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Faecal particle size and tooth wear of the koala
(Phascolarctos cinereus)
William Ellis
A,B,E
, Rachael Attard
C
, Stephen Johnston
B
, Peter Theileman
D
, Allan McKinnon
D
and David Booth
C
A
Centre for Mined Land Rehabilitation, Sustainable Minerals Institute, The University of Queensland, Brisbane,
Qld 4072, Australia.
B
Wildlife Biology Unit, School of Agriculture and Food Sciences, The University of Queensland, Gatton,
Qld 4343, Australia.
C
School of Biological Science, The University of Queensland, Brisbane, Qld 4072, Australia.
D
Queensland Department of Environment and Heritage Protection, Moggill Koala Hospital, Moggill,
Qld 4070, Australia.
E
Corresponding author. Email: w.ellis@uq.edu.au
Abstract. We used computer-aided image analysis of leaf fragment particles found in faecal pellets of 45 koalas,
representing the range of tooth wear in this species, to investigate how tooth wear in the koala influences faecal particle sizes.
Although the range of sizes of particles produced did not vary between koalas across different tooth wear classes, with all
koalas producing small, medium and large particles, koalas with advanced tooth wear produced a greater proportion of larger
particles. This observation may prove useful for demographic population analyses based on scat surveys since the broad age
class of individual koalas can be estimated from faecal pellet analysis. Older koalas produced faecal pellets containing a
higher proportion of the largest-sized particle sizes (those greater than 0.59 mm
2
) than either young or mature koalas but there
was no difference detected between mature and young koalas.
Additional keywords: faecal pellets, population age structure, tooth wear.
Received 10 October 2013, accepted 3 December 2013, published online 4 March 2014
Introduction
Faecal pellet searches are often used in surveys to detect koala
(Phascolactos cinereus) presence and examination of the leaf
fragments that constitute the pellets can reveal the diet of the
koalas that produced them (Ellis et al.1999). The leaf particle
sizes in the digestive tract of koalas have been shown to reflect
tooth wear, which, in turn, is an index of age and consequently an
important parameter in understanding the dynamics and life
history of species (Logan and Sanson 2002b). Non-invasive
methods of evaluating koala distribution, such as mapping faecal
pellet distributions, are important tools for conserving such
cryptic species because they produce an unequivocal record of
presence with minimal effort (Rhodes et al.2011; Ellis et al.
2013). The analysis of faecal pellet distributions has been
particularly useful for studying koala population trends
(Seabrook et al.2011) because they can have large home ranges
of up to 100 ha (Ellis et al.2002) and are often difficult to observe
during surveys of their habitat (Dique et al.2003; Phillips and
Callaghan 2011; Woosnam-Merchez et al.2012). In addition
to information about which trees koalas use and eat, recent
work suggests that fresh pellets may be analysed to produce
information on endocrine profiles (Davies et al.2013; Narayan
et al.2013) and genetic information for free-ranging koalas
(Wedrowicz et al.2013). It is necessary to identify the age
distribution of a population to examine and understand
population trends (Caughley and Gunn 1993): for koalas, the
collection and analysis of skeletal material has revealed patterns
of mortality across a wide geographical range (Melzer et al.
2011), but perhaps faecal pellet collections could be used to non-
invasively collect data on the age structure of a population in situ.
Digestive efficiency in the koala, as for other herbivores, is
related to food particle size in the gut, which, in turn, is primary
determined by mastication (Logan and Sanson 2002a). The
efficiency by which koalas can produce small particles is dictated
by tooth wear: animals with worn teeth produce fewer small
particles, and such animals may have to depend on strategies
such as merycism (rumination-like behaviour) (Logan 2001)or
selection of younger leaves to produce small particles. Indeed,
the relationship between tooth wear and digestive efficiency is
considered so close in koalas that tooth wear is described as
the most significant consequence of ageing because it impacts
on many life-history attributes such as resource protection and
Journal compilation Australian Mammal Society 2014 www.publish.csiro.au/journals/am
CSIRO PUBLISHING
Australian Mammalogy, 2014, 36,90–94
http://dx.doi.org/10.1071/AM13033
socialisation (Logan and Sanson 2002b). Ultimately, like other
herbivores, the decrease in chewing efficiency is accompanied by
a decrease in nutritional uptake and loss of body condition until
the koala becomes too weak to survive (Lanyon and Sanson
1986).
Previous studies have revealed a relationship between tooth
wear and particle size in the digestive tract of the koala (Logan and
Sanson 2000): here we test whether such a relationship exists in
the faeces of koalas, which could provide a tool for demographic
estimation based on faecal sampling. Our testable hypothesis was
that faecal particle size could be used to calculate chronological
age in koalas.
Materials and methods
Study animals and faecal samples
Faecal samples used in this study were sourced from koalas at the
Queensland Department of Environment and Heritage Protection
Koala Hospital, at Moggill (Queensland), where sick, injured and
orphaned koalas from south-east Queensland are bought for care.
The koalas that provided faecal pellets for this study were trauma
victims that were placed alone in small aluminium holding cages
(1 m 0.5 m 0.5 m) in the hospital ward at the Moggill facility
upon arrival. Faecal pellets were collected within 24 h of arrival to
ensure that faeces contained plant material from food consumed
before admission; a minimum of three individual koalas per tooth-
wear category were sampled in this study (Table 1).
Each koala was also assigned to a tooth-wear category
from 1 to 13+ (determined by P. Thieleman for all subjects),
as described in Gordon (1991) (Table 1). To ensure that a
comparative set of otherwise healthy koalas was sampled, each
koala was initially assessed and assigned a body condition score
between 1 and 10 (Ellis and Carrick 1992), as determined by a
single judge (P. Thieleman) for consistency. Younger koalas with
poor body condition scores (less than 6) were excluded, since
poor body condition in young koalas may indicate a nutritional
deficiency due to undiagnosed health conditions that could
compromise the project. However, we had to include older koalas
with a body condition score of less than 6 because (a) a decrease in
body condition is expected to occur with advanced stages of tooth
wear (Skogland 1988) and (b) particularly for the very advanced
tooth-wear classes, no individuals with body score greater than 6
were encountered.
Particle size analysis
Ten faecal pellets were collected from each koala; five of these
were used to produce microscopic slide preparations for faecal
particle size analysis. These pellets were first crushed between
the fingers and the resulting crushed material placed into a
4cm4 cm plastic weighboat (Cole Parmer, Australia)
containing 50 mL of water and a single drop of dishwashing
liquid (Colgate-Palmolive Co, USA) to help separate the
particles. After mixing with a plastic stirring rod to further break
up any aggregations of material, the weigh boat was agitated
by hand and 1 mL of mixture drawn into a plastic pipette. This
mixture was expelled onto a 76 mm 25 mm microscope slide,
left exposed to dry for ~2 h at room temperature and stored
uncovered. Three such slides were created for each faecal pellet,
resulting in 15 slides per koala.
Computer-aided image analysis was used to analyse faecal
particle size because it is an accurate and rapid method of
comparing the measurements of numerous non-geometric
particles (Logan and Sanson 2000). Each slide was viewed
under a compound microscope under 40 magnification, using
a Q Imaging Micropublisher 3.3 RTV camera mounted on the
microscope. ‘Q Capture’(Q Capture Suite Plus, Q Imaging,
BC, Canada) software was used to capture five images per slide,
which allowed measurement of at least 100 particles per slide.
Hence, for each pellet, at least 1500 particles were measured,
resulting in at least 7500 particles being measured for each koala.
Each resulting image was then converted to greyscale so objects
could be distinguished clearly from the background using the
software package ‘IrfanView’(Irfan Skiljan, http://www.
irfanview.com). The visible area of each particle was measured
using the image analysis software ‘Image J’(National Institute of
Health, Research Services Branch, http://rsbweb.nih.gov), using
a 1-mm scale object for reference, to obtain an indication of
particle size. Very small particles and bacterial cells were
excluded from image analysis because the magnification of the
microscope was not sufficient to detect particles of this size
(Logan and Sanson 2000). The ‘Image J’program measures and
records particle size in terms of pixels, and the 1-mm scale object
Table 1. Tooth wear classes and descriptions (reproduced from Gordon 1991) and number of
koalas in each class during the study
Tooth wear class
(Gordon et al.1988)
Description Mean age (years)
(Gordon 1991)
No. of koalas
sampled in each
tooth wear class
0 No dentine exposed on P
4
<10
1P
4
spots of wear 1.2 6
2P
4
one line of wear 2 3
3P
4
two lines of wear 2.7 5
4P
4
circle of wear 4.3 6
5, 6 P
4
flat, M
1
not flat 5.5–7.3 9
7, 8 M
1
flat, M
2
not flat 9+ 6
9,10 M
2
flat, M
3
not flat 9+ 3
11,12 M
3
flat, M
4
not flat 9+ 3
13 M
4
flat 9+ 4
Faecal particle size in the koala Australian Mammalogy 91
measured 1300 pixels; hence, this scaling factor was used to
convert pixels to square millimetres, which are the units we report
here. To ascertain the sampling protocol required to ensure that
all size classes of particles present on a slide were detected, we
captured multiple images from nine sample slides and compared
particle size across the cumulative data from each successive slide
[similar in fashion to the species area curve concept (Preston
1962)]; this approach confirmed that five slides were sufficient to
accurately estimate the frequency of all size classes.
Statistical analysis
Particles in the faeces were sorted into seven size classes based on
an arbitrary measure for analysis. These size classes were: less
than 5.9 10
6
mm
2
, 6.0 10
6
–5.9 10
5
mm
2
, 6.0 10
5
–
5.9 10
4
mm
2
, 6.0 10
4
–5.9 10
3
mm
2
, 6.0 10
3
–5.9
10
2
mm
2
, 6.0 10
2
–0.59 mm
2
and particles greater than
0.59 mm
2
. Thereafter we conducted simple statistical tests to
ascertain whether the material presented on the slide could be
interpreted to reveal the tooth wear of the koala. First, we
compared particle size variation between tooth wear classes,
testing whether older koalas (with greater tooth wear) produced
a broader spread of particle sizes. Second, we compared the
average size of particles across the range of tooth wear classes, to
test whether the average particle size on the slides we made was
correlated with tooth wear. Finally, we tested the relationship
between the proportional representation of the largest particles
in slides and their corresponding tooth wear classes, again
attempting to provide a simple test of age using slides made from
faecal pellets. To determine whether the variation between each
tooth wear category was significantly different, a weighted
regression model was fitted to the log
10
-transformed data and
compared with an unweighted regression model of the same data
using a ratio test to test for heteroscedasticity. We then conducted
a non-parametric correlation analysis of average particle size
for each tooth wear category to assess the relationship between
these measures and finally we conducted the same test using the
proportion of largest-sized fragments for each tooth wear class.
Statistical analyses were performed using the software
package R 2.9.2. (Venables and Smith, R Development Core
Team) and StatPlus (AnalystSoft, www.analystsoft.com).
Results
The average size of particles in faeces was significantly correlated
with tooth wear classes (weighted regression analysis
P=110
4
,n= 45). Faecal pellets from koalas with tooth wear
between Class 1 and Class 7 contained significantly fewer of the
largest-sized particles (>0.59 mm
2
) than those from koalas with
tooth wear of Class 7 or above (t
14
= 2.81, P= 0.00694). We
calculated the covariance between the proportions of each size
class of particles in the faeces and the tooth wear class of the koala.
As expected, the proportions of the largest particles increased
with advancing tooth wear while the proportions of the smallest
particles decreased as tooth wear increased (Table 2). Coefficients
of correlation between these variables (proportion of particles that
were in each size class) were non-significant except for the three
largest particle classes, the proportions of all of which were
correlated with tooth wear (Table 2).
Most of particles were smaller than 2.95 10
5
mm
2
in size,
and within this size range most particles were less than
6.0 10
6
mm
2
. These extremely small particles, however,
comprised less than 1% of biomass (assuming two-dimensional
particles, less if calculated in three dimensions), and we are
not confident that these represent leaf fragments rather than
endogenous cells, sloughed gut lining or even microbes.
Together, size Classes 1, 2 and 3 (5.9 10
6
mm
2
,
6.0 10
6
–5.9 10
5
mm
2
and 6.0 10
5
–5.9 10
4
mm
2
)
accounted for less than 7% of biomass identified in the slides, yet
they constituted the most abundant fragments identified (95%
of fragments from koalas of tooth wear Classes 1–7, 93% of
fragments from koalas of tooth wear Classes >7). From a
biological perspective, the amount of material that falls into
each size class (and hence its gut passage rate and digestibility)
should determine its impact on the life history of the koala.
Hence, it follows that biologically meaningful analyses should
be conducted on these size classes and this was evidenced in our
further analyses.
Koalas with advanced tooth wear (greater than Class 7)
produced faeces that contained a greater standard deviation in
Table 2. Analysis of covariance and Spearman’s coefficient of
correlation (with associated significance value) results for data on tooth
wear class and proportion of each particle size class found in faeces from
koalas of that tooth wear class
For the largest three size classes there was a significant correlation between the
proportion of the particles found in faeces and the tooth wear of the koala that
produced the faeces
Size category Covariance Coefficient of
correlation
P
Larger than 0.59 mm 0.28 0.512 0.0005
6.0 10
2
–0.59 mm 0.27 0.512 0.0005
6.0 10
3
–5.9 10
2mm
0.64 0.415 0.006
6.0 10
4
–5.9 10
3mm
1.92 0.340 0.026
6.0 10
5
–5.9 10
4mm
4.39 0.210 0.177
6.0 10
6
–5.9 10
5mm
–2.86 –0.182 0.242
Smaller than 5.9 10
6mm
–5.642 –0.278 0.071
0
2
4
6
8
10
12
14
16
Class 1–4
Proportion of all particles larger than 0.059
× 0.059 mm + 1 SD
Average particle size considering particles
greater than 0.0006 × 0.0006 mm + SEM
Tooth wear class
Class 4.5–7 Class 7.5+
Fig. 1. The appearance of the larger faecal particles in pellets from koalas in
age class ‘young’(1–4), ‘mature’(4.5–7) and ‘old’(7.5+). Dark bars indicate
the proportion (percentage) of all particles that fall in the largest size category.
Light bars indicate the average size (10
2
) of particles in faeces, considering
only particles greater than 0.0006 mm
2
in size.
92 Australian Mammalogy W. Ellis et al.
average particle size when compared with koalas with less tooth
wear (Fig. 1). This was statistically assessed using a ratio test
comparing a weighted and unweighted regression model
(P= 0.0227, n= 45).
The analysis of variation in particle size between individual
tooth wear classes was affected by small sample sizes for each
tooth wear class (Table 1), so koalas were further assigned to age
groups ‘young’(tooth wear Classes 1–4), ‘mature’(tooth wear
Classes 4–7) and ‘old’(tooth wear Classes >7). Tests of
heteroscedacity revealed unequal variances between each of
these groups when compared for most particle size classes. Only
for the second largest particle size group (0.06–0.59 mm
2
), for
comparison between young and mature koalas, were the
variances equal (F= 1.14, F
crit
= 3.049, P
(2 tailed)
= 0.79032).
Older koalas produced a higher proportion of the largest-sized
particle sizes (those greater than 0.59 mm
2
) than either young
(t
11
= 3.10059, P= 0.01) or mature koalas (t
11
= 3.00565,
P= 0.006) but there was no difference detected between mature
and young koalas (t
15
= 0.86311, P= 0.20083) (Fig. 1).
Discussion
Koalas have recently been added to the list of species protected by
the Environment Protection and Biodiversity Conservation Act
(Cth) 1999 in Australia, which attempts to protect the habitat of
protected species as well as the individuals of that species. Faecal
pellet surveys are a key element in identifying koala habitat, and
these searches have also been used to investigate elements of the
ecology of this species, including tree use (Callaghan et al.2011)
and diet (Ellis et al.2002). Tooth wear in the koala is, with some
exceptions (Melzer et al.2011), closely linked to age of the koala
(Gordon 1991). By investigating the particle size distribution of
these pellets, we aimed to test the potential for pellets to reveal
information about the koala population age structure at locations
without the need for intensive methods such as capture.
We proposed to develop a tool, based simply on fragment size
in faecal pellets, that could be used to estimate the tooth wear (and
hence age) of a koala. Our results were equivocal with regard to an
association between particle size variation and age in the koala,
and we did not find evidence among our samples to support the
hypothesis that the average size of faecal particles indicated age
accurately for koalas. However, we did find a significant increase
in the proportion of large particles in faecal pellets from koalas
with advanced tooth wear. For example, using our size classes, a
koala is likely to be in age Class 7 or above if the proportion of
faecal particles greater than 0.06 mm
2
in area exceeds 2%. Our
data provide evidence that faecal pellets produced by older koalas
can be distinguished from those produced by younger koalas, on
the basis of the proportion of faecal particles that are greater than
0.06 mm
2
.
Although the proportion of larger particles in faeces increases
as tooth wear increases (Fig. 1), the distribution of particle sizes
relative to the average particle size is not sufficient to distinguish
tooth wear classes. Hence, the spread of particle sizes in faecal
pellets does not appear to be a useful index of the age of a koala, a
finding that concurs with that of Lanyon and Sanson (1986): the
youngest molar wear class produced a similar ratio of small to
large particles in digesta from the stomach as seen in the oldest
molar wear class in their study.
Our results suggest that by focusing attention on the largest
particles that we identified in the faeces of koalas, a guide to the
age structure of a koala population can be produced, but the
information gathered in this manner may be imprecise. While
our approach to sorting particles into size classes made the basic
analyses straightforward, the results indicate that paying greater
attention to variation within the larger size classes should reveal
more about the tooth wear of the koala that produced the pellet.
Lanyon and Sanson (1986) investigated particle size in the
stomach and caecum of koalas, determining particle size
distributions using a wet sieving technique. They concluded that
koalas with very advanced stages of tooth wear had an increased
proportion of larger particles in the stomach compared with
younger koalas with minimal tooth wear. Despite this, they found
that within the caecum there was only a small increase in the
proportion of the largest particle size class. Therefore koalas with
advanced tooth wear still exhibited some selective retention of
proportionally smaller particles in the caecum, even though
they were producing fewer small particles. Our study also found
that koalas with advanced tooth wear were able to produce the
small particles –as indicated by the similar faecal particle size
distribution of old and young koalas. Hence the present study
confirms the findings of Lanyon and Sanson (1986), that older
koalas may have the ability to compensate for reduced
masticatory effectiveness as indicated by the high proportion of
small particles in the faeces of animals of all tooth wear categories.
Tooth wear not only has adverse effects on the feeding ecology
of koalas, but has the potential to interfere with their physiology,
behaviour and fecundity (Logan and Sanson 2002c). Logan and
Sanson (2002b) found that male koalas with advanced tooth wear
spent more time and effort feeding, with a daily increase in the
amount of leaves consumed, and an increase in chew rate, chews
per leaf, and total number of chews. This means that male koalas
invested more time and energy in processing each leaf and spent
less time moving between trees, resulting in a decrease in home-
range size and sociality. This could reduce their reproductive
effort and the number of offspring they sire, and it also explains
why we may not find changes in the faecal pellet particle sizes we
expected to see accompany advancing tooth wear. However, like
most species, advancing age is not likely to be accompanied by a
linear incremental decrease in masticatory efficiency across the
life span of the koala. Tooth wear in koalas will reflect their
chronological age, depending on factors such as diet over time.
From the perspective of demographic forecasting, it may be more
important to identify the ratio of immature, mature and old
individuals in a population and this is what our attention to the
larger particles and comparison of grouped toothwear classes
(Fig. 1) attempted. While our method does not currently result in
an accurate and repeatable index of koala age, the proportion of
larger-sized particles in the faeces of koalas can be used to
distinguish pellets produced by old koalas from those of younger
individuals.
Acknowledgements
Queensland Department of Environment and Heritage Protection (DEHP)
provided the Scientific Purposes Permits for this research (WISP00491302)
and all animal procedures were carried out in accordance with University of
Queensland Animal Ethics approval (ZOO/ENT/115/04/RT). Rebecca Larkin
of DEHP provided valuable veterinary assistance, as did the volunteers at the
Faecal particle size in the koala Australian Mammalogy 93
Moggill Koala Hospital. Simon Blomberg assisted with statistical analyses
and an anonymous reviewer provided valuable direction.
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