Journal of Mammalogy, 94(6):1237–1247, 2013
Facultative geophagy at natural licks in an Australian marsupial
EMILY C. BEST,* JULIA JOSEPH,
AND
ANNE W. GOLDIZEN
School of Biological Sciences, The University of Queensland, Brisbane, Queensland 4072, Australia (ECB, JJ, AWG)
Faculty of Nature and Engineering, University of Applied Sciences, Bremen 28199, Germany (JJ)
* Correspondent: [email protected]
For many herbivorous mammal species across the world, geophagy, the consumption of soil, is an important
method for obtaining minerals, especially sodium. However, this behavior has not been recorded in marsupials.
The eastern grey kangaroo (Macropus giganteus), an intensively studied macropod species, is known to use
physiological and micromorphological adaptations to conserve sodium. We present results of another adaptation,
the use of natural licks, by this species and 3 other macropod species at Sundown National Park, Australia.
Natural licks had significantly higher levels of sodium, magnesium, and sulfur than surrounding soils. We
examined patterns of lick use by kangaroos to test 3 possible proximate causes of geophagy: whether lick use
was affected by dietary mineral content, life-history stage, and thermoregulation. The number of kangaroos
visiting the licks increased with temperature and mean cloud cover, varied among months, and was marginally
significantly influenced by dietary mineral content. Visit durations to one lick increased with temperature and
were influenced by month and life-history stage; females with high lactation demand and large males spent the
most time at the lick. The proportion of time spent in geophagy when at a focal lick varied with month and
reproductive state. Therefore geophagy is not restricted to eutherian mammals, and kangaroos, like many
eutherian species, appear to adjust this behavior in response to their mineral demand. Geophagy in kangaroos is
facultative, rather than obligative, and has not been detected in other intensively studied populations. In areas of
Australia with low levels of sodium, high temperatures, and suitable lick sites, geophagy may play a key role in
marsupial ecology.
Key words: eastern grey kangaroo, Macropus giganteus, mineral homeostasis, sodium, soil, thermoregulation
Ó 2013 American Society of Mammalogists
DOI: 10.1644/13-MAMM-A-054.1
Geophagy, the consumption of soil, clay, or sediments from
localized sites called mineral licks, salt licks, or natural licks,
has been widely documented for many mammalian species.
Geophagy is found predominantly in species exhibiting
herbivorous or omnivorous diets that are found across North
and South America, Eurasia, and Africa (for review see Klaus
and Schmid 1998). Natural licks are usually found along the
edges of streams or as deposits of high concentrations of
soluble minerals exposed by erosion above less-permeable
layers, and are sometimes associated with areas of high clay
content (Weeks 1978; Kreulen 1985). Levels of sodium have
been found to be higher at licks compared to the surrounding
soil at almost all licks used by grazing mammals (Weir 1969;
Moe 1993; Tracy and McNaughton 1995). Licks may also
occasionally have high levels of potassium, calcium, magnesium, and sulfur (Klaus and Schmid 1998); for example, in the
absence of available sodium licks, African elephants (Loxodonta africana) use termite mounds that have high concentrations of all of these minerals except sulfur (Weir 1969).
Many reasons for geophagy by mammals have been
suggested. Geophagy may help compensate for dietary mineral
deficiencies (Robbins 1993), and the ingestion of clay may
counteract acidosis (Kreulen 1985) or secondary plant
compounds (Oates 1978) or may absorb bacteria and their
toxins (Mahaney et al. 1995). Although the causes of
geophagy, and the relative importance of these different
causes, may vary among species, or populations in different
locations, and at different times of year, it is generally believed
that the main cause of geophagy in grazing mammals is sodium
demand for the maintenance of mineral homeostasis (Kreulen
and Jager 1984; Jones and Hanson 1985). The use of licks
often varies with season, usually peaking in spring and summer
(Weeks and Kirkpatrick 1976; Moe 1993; Ayotte et al. 2008;
Ping et al. 2011). There are 3 main causes of increased sodium
1237
www.mammalogy.org
1238
Vol. 94, No. 6
JOURNAL OF MAMMALOGY
demand during these seasons, which may not be mutually
exclusive: the growth of lush, green foliage in spring,
containing high levels of potassium, compromises sodiumconserving mechanisms, so that sodium is lost in the feces
(Jones and Hanson 1985); variation in the need for sodium
during different life-history stages such as pregnancy and
lactation can cause peaks in the need for sodium when females
are in particular reproductive states (Tracy and McNaughton
1995); and increased sodium loss is caused by sweating in hot
weather.
Given the geographically widespread reports of the use of
licks and their importance to the ecology of many herbivorous
mammal species, the absence in the literature of any
description of the use of natural licks by native Australian
mammals is notable and surprising. To our knowledge, the
only record of geophagy in Australia was reportedly from
stomachs of feral donkeys (Equus asinus) in northern Australia
that contained clay (Freeland and Choquenot 1990). Gilardi et
al. (1999) and Diamond et al. (1999) refer to Smith’s (1979)
description of geophagy in captive koalas (Phascolarctos
cinereus); however, this reference relates to the ingestion of
gravel by a few individuals in their enclosures, which does not
fit the definition of geophagy.
Salt concentrations in soil are known to be low across large
areas of Australia. These areas tend to be too far inland (more
than 150 km from the coast) to receive marine salt content in
rain, yet lack the increased evaporation found in the inland
desert, where salt accumulation tends to occur (Hutton and
Leslie 1958). Few plant species require sodium and therefore it
is rarely accumulated in vegetation and can be easily leached
from ecosystems receiving moderate levels of precipitation
(Robbins 1993), a process accentuated by freezing and thawing
of the ground. Blair-West et al. (1968) showed that eastern
grey kangaroos (Macropus giganteus) in these sodium-scarce
areas have adapted by possessing enlarged adrenal glands
(especially the zona glomerulosa), which synthesize and
secrete aldosterone (sodium-retaining hormone). Blair-West
et al. (1968) also found structural changes in the salivary
glands adaptive for conserving sodium, namely more extensive
duct systems of the parotid and submandibular glands, and
more-abundant blood vessels around the striated ducts. Urine
sodium concentrations were virtually zero in kangaroos from
these areas compared to animals residing in coastal regions,
where sodium levels were much higher. Since these studies
were undertaken it has been widely assumed that macropods
rely on these physiological and micromorphological adaptations for mineral homeostasis, and do not use geophagy
(Milewski and Diamond 2008), although kangaroos have been
known to travel to artificial sodium sources (Blair-West et al.
1968; Abraham et al. 1973).
The eastern grey kangaroo is the most frequently and
intensively studied macropod species; studies have been
undertaken at numerous sites across the species’ range (Fig.
1; see Coulson [2009] for a review). None of these studies have
reported geophagy, suggesting that it did not occur at those
sites, although of course observations of geophagy may simply
not have been reported. In contrast to the assumption that
eastern grey kangaroos do not exhibit geophagy, we describe
the use of natural licks by this species and report observations
of their use by other macropod species. Because this is the 1st
report of geophagy by any marsupial, our initial aim is to
compare the soil mineral contents of the natural licks with
those of random locations within the study area, to test whether
sodium demand drives geophagy in the kangaroos as has been
found for other mammals. Second, we test possible proximate
causes of the patterns in the use of licks, in particular whether
their use was affected by dietary mineral content, increased
demand for minerals due to life-history characteristics (males’
sizes or females’ lactational demands, categorized by reproductive state), or salt loss through thermoregulatory armlicking behavior, measured using ambient temperature as a
proxy. Resting eastern grey kangaroos do not sweat, but
instead rely on dry conductance through peripheral vascular
adjustments and evaporative heat loss for thermoregulation,
divided almost equally between panting and arm licking, at
ambient temperatures below 338C (Dawson et al. 2000).
MATERIALS
AND
METHODS
The study was conducted in Sundown National Park,
Queensland, Australia (28855 0 03 00 S, 151834 0 46 00 E). The park
lies near the center of the species’ north–south range,
approximately 200 km inland from the coast (Fig. 1), in trap
rock country. Trap rock is hard, dense rock formed from
ancient marine sediments modified by heat and pressure. The
site consists of a mosaic of open grassy fields grazed by the
kangaroos, where Eragrostis leptostachya, Austrostipa scabra,
Cymbopogon refractus, and Bothriochloa decipiens are the
predominant grass species. These fields are surrounded by
mixed open woodland containing silver-leaved ironbark
(Eucalyptus melanophloia) and cypress pine (Callitris intratropica). The site was grazed by approximately 240 female
kangaroos and notably fewer males. Predation risk for adult
kangaroos was very low; there were no dingoes (Canis lupus
dingo) within the park, but wedge-tailed eagles (Aquila audax)
were occasionally seen and foxes (Vulpes vulpes) were known
to hunt juvenile kangaroos. There were 13 natural licks within
the 37.4-ha study area; most (minor licks) were only 1–2 m2
and used sporadically by 1 kangaroo at a time, whereas 2 were
larger and frequently had groups of 2–15 kangaroos present
(Fig. 2). These 2 larger licks were selected for focal behavioral
observations based on their frequent use by the kangaroos and
the ability to film each lick in its entirety within a camera’s
field of view. The dimensions of these 2 licks were
approximately 8 3 12 m (lick I) and 12 3 15 m (lick O), but
they increased in size slightly during the course of this study
through heavy use by the kangaroos.
Aim 1: comparison of soil mineral contents of the licks and
random sites.—To compare the mineral contents of the licks to
background levels across the study area, five 50-g soil samples
were collected from each of the 2 focal natural licks,
specifically targeting patches frequently used by the
December 2013
BEST ET AL.—GEOPHAGY IN THE EASTERN GREY KANGAROO
1239
FIG. 1.—The species range of the eastern grey kangaroo (Macropus giganteus), based on Coulson (2008), with locations of studies that could
have identified geophagy if it had been present at those sites (adapted from Coulson 2009). Kangaroos show physiological adaptations for sodium
conservation in areas with low soil sodium levels (Canberra and the Snowy Mountains) but in areas with higher soil sodium they do not (Broken
Hill and Coastal Victoria—Blair-West et al. 1968). We observed geophagy at Sundown National Park and Warrumbungle National Park (the
former is known to have low sodium levels apart from the licks). QLD: Queensland, NSW: New South Wales, VIC: Victoria, TAS: Tasmania.
kangaroos. An additional sample was later collected from lick I
after the kangaroos began to dig and eat the soil around a
neighboring ant nest midway through the study. Ten control
soil samples were collected from haphazardly chosen locations
across the study area and a soil sample also was collected from
each of the 11 minor licks at the study site. All soil samples
were analyzed (University of Queensland, School of Land and
Food Sciences) for cations Na, Mg, Ca, K, P, Mn, Zn, Cu, Fe,
and Co, and for S, C, and N. Each soil sample was air dried and
passed through a 2-mm sieve to homogenize the sample before
chemical analysis (Dormaar and Walker 1996; Ayotte et al.
2006), which was undertaken following the procedures
described in Rayment and Lyons (2011).
Aim 2: patterns and causes of use of natural licks.—
Between June 2011 and February 2012, a video camera was
mounted in a water-resistant case on a tree at each of the 2
focal licks (lick O: Sony Handycam CDR-SX65E; Sony,
Tokyo, Japan; lick I: Sony Handycam HDR-CX190; Sony).
The cameras recorded for 2 h after dawn and 2 h before sunset
on 7 days each month, including during light but not heavy
rain. The videos were later analyzed, with the sex and
reproductive state of each visitor to each lick recorded, along
with the duration of the visit for individuals whose arrival and
departure were observed. Adult females’ reproductive states
were divided into 6 categories: females with no pouch-young;
females with a small pouch-young; females with a medium
pouch-young that occasionally stuck its head out of the pouch;
females with a large pouch-young that was too large to
completely fit inside the pouch; females with a young-at-foot
that had permanently left the pouch but still nursed; and
females with both a small pouch-young and a young-at-foot.
Males were categorized as medium males that were a similar
size to adult females and large mature males that were larger
than adult females. The final category was subadults of both
sexes because we were unable to separate them on the videos.
Temperature, wind speed (measured using a Kestrel 1000
Pocket Wind Meter; Nielsen-Kellerman Co., Boothwyn,
Pennsylvania), and percent cloud cover (estimated to nearest
5%) also were recorded at the start and end of each video
session and the mean values were calculated.
Mineral content of the kangaroos’ diets.—To establish the
mineral contents of the kangaroos’ diets, 10–12 grass samples
were collected during each of August, October, November,
December, January, and February from 1-m2 plots, randomly
located within pasture areas across the study site. The same
plots were sampled each month and approximately 25 g of
grass was collected for each sample. Care was taken to select
grass leaves, which make up the majority of the diet of
1240
JOURNAL OF MAMMALOGY
Vol. 94, No. 6
FIG. 2.—A map showing the locations of the focal and minor natural licks within the Sundown National Park study site (the park’s location
within the species range also is shown), and photo of typical feeding behavior at natural lick I. Kangaroos scrape the soil with their incisors and
stick their heads into holes at preferred feeding spots. Aggressive behavior is frequently observed at preferred feeding spots.
kangaroos (Taylor 1983). The samples were air-dried in the
field and later oven-dried before being ground and sieved. We
then digested 0.25 g from each sample with 15 ml of 5:1
nitric : perchloric acid and analyzed the samples using an
inductively coupled plasma–atomic emission spectrometer for
macroelements (Na, Mg, K, Ca, and P) as well as trace
elements (Al, B, Co, Cu, Fe, Mn, S, and Zn). To establish when
the majority of grass available to the kangaroos changed from
being brown, dead grass in winter to green, lush, fresh grass,
monthly parallel transects 50 m apart were conducted across
the entire study site. A quadrat was placed on the ground every
25 m along each transect (n ¼ 110 quadrats), and the
percentages of cover of brown and green grass were each
estimated. These values were averaged across the study area
each month.
Statistical analysis.—All statistical analyses were
undertaken using R (R Development Core Team 2012). The
mineral contents of soil samples collected from the focal and
minor licks and the control sites were compared using simple
1-way analyses of variance. To determine the factors affecting
the number of kangaroos visiting the natural licks during each
2-h session we ran a generalized linear model using a Poisson
distribution with the following explanatory variables: mean
temperature, mean wind speed, and mean cloud cover for the
session; month; time of day (am or pm); and lick identity (I or
O). We also included interactions between mean wind speed
and lick and between mean temperature and mean cloud cover.
We included the climate variables to test the hypothesis that
kangaroos need extra sodium during hot weather because of
sodium loss from arm licking for thermoregulation. To
investigate the effect of the presence of fresh green grass in
the kangaroos’ diets on the number of kangaroos visiting the
licks, we ran a 2nd model replacing the variable ‘‘month’’ in the
previous analysis with ‘‘grass,’’ a variable that divided the data
into periods when the majority of the grass was brown or green
as determined from the monthly transect data. This allowed us
to test the hypothesis that increased intake of green grass (and
thus high levels of potassium) increased the need for sodium,
whereas the previous model tested for monthly variation in lick
use.
To determine the factors affecting the duration of time
individuals spent at the lick, we restricted the data to that from
lick I because of the superior visibility of the kangaroos at this
lick, resulting from its flatter profile. We ran a linear mixedeffects model with the following explanatory variables: mean
temperature, mean wind speed, and mean cloud cover for the
session; sex/reproductive state; number of kangaroos visiting
the lick in that session; and month and time of day (am or pm).
Session was included as a random effect to control for the fact
that on multiple sessions, data were recorded for several
kangaroos. P-values for the categorical variables month and
sex/reproductive state were calculated based on posterior
Markov chain Monte Carlo estimates of posterior distributions
for the parameters. The inclusion of sex/reproductive state in
December 2013
1241
BEST ET AL.—GEOPHAGY IN THE EASTERN GREY KANGAROO
TABLE 1.—Mean 6 SE mineral contents of soil samples taken from licks and of control samples taken from nonlick areas in the study site
(measured as milligrams per kilogram except for C and N, which were measured as Wt %, where Wt % ¼ mg1 kg1 10,0001). Measurements in
boldface type were significantly different from those from control samples. Samples from the focal licks include 5 taken from lick O and 6 from
lick I, whereas 1 sample was take from each of the 11 minor licks. Na and Mg levels did not differ significantly between the focal licks and the
minor licks.
Mineral
Ca
Co
Cu
Fe
K
Mg
Mn
Na
P
S
Zn
C
N
Focal licks (n ¼ 11)
563.81
0.22
0.47
23.15
155.27
644.64
13.03
846.81
11.08
57.00
0.24
0.41
0.12
6
6
6
6
6
6
6
6
6
6
6
6
6
120.80
0.09
0.08
5.88
14.32
105.58
3.82
137.40
2.49
16.77
0.06
0.06
0.01
this model allowed us to test whether particular classes of
kangaroos spent longer at the licks, as predicted if they
required more sodium, as well as testing the hypothesis relating
to thermoregulation using the climatic variables.
To investigate which factors affected the proportions of time
individuals spent eating the soil when at the lick, we randomly
selected females visiting lick I and recorded the amounts of
time they spent eating soil (as opposed to just being vigilant,
interacting with other kangaroos, or nursing their young-atfoot) during the 10 min after they commenced feeding at the
lick. We ran a generalized linear model with a gamma
distribution, with the following explanatory variables: mean
temperature, mean wind speed, and mean cloud cover;
reproductive state; the number of kangaroos present when the
individual arrived at the lick; and month and time of day (am or
pm).
RESULTS
Aim 1: comparison of soil mineral content of the licks and
random sites.—Soil analysis revealed that the 2 large focal
licks had significantly higher levels of Mg, Na, and S compared
to control samples, with the greatest difference occurring for
Na levels (Mg: F1,20 ¼ 21.639, P , 0.001; Na: F1,20 ¼ 32.117,
P , 0.001; S: F1,20 ¼ 9.089, P ¼ 0.007; Table 1). Minor licks
were significantly higher in Co, Mg, and Na compared to
controls (Co: F1,20 ¼ 6.249, P ¼ 0.022; Mg: F1,20 ¼ 13.221, P ¼
0.002; Na: F1,20 ¼ 16.330, P ¼ 0.001; Table 1), and there were
no significant differences in the Mg and Na levels between the
focal and minor licks (Na: F1,21 ¼ 2.945, P ¼ 0.102; Mg: F1,21
¼ 0.200, P ¼ 0.660; Table 1). Fe, P, and C were significantly
less abundant at the focal licks compared to control samples
(Fe: F1,20 ¼ 15.347, P , 0.001; P: F1,20 ¼ 45.183, P , 0.001;
C: F1,20 ¼ 32.716, P , 0.001; Table 1), as were Fe, K, P, C,
and N at the minor licks (Fe: F1,20 ¼ 24.103, P , 0.001; K:
F1,20 ¼ 9.464, P ¼ 0.006; P: F1,20 ¼ 146.780, P , 0.001; C:
F1,20 ¼ 41.145, P , 0.001; N: F1,20 ¼ 8.281, P ¼ 0.010; Table
Minor licks (n ¼ 11)
1298.91
0.80
0.45
26.03
121.45
729.36
23.21
534.64
3.06
25.85
0.42
0.34
0.07
6
6
6
6
6
6
6
6
6
6
6
6
6
263.83
0.25
0.09
3.00
15.00
157.52
7.15
119.23
0.78
11.57
0.08
0.04
0.00
Control (n ¼ 10)
783.50
0.15
0.33
53.21
186.2
126.00
23.84
27.70
35.75
3.84
0.76
1.26
0.13
6
6
6
6
6
6
6
6
6
6
6
6
6
136.23
0.03
0.12
4.78
14.65
11.07
6.15
5.17
2.70
0.50
0.22
0.14
0.02
1). Observations of the soil at the licks compared to the control
samples suggested that the licks had a high clay content
compared to surrounding soils.
Aim 2: patterns and causes of use of natural licks.—
Analysis of 488 h of video revealed the following numbers of
observations of different species visiting and eating soil at the
licks: 1,583 of eastern grey kangaroos, 11 of female eastern
wallaroos (Macropus robustus robustus), 3 of red-necked
wallabies (Macropus rufogriseus), and 3 of swamp wallabies
(Wallabia bicolor). Foxes were observed more frequently
around the licks than in the rest of the study area. They
appeared to be attracted by the kangaroos rather than the lick
itself; we observed them engaging in stalking behavior and
attacks on young kangaroos but not geophagy. Feral fallow
deer (Dama dama) were observed occasionally sniffing the soil
at the licks but not ingesting it. However, numerous deer tracks
were found at the licks on mornings after rainy nights; thus, it
is possible that they used them after dark. Wet kangaroos
(including those with large pouch-young), whose grazing home
ranges were not within the study site, were periodically
observed at the licks on dry days. We assume that they had
swum across the nearby river to visit the licks. It is unknown
whether kangaroos used natural licks on the other side of the
river, although limited searches did not find any.
Kangaroos scraped off chunks of exposed soil at the licks
with their incisors and chewed them before swallowing, often
while in an upright vigilant position. Kangaroos also were
observed digging with their forepaws to loosen the soil before
scraping at it with their teeth. A few females repeatedly used an
alternative method of pulling off chunks with their forepaws,
then standing and eating out of their paws while being vigilant.
Because of high intensity of use, preferred feeding spots often
developed into holes or overhangs and the kangaroos put their
heads into the former and occasionally lay on their sides to
reach the soil at the latter (Fig. 2).
Mineral content of the kangaroos’ diets.—Examination of
monthly grass quadrat data showed that the majority of grass
1242
Vol. 94, No. 6
JOURNAL OF MAMMALOGY
FIG. 3.—Significant monthly variation in the mean 6 SE number of
kangaroos visiting the licks, shown here averaged across the 2 licks
(monthly numbers of eastern grey kangaroos [Macropus giganteus]
visiting the licks: v28,229 ¼ 165.504, P , 0.001). Monthly mean
temperatures (left y-axis) and percent cloud cover (right y-axis) also
are shown and significantly affected the number of kangaroos visiting
the licks (temperature: v21,229 ¼ 13.280, P , 0.001; cloud cover:
v21,229 ¼ 5.497, P ¼ 0.019).
available to the kangaroos became fresh, green grass in
September following a winter dominated by brown, dead grass
(see Supporting Information S1, DOI: 10.1644/
13-MAMM-A-054.S1). Therefore, we divided the mineral
analyses of grass samples into 2 groups: June–August and
September–February. Although the percent cover of each grass
category was not quantified in January and February,
observations suggested that there was little difference
between these months and the month of December. The
comparisons of the mineral contents of grass between these
periods revealed that levels of K were significantly higher in
the September–February period (F1,66 ¼ 87.594, P , 0.001,
see Supporting Information S2, DOI: 10.1644/
13-MAMM-A-054.S2), as were levels of Co (F1,66 ¼ 14.613,
P , 0.001), Mg (F1,66 ¼ 6.011, P ¼ 0.017), P (F1,66 ¼ 25.264,
P , 0.001), and S (F1,66 ¼ 18.880, P , 0.001), whereas Fe
(F1,66 ¼ 8.943, P , 0.004) was significantly lower and other
minerals showed no significant differences.
Factors affecting the number of kangaroos visiting the
licks.—The number of kangaroos visiting the licks significantly
increased with mean temperature (v21,229 ¼ 13.280, P , 0.001)
and mean cloud cover (v21,229 ¼ 5.497, P ¼ 0.019). Month
(v28,229 ¼ 165.058, P , 0.001; Fig. 3) had a significant effect
with the highest number of kangaroos visiting in December and
February. There also was a significant interaction between
wind and lick, because mean wind speed increased the effect of
lick identity on the number of kangaroos visiting decreased
(v21,229 ¼ 23.195, P , 0.001). There was no significant effect
of time of day on the number of kangaroos visiting the licks
(v21,229 ¼ 0.013, P ¼ 0.910), nor was there an interaction
between temperature and cloud cover (v21,229 ¼ 2.059, P ¼
0.150). When month was replaced with grass type and the was
model rerun, the model showed a strong trend for an effect of
grass type on the number of kangaroos visiting the licks
(v21,235 ¼ 3.773, P ¼ 0.052). Other than mean cloud cover,
which became nonsignificant (v21,235 ¼ 3.271, P ¼ 0.071), all
significant variables in the previous model remained
significant, and those that had been nonsignificant remained
non-significant (see Supporting Information S3, DOI: 10.1644/
13-MAMM-A-054.S3).
The durations of time kangaroos spent at lick I were
analyzed for 650 visits by individual kangaroos. The durations
of visits increased significantly with temperature (v21,23 ¼
4.433, P ¼ 0.035) and were influenced by the sex/reproductive
state of the kangaroos (Markov chain Monte Carlo P ¼ 0.018),
with large males and females in the reproductive states of
having a large pouch-young and having both a small pouchyoung and a young-at-foot feeding for longest time at the licks
(Fig. 4). Visit durations were not significantly influenced by
month (Markov chain Monte Carlo P ¼ 0.064), mean wind
speed (v21,23 , 0.001, P ¼ 0.991), mean cloud cover (v21,23 ¼
0.110, P ¼ 0.740), number of kangaroos visiting the lick during
the session (v21,23 ¼ 2.485, P ¼ 0.115), or session (v21,23 ¼
1.171, P ¼ 0.279).
The proportions of time that 142 females spent in geophagy
during the first 10 min of their visits to lick I were significantly
affected by individuals’ reproductive state (v24,124 ¼ 15.676, P
¼ 0.004; Fig. 5, panel a), with females with no pouch-young
feeding for the highest proportions of time and those with large
pouch-young feeding for the least amount of time, and by
month (v28,124 ¼ 22.977, P ¼ 0.003; Fig. 5, panel b), with the
highest proportions occurring in December and the lowest in
June. However, there was no significant interaction between
month and reproductive state (v225,99 ¼ 0.419, P ¼ 0.276).
Neither was there any significant effect of time of day (v21,124
¼0.025, P ¼ 0.686), mean temperature (v21,124 ¼0.125, P ¼
0.368), mean wind speed (v21,124 ¼ 0.155, P ¼ 0.317), mean
cloud cover (v21,124 ¼ 0.095, P ¼ 0.433), or the number of
other kangaroos feeding at the lick when the focal females
arrived (v21,124 ¼ 0.104, P ¼ 0.411).
DISCUSSION
This study presents the 1st published description of
geophagy at natural licks by any native Australian mammal
and a 1st for marsupials in general, as far as we are aware. Our
observation greatly expands the taxonomic breadth of our
understanding of the importance of natural licks to mammals.
Because the eastern grey kangaroo is the most frequently and
intensively studied macropod species, the absence of previous
reports of geophagy implies that it is a facultative behavior in
this species. As found in studies on natural licks from around
the world (Klaus and Schmid 1998), our licks had significantly
higher levels of sodium, as well as magnesium and sulfur, than
did control samples taken from other areas within the study
December 2013
BEST ET AL.—GEOPHAGY IN THE EASTERN GREY KANGAROO
1243
FIG. 4.—Significant variation in the durations of complete visits observed at lick I by individuals in each of the different sex/reproductive state
categories (Markov chain Monte Carlo P ¼ 0.018, n ¼ 650 visits). The thick lines represent medians, whereas the tops and bottoms of boxes show
the 25% and 75% quartiles of the data. Values within the boxes represent sample sizes for each category.
area. Within our study area, natural licks were frequently
visited by eastern grey kangaroos and occasionally used by
eastern wallaroos, red-necked wallabies, and swamp wallabies.
Although the wallabies were regularly seen within the study
area, they were much less abundant than the kangaroos. By
contrast, eastern wallaroos were only rarely observed within
the study site (they are usually found on steeper, rockier
terrain); it is probable that they traveled from these areas
specifically to the licks and then returned to their normal home
ranges.
Comparison of soil sodium levels at our study site to those
previously reported in association with kangaroos’ physiological sodium status suggests that kangaroos in our study also
may have needed to adapt to low environmental sodium levels.
FIG. 5.—Significant variation in the proportion of time spent in geophagy during the first 10 min of visits to lick I by female eastern grey
kangaroos (Macropus giganteus) in a) different reproductive states (v24,124 ¼ 15.676, P ¼ 0.0035, n ¼ 142 visits) and b) different months (v28,124 ¼
22.977, P ¼ 0.0034). The thick lines represent medians, whereas the tops and bottoms of boxes show the 25% and 75% quartiles of the data.
Values within the boxes represent sample sizes for each category.
1244
JOURNAL OF MAMMALOGY
Blair-West et al. (1968) found that sodium levels in the soil
were much lower in locations where kangaroos showed
physiological adaptations for sodium conservation (Snowy
Mountains, 11.5 mg/kg, and Canberra, 18.4 mg/kg; Fig. 1),
compared to locations where they did not (Broken Hill, 82.8
mg/kg, and Victorian coast, 75.9 mg/kg; Fig. 1). Mean 6 SE
sodium levels from soil samples haphazardly collected at
Sundown National Park were only slightly higher than those
from the low-sodium locations (Sundown National Park, 27.7
6 5.2 mg/kg). Experiments in the Snowy Mountains showed
that eastern wallaroos traveled to feed on artificial licks and
showed an unequivocal preference for sodium over potassium,
magnesium, calcium chloride, or water, especially for females
with pouch-young (Abraham et al. 1973). Because the mineral
content of grass is partly influenced by soil fertility (Denton
1982), it is probable that kangaroos at our site also were
seeking sodium at the licks due to low dietary sodium, because
it is one of the most important minerals in animal physiology
(Denton 1982). However, we cannot completely rule out
benefits derived from ingesting clay, magnesium, or sulfur as
driving forces behind the observed geophagy.
For other species in which geophagy has been attributed to
sodium demand for mineral homeostasis, lick use showed
seasonal fluctuations (Weeks and Kirkpatrick 1976; Moe 1993;
Ayotte et al. 2008; Ping et al. 2011). We also found significant
fluctuations in the use of licks between months, with peak use
occurring in December and February. Increased use of licks in
spring and summer has often been attributed to an increase in
dietary potassium due to the growth of new grass, but dietary
mineral content has rarely been measured (for exceptions see
Risenhoover and Peterson [1986] and Ayotte et al. [2006]). We
found significantly higher potassium levels during months
when there was more green grass than during months when
most grass was brown. The number of kangaroos visiting the
licks was marginally significantly higher during months when
there was more green grass and thus dietary mineral content,
and particularly potassium, was likely to have affected the use
of licks in our study. Kangaroos had wetter, greener fecal
pellets in spring and some individuals showed signs of diarrhea
during this period (E. Best, pers. obs.); such signs may indicate
that potassium had decreased osmotic pressure in the fecal
mass, reducing water and sodium absorption (Weeks and
Kirkpatrick 1976). It is noteworthy that during this period
kangaroos were observed eating brown grass stalks, which they
had previously avoided during winter (E. Best, pers. obs.).
We found that there was a strong influence of reproductive
state on the length of time females spent at lick I; females with
large pouch-young and those with both a small pouch-young
and a young-at-foot simultaneously stayed longer that those in
other reproductive states. This supports the hypothesis that
lactation demand influences the use of licks. In white-tailed
deer (Odocoileus virginianus) in Indiana and sika deer (Cervus
nippon) in southern China, females also increased their use of
licks during lactation (Atwood and Weeks 2002; Ping et al.
2011). Large male kangaroos also spent long periods at the
lick; this could be due to a number of causes. First, large males
Vol. 94, No. 6
may have experienced a higher sodium demand. Second, large
males may have been able to defend their position and thus
remain for longer; aggression was much more frequent and
intense at preferred feeding spots at the licks compared to
during grazing on grass (E. Best, pers. obs.). Third, large males
may have remained at the licks because doing so would have
allowed inspection of multiple females in a single location
rather than roving widely in search of receptive females.
The proportion of time animals spent feeding while they
were at lick I was significantly influenced by month and
reproductive state, but there was no interaction between these
variables. It is interesting that time spent eating soil was lowest
for females with large pouch-young and highest for those with
no pouch-young. This does not fit what would be expected
based on lactation-driven sodium demand; sodium content in
macropod milk is highest at the start and end of lactation but
the greatest sodium demand on the mother is toward the end of
lactation when milk volume also is high (Green et al. 1980;
Merchant et al. 1989). The lower feeding time in females with
large pouch-young may reflect higher proportions of time
devoted to vigilance by these females whose young are more
vulnerable to predation. The longer duration, on average, of
visits to licks by these females probably reflects a vigilance–
foraging trade-off.
Despite the frequent finding that lick use peaks in spring and
summer in grazing mammals, the effect of ambient temperature
on the use of licks has not yet been examined. We found that
the number of kangaroos visiting the licks and the lengths of
time spent at lick I both showed strong positive relationships
with mean ambient temperature. However, temperature did not
have a significant effect on the proportion of time kangaroos
spent feeding when at lick I, which suggests it was less costly
for kangaroos to increase the lengths of their visits than to alter
their vigilance–feeding trade-offs during geophagy. Although
evaporative heat loss through panting and arm licking only
accounts for around 10% of metabolic heat production at
ambient temperatures of 158C, evaporative heat loss increases
significantly to 30% at 258C and increases again by 338C
(Dawson et al. 2000). It is likely that arm licking is costly in
terms of electrolyte loss (Forbes and Tribe 1969; Needham et
al. 1974) and therefore as ambient temperatures increase above
158C, kangaroos likely experience increased sodium loss in the
saliva they lick onto their arms. However, it is possible that
some of that sodium is reingested when they again lick their
arms.
Cloud cover and wind speed also affected lick use. The
increase in the number of kangaroos that visited licks with
increasing cloud cover may have been due to kangaroos
avoiding visiting the exposed licks during hot, cloudless days.
Eastern grey kangaroos are known to use behavioral
thermoregulation by seeking shade in hot conditions (Dawson
et al. 2006) and thus may delay their visits to the licks until
after sunset on the hottest days. Observations throughout the
day and night would be needed to test this. At our site there
also was a general trend for higher cloud cover in summer,
when temperatures were hotter, due to the increased frequency
December 2013
BEST ET AL.—GEOPHAGY IN THE EASTERN GREY KANGAROO
of storms. Wind speed influenced the number of kangaroos
visiting the licks by reducing the effect of lick identity; as wind
speed increased, the preference of kangaroos for lick I
decreased (lick I was more exposed than lick O, which was
surrounded by trees on 3 sides). This trend may reflect a higher
degree of perceived safety among the trees at lick O during
windy weather when kangaroos are more fearful because it is
more difficult for them to detect predators.
In conclusion, the use of natural licks by kangaroos in our
study shows similarities to that described for many eutherian
species around the world. Geophagy in kangaroos is a
facultative behavior because it has not been reported in other
intensively studied populations. This raises the question of why
this behavior occurs at Sundown National Park and how
widespread it is in this species and other marsupials. We suggest
that geophagy is most likely to be found in areas with high
temperatures that are naturally low in sodium but have suitable
licks (previous places where this species has been studied may
not have met all these criteria). During December 2011 eastern
grey kangaroos were observed engaged in geophagy at localized
sites in the Warrumbungle National Park, New South Wales,
Australia (31817 0 21 00 S, 149800 0 11 00 E); the soil at these licks
appeared similar to that at the licks at our study site (E. Best,
pers. obs.).
Facultative geophagy can be added to the list of mechanisms
including physiological and micromorphological adaptations
by which kangaroos regulate their mineral homeostasis. It is
probable that all 3 proposed proximate causes of geophagy
may be important in the kangaroo population in our study.
First, the mineral content of the grass appeared to influence the
number of kangaroos visiting the licks. Second, life-history
characteristics, such as females’ reproductive states (and thus
lactation demands) and the sizes of males significantly
influenced the durations of visits to lick I. Reproductive state
also influenced the proportions of time that kangaroos spent in
geophagy when at lick I. Third, temperature, a proxy for
sodium loss through arm licking, which is a thermoregulatory
behavior, positively influenced the number of kangaroos
visiting the licks and the durations of their visits. We have
reported on the use of natural licks by all 4 macropod species
present in our study area. Thus, it is possible that the minerals
present in licks may be important for many threatened and
endangered macropod species living in areas naturally low in
sodium. Therefore, especially given the ease of putting out salt
blocks, sodium demand should be considered during conservation planning and translocations of threatened macropod
species.
ACKNOWLEDGMENTS
We thank C. Menz for help with the collection of grass samples in
January and February 2011 and I. Elms, Queensland Parks and
Wildlife Service ranger at Sundown National Park, for his support of
our work. We are very grateful to R. Dwyer for considerable
assistance in producing Figs. 1 and 2. This research was conducted
under a Scientific Purposes Permit from Queensland’s Environmental
1245
Protection Agency and funded by the University of Queensland. ECB
was funded by a Northcote graduate scholarship.
SUPPORTING INFORMATION
SUPPORTING INFORMATION S1.—Mean percentages of cover of
green and brown grass each month averaged across 110
quadrats spread over the study site. Error bars represent SE.
The combined percentages of cover of green and brown grass
do not add up to 100% because the percent cover of bare
ground also was estimated.
Found at DOI: 10.1644/13-MAMM-A-054.S1
SUPPORTING INFORMATION S2.—Mean 6 SE mineral contents
of grass during the winter period when there was mainly dead,
brown grass (June–August, n ¼ 10 samples), and the spring–
summer period of lush, green grass (September–February, n ¼
58 samples). All values are in milligrams per kilogram except
those with an asterisk (*), which are in Wt %, where Wt % ¼
mg1 kg1 10,0001. Values that differed significantly between
the 2 periods are shown in boldface type.
DOI: 10.1644/13-MAMM-A-054.S2
SUPPORTING INFORMATION S3.—Factors affecting the number
of kangaroos visiting the licks during each 2-h session between
June 2011 and February 2012 (n ¼ 244 sessions). Results were
generated using a generalized linear model using a Poisson
distribution.
DOI: 10.1644/13-MAMM-A-054.S3
LITERATURE CITED
ABRAHAM, S. F., ET AL. 1973. New factors in control of aldosterone
secretion. Pp. 733–739 in Proceedings of the Fourth International
Congress of Endochrinology (R. O. Scow, ed.). Excerpta Medica,
Amsterdam, Netherlands.
ATWOOD, T. C., AND H. P. WEEKS, JR. 2002. Sex- and age-specific
patterns of mineral lick use by white-tailed deer (Odocoileus
virginianus). American Midland Naturalist 148:289–296.
AYOTTE, J. B., K. L. PARKER, J. M. AROCENA, AND M. P. GILLINGHAM.
2006. Chemical composition of lick soils: functions of soil
ingestion by four ungulate species. Journal of Mammalogy
87:878–888.
AYOTTE, J. B., K. L. PARKER, AND M. P. GILLINGHAM. 2008. Use of
natural licks by four species of ungulates in northern British
Columbia. Journal of Mammalogy 89:1041–1050.
BANKS, P. B. 2001. Predation-sensitive grouping and habitat use by
eastern grey kangaroos: a field experiment. Animal Behaviour
61:1013–1021.
BANKS, P. B., A. E. NEWSOME, AND C. R. DICKMAN. 2000. Predation by
red foxes limits recruitment in populations of eastern grey
kangaroos. Austral Ecology 25:283–291.
BELL, H. M. 1973. The ecology of three macropod marsupial species
in an area of open forest and savannah woodland in north
Queensland, Australia. Mammalia 35:527–544.
BENDER, H. 2003. Deterrence of kangaroos from agricultural areas
using ultrasonic frequencies: efficacy of a commercial device.
Wildlife Society Bulletin 31:1037–1046.
BLAIR-WEST, J. R., ET AL. 1968. Physiological, morphological and
behavioural adaptations to a sodium deficient environment by wild
1246
JOURNAL OF MAMMALOGY
native Australian and introduced species of animals. Nature
217:922–928.
CARTER, A. J., S. L. MACDONALD, V. A. THOMSON, AND A. W.
GOLDIZEN. 2009a. Structured association patterns and their energetic
benefits in female eastern grey kangaroos, Macropus giganteus.
Animal Behaviour 77:839–846.
CARTER, A. J., O. PAYS, AND A. W. GOLDIZEN. 2009b. Individual
variation in the relationship between vigilance and group size in
eastern grey kangaroos. Behavioral Ecology and Sociobiology
64:237–245.
CAUGHLEY, G. 1964a. Density and dispersion of two species of
kangaroo in relation to habitat. Australian Journal of Zoology
12:238–249.
CAUGHLEY, G. 1964b. Social organization and daily activity of the red
kangaroo and the grey kangaroo. Journal of Mammalogy 45:429–
436.
CLARKE, E., I. BEVERIDGE, R. SLOCOMBE, AND G. COULSON. 2006.
Fluorosis as a probable cause of chronic lameness in free ranging
eastern grey kangaroos (Macropus giganteus). Journal of Zoo and
Wildlife Medicine 37:477–486.
CLARKE, J. L., M. E. JONES, AND P. J. JARMAN. 1989. A day in the life of
a kangaroo: activities and movements of eastern grey kangaroos
Macropus giganteus at Wallaby Creek. Pp. 611–618 in Kangaroos,
wallabies and rat-kangaroos (G. Griggs, P. Jarman, and I. Hume,
eds.). Surrey Beatty, Sydney, Australia.
COLAGROSS, A. M. L., AND A. COCKBURN. 1993. Vigilance and
grouping in the eastern grey kangaroo, Macropus giganteus.
Australian Journal of Zoology 41:325–334.
COULSON, G. 1990. Habitat separation in the grey kangaroos,
Macropus giganteus Shaw and Macropus fuliginosus (Desmarest)
(Marsupialia: Macropodidae), in Grampian National Park, western
Victoria. Australian Mammalogy 13:33–40.
COULSON, G. 1997. Repertoires of social behaviour in captive and freeranging grey kangaroos, Macropus giganteus and Macropus
fuliginosus (Marsupialia: Macropodidae). Journal of Zoology
(London) 240:119–130.
COULSON, G. 1999. Monospecific and heterospecific grouping and
feeding behavior in grey kangaroos and red-necked wallabies.
Journal of Mammalogy 80:270–282.
COULSON, G. 2008. Eastern grey kangaroo, Macropus giganteus
(Shaw, 1970). Pp. 335–338 in The mammals of Australia (S. Van
Dyck and R. Strahan, eds.). Reed New Holland, Sydney, Australia.
COULSON, G. 2009. Behavioural ecology of red and grey kangaroos:
Caughley’s insights into individuals, associations and dispersion.
Wildlife Research 36:57–69.
COULSON, G., C. D. NAVE, G. SHAW, AND M. B. RENFREE. 2008 Longterm efficacy of levonorgestrel implants for fertility control of
eastern grey kangaroos (Macropus giganteus). Wildlife Research
35:520–524.
DAWSON, T. J., C. E. BLANEY, A. J. MUNN, A. KROCKENBERGER, AND S.
K. MALONEY. 2000. Thermoregulation by kangaroos from mesic and
arid habitats: influence of temperature on routes of heat loss in
eastern grey kangaroos (Macropus giganteus) and red kangaroos
(Macropus rufus). Physiological and Biochemical Zoology 73:374–
381.
DAWSON, T. J., K. J. MCTAVISH, AND B. A. ELLIS. 2004. Diets and
foraging behaviour of red and eastern grey kangaroos in arid
shrubland: is feeding behaviour involved in the range expansion of
the eastern grey kangaroo into the arid zone? Australian
Mammalogy 26:169–178.
DAWSON, T. J., K. J. MCTAVISH, A. J. MUNN, AND J. HOLLAWAY. 2006.
Water use and the thermoregulatory behaviour of kangaroos in arid
regions: insights into the colonisation of arid rangelands in
Vol. 94, No. 6
Australia by the eastern grey kangaroo (Macropus giganteus).
Journal of Comparative Physiology, B. Biochemical, Systematic,
and Environmental Physiology 176:45–53.
DENTON, D. A. 1982. The hunger for salt: an anthropological,
physiological and medical analysis. Springer-Verlag, Berlin,
Germany.
DIAMOND, J., K. D. BISHOP, AND J. D. GILARDI. 1999. Geophagy in New
Guinea birds. Ibis 141:181–193.
DORMAAR, J. F., AND B. D. WALKER. 1996. Elemental content of animal
licks along the eastern slopes of the Rocky Mountains in southern
Alberta, Canada. Canadian Journal of Soil Science 76:509–512.
FORBES, D. K., AND D. E. TRIBE. 1969. Salivary glands of kangaroos.
Australian Journal of Zoology 17:765–775.
FREELAND, W. J., AND D. CHOQUENOT. 1990. Determinants of herbivore
carrying capacity: plants, nutrients, and Equus asinus in northern
Australia. Ecology 71:589–597.
GILARDI, J. D., S. S. DUFFEY, C. A. MUNN, AND L. A. TELL. 1999.
Biochemical functions of geophagy in parrots: detoxification of
dietary toxins and cytoprotective effects. Journal of Chemical
Ecology 25:897–922.
GREEN, B., K. NEWGRAIN, AND J. C. MERCHANT. 1980. Changes in milk
composition during lactation in the tammar wallaby (Macropus
eugenii). Australian Journal of Biological Sciences 33:35–42.
HEATHCOTE, C. F. 1987. Grouping of eastern grey kangaroos in open
habitat. Australian Wildlife Research 14:343–348.
HILL, G. J. E. 1981a. A study of grey kangaroo density using pellet
counts. Australian Wildlife Research 8:237–243.
HILL, G. J. E. 1981b. A study of habitat preference in the grey
kangaroo. Australian Wildlife Research 8:245–254.
HILL, G. J. E. 1982. Seasonal movement patterns of the eastern grey
kangaroo in southern Queensland. Australian Wildlife Research
9:373–387.
HUTTON, J. T., AND T. I. LESLIE. 1958. Accession of non-nitrogenous
ions dissolved in rainwater to soils in Victoria. Australian Journal of
Agricultural Research 9:492–507.
JAREMOVIC, R. V., AND D. B. CROFT. 1987. Comparison of techniques
to determine eastern grey kangaroo home range. Journal of Wildlife
Management 51:921–930.
JAREMOVIC, R. V., AND D. B. CROFT. 1991a. Social organisation of the
eastern grey kangaroo (Marsupialia: Macropodidae) in southeastern
New South Wales. I. Groups and group home ranges. Mammalia
55:169–185.
JAREMOVIC, R. V., AND D. B. CROFT. 1991b. Social organisation of the
eastern grey kangaroo (Marsupialia: Macropodidae) in southeastern
New South Wales. II. Association within mixed groups. Mammalia
55:543–554.
JARMAN, P. J., ET AL. 1989. Macropod studies at Wallaby Creek. VIII.
Individual recognition of kangaroos and wallabies. Australian
Wildlife Research 16:179–185.
JARMAN, P. J., AND C. J. SOUTHWELL. 1986. Grouping, associations, and
reproductive strategies in eastern grey kangaroos. Pp. 339–428 in
Ecological aspects of social evolution (D. I. Rubenstein and R. W.
Wrangham, eds.). Princeton University Press, Princeton, New
Jersey.
JARMAN, P. J., AND R. J. TAYLOR. 1983. Ranging of eastern grey
kangaroos and wallaroos on a New England pastoral property.
Australian Wildlife Research 10:33–38.
JARMAN, P. J., AND S. M. WRIGHT. 1993. Macropod studies at Wallaby
Creek. IX. Exposure and responses of eastern grey kangaroos to
dingoes. Wildlife Research 20:833–843.
JOHNSON, C. N., AND P. J. JARMAN. 1987. Macropod studies at Wallaby
Creek. VI. A validation of the use of dung-pellet counts for
December 2013
BEST ET AL.—GEOPHAGY IN THE EASTERN GREY KANGAROO
measuring absolute densities of populations of macropodids.
Australian Wildlife Research 14:139–145.
JOHNSON, C. N., P. J. JARMAN, AND C. J. SOUTHWELL. 1987. Macropod
studies at Wallaby Creek. 5. Patterns of defecation by eastern grey
kangaroos and red-necked wallabies. Australian Wildlife Research
14:133–138.
JONES, R. L., AND H. C. HANSON. 1985. Mineral licks, geophagy and
biochemistry of North American ungulates. Iowa State University
Press, Ames.
KAUFMANN, J. H. 1975. Field observations of the social behaviour of
the eastern grey kangaroo, Macropus giganteus. Animal Behaviour
23:214–221.
KLAUS, G., AND B. SCHMID. 1998. Geophagy at natural licks and
mammal ecology: a review. Mammalia 62:481–497.
KREULEN, D. A. 1985. Lick use by large herbivores: a review of
benefits and banes of soil consumption. Mammal Review 15:107–
123.
KREULEN, D. A., AND T. JAGER. 1984. The significance of soil ingestion
in the utilization of arid rangelands by large herbivores, with special
reference to natural licks on the Kalahari pans. Pp. 204–221 in
Herbivore nutrition in the subtropics and tropics (F. M. C. Gilchrist
and R. I. Mackie, eds.). Science Press, Johannesburg, South Africa.
MAGUIRE, G., D. RAMP, AND C. COULSON. 2006. Foraging behaviour
and dispersion of eastern grey kangaroos (Macropus giganteus) in
an ideal free framework. Journal of Zoology (London) 268:261–
269.
MAHANEY, W. C., ET AL. 1995. Geophagy amongst rhesus macaques on
Cayo Santigo, Puerto Rico. Primates 36:323–333.
MCCULLOUGH, D. R., AND Y. MCCULLOUGH. 2000. Kangaroos in
Outback Australia: comparative ecology and behaviour of three
coexisting species. Columbia University Press, New York.
MERCHANT, J. C., B. GREEN, M. MESSER, AND K. NEWGRAIN. 1989. Milk
composition in the red-necked wallaby Macropus rufogriseus
banksianus (Marsupialia). Comparative Biochemistry and Physiology, A. Physiology 93:483–488.
MILEWSKI, A. V., AND R. E. DIAMOND. 2008. Why are very large
herbivores absent from Australia? A new theory of micronutrients.
Journal of Biogeography 27:957–978.
MOE, S. R. 1993. Mineral content and wildlife use of soil licks in
southwestern Nepal. Canadian Journal of Zoology 71:933–936.
MOORE, B. D., G. COULSON, AND S. WAY. 2002. Habitat selection by
adult female eastern grey kangaroos. Wildlife Research 29:439–
445.
NAVE, C. D., G. COULSON, A. POIANI, G. SHAW, AND M. B. RENFREE.
2002. Fertility control in the eastern grey kangaroo using
levonorgestrel implants. Journal of Wildlife Management 66:470–
477.
NEEDHAM, A. D., T. J. DAWSON, AND J. R. S. HALES. 1974. Forelimb
blood flow and saliva spreading in the thermoregulation of the red
kangaroo, Megaleia rufa. Comparative Biochemistry and Physiology Part A: Physiology 49:555–565.
OATES, J. F. 1978. Water-plant and soil consumption by guereza
monkeys (Colobus guereza): a relationship with minerals and toxins
in the diet? Biotropica 10:241–253.
PAYS, O., M. GOULARD, S. P. BLOMBERG, A. W. GOLDIZEN, E. SIROT,
AND P. J. JARMAN. 2009. The effect of social facilitation on vigilance
in the eastern gray kangaroo, Macropus giganteus. Behavioral
Ecology 20:469–477.
PAYS, O., AND P. J. JARMAN. 2008. Does sex affect both individual and
collective vigilance in social mammalian herbivores: the case of the
eastern grey kangaroo? Behavioral Ecology and Sociobiology
62:757–767.
1247
PAYS, O., P. J. JARMAN, P. LOISEL, AND J. F. GERARD. 2007.
Coordination, independence or synchronization of individual
vigilance in the eastern grey kangaroo? Animal Behaviour
73:595–604.
PING, X., C. LI, Z. JIANG, W. LIU, AND H. ZHU. 2011. Sexual difference
in seasonal patterns of salt lick use by south China sika deer Cervus
nippon. Mammalian Biology 76:196–200.
POIANI, A., G. COULSON, D. SALAMON, S. HOLLAND, AND C. D. NAVE.
2002. Fertility control of eastern grey kangaroos: do levonorgestrel
implants affect behavior? Journal of Wildlife Management 66:59–
66.
RAMP, D., AND G. COULSON. 2002. Density dependence in foraging
habitat preference of eastern grey kangaroos. Oikos 98:393–492.
RAMP, D., AND G. COULSON. 2004. Small-scale patch selection and
consumer–resource dynamics of eastern grey kangaroos. Journal of
Mammalogy 85:1053–1059.
RAYMENT, G. E., AND D. J. LYONS. 2011. Soil chemical methods:
Australasia. CSIRO Publishing, Collingwood, Victoria, Australia.
R DEVELOPMENT CORE TEAM. 2012. R: a language and environment for
statistical computing. R Foundation for Statistical Computing,
Vienna, Austria.
RISENHOOVER, K. L., AND R. O. PETERSON. 1986. Mineral licks as a
sodium source of Isle Royale moose. Oecologia 71:121–126.
ROBBINS, C. T. 1993. Wildlife feeding and nutrition. Academic Press,
New York.
SMITH, M. 1979. Behaviour of the koala, Phascolarctos cimereus
Goldfuss, in captivity 1. Non-social behaviour. Australian Wildlife
Research 6:117–129.
SOUTHWELL, C. J. 1984a. Variability in grouping in the eastern grey
kangaroo, Macropus giganteus. I. Group density and group size.
Australian Wildlife Research 11:423–435.
SOUTHWELL, C. J. 1984b. Variability in grouping in the eastern grey
kangaroo, Macropus giganteus. II. Dynamics of group formation.
Australian Wildlife Research 11:437–449.
TAYLOR, R. J. 1982. Group size in the eastern grey kangaroo,
Macropus giganteus, and the wallaroo, Macropus robustus.
Australian Wildlife Research 9:229–237.
TAYLOR, R. J. 1983. The diet of the eastern grey kangaroo and
wallaroo in areas of improved and native pasture in the New
England Tablelands. Australian Wildlife Research 10:203–211.
TAYLOR, R. J. 1984. Foraging in the eastern grey kangaroo and the
wallaroo. Journal of Animal Ecology 53:65–74.
TAYLOR, R. J. 1985. Habitat use by the eastern grey kangaroo and
wallaroo in an area of sympatry. Mammalia 49:173–186.
TRACY, B. F., AND S. J. MCNAUGHTON. 1995. Elemental analysis of
mineral lick soils from the Serengeti National Park, the Konza
Prairie and Yellowstone National Park. Ecography 18:91–94.
WEEKS, H. P., JR. 1978. Characteristics of mineral licks and behavior
of visiting white-tailed deer in southern Indiana. American Midland
Naturalist 100:384–395.
WEEKS, H. P., JR., AND C. M. KIRKPATRICK. 1976. Adaptations of whitetailed deer to naturally occurring sodium deficiencies. Journal of
Wildlife Management 40:610–625.
WEIR, J. S. 1969. Chemical properties and occurrence on Kalahari
sand of salt licks created by elephants. Journal of Zoology (London)
158:293–310.
Submitted 20 February 2013. Accepted 1 August 2013.
Associate Editor was Chris R. Pavey.