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Article
Age-Dependent Utilization of Shelters and Habitat in
Two Reptile Species with Contrasting
Intraspecific Interactions
Aleksandra Kolanek 1, 2, * , Stanisław Bury 2,3, Edyta Turniak 2and Mariusz Szymanowski 1
1Department of Geoinformatics and Cartography, Institute of Geography and Regional Development,
University of Wroclaw, pl. Uniwersytecki 1, 50-137 Wrocław, Poland; mariusz.szymanowski@uwr.edu.pl
2NATRIX Herpetological Association, ul. Legnicka 65, 54-206 Wrocław, Poland;
stanislaw.bury@gmail.com (S.B.); edyta.turniak@gmail.com (E.T.)
3Institute of Environmental Sciences, Jagiellonian University, ul. Gronostajowa 7, 30-387 Kraków, Poland
*Correspondence: aleksandra.kolanek@uwr.edu.pl
Received: 23 September 2019; Accepted: 15 November 2019; Published: 18 November 2019
Simple Summary:
Intraspecific interactions are known to affect habitat use in birds and mammals
but their role in spatial ecology of reptiles is far less recognized. Our comparative study shows
that species known to exhibit intraspecific predation (smooth snake Coronella austriaca) express
clearly different patterns of habitat and shelter occupancy than a species with no such cannibalistic
behavior (slow worm Anguis fragilis). Specifically, juvenile smooth snakes prefer sites and shelters
not occupied by the adults, even despite suboptimal habitat conditions. We propose that such
division indicates an avoidance of predation pressure set by larger individuals on the younger and
smaller ones. On the contrary, in slow worms no tendency for intraspecific avoidance are observed,
since specimens of different ages commonly share the same area and shelters. This points to higher
flexibility in habitat use in slow worms, while the smooth snake population is spatially structured,
with juveniles dispersed to the margins of the population range. For endangered smooth snakes,
habitat conservation should therefore include a wide buffer zone to maintain the youngest fraction of
the population. Future studies on habitat utilization in squamates needs to pay more attention to the
social cues, a commonly overlooked aspect in the spatial ecology of reptiles.
Abstract:
Reptiles undergo worldwide decline driven mostly by habitat change. Detailed recognition
of factors underlying spatial structure and habitat utilization is therefore a prerequisite of effective
conservation of this group. While the body of data on spatial ecology of reptiles is rapidly growing,
studies on social factors remain still underrepresented. We studied age-specific patterns of shelter
use, range size, and habitat preferences in the context of intraspecific interactions in the smooth
snake Coronella austriaca—known to exhibit intraspecific predation—and the limbless lizard slow
worm Anguis fragilis—with no such behavior observed. Despite smaller availability of preferred
microhabitats, juveniles of smooth snakes occupied habitat and shelters located at the edge of the
population range that did not overlap with adults. No such pattern was observed in the slow worm.
Our study indicates that intraspecific interactions affect the spatial ecology of squamates. Passive and
active protection of habitat must include wide buffers to preserve the poorly detectable young fraction
of the population.
Keywords: age-dependence; spatial ecology; intraspecific predation; reptiles; habitat use
Animals 2019,9, 995; doi:10.3390/ani9110995 www.mdpi.com/journal/animals
Animals 2019,9, 995 2 of 12
1. Introduction
Loss of natural habitats and changes in their structure are among the major challenges in
biodiversity conservation [
1
]. Understanding how species use their habitats is therefore helpful to
orientate management and planning of protected areas [
2
]. Most studies on habitat utilization of
terrestrial vertebrates have focused on mammals (e.g., [
3
]) and birds (e.g., [
4
]), with amphibians [
5
]
and reptiles receiving less attention (e.g., [
6
]). In snakes, patterns of habitat use are most commonly
interpreted through the lens of size-dependent trophic niche partitioning, i.e., ontogenetic differences
in diet [
7
] or, sometimes, by variation in thermoregulatory strategies [
8
]. However, recent findings
suggest that social interaction may be an important, although overlooked, factor in snake ecology [
9
,
10
].
Dietary preference is commonly different between adult and juvenile snakes (e.g., [
11
]), and it
might also differ due to sex-specific body size variation [
12
,
13
]. Although dietary niche partitioning is
important in snakes, not all shifts in space utilization can be explained by variation in dietary niches
(e.g., [
14
]). Studies have shown that the scent of conspecific may attract snakes and affect the direction
of their movement [
15
]. The opposite reaction, the avoidance of conspecifics, is likely to occur in species
exhibiting intraspecific antagonistic behaviors such as cannibalism. Intraspecific predation is expected
to promote shifts in habitat choice mainly in juveniles, expected to avoid competition with large-sized
adults. So far only studies on other squamates, lizards, show such spatial division between juveniles
and adults choosing different branches in trees and shrubs in the cannibalistic common chameleons
(Chamaeleo chamaeleon; [
16
]). The avoidance behavior is proposed to be a factor of population regulation
in snakes [17], but it still remains unknown whether it could be affected by intraspecific predation.
We aimed to investigate patterns of habitat use in the context of age and intraspecific interactions.
We compared two sympatric species of reptiles, the smooth snake Coronella austriaca and the legless
lizard, slow worm Anguis fragilis. These two species show similar habitat preferences, comparable
body size, and both have a viviparous mode of reproduction. However, the smooth snake is known
to exhibit cannibalism [
17
,
18
], whereas the legless lizard is a non-territorial species that does not
exhibit cannibalism [
19
]. Since cannibalistic behavior exerts the strongest pressure from adults towards
juveniles, we assume the presence of age-dependent shifts in artificial shelter utilization and spatial
distribution by those snakes as an indication of adult avoidance by juveniles. We expect adult and
juvenile snakes to occupy different shelters (without overlapping) and to exhibit no tendency for spatial
clustering, understood as reduced distance between individuals compared to random placements [
20
].
In contrast, adult and juvenile legless lizards are expected to either co-occur in the same shelter or to
show clustered spatial distribution. Next to social cues, microhabitat conditions can also drive spatial
distribution, therefore we have additionally controlled for the variation in microhabitat parameters in
the studied area. Snake habitat use is generally related to climate, land cover structure, vegetation,
and topography [
21
–
24
]. Given the small scale of the study area, we used the potential insolation and
vegetation height to measure environmental conditions around each artificial shelter. These two factors
(relatively constant from year to year and differentiated in our study area) can potentially strongly
affect the choice of living places by the smooth snake, especially because it is a sedentary species,
living in open areas, e.g., moors or glades [
25
,
26
]. It is likely that environmental effects have a positive
correlation with the occurrence of reptiles in places with greater potential insolation and with lower
vegetation. Alternatively, juveniles may occupy more overgrown sites to hide from larger individuals,
but at the expense of thermoregulatory opportunities.
Concluding, such data could substantially enhance our understanding of the commonly overlooked
cues in spatial ecology of squamates and thus could contribute to the habitat conservation regarding
species-specific intraspecific relations.
Animals 2019,9, 995 3 of 12
2. Materials and Methods
2.1. Study Area
The study was carried out in a former limestone quarry located in SW Poland, in Opolskie
Voivodeship (Figure 1). The study area is about 21 hectares. It is naturally limited on all sides, from the
south, east, and west by steep walls, and from the north by unfavorable habitat conditions—humid areas
and active limestone excavation. The area was afforested with pioneer species: pine Pinus sylvestris
as dominant species and birch Betula pendula and alder Alnus sp. as admixture. The average age of
trees is 20–30 years. The coniferous canopy cover is ca. 32% of the study area, and most of the area
lies at elevation from 185 to 190 m a.s.l. The average monthly (Apr–Oct) temperatures were: 9.4, 15.2,
18.3, 19.1, 17.9, 16.0, and 9.2
◦
C respectively. The spring and autumn were a little bit warmer and the
summer was cooler than the long-term average for the nearest meteorological station (Opole), distant
approx. 20 km [
27
]. The amount of rainfall during the research period was 369.55 mm, which was ca
61 mm less than the long-term average sum for the meteorological station in Opole.
Figure 1. Study area and location of artificial reptile refuges.
2.2. Experimental Design and Sampling Data
Artificial reptile refuges (n =43), made of 1 m
×
2 m fragments of roofing felt, were individually
numbered and evenly placed in the area (Figure 1). The mean distance between adjacent artificial
refuges was 70 m (median =71 m, range =21–83 m). Each artificial refuge was surveyed 24 times
weekly from April to October 2016. During each visit, we checked for the presence or absence of
reptiles on/under the artificial shelters. All specimens observed had their body mass, body length, age,
and sex recorded. Body mass was registered using a spring balance (precision = +/
−
0.3% of 300 g
maximum lifting capacity). We took length measurements three times for each specimen and used the
average as body length. We used snout-vent length (SVL) and tail length (TL) in snakes and SVL in
lizards, due to the possibility of autotomy. Snakes with more than 400 mm of body length (which is
ca. 46% of a smooth snake’s maximum body length reported in Poland, according to Juszczyk [
28
])
were categorized as adults, whereas smaller specimens were registered as juveniles. Snake sex was
determined only for adult specimens based on the thickening of the cloacal area (presence of hemipenes)
and on the proportion of tail length to the total length (average 20% in males, 16% in females, according
Animals 2019,9, 995 4 of 12
to Juszczyk [
28
]). In lizards the body length threshold was 140 mm SVL (which is ca. 53% of a slow
worm’s maximum body length reported in Poland, according to Juszczyk [
28
]). The adult lizards were
sexed based on the presence or absence of hemipenes. The size-based distinction fits with the data on
maturation in both species in southern Poland [
28
]. Additionally, every smooth snake specimen was
marked by ventral scale clipping [
29
], and the head pattern was photographed. Every slow worm was
marked by using pen-like medical cautery units [30].
The base for further analyses was a set of data points containing the geographical location of
artificial refuges with information about each individual found, date of observation, morphometry,
and information about their age and sex.
2.3. Data Analysis
We used the chi-square frequency test to check if the number of artificial shelters occupied by
adult snakes, young snakes and both groups is different from the expected number (equal frequencies
in all three groups of artificial shelters).
To determine whether adult and juvenile subpopulations of reptiles occupy different ranges, two
different methods are available, the minimum convex polygon (MCP) and kernel density estimation
(KDE). Both approaches have their drawbacks as well as advantages [
31
–
33
]. The main advantage
of MCP is its simplicity, especially to determine the spatial extent of the population and estimate the
boundaries of the area occupied [
34
]. But it is not free from flaws, for instance, MCP does not consider
the probability of settling individual parts of the area [
35
,
36
]. Although KDE can be a solution for
this later issue, it shows problems with choosing the proper smoothing factor for KDE, which has
made its use less preferable over MCP in herpetofauna research [
37
], a recommendation we followed
here. To quantify if any spatial differentiation among reptiles was due to the age group, we used two
measures of the central tendency: the mean center and the weighted mean center, to compare the
centroids of the subpopulation ranges [
38
]. The first measure determines the geographical center of
the area occupied by the given set of observations (animals), whereas the second metrics weights the
geographical center by the number of individuals found in each location. If these centers are close one
to another, it means that none of the artificial refuges were occupied by a significantly larger number of
individuals than the others. If the weighted means are shifted to one direction, it means that some
parts of the area were preferred by more specimens.
We checked the spatial distribution of individuals within their specific age-groups by means
of the average nearest neighbor (ANN) method [
20
]. This method is sensitive to the area extent
(subpopulation range), because it is based on the average distance from each focal point (individual)
to its neighbors in relation to an average distance calculated for randomly spaced points within the
area extent [
38
]. The ANN statistics were calculated separately for snakes and lizards, since we were
interested in mutual spatial relations of individuals of each species within their overall population
range. If the average distance between observations is smaller than that expected by chance, the pattern
is classified as clustered. If the average distance is greater than the random one, then the spatial pattern
is classified as dispersed [
20
]. In both adults and juveniles of smooth snakes we expected a dispersed
distribution due to the risk of intraspecific predation. Conversely, the slow worm, a non-territorial
lizard species [
19
], should be characterized by a cluster or random distribution, because they would
not avoid each other.
Environmental data were obtained on the basis of two raster layers covering the study area,
provided by the Geodesic and Cartographic Documentation Center: Digital Elevation Model (DEM)
and Digital Surface Model (DSM) (both layers with 1 m/px resolution). DEM is a digital record of
ground surface (in meters above sea level), and DSM, in the absence of buildings in this study area,
reflects the vegetation over the ground or the ground itself in non-vegetated places, similarly expressed
in meters above sea level. Based on the differences between DSM and DEM, a new raster layer with
information about the vegetation height at each point (raster cell) of the study area was received.
Insolation (incoming solar radiation) is a physical term meaning the amount of solar radiation incoming
Animals 2019,9, 995 5 of 12
to a unit area of the Earth’s surface [
39
]. In the ArcGIS software it is counted as the sum of solar energy
(Wh m
−2
) for each raster cell (in our case: 1 m
2
of the ground) for the given period, assuming clear
sky conditions (potential insolation) and can be calculated using the Area Solar Radiation tool [
40
].
This tool does not allow for the impact of cloud cover in calculations, but includes various factors such
as terrain (slope inclination, aspect, and hillshading) and astronomical and atmospheric elements [
41
].
The basis for calculations was DSM.
To check whether the habitat conditions (potential insolation and vegetation height) around
refuges differ from those for the entire study area, we used the Student’s t-test. For that, we defined
three zones: the entire study area (a) and areas around shelters inhabited by juveniles (b) and adult
(c) snakes. The size of neighborhood around the inhabited shelter was defined as an area of 10 m
radius, based on the diurnal displacement of snakes given by [
42
]. The environmental conditions
were characterized by areal statistics (means, standard deviations, and number of cells) calculated for
each environmental variable and each zone separately using the Zonal Statistics tool in ArcGIS [
40
].
Student’s t-test was then applied for each combination of zones: (a) vs (b), (a) vs (c), (b) vs (c).
Due to the binary nature of the reptile-to-shelter information at each visit (1—the reptile was found
under artificial refuge during the visit; 0—the reptile was not found), we decided to use the logistic
regression method [
43
] to determine if there is a significant relationship between lizard occurrence on
snake presence or absence and vice versa.
Spatial analyses were performed in a projected coordinate system EPSG: 2180 (“PUWG 1992”),
and the processing extent was limited to the MCP [20], covering all artificial refuges plus 20 m buffer
around. Analyses were performed in ArcGIS 10.2 [
44
], QGIS 3.0 [
45
], R 3.4.3 [
46
], and Python 2.7 [
47
].
All applicable institutional and/or national guidelines for the care and use of animals were followed
(permits from Regional Directorates for Nature Conservation in Opole no. WPN.6401.21.2015.TB and
WPN.6401.88.2015.Msz).
3. Results
During the fieldwork, we observed 43 smooth snakes, including 9 recaptured individuals (number
of unique specimens: juveniles n =17, adults n =17), and 110 slow worms (60 marked unique
specimens: juveniles n =14, adults n =46). Snakes were observed under 41.8% (n =18) of 43 artificial
refuges, and juveniles and adults always occupied different shelters with one exception. Slow worms
were observed under 67.4% (n =29) of all artificial refuges. Among those artificial refuges occupied
by the slow worms (n =29), adults and juveniles were found together in 58.6% (n =17) of the
shelters (Figure 2).
Animals 2019,9, 995 6 of 12
Figure 2.
Comparison of the number of adults and juvenile specimens under particular occupied
shelters (the IDs according to Figure 1).
The differences between three groups of artificial refuges (occupied by adults, juveniles, and
occupied by both age groups) were statistically significant: for slow worm
χ
2=10.786 (p-value =0.0045,
df =2), for smooth snake
χ
2=6.333 (p-value =0.0421, df =2). The frequency of shelters occupied
simultaneously by snakes of both age groups was lower than the expected, with the opposite pattern
in the slow worm. The size of the population range determined by the MCP method was 133,673.6 m
2
for snakes and 166,187.2 m
2
for lizards (the whole study area was 212,116.2 m
2
). Spatial distribution of
lizards was wider and more evenly spread than that of snakes (Figures 3and 4).
Animals 2019,9, 995 8 of 12
Table 1. Average Nearest Neighbor results.
Group Character of the Distribution ANN Ratio (p-Value)
All snakes dispersed 1.735 (<0.01)
Adult unique snakes dispersed 1.440 (<0.05)
Juvenile unique snakes dispersed 4.305 (<0.01)
All lizards clustered 0.338 (<0.01)
Adult unique lizards clustered 0.687 (<0.01)
Juvenile unique lizards random 0.824 (>0.1)
Adult lizards were found throughout the area (Figure 4). Weighted centers were shifted to the SE
from corresponding mean centers (Figure 4)—43.1 for juveniles, 16.3 for adults. This means that more
lizards were observed in the SE part of the area than the NW. The distance between mean centers of the
spatial distribution of adult and juvenile lizards was 17.5 m. The size and shape of the population range
of both age groups of lizards were similar (MCP of juveniles: 141,710 m
2
, MCP of adults: 166,290 m
2
).
Both areas overlapped in 67.9% of study area (Figure 4) and juvenile and adult specimens were found
under the same 17 artificial refuges (Figure 2).
The spatial distribution of snake specimens was dispersed, regardless of the age group of the
population. Using the MCP method, juvenile smooth snakes occupied a wider area than adults
(MCP of juveniles: 128,697 m
2
, MCP of adults: 57,494 m
2
), which occupied only part of the study
area (in contrast to adult lizards), and juvenile snakes were not found in the center of adult snakes’
range, only on the edge and outside (Figure 3). Due to that, quantification of overlapped areas is not
possible. The shift of the weighted center for the juvenile snakes was 76.3 m to SE from mean center
—there were more juveniles in the southeastern part of the study area. Adult snakes occupied their
area evenly, so both centers lay almost in the same place (3 m difference). The distance between mean
centers (91.4 m) for juvenile and adult snakes was greater than that in lizards and its shift towards the
NE expresses differences in the spatial distribution of these two groups (Figure 3).
Juvenile snakes occupied artificial refuges located in areas with lower average potential insolation
(14,451.6 Wh m
−2
) and higher average vegetation (1.6 m) than artificial refuges occupied by adults
(respectively: 15,603.7 Wh m
−2
and 1.1 m). The average potential insolation and average vegetation
height for the whole study area were, respectively, 13,193.4 Wh m
−2
and 2.3 m. For both variables
there were statistically significant differences between zones (a) vs (b), (a) vs (c), and (b) vs (c) at 0.1
confidence level and with p-value <0.1.
The result of the logistic regression showed no relationship between the occurrence of slow worms
and smooth snakes and vice versa (for both situations: Z value =0.033, p-value =0.0974).
4. Discussion
Smooth snake and slow worm—two species different in terms of intraspecific behaviors—revealed
different patterns in the use of shelters. In the cannibalistic smooth snake, juveniles generally did not
share refugees with adults and choose shelters in areas devoid of adults (Figure 3). Such avoidance
behavior was absent for the slow worm, with specimens of both age-groups often sharing artificial
shelters (Figure 4). Spatial distribution followed different patterns in both species. In the smooth snake
no tendency towards clustering was observed, and the juvenile snakes occupied areas outside the
range occupied by the adults (Figure 3), even despite lower availability of microhabitats preferred by
the species. In contrast, slow worm specimens tended to cluster and were not spatially divided in
terms of their age. The patterns observed in the smooth snake represent the outcome of conspecific
avoidance, with no such indications in the slow worm. Overall, our results indicate that behavioral
cues are important to shape patterns of habitat utilization in reptiles.
The effect of intraspecific behavior on microhabitat choice has been reported in arboreal lizards [
16
].
However, in terrestrial flat environments the directions of movements are narrowed totwo-dimensional
space, which may impose a constraint in the availability of microhabitats. In fact, shelters represent
Animals 2019,9, 995 9 of 12
limited resources which access may impact population density and trophic relations in snakes [
9
,
48
] and
lizards [
49
] According to our data, reptiles with intraspecific predation may appear more susceptible
to such constraints, since avoidance of conspecifics limits the simultaneous use of a shelter by a larger
number of specimens and may impose a higher dispersal rate of snakes searching for refugees. On the
other hand, in species such as slow worm, with no cannibalistic behavior, shelters may effectively be
utilized even by several individuals at the same time. Therefore, those species are more likely to cope
and persist in habitats with low availability of refuges.
Secondly, the mode of intraspecific relations may impact patterns of spatial distribution. The larger
area occupied by juvenile smooth snakes compared to adults indicates higher movement distances of
juvenile snakes [
50
] which can be a direct outcome of the avoidance of intraspecific predation and,
through this, enhanced by searching for vacant shelters. Although most available data suggest adults
to be the more migratory fraction of the population in snakes [
51
,
52
], our data suggest that this is
not to be the case in the smooth snake. In fact, previous studies confirm that juvenile smooth snakes
exhibit larger movement distances, reaching up to 700 m [
50
] compared to adult snakes, for which only
around up to 450 m was recorded [
53
]. Therefore, intraspecific predation may serve as a behavioral
mechanism underlying dispersion, which, on the other hand, may increase the mortality risk of juvenile
snakes. No such pattern was observed in the slow worm, a species that is more sedentary [
54
] and
rather tends to cluster, which corroborates experimental studies showing a tendency to choose sites
with conspecific scent [
19
]. Although this pattern may reduce mortality associated with movements,
it also increases susceptibility towards habitat loss. Such a tendency was already proposed for species
representing sit-and-wait foraging strategy [
55
], and here we propose that it may concern a broader
range of sedentary reptile species.
While we have ruled out environmental cues, and our model species seem to rely on intraspecific
predation or its lack, one cannot excluded further explanations associated with social behavior that may
apply to other species as well. These include mainly territorial behavior and the opposite, i.e., guarding
of conspecifics such as offspring, as observed in rattlesnakes [
10
]. Our study was performed on two
reptile species, therefore it is necessary for future research to include a wider array of species that differ
in terms of intraspecific behavior to get insight in the global patterns of behaviorally driven patterns of
space utilization, mainly in snakes.
Our findings also provide a contribution to reptile conservation. As we have shown, the two
species studied by us exhibit entirely different patterns of space utilization, which may have significant
consequences for population viability in relation to any changes in habitat structure. In the smooth
snake the wider range of area occupied by juveniles than adults indicated the need for planning
wide margins of protected areas. This is especially relevant since juvenile smooth snake are more
difficult to detect in field surveys which poses the risk of underestimating the area occupied by the
population. Moreover, the availability of shelters, commonly underestimated, needs to be taken into
account whenever smooth snake habitat is managed. Although slow worm seemed to be more flexible
in shelter use and its tendency to clustering may allow it to cope with small habitat patches, it also
imposes a higher risk of extinction whenever habitat loss occurs. For both species, as well as many
others, we propose the use of geoinformatics along with traditional field surveys. Such a GIS-based
approach allows extracting the patterns of habitat use far more precisely than regular surveys and thus
may improve habitat-based conservation.
5. Conclusions
•Smooth snakes and slow worms showed different age-dependent spatial distribution.
•
In the case of the smooth snake, we discovered that juvenile specimens occupied different artificial
shelters from adults. In the case of lizards, there were no such dependencies.
•
Juvenile snakes chose sites with suboptimal habitat conditions probably because sites with better
habitat condition are occupied by adult snakes.
Animals 2019,9, 995 10 of 12
•
Taken together, our results provide strong support for the role of age and behavioral cues in
shaping the spatial ecology of terrestrial squamates.
•
Our findings may also indicate that habitat-based reptile conservation needs to account for the
social mode of a given species and associated spatial structuring of the population.
6. Licenses
Numbers of licenses to use materials from the Polish Geodesic and Cartographic Documentation
Center: DIO.7211.796.2016_PL_N and DIO.DFT.7211.10225.2015_PL_N.
Author Contributions:
Conceptualization, A.K. and S.B.; methodology, A.K., E.T., and M.S.; validation,
A.K.; formal analysis, A.K.; investigation, A.K. and E.T.; writing—original draft preparation, A.K. and S.B.;
writing—review & editing, A.K., S.B., M.S, and E.T.; visualization, A.K.; supervision, M.S.
Funding: This study was funded by NATRIX Herpetological Association (statutory funds).
Acknowledgments:
We thank Magda A. Mielczarek for her time spent reading the part of manuscript, Mario R.
Moura and two anonymous reviewers for their valuable comments.
Conflicts of Interest: The authors declare no conflict of interest.
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