned), digestible DMI (g kg–0.75
day–1; YAF vs weaned) and digestible OMI (g
kg–0.75 day–1; YAF vs weaned).
Proportional data for all digestibilities were arcsine transformed
(Zar, 1999).
Significant differences detected by ANOVA were further investigated using a
Tukey's Honest Significant Differences (HSD) post hoc test.
Significant differences detected by Friedman's test were investigated using
equation 11.3 from Zar (Zar,
1999) with standard error adjusted for repeated measures
(Zar, 1999; Equation 12.53).
ANOVA, Tukey HSD and Friedman's tests were performed using Minitab for Windows
12.1 (1998; Minitab Inc., PA, USA).
|
Results |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
|
|
On the poor-quality chopped oaten hay, gross DMI (g day–1)
by the mature female kangaroos was not significantly lower than that on
chopped lucerne (Table 3). This
was not the case, however, for the juvenile red kangaroos, which had DMIs (g
day–1) of chopped oaten hay that were less than half that of
chopped lucerne (P<0.01; Table
3). The apparent digestibly of DM from the oaten hay diet was
similar across all age classes (43–45%; P>0.05)
(Table 3). However, it must be
remembered that the YAF animals on this diet also received a small portion of
artificial milk (80 ml day–1). Preliminary trials indicated
that the YAF would not have survived on chopped oaten hay alone (see
Munn and Dawson, 2003a).
Assuming a milk–DM digestibility of 95%
(Penning et al., 1977;
Roy, 1980;
Ternouth et al., 1985), the
apparent digestibility of DM from the chopped oaten hay alone (i.e. excluding
milk) by the YAF kangaroos was just 34.2±3.1%, significantly lower than
that by weaned or adult kangaroos (Table
3).
Fibre digestion
The digestibility of soluble cell contents by juvenile and adult red
kangaroos fed chopped lucerne hay was high (75–79%) and not
significantly different between age groups
(Table 4). Differences were
apparent, however, in their ability to digest forage fibre. The YAF kangaroos
digested significantly less NDF, ADF, cellulose and hemicellulose than did the
mature female kangaroos (Table
4). YAF also digested significantly less NDF, ADF and cellulose
(but not hemicellulose) than the weaned juveniles
(Table 4).
|
On the higher fibre forage of chopped oaten hay, the digestibility of
soluble cell contents by YAF, weaned and mature female kangaroos was
significantly lower than on chopped lucerne
(Table 4). The YAF kangaroos
also digested significantly less soluble cell contents from oaten hay than did
weaned or adult kangaroos, by 5–7 percentage units. The
digestibility of NDF from chopped oaten hay was also lower in all age groups,
by around 10 precentage units, compared with chopped lucerne. These
differences were greatest for the YAF kangaroos, which digested significantly
less NDF, ADF, cellulose and hemicellulose than either the weaned or mature
females (Table 4). The pattern
of fibre digestibility by weaned juveniles was generally intermediate between
the YAF and adult kangaroos (Table
4).
Digesta mean retention times and gastrointestinal DM contents (DM gut fill)
Cumulative elimination curves describing the pattern of solute and
particulate passage through the gastrointestinal tract of our kangaroos are
outlined in Fig. 1. Solute and
particle markers were completely eliminated from the digestive tract of the
YAF, weaned and adult kangaroos by 60 h and 96 h post dose, respectively.
There was significant separation of solute and particle digesta markers in the
YAF, weaned and mature female kangaroos on both chopped lucerne and oaten
hays, with the solute marker universally eliminated faster than the particle
marker (Fig. 1;
Table 5; P<0.01).
Overall, the juvenile red kangaroos showed the greatest response in their
patterns of solute and particle elimination in relation to diet.
|
|
Differences in the elimination patterns of particle and solute markers
between the juvenile and mature female kangaroos were apparent when we
considered overall MRTs. On high-quality, chopped lucerne hay, the MRTs for
the solute marker were significantly shorter in the YAF and weaned kangaroos
than in adults, by 4 h. Particle marker MRTs on chopped lucerne, however,
were not significantly different between age groups
(Table 5). However, on the more
fibrous chopped oaten hay, MRTs for solutes and particles were significantly
longer than on the chopped lucerne in both the YAF and weaned kangaroos; the
solute marker by 6 h and the particle marker by 10 h in each case.
Conversely, MRTs for solute and particle markers through mature females were
not significantly affected by diet (Table
5).
As expected, indices of gastrointestinal DM contents (i.e. DM gut fill; in g) on chopped lucerne and oaten hays were lowest in the YAF red kangaroos, followed by weaned and then mature females (Table 6). However, there was considerable variation around the mean in both the YAF and weaned kangaroos, and differences in DM gut fill between the younger ages were not significant, though weaned animals tended to have greater fills on both diets at P=0.09 (Table 6). When offered chopped lucerne hay, the YAF kangaroos had the highest mass-specific DM gut fills (i.e. g kg–1), significantly higher than that of mature females (P<0.05) and tending toward significance when compared with weaned animals (P=0.07). When offered chopped oaten hay, however, there were no significant differences in mass-specific DM gut fills of YAF, weaned or mature female kangaroos. In other words, on high-quality chopped lucerne, the mature female kangaroos had mass-specific DM gut fills that were just 65% of that seen in the YAF, but significantly increased DM gut fill on chopped oaten hay by around 1.6-fold. Conversely, mass-specific DM gut fill in YAF and weaned kangaroos was not significantly affected by diet (Table 6). On an allometric basis (i.e. g DM kg–0.75), there were no significant differences in DM gut fill among the YAF, weaned and mature females on chopped lucerne hay, though variation was high, particularly in the juveniles (Table 6). On chopped oaten hay, allometrically related DM gut fill in mature females was not significantly different from that of weaned and YAF kangaroos (P=0.15 and P=0.11, respectively), but was significantly greater than that of adults fed chopped lucerne (Table 6).
|
|
Discussion |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
). The
mature females in our study were older than four years and had body masses of
25–30 kg. Mature males, on the other hand, can attain average body
masses of 60–80 kg by 15 years of age
(Dawson, 1995). Our mature
females were not lactating and ingested half as much chopped lucerne hay (414
g DM day–1; Table
3) as did mature male red kangaroos (823 g DM
day–1; N=3, body mass=62±5 kg;
McIntosh, 1966). Apparent
digestibility of DM from chopped lucerne hay by our females was identical to
that by McIntosh's males, averaging 56%
(McIntosh, 1966). Thus, on an
allometric basis (i.e. per kg0.75), digestible DMI by our mature
female kangaroos on chopped lucerne hay was the same as that by mature males
(McIntosh, 1966), at
21±2 g kg–0.75 day–1
(Table 3). Hume reported higher
intakes of chopped lucerne hay by smaller, younger male red kangaroos (29 g
kg–0.75 day–1; N=3, body mass
27–33 kg) (Hume, 1974),
probably because these still-growing males required additional energy and
nutrients for growth. Munn and Dawson showed that, in red kangaroos, growth
energy requirements have a significant impact on overall food intake
(Munn and Dawson, 2003b). The
YAF and weaned red kangaroos in this study were growing rapidly and had
digestible DMIs (g kg–0.75 day–1) on chopped
lucerne hay significantly greater than that by mature, non-lactating females
(Table 3), and similar to or
slightly greater than that of Hume's young red kangaroos
(Hume, 1974).
On the high-quality chopped lucerne hay, the YAF and weaned red kangaroos
were able to sustain growth at levels comparable with those reported by
Sharman et al. for ideal conditions
(Sharman et al., 1964). YAF
red kangaroos at this stage normally would be taking some milk from their
mothers. Our results indicate that provided sufficient high-quality forage is
available, YAF red kangaroos can subsist on forage alone, at least when their
energy requirements for thermoregulation are minimal. Juveniles may not be as
successful under cold conditions because of their higher energy costs for
thermoregulation relative to larger adults
(Munn and Dawson, 2001). Cold
conditions and poor-quality forage together are likely to be particularly
taxing for the smaller juvenile kangaroos. YAF kangaroos on the chopped oaten
hay did not sustain growth rates. They averaged losses of 2.3% of their body
mass over 5 days, even when receiving a small milk supplement
(Table 2). Loss of body
condition by the YAF was partially explained by a poor digestibility of the DM
of the oaten hay, leading to lower digestible DMIs (g kg–0.75
day–1) compared with weaned and adult female kangaroos
(Table 3).
The poor digestibility of DM by YAF red kangaroos fed chopped oaten hay
forage (i.e. after assuming a milk-DM digestibility of 95%) was partially
associated with their lower digestibility of cell contents compared with
weaned and adult kangaroos (Table
4). Digestibilities of cell contents by our red kangaroos (range:
60–79%) were lower than those reported for medium sized males (88%;
Hume, 1974), most probably
because of differences in forage age and preparation. In juvenile and adult
kangaroos the digestibility of cell contents was lower on chopped oaten hay
than on lucerne (Table 4). This
may be particularly important for juvenile and adult kangaroos during drought
conditions, as dry, senescent grasses predominate
(Dawson and Ellis, 1994).
Ballard et al. found that the in vitro digestibility of cell contents
(mainly soluble carbohydrates) declined with increasing plant age in ryegrass
(Lolium rigidium) (Ballard et al.,
1990). Also, as the proportion of soluble carbohydrates declines
with maturity in grasses, the relative content of hard-to-digest structural
carbohydrates (i.e. cellulose and hemicellulose) increases, thereby reducing
overall dry matter digestibility (Short et
al., 1974; Ballard et al.,
1990).
The digestibilities of forage fibre fractions (NDF, ADF) by our mature
female kangaroos were comparable to those reported for similarly sized mature
males on similar forage (Hume,
1974). The smaller, juvenile kangaroos were less capable of
digesting fibre fractions than were the adults. Even on the chopped lucerne
hay, the YAF kangaroos digested significantly less NDF than did weaned or
adult kangaroos (Table 4).
Overall, fibre digestion improved with increasing body mass from YAF to weaned
and adult kangaroos (Table 4).
Similar patterns in fibre digestion are seen between herbivore species of
markedly different body sizes. For example, Mould and Robbins found that the
digestibility of NDF from chopped lucerne hay by white-tailed deer
(Odocoileus virginianus, body mass=36 kg) was 10–15% lower that
that by elk (Cervus elaphus nelsoni, body mass=187 kg)
(Mould and Robbins, 1982). Our
YAF red kangaroos were, on average, four times smaller than our adult females,
but could a small body size alone explain their lower performance on the
higher fibre forage, or are other factors involved?
It could be argued that, compared with weaned juveniles and adult
kangaroos, the digestive system of the YAF was poorly developed by this stage.
However, Norton and Dawson (M. A. Norton and T. J. Dawson, unpublished data)
found that the capacity of the foregut in red kangaroos, the main site for
fermentative digestion in macropodids, scaled isometrically with body mass
across a wide range of age/size classes (N=22; body mass range
7–31 kg). Consequently, the fermentative capacity of the YAF foregut
should be no different from that expected for an adult kangaroo of a similar
body mass, assuming the microbial ecosystem of the juvenile foregut is
comparable with that of adults. Griffiths and Barton showed that chemically,
histologically and enzymatically the juvenile foregut in red kangaroos was
comparable with that of adults by the time they reached permanent-pouch-exit
(Griffiths and Barton, 1966).
By this stage, young kangaroos are ingesting significant quantities of
herbage, and milk intakes are declining rapidly
(Griffiths and Barton, 1966;
Dawson, 1995). Similar
ontological changes are seen in young ruminants during weaning. The rumen of
young lambs, for example, is functionally equivalent to that of adults by 20
days after peak lactation [i.e. after they begin weaning; see Langer
(Langer, 1994)]. Furthermore,
by the time of final weaning our juvenile kangaroos were able to ingest as
much digestible DM (g kg–0.75 day–1) from
chopped oaten hay as were adult females
(Table 3). Munn and Dawson,
however, found that, on an allometric basis, weaned kangaroos had total daily
energy requirements (kJ kg–0.75 day–1) for
maintenance plus growth that were some 1.8 times that of adult females
(Munn and Dawson, 2003b).
Therefore, although the weaned kangaroos were able to digest chopped oaten hay
DM with as much efficacy as that of adults
(Table 3), they were unable to
process enough of this poor-quality forage to meet their proportionally higher
nutrient requirements.
The volume of forage that an animal can process depends largely on the
refractory properties of the digesta and the amount of time it spends in the
gut (Robbins, 1993). This is
usually different for solutes (e.g. cell contents) and particles (e.g. fibrous
components). Kangaroos and their relatives show digesta retention patterns
typical of most non-ruminant vertebrates
(Dellow, 1982;
Stevens and Hume, 1995), where
solutes pass through the gastrointestinal tract more rapidly than particles
(Fig. 1). Notably, this is the
first study in which MRTs have been measured in kangaroos using a mordanted
marker for particles. Previous studies have used either stained hay particles
(which lack precision) or the particle-associated marker
ruthenium–phenanthroline, which migrates from larger to smaller
particles during digestion (see p. 236 in
Hume, 1999). Digesta
separation in adult kangaroos occurs in the foregut
(Dellow, 1982), where larger,
fibrous particles are fermented more slowly. A typical response of red
kangaroos to increasing dietary fibre content is an increase in the time that
particles remain in the foregut and, consequently, a reduction in food intake
(Foot and Romberg, 1965;
McIntosh, 1966;
Forbes and Tribe, 1970). Our
adult red kangaroos, however, did not show comparable reductions in food
intake when switched from low-fibre chopped lucerne to the high-fibre chopped
oaten hay (Table 3), and there
were also no concurrent changes in the MRT for particles or solutes
(Table 5). Conversely, MRTs for
solute and particle markers were significantly greater in both the YAF and
weaned kangaroos when they switched from low- to high-fibre forage
(Table 5), leading to
significant reductions in DMI (g day–1) of 52–55%
(Table 3). This suggests that
for adult kangaroos, adjustments in gut fill, rather than digesta retention
times, may be an important response to changes in forage quality. Juvenile
kangaroos, however, appeared to be at or near maximal gut fill (at least for
DM) regardless of diet quality. Although we could not measure this directly,
the increased MRTs in juveniles on the poor-quality oaten hay strongly
suggests that they were at their limits for gut fill (g DM) on this diet
(Table 6).
Our results are consistent with foraging models that indicate that
metabolic-gut-capacity (i.e. gut capacity relative to metabolic rate)
increases with increasing body mass
(Parra, 1978;
Demment and Van Soest, 1985;
Illius and Gordon, 1992).
Also, we have shown that intra-specifically, larger animals are capable of
greater flexibility in gut fill compared with younger, smaller animals. When
offered low-fibre chopped lucerne hay, mass-specific DM gut fill (g
kg–1) in the adult red kangaroos was just 57% of that of the
YAF (Table 6). Only when fed
poor-quality oaten hay did the adult female kangaroos increase mass-specific
DM gut fill (g kg–1) to levels comparable to that of
juveniles (Table 6). Increasing
gut fill allowed the mature females to maintain DMI of chopped oaten hay at
levels not significantly different from chopped lucerne
(Table 2). Furthermore, when
the adult kangaroos were switched from lucerne to oaten hay they increased DM
gut fill relative to their metabolic body mass (i.e. kg–0.75)
some 1.6 times (Table 6). Thus,
when fed high-quality forage the larger, mature female kangaroos were able to
reduce DM gut fill, presumably as a consequence of their lower metabolic
energy requirements (Munn and Dawson,
2001; Munn and Dawson,
2003b). Because the smaller juvenile kangaroos appeared unable to
compensate for lower forage quality by increasing gut fill, they could not
extract sufficient nutrients from the chopped oaten hay to maintain growth
(Table 2).
The age/body size at which red kangaroos may be able to relax DM gut fill
on higher quality forage is unknown, but may occur around sexual maturity, at
least in females. The apparent `reserve gut fill' available to the mature
females feeding on high-quality forage might be important for allowing the
higher levels of food intake necessary to sustain peak lactation. The energy
costs associated with supporting an offspring close to permanent-pouch-exit
(i.e. the period of peak lactation) can be as much as 50% of the mother's
maintenance requirements (Prince,
1976), presumably necessitating higher food intakes. Increases in
DM gut fill in relation to the increased energy requirements for lactation
have been reported for a range of ungulate species (see
Gross et al., 1996 and
references therein). Red kangaroos usually cease lactating during severe or
prolonged drought (Frith and Sharman,
1964; Newsome,
1964a; Newsome,
1964b), which may be related to maximal gut fill on forages
insufficient to supply the nutrients needed for milk production. It would be
interesting to measure how milk production changes with diet quality and gut
fill in this species, particularly as DM gut fill in our mature red kangaroos
was considerably less than that seen in ruminants (range 2 to >4% body
mass) (see Gross et al.,
1996), averaging just 1.7 % body mass on chopped oaten hay.
However, that the MRTs for solute or particle markers were not increased in
the mature females on chopped oaten hay suggests that they were not at their
maximal gut fill on this diet.
The flexibility in gut fill in our mature female kangaroos could be due to
physical expansibility of the gut or to gut hypertrophy, which is seen in
other mammals and particularly those inhabiting highly seasonal environments
(e.g. Weckerly, 1989;
Jenks et al., 1994;
Hume et al., 2002). However,
in light of the ecology of red kangaroos, expansibility of the gut may be more
important than hypertrophy for ameliorating the problems associated with
stochastic food supplies and quality. Because of the pressures associated with
continually breeding in good times (i.e. full gut) and of the extra gut
reserve needed to satisfy their own nutritional needs in bad times, there may
be little selective pressure for rapid gut re-modelling in the mature female
kangaroos.
To the best of our knowledge, this is the first study to show a large
marsupial herbivore adjusting gut fill in response to diet quality. Plasticity
in gut fill has important consequences for models of optimal foraging and
digestion. These models generally assume that maximal digesta loads are
directly proportional to body mass and are also the main determinant of the
cessation of food intake (Demment and Van
Soest, 1985; Illius and
Gordon, 1992; Cork,
1994; Yearsley et al.,
2001). The regulation of food intake by our mature kangaroos on
the high-quality forage, however, was apparently related to factors other than
the physical stimulus of gut distension. Current models using maximal digesta
load as a determinant of food intake do not address situations when gut fill
is not maximised. This may be particularly important when considering the
foraging strategies of red kangaroos in light of their highly unpredictable
environment and temporally patchy resources. Another assumption in many
herbivore studies is that animals forage to maximise food (energy) intake (for
a review, see Bergman et al.,
2001). However, that our adult red kangaroos were not maximising
DM gut fill on the high-quality lucerne hay suggests that they may not have
been maximising food (energy) intake on this diet. More likely, our mature,
non-lactating females were feeding to satisfy energy requirements rather than
maximise intake (van Gils et al.,
2003; Hume, 2005);
the energy requirements of mature female red kangaroos being proportionally
lower than those of still-growing juveniles
(Munn and Dawson, 2003b).
Conclusion
Our data support field studies indicating that juvenile red kangaroos are
limited in terms of condition and growth mainly by the availability of
high-quality forage (Watson and Dawson,
1993; Dawson,
1995; Moss and Croft,
1999). As forage fibre levels increased to 40–50% NDF, the
juvenile kangaroos could not sustain growth, being limited by gut capacity and
higher energy requirements than adults. On chopped oaten hay, juvenile
kangaroos also suffered higher nitrogen losses compared with adults
(Munn et al., in press),
further compromising growth and survival. Therefore, it is easy to appreciate
that juvenile red kangaroos have the highest drought-related mortalities of
any cohort (Newsome et al.,
1967; Bayliss,
1985a; Robertson,
1986; Dawson,
1995). Kirkpatrick and McEvoy found similar age-structured
mortality in drought-affected eastern grey kangaroos
(Kirkpatrick and McEvoy,
1966), and Arnold et al. suggested that high rates of juvenile
mortality are a general feature regulating kangaroo populations
(Arnold et al., 1991). Our
results provide the first mechanistic explanation linking the physiological
constraints faced by juvenile red kangaroos in relation to their
drought-related mortalities, rainfall and forage quality, the three principal
factors affecting recruitment and overall population dynamics
(Bayliss, 1987;
Shepherd, 1987;
Cairns and Grigg, 1993;
Dawson, 1995).
|
Acknowledgments |
|---|
|
References |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Arnold, G. W., Grassia, A., Steven, D. E. and Weeldenburg, J. R. (1991). Population ecology of western grey kangaroos in a remnant of wandoo woodland at Bakers Hill, southern Western Australia. Wildl. Res. 1,561 -575.[CrossRef]
Bailey, P. T., Martenesz, P. N. and Barker, R. (1971). The red kangaroo, Megaleia rufa (Desmarest), in north-western New South Wales. II. Food. CSIRO Wildl. Res. 16,29 -39.
Ballard, R. A., Simpson, R. J. and Pearce, G. R. (1990). Loss of digestible components of annual ryegrass (Lolium rigidum Gaudin) during senescence. Aust. J. Agric. Res. 41,719 -731.[CrossRef]
Barker, R. D. (1987). The diet of herbivores in the sheep rangelands. In Kangaroos, their Ecology and Management in Sheep Rangelands of Australia (ed. G. Caughley, N. Shepherd and J. Short), pp. 69-83. Cambridge: Cambridge University Press.
Bayliss, P. (1985a). The population dynamics of red and western grey kangaroos in arid New South Wales, Australia. I. Population trends and rainfall. J. Anim. Ecol. 54,111 -125.
Bayliss, P. (1985b). The population dynamics of red and western grey kangaroos in arid New South Wales, Australia. II. The numerical response function. J. Anim. Ecol. 54,127 -135.
Bayliss, P. (1987). Kangaroo dynamics. In Kangaroos, their Ecology and Management in Sheep Rangelands of Australia (ed. G. Caughley, N. Shepherd and J. Short), pp.119 -134. Cambridge: Cambridge University Press.
Blaxter, K. L., McGraham, N. M. and Wainman, F. W. (1956). Some observations on the digestibility of food by sheep and on related problems. Br. J. Nutr. 10, 69-91.[CrossRef][Medline]
Bergman, C. A., Fryxell, J. M., Gates, C. C. and Fortin, D. (2001). Ungulate foraging strategies: energy maximisation or time minimizing? J. Anim. Ecol. 70,289 -300.[CrossRef]
Burton, G. W., Knox, F. E. and Beardsley, D. W.
(1964). Effect of age on the chemical composition, palatability
and digestibility of grass leaves. Agron. J.
56,160
-162.
Cairns, S. C. and Grigg, G. C. (1993). Population dynamics of red kangaroos (Macropus rufus) in relation to rainfall in South Australian pastoral zone. J. Appl. Ecol. 30,444 -458.
Caton, J. M., Hill, D. M., Hume, I. D. and Crook, G. A. (1996). The digestive strategy of the common marmoset, Callithrix jacchus. Comp. Biochem. Physiol. 114A, 1-8.[CrossRef][Medline]
Caughley, G., Grigg, G. C. and Smith, L. (1985). The effect of drought on kangaroo populations. J. Wildl. Manage. 49,679 -685.
Chippendale, G. M. (1968). The plants grazed by red kangaroos, Megaleia rufa (Desmarest) in central Australia. Proc. Linn. Soc. N. S. W. 93, 98-110.
Clutton-Brock, T. H., Price, O. F., Albon, S. D. and Jewel, P. A. (1992). Early development and population fluctuations in Soay sheep. J. Appl. Ecol. 61,381 -396.
Cork, S. J. (1994). Digestive constraints on the dietary scope in small and moderately small mammals: how much do we really understand? In The Digestive System in Mammals: Food, Form and Function (ed. D. J. Chivers and P. Langer), pp.337 -369. Cambridge: Cambridge University Press.
Dawson, T. J. (1995). Kangaroos: Biology of the Largest Marsupials. Sydney: UNSW Press.
Dawson, T. J. and Ellis, B. A. (1994). Diets of mammalian herbivores in Australian arid shrublands: seasonal affects on overlap between red kangaroos, sheep and rabbits and on dietary niche breadths and electivities. J. Arid Environ. 26,257 -271.
Dawson, T. J., Denny, M. J. S., Russell, E. M. and Ellis, B. (1975). Water usage and diet preferences of free ranging kangaroos, sheep and feral goats in the Australian arid zone during summer. J. Zool. Lond. 177,1 -23.
Dellow, D. W. (1982). Studies on the nutrition of macropodine marsupials. III. The flow of digesta through the stomach and intestine of macropodines and sheep. Aust. J. Zool. 30,751 -765.[CrossRef]
Demment, M. W. and Van Soest, P. J. (1985). A nutritional explanation for body-size patterns of ruminant and nonruminant herbivores. Am. Nat. 125,641 -672.[CrossRef]
Ellis, B. A., Russell, E. M., Dawson, T. J. and Harrop, C. J. F. (1977). Seasonal changes in diet preferences of free ranging red kangaroos, euros and sheep in western New South Wales. Aust. Wildl. Res. 4,127 -144.[CrossRef]
Foot, J. Z. and Romberg, B. (1965). The utilisation of roughage by sheep and the red kangaroo, Macropus rufus (Desmarest). Aust. J. Agric. Res. 16,429 -435.[CrossRef]
Forbes, D. K. and Tribe, D. E. (1970). The utilization of roughages by sheep and kangaroos. Aust. J. Zool. 18,247 -256.[CrossRef]
Forchhammer, M. C., Clutton-Brock, T. H., Lindstorm, J. and Albon, S. D. (2001). Climate and population density induce long-term cohort variation in a northern ungulate. J. Anim. Ecol. 70,721 -729.[CrossRef]
Frith, H. J. and Calaby, J. H. (1969). Kangaroos. Melbourne: F. W. Cheshire.
Frith, H. J. and Sharman, G. B. (1964). Breeding in wild populations of the red kangaroo, Megaleia rufa. CSIRO Wildl. Res. 9,86 -114.
Gaillard, J., Festa-Bianchet, M. and Yoccoz, N. (1998). Population dynamics of large herbivores: Variable recruitment with constant adult survival. Trends Ecol. Evol. 13,58 -63.
Gaillard, J. M., Festa-Bianchet, M., Yoccoz, N. G., Loison, A. and Toïgo, C. (2000). Temporal variation in fitness and population dynamics of large herbivores. Ann. Rev. Ecol. Syst. 31,367 -393.[CrossRef]
Griffiths, M. and Barker, R. (1966). The plants eaten by sheep and by kangaroos grazing together in a paddock in south-western Queensland. CSIRO Wild. Res. 11,145 -167.
Griffiths, M. and Barton, A. A. (1966). The ontogeny of the stomach in the pouch young of red kangaroos. CSIRO Wildl. Res. 11,169 -185.
Gross, J. E., Alkon, P. U. and Demment, M. W. (1996). Nutritional ecology of dimorphic herbivores: digestion and passage rates in Nubian ibex. Oecologia 107,170 -178.[CrossRef]
Hayssen, V. and Lacy, R. C. (1985). Basal metabolic rates in mammals: taxonomic differences in the allometry of BMR and body mass. Comp. Biochem. Physiol. 81A,741 -754.[Medline]
Holleman, D. F. and White, R. G. (1989). Determination of digesta fill and passage rate from non-absorbed particulate phase markers using the single dosing method. Can. J. Zool. 67,488 -494.
Hume, I. D. (1974). Nitrogen and sulphur retention and fibre digestion by euros, red kangaroos and sheep. Aust. J. Zool. 22,13 -23.[CrossRef]
Hume, I. D. (1999). Marsupial Nutrition. Cambridge: Cambridge University Press.
Hume, I. D. (2005). Concepts of digestive efficiency. In Physiological and Ecological Adaptations to Feeding in Vertebrates (ed. J. M. Starck and T. Wang), pp.43 -58. Enfeild, NH: Science Publishers Inc.
Hume, I. D., Beiglböck, C., Ruf, T., Frey-Roos, F., Bruns, U. and Arnold, W. (2002). Seasonal changes in morphology and function of the gastrointestinal tract of free-living alpine marmots (Marmota marmota). J. Comp. Physiol. 172B,197 -207.
Illius, A. W. and Gordon, I. J. (1992). Modelling the nutritional ecology of ungulate herbivores: evolution of body size and competitive interactions. Oecologia 89,428 -434.
Jenks, J. A., Leslie, D. M., Jr, Lochmiller, R. L. and Melchiors, M. A. (1994). Variation in gastrointestinal characteristics of male and female white-tailed deer: implications for resource partitioning. J. Mammal. 75,1045 -1053.
Kirkpatrick, T. H. and McEvoy, J. S. (1966). Studies of Macropodidae in Queensland 5. Effects of drought on reproduction in the grey kangaroo (Macropus giganteus). Queensl. J. Agric. Anim. Sci. 23,439 -442.
Kleiber, M. (1975). The Fire of Life. New York: Krieger Publishing Company.
Langer, P. (1994). Weaning time and bypass structures in the forestomachs of Marsupialia and Eutheria. In The Digestive System in Mammals: Food, Form and Function (ed. D. J. Chivers and P. Langer), pp. 264-286. Cambridge: Cambridge University Press.
Mambrini, M. (1990). Etude du temps de sejour des residus alimentaires dans le tube digestif des vaches laiteres: aspects méthodologiques et facteurs de variation. PhD thesis, University of Rennes, France.
McCullough, D. R. and McCullough, Y. (2000). Kangaroos in Outback Australia: Comparative Ecology and Behavior of Three Coexisting Species. New York: Columbia University Press.
McIntosh, D. L. (1966). The digestibility of two roughages and the rates of passage of their residues by the red kangaroo, Megaleia rufa (Desmarest), and the merino sheep. CSIRO Wildl. Res. 11,125 -135.
Moss, G. L. and Croft, D. B. (1999). Body condition of the red kangaroo (Macropus rufus) in arid Australia: the effect of environmental condition, sex and reproduction. Aust. J. Ecol. 24,97 -109.
Mould, E. D. and Robbins, C. T. (1982). Digestive capabilities in elk compared to white-tailed deer. J. Wildl. Manage. 46,22 -29.
Munn, A. J. and Dawson, T. J. (2001). Thermoregulation in juvenile red kangaroo (Macropus rufus) after pouch exit: higher metabolism and evaporative water requirements. Physiol. Biochem. Zool. 74,917 -927.[CrossRef][Medline]
