Behavioral Ecology Vol. 10 No. 2: 136-140
© 1999 International Society for Behavioral Ecology
Olfactory discrimination in scat-piling lizards
School of Biological Sciences, Flinders University, GPO Box 2100, Adelaide, South Australia 5001
Address correspondence to C. M. Bull. E-mail: michael.bull{at}cc. flinders.edu.au
Received 28 April 1998; accepted 10 July 1998.
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ABSTRACT |
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Several lizard species in the Australian scincid genus Egernia have been reported to deposit scats in piles. We show that E. striolata, which does produce scat piles, and E. inornata, which does not, can both discriminate their own secretions, on paper substrates, from those of unfamiliar conspecifics. This was indicated by elevated tongue flick rates and more time in contact with the unfamiliar stimulus. This was not just a response to a novel stimulus because the secretions from another species (E. stokesii) elicited lower responses. When scats were presented, only striolata demonstrated discrimination between their own scats and those of unfamiliar conspecifics. This suggests that scats could be used to produce individual signals, perhaps indicating residence status, in scat-piling species. For striolata the signal from scats became less effective as the scats became older, suggesting the need to pile scats to renew the signal.
Key words: communication, Egernia, lizards, recognition, scats, skinks.
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INTRODUCTION |
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Scat piling is where feces, or scats, are deposited by individuals in a specific place and accumulate into piles. Many mammals show this behavior (Braun and Mares, 1996
;
Palomares, 1993). Several
individuals may contribute to a pile, and the site is usually visited
regularly for fresh deposition. The piles of scats produced by mammals are
often referred to as latrines. They are considered to have a social function,
for instance marking the edges of a territory in badgers
(Doncaster and Woodroffe,
1993; Roper et al.,
1993), or indicating the presence of a dominant individual in
rabbits (Mykytowycz and Gambale,
1969; Sneddon,
1991). More than 100 mammal species are known to have glands
associated with the anal region
(Mykytowycz, 1970) which could
lead to the secretion of pheromones onto the fecal excretions. In nonmammal
vertebrate species, individual scats may also contain pheromones (e.g., in
salamanders; Simons and Felgenhauer,
1992), but the use of scat piles as social signals does not appear
to be common.
Many lizards produce olfactory signals, with secretions from the skin
(Mason and Gutzke, 1990;
Weldon and Bagnall, 1987),
femoral pores (Alberts, 1990;
Cole, 1966;
La Nafie et al., 1995), or
from glands near the cloaca (Cooper and
Trauth, 1992; Trauth et al.,
1987). Lizards use tongue flicking to detect olfactory signals
(Cooper, 1994). Some lizard
species have been shown to increase their tongue flick rate in response to
signals from unfamiliar conspecifics compared to their own signals or signals
from familiar conspecifics (Alberts,
1992; Cooper, 1996;
Graves and Halpern, 1991).
Cloacal pheromones are one group of signals that permit this level of
discrimination in lizards (Cooper,
1995, 1996;
Cooper and Trauth, 1992), and
the excretory products from the lizard cloaca have been suggested to contain
individual social signals (Glinski and
Krekorian, 1985). Snakes may also use scats as social signals
because captive snakes produced more scats after their cages were cleaned than
before (Stow and Shine, 1993).
However, so far no report has indicated that lizards or snakes deliberately
accumulate piles of scats to use as a social marker in the way that mammals
do. For scat piles to function as a social signal, individuals should be able
to discriminate at least between their own scats and those of other
conspecific individuals.
Six of the 26 species of the Australian skink genus Egernia are
reported to deposit piles of scats close to basking sites
(Greer, 1989). Egernia
cunninghami has certain areas more favored for defecation, where there
may be 40-50 scats in a heap (Barwick,
1965). Egernia stokesii has small accumulations of scats
near basking sites (Swan,
1990; White,
1976). Egernia whitii defecates at a definite site
(Hickman, 1960;
Swan, 1990). Egernia
hosmeri has communal defecation sites, with large deposits of scats
(Shea, 1995;
Stammer, 1976). Egernia
kintorei has a single defecation spot
(Webber, 1978), and
Egernia striolata, basking on tree stumps, has a regular defecation
site on top of the stump, usually near the edge where it basks, and where
scats collect (Bustard,
1970).
In the other 20 Egernia species there are no records of scat
piles. This may reflect a lack of study in some species. However, Egernia
inornata showed no evidence for a single defecation spot in the field,
and captive individuals performed discrete defecation away from basking areas
(Webber, 1978).
There have been few attempts to explain scat-piling behavior in
Egernia. Barwick
(1965) suggested that scat
piles could mark territories in Egernia cunninghami. Alternatively,
he suggested, they may simply coincide with favored basking sites where the
lizard first reaches temperatures adequate to induce defecation, and they may
have no specific communication function. Swan
(1990) stated that Egernia
stokesii marked its territory with scat piles but presented no evidence
for that function.
If the scat piles in Egernia act as social signals, then individual lizards should be able to discriminate between their own scats and those of other conspecific lizards and also between scats from conspecific and non-conspecific lizards. In this study we tested the responses of lizards in two Egernia species, E. striolata and E. inornata, to different scats.
Egernia striolata is reported to be strongly territorial and to
deposit scat piles (Bustard,
1970), whereas E. inornata shows no evidence of scat
piling (Webber, 1978). We
predicted that striolata would show greater ability to discriminate
between scats of different origin than inornata. Skinks commonly use
body secretions to identify conspecifics
(Cooper, 1994). We predicted
that the two species would have equal ability to discriminate between body
secretions of different origin. The central hypothesis of this study was that
a scat-piling Egernia species has evolved the use of scats as an
additional discriminatory signal.
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METHODS |
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We collected both species from the Middleback Ranges (33°15' S, 137°7' E), west of Whyalla, South Australia. Additional inornata were collected from close to Roxby Downs, South Australia (30°42' S, 136°42' E). We captured 17 adult inornata by pit fall, or by excavation of their sandy burrows, and 14 adult striolata from crevices in rock outcrops. The sex of these adults could not be determined by conventional methods. Experiments were conducted outside the spring mating period.
We housed the lizards individually in glass tanks (75 x 30 x 35 cm for striolata, 58 x 37 x 35 cm for inornata) in a 25°C room under a 12 h light:12 h dark photoperiod. For 7 h during the light phase, 60-W heat lamps were turned on above one end of each tank to raise surface temperature to 32°C. We provided each tank with a newspaper substrate and a 11 x 11 cm brick tile as a basking site under the heat lamp. We provided plastic boxes (16 x 16 x 8 cm) as refuges for each lizard. For inornata, we provided sand for burrowing in a 15 x 37 cm pit in the floor of the tank. We fed the lizards three times a week on insects, chopped fruit and vegetables, and provided water ad libitum.
Position of scats
We removed scats from each tank each day or each second day. The floor of
each tank was divided into four equal sections. The basking tile was in one
section. Each day for 4 weeks we recorded the section where each scat was
deposited in 14 striolata and 10 inornata tanks. Then for
each tank we determined the accumulated number of scats in the quadrat with
the basking tile and the average number of scats in each of the other three
quadrats. If either species piled scats near the basking site, we expected to
find more scats in that quadrat. We used paired t tests for each
species to compare the number of scats in the basking tile quadrat with the
average number in the other three quadrats, using tanks as replicate
samples.
Response to own, unfamiliar conspecific, and non-conspecific
stimuli
We conducted experimental trials, each lasting 1 h, during periods of the
day when the heat lamps were turned on. In each trial we presented three
alternative stimuli to a test lizard on the basking tile in its tank. We used
two types of experimental stimulus, scats and paper substrates. We collected
fresh scats on the morning of the trial. We left filter paper substrates under
lizard refuges for 7 days to accumulate body secretions from frequent contact
with the resident lizard. We cut a single 2.5 x 2.5 cm square from the
filter paper from each refuge to use as a stimulus.
For each trial the stimuli (scats or paper) came from three sources: the test lizard's own tank, the tank of an unfamiliar conspecific lizard, and from a tank from a laboratory colony of a non-conspecific lizard Egernia stokesii. The three stimuli were placed on the basking tile, arranged in a triangle about 6 cm apart. In separate trials of the same experiment we randomly ordered the positions of alternative stimuli.
We monitored the response of the test lizard to the stimuli by video recording for 1 h. Lizards retreated to their refuge when the stimuli were placed in the tank and when the video recording was started. In all trials the lizards emerged within the next 60 min and climbed onto the basking tile. Within the first minute on the tile, they either investigated each stimulus by deliberately approaching it and tongue flicking it, usually 1-3 times, or they ignored it. After this initial response lizards usually remained on the tile and ignored all stimuli for the remainder of the recorded time, although in some trials they approached and tongue flicked a stimulus a second time. We counted the number of tongue flicks the lizard directed toward each stimulus and the time it spent with the tip of its nose within 1 cm of the stimulus.
Each lizard was tested three times with scats and three times with paper substrate stimuli. No lizard was used in a trial more than once on a day. In separate trials for a test lizard, different conspecific individuals were chosen to provide the unfamiliar stimulus. In the subsequent analyses there was one data point for each lizard, an average of the response parameter (number of tongue flicks or time in contact) for the three trials involving that lizard with that stimulus type.
Because individual lizards were presented with the three stimuli at the same time, their responses to the stimuli were not independent. We used repeated-measures ANOVA tests in which the source of the stimulus (own, stokesii, or unfamiliar) was the within-subject factor and lizard species (striolata or inornata) was the between-subject factor. In these and in all subsequent repeated-measures ANOVA tests, we used log10 (x + 1) transformations of the data and established that there was homogeneity of variances (Levene test) and sphericity of data (Mauchly's test). The untransformed data did not always meet these assumptions of the analysis.
We used further repeated-measures ANOVA tests to compare the responses to the three stimuli within each species. Then we used post-hoc Student-Newman-Keuls tests and paired t tests to determine which pairs of responses were homogeneous.
Age of signals
The age of signals experiment involved only six of the striolata
individuals. In each trial we presented a lizard with one of its own fresh
scats, less than 1 day old, and three scats of different ages (fresh, 1 week,
and 2 weeks old) from one unfamiliar conspecific. We had collected aged scats
7 or 14 days before the experiment and stored them in sealed plastic vials.
There were 30 trials with each lizard trialed once with the scats from each of
the other five lizards. We were testing whether the responses to unfamiliar
scats decreased with the age of the scat. Analysis was similar to the previous
experiment.
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RESULTS |
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Position of scats
We did not quantify the amount of time that lizards spent in each quadrat in their tanks, although the video recordings indicated that most of their active time was spent basking on the tiles. Scat production was rarely observed in the 1-h video recordings. Table 1 shows the spatial pattern of scat deposition in the glass tanks. E. striolata deposited the majority of its scats on or near the basking tile. A paired t test showed significant differences between the number of scats in the tile quadrat and the average number of scats in each of the other three quadrats (t13 = 10.09; p <.001). In contrast, inornata deposited no more scats in the tile quadrat than in the other quadrats (t9 = 0.81; p =.44).
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Response to paper substrates
Table 2 shows the response
of lizards to paper substrates from the three sources, own, stokesii,
and unfamiliar conspecific. The trends were similar for the two parameters
measured, number of tongue flicks and time in contact. The repeated-measures
ANOVA tests showed a significant effect of species, with striolata
showing a stronger response than inornata overall. There was also a
significant effect of the source of the paper substrate. There was no
significant interaction effect between lizard species and paper source,
indicating that the changing responses to the three stimuli were consistent
across the two species. Repeated-measures ANOVA tests performed within each
species (Table 2) confirmed
that there were significant differences in the responses to the three paper
substrate stimuli. Post-hoc Student-Newman-Keuls tests showed no pair of
response values was homogeneous for striolata, and that for
inornata responses to own and stokesii paper substrates were
homogeneous, but both were significantly lower than the response to paper from
unfamiliar conspecifics. Paired t tests
(Table 3) confirmed that paper
substrates from unfamiliar conspecifics elicited significantly more tongue
flicks and more time in contact than either of the other two stimuli in both
species.
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Response to scats
Table 2 also shows the
response of lizards to scats from the three sources, own, stokesii,
and unfamiliar conspecific, and again shows the trends were similar for the
two parameters measured, number of tongue flicks and time in contact. The
repeated-measures ANOVA tests showed a significant effect of species, with
striolata showing a stronger response than inornata to
scats. There was also a significant effect of the source of the scats. In
contrast to the results from paper substrates, there was a significant
interaction effect between lizard species and scat source, indicating that the
two species responded differently to the three scat stimuli. Repeated-measures
ANOVA tests performed within each species
(Table 2) confirmed that there
were significant differences in the responses to the three scat stimuli by
striolata. However, inornata showed no overall difference in
the number of tongue flicks to the three scat stimuli and only a marginally
significant difference in the amount of time spent with each. Post-hoc
Student-Newman-Keuls tests showed no pair of response values was homogeneous
for striolata, but all pairs of responses were homogeneous for
inornata for both tongue flicks and time in contact assays. Paired
t tests (Table 3)
confirmed that scats from unfamiliar conspecifics elicited significantly more
tongue flicks and more time in contact than either of the other two stimuli in
striolata but that unfamiliar conspecific scats received no more
attention than either of the other two stimuli in inornata.
The important difference between the species is that paper substrate from unfamiliar conspecifics produced a strong response in both species, but scats from unfamiliar conspecifics produced a strong response only in striolata.
Age of signal
There was a significant difference in the tongue flick response of
striolata to the scats of different ages
(Table 4;
F3,15 = 40.07, p <.001). Post-hoc
Student-Newman-Keuls tests showed that tongue flick responses to fresh and
1-week-old scats from unfamiliar conspecifics were homogeneous, but that there
were significant differences among all other groupings. Individual paired
t tests (on log-transformed data;
Table 5) showed that all three
aged scats from the unfamiliar conspecific lizard elicited a greater number of
tongue flicks than the lizard's own fresh scat. The response to fresh and
1-week-old scats from the unfamiliar conspecific were not significantly
different, but they both elicited a significantly higher response than did the
2-week-old scats from the same unfamiliar lizards.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Position of scats
The behavior of lizards isolated in small glass tanks is unlikely to reflect their behavior in the field. Nevertheless, the two species in the laboratory showed marked differences in the patterns of scat deposition, with striolata tending to concentrate scats around the basking tile and inornata spreading scats more evenly. These observations conform closely with earlier reports of the field behavior and scat deposition patterns of the two species. In those reports striolata were observed to deposit piles of scats near basking sites (Bustard, 1970
), whereas
inornata had no tendency to clump scats in one place
(Webber, 1978).
Response to paper substrate
The responses to paper substrates were consistent across the species. They
showed that each species could discriminate between its own signals and those
of an unfamiliar conspecific. This was not just a response to a novel stimulus
because they responded more strongly to unfamiliar conspecifics than to
another Egernia species. The lizards were probably responding to skin
or cloacal gland secretions that had adhered to the paper during prolonged
contact. The responses to paper substrates also showed that the laboratory
conditions were appropriate for each species to display its discriminatory
ability and that the assay was sufficiently sensitive to detect significant
discrimination even with the relatively small sample size available and the
simple experimental design.
Response to scats
The responses to scats were not consistent between the species. Egernia
striolata, but not inornata, discriminated between their own
scats and scats of unfamiliar conspecifics. Again, with striolata,
the response to scats from unfamiliar conspecifics was stronger than the
response to novel scats from another species. If striolata can
discriminate scats similarly in the field, scat piles have the potential to be
a useful signal of territory ownership. It is significant that
striolata, the species that produces piles of scats in the field and
that localized scat production in the laboratory tanks, can discriminate scats
in the laboratory, while inornata, which shows no scat piling,
cannot. This provides strong support for the hypothesis that scat piling may
have a function of signaling residence.
E. striolata still responded more strongly to unfamiliar scats than to their own fresh scats, even when the unfamiliar scats were 2 weeks old. However, the response to unfamiliar scats declined with scat age. The signal is probably a volatile chemical to elicit the tongue flick response, but of relatively low volatility, to retain the signal over time. Nevertheless, the gradual reduction in signal quality probably explains the need for lizards to continue to deposit fresh scats in the pile to retain the immediacy of the signal.
The nature of the signal has not yet been determined, although it is
possible that scats produced in the hind gut could become coated with a
secretion from cloacal glands as they pass out of the cloaca. Urodael glands
situated close to the cloaca and producing species-specific pheromones have
been described in Eumeces skinks
(Trauth et al., 1987).
Although scat piling has not been reported, to our knowledge, in any other
lizard genus, it appears in at least six species of the Australian skink genus
Egernia. This study shows that one of these scat-piling
Egernia species can discriminate between the scats of conspecific
individuals, and one non—scat-piling Egernia species cannot.
This provides evidence that the scat piles are used as markers of residence
status, as speculated in some earlier anecdotal reports
(Barwick, 1965;
Swan, 1990). We believe this
is the first evidence that lizards may use scat piles as a means of
communication and maintenance of social structure within a population.
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ACKNOWLEDGEMENTS |
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We thank Matthew Bonnett, Robert Sharrad, and Elvira Lanham for providing additional Egernia lizards, Cheryl Greaves and Leah Correll for animal care, and the Australian Research Council and Flinders University, School of Biological Sciences, for research funding.
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