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Bull CM, Godfrey SS, Ebrahimi M, Fenner AL (2015) Long and short term residence in refuge burrows by endangered pygmy bluetongue lizards. Amphibia Reptilia 36, 119-124
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1
Long and short term residence in refuge burrows by endangered pygmy bluetongue 1
lizards 2
C. Michael Bull1, Stephanie S. Godfrey1,2, Mehregan Ebrahimi1,3 and Aaron L. Fenner1 3
1School of Biological Sciences, Flinders University, Adelaide, South Australia 4
2 School of Veterinary and Biomedical Sciences, Murdoch University, Murdoch, 5
Western Australia 6150, Australia.
6
3 Department of Biology, Shiraz University, Shiraz 71454, Iran.
7
Corresponding author: [email protected] 8
Manuscript type: Article 9
Word count: 3420 10
Abstract word count: 125 11
12 13 14 15 16 17 18 19 20 21 22 23 24 25
2 Abstract
26
The pygmy bluetongue lizard (Tiliqua adelaidensis) is an endangered species which is 27
restricted to native grassland remnants in South Australia. Individuals live in vertical 28
burrows with a single entrance from which they ambush invertebrate prey. We 29
monitored marked burrows over two entire spring-summer seasons, the period when the 30
lizards are active, and found that the population contained a mixture of dispersers that 31
remained in a burrow briefly, and residents that occupy a burrow for the entire study 32
period. There were more females than males among the residents and most of the 33
burrow abandonment happened in the early spring, the time when male lizards probably 34
move around to seek matings. Our study described burrow occupancy dynamics, and 35
will assist the conservation management of this endangered species.
36
Key words: Scincid lizards; burrows; long-term residency; conservation 37
Introduction 38
Effective conservation management of endangered species requires thorough 39
understanding of ecological factors that are associated with population dynamics and 40
critical resources (Macdonald and Willis, 2013), such as refuges and space to live in.
41
For many species, these spatial resources are often in short supply within the best 42
patches of habitat, and individuals need to compete for space by defending core home 43
range areas or territories (Krebs et al, 1978). Local population structure in those species 44
often reflects a balance between established residents who control those resources, and 45
dispersers intending to settle there (Stamps and Krishnan, 1994). Understanding the 46
ecological processes that generate this balance allows more effective advice on how to 47
manage those populations and maintain high numbers. Refuges against extreme climate 48
and predators are among the resources that are competed for within populations.
49
3
For species in many taxa, refuge tree hollows and burrows are an important 50
component in conservation management (Barclay, 2008; Gibbons and Lindenmayer, 51
2002). Lizards often occupy stable home ranges (Bull and Freake, 1999), within which 52
they can select several alternate refuges (Duffield and Bull, 2002; Kerr et al, 2003).
53
Lizard species that adopt a sit and wait foraging strategy can often combine their refuge 54
and ambush site, making refuges particularly important resources (Fenner et al, 2012).
55
The endangered pygmy bluetongue lizard Tiliqua adelaidensis (Scincidae) was 56
considered extinct until 1992, when it was rediscovered near the town of Burra in South 57
Australia (Hutchinson et al, 1994). In the subsequent 20 years research on pygmy 58
bluetongue lizards focused on its natural history and developing recommendations for 59
its management and conservation. The lizard uses vertical burrows with single entrances 60
constructed by mygalomorph and lycosid spiders for refuges and ambush sites (Milne et 61
al, 2003). This lizard species is now restricted to a few small remnants of native 62
grassland in the mid-north region of South Australia where its persistence is threatened 63
by agricultural activities (Souter et al, 2007). Lizard life span is unrecorded, although 64
one adult pygmy bluetongue lizard was found to have lived for 15 years in captivity (M.
65
Hutchinson pers. comm.). Adult lizards are mostly solitary and prefer to occupy deep 66
burrows with a narrow entrance (Milne and Bull, 2000), a resource typically in short 67
supply (Fellows et al, 2009). Local population density can be enhanced by adding 68
appropriately sized artificial burrows (Souter et al, 2004).
69
Once established in a burrow, a pygmy bluetongue lizard typically will spend 70
most of its time either refuged in the burrow or half emerged at the burrow entrance.
71
Resident lizards will rarely move out of the burrow, except for occasional short 72
excursions for defecation or to capture passing invertebrate prey (Milne et al, 2003;
73
Pettigrew and Bull, 2012; Pettigrew and Bull, 2014). As a result the normal home-range 74
4
area of a pygmy bluetongue lizard extends to less than a metre from the burrow 75
entrance. Resident lizards of both sexes aggressively defend their burrows against 76
conspecific intruders who come close to the burrow entrance (Fenner and Bull, 2011).
77
However, both pitfall trapping and genetic analysis show that some individuals move 78
about on the surface (Schofield et al, 2012; Schofield et al, 2014), presumably both to 79
relocate to more suitable burrows and to seek mating partners. Previous research has 80
suggested that as lizards move about between burrows they are at risk both from 81
predation and from dispersing out of suitable habitat (Fellows et al, 2009; Fenner et al, 82
2008a; Fenner et al, 2008b).
83
One critical question in pygmy bluetongue lizard conservation concerns the 84
residency of lizards within single burrows. Do they establish in a burrow and remain 85
there for a long time, or do they move around selecting alternative burrows at regular 86
intervals? From an ecological perspective long term residency might suggest the 87
population is stable. Because suitable burrows are a critical limiting resource (Fellows 88
et al, 2009), annual recruits might occupy vacated burrows or disperse to new 89
population sites. The relevance for conservation management relates to the strategy of 90
augmenting the number of burrows to enhance population density, as well as for any 91
planned translocations where the release site should have adequate burrow resources.
92
Methods 93
Study site 94
The study was conducted in a 1 ha plot of native grassland within the “Tiliqua” property near Burra, 95
South Australia (33.67OS; 138.93OE), over two austral spring and summer seasons 2011/2012 and 96
2012/2013. The study area has a Mediterranean climate with cool wet winters and hot dry summers, and 97
an average annual rainfall at Burra of 430mm. Spring and summer is the period of the year when the 98
lizards are active. They remain inactive inside burrows over the cooler months of autumn and winter.
99
Previous sampling (Fellows et al, 2009; Schofield et al, 2014) has shown an equal sex ratio of pygmy 100
bluetongue lizards at this site.
101
5 Plot sampling and monitoring
102
The study plot was searched for burrows that were occupied by adult pygmy bluetongue lizards in 103
September of each year. We used 60 CCTV cameras (SONY Effio 2.8mm-10mm, 30 fps), that were 104
positioned, each month, 100 cm above the burrow entrances and the immediate surrounding area of 23 105
(2011/2012) or 20 (2012/2013) of those occupied burrows. We filmed lizard activity simultaneously 106
around each burrow for ten days of each month for six months from Oct to March in each season (120 107
days of filming). This allowed us to monitor all of the lizards simultaneously. Burrow GPS locations were 108
recorded, and permanent, numbered marker pegs were used to relocate burrows for each filming session.
109
We could not identify individual resident lizards from the video records because the quality of the footage 110
was not sufficiently detailed. Instead we captured and identified individual lizards using previous toe clip 111
markings, before and after each filming session to confirm that the same lizards stayed in the same 112
burrow.
113
Lizards were captured for identification by luring them from their burrows with tethered 114
mealworms. Sex was determined for most lizards by relative body proportions, with males having shorter 115
bodies and wider heads than females (Hutchinson et al, 1994; Schofield et al, 2012), and confirmed for 116
many of them by video recordings of reproductive activity. Each lizard was returned to its burrow within 117
10 min.
118
Data interpretation 119
We determined occupancy time from the number of months when the same lizard was in the same 120
burrow. If the same lizard was identified in the same burrow on two separate occasions within a season 121
and if the burrow had a lizard that could not be lured out during some filming months in between, we 122
assumed the same lizard had retained residency over that whole period. Similarly, if the same lizard was 123
recorded in a burrow at the end of the 2011/2012 season and at the beginning of the 2012/2013 season, 124
we assumed it had remained in the same burrow over the winter in between.
125
In some cases (see results for numbers of cases), burrows that had been occupied and filmed in 126
one month, were vacant in the next month. For some of those burrows, we continued to film the empty 127
burrow, anticipating that the same lizard might return, or another lizard might take over the burrow. In 128
other cases, when a burrow was vacated we moved the camera to film another nearby occupied burrow.
129
Burrow occupations that occurred before or after the monitoring period for individual burrows were not 130
accounted for and estimates of occupancy time should be regarded as minimum values.
131
6 Results
132
We had records for 50 individual lizards over the two seasons, 12 males, 20 females and 133
18 of unknown sex (Fig 1). Among the 18 lizards of unknown sex, one stayed in the 134
same burrow for five months, but the other 17 moved from their burrow during or after 135
a single filming period and before we had an opportunity to determine their sex.
136
Although we continued to film burrows that had been abandoned by lizards we had no 137
records of a lizard coming back to its empty burrow.
138
The temporal sequences of burrow occupancy are shown in Fig 1. Among the 26 139
lizards recorded in the first season (2011/12), 16 lizards stayed in the same burrow for 140
four or more months and were still in the same burrows in the last survey in March.
141
These included ten females, five males and one adult of unknown sex. One male and 142
two extra females were known to occupy the same burrows in March 2012 that they had 143
occupied for at least two or three months. A further seven lizards left the burrows they 144
initially occupied (Fig 1). These lizards were recorded in burrows for one month (five 145
lizards), two months (one lizard) and five months (Oct – Feb; one female).
146
Of the 19 lizards in burrows in March 2012, eight were no longer in their 147
burrows in the following spring, but 11 (seven females; four males) were still in the 148
same burrows at the start of the next season (Sep 2012). All of those 11 overwintering 149
lizards and another six newly monitored individuals (total 12 females; five males) 150
remained in the same burrows for five or more months in the second season. Another 151
three males were in the same burrows for at least three months from Jan – March 2013.
152
An additional 15 adult lizards (unknown sex) were recorded in a burrow for only a 153
single month.
154
In summary, at least 11 (seven females; four males) of the lizards we observed 155
were resident in the same burrows for as long as we had records, for periods of 14 to 18 156
7
months, including two complete seasons of lizard activity. An additional 15 lizards 157
(nine in season one; six in season two) were present in the same burrow for most of one 158
season (five – seven months). One of the 26 long-term residents was of unknown sex.
159
Among the remaining 25, there were significantly more female (17) than male (8) 160
lizards (chi-squared = 4.84; d.f. = 1; P = 0.027).
161
There were 20 cases where lizards were only recorded in a burrow in one month 162
and had departed from that burrow the next month, and 18 of those (90%) occurred in 163
the spring (Oct/Nov). These lizards had dispersed before we had determined their sex.
164
Discussion 165
From an ecological perspective, our data provide substantial new insights into the 166
dynamics of burrow occupancy within pygmy bluetongue lizard populations. They 167
confirm a number of inferences that have previously been made about pygmy 168
bluetongue lizard population dynamics, and provide additional new insights. First, our 169
results suggest that the overall population of lizards during an activity season contained 170
a mixture of long term residents and drifter lizards. The drifters appeared to disperse 171
into the monitored area, remain for a short time and then disperse away again. These 172
findings are consistent with previous observations over shorter time periods on pygmy 173
bluetongue lizards (Fenner et al, 2011). Importantly, Fenner et al (2011) showed that 174
parasite transmission around the population was driven by the dispersers, probably 175
because they are more likely than residents to contact other lizards.
176
Second, our study has provided greater insights into when most dispersal occurs 177
and indirectly, the likely time of parasite transmission. Most of the very short burrow 178
occupancies were focused in the spring months of October and November in each 179
season, when mating occurs. This spring peak in movements is consistent with the 180
pitfall trapping records by Schofield et al (2012), a paternity study by Schofield et al 181
8
(2014), and a study recording when males visit females in burrows (Ebrahimi et al, 182
2015). Thus males, at least, are likely to focus the timing of dispersal away from 183
occupied burrows in the spring, as our current results indicate.
184
Third our study showed that more females than males tend to be long term 185
burrow residents, consistent with lower rates of capture of females in pitfall traps 186
(Schofield et al, 2012). Males that have moved to find a mating partner, may either not 187
be able to relocate their original burrow, or may get predated during their on ground 188
movements before they can get back to their original burrow. Established females 189
appear to pheromonally advertise their burrow location during the mating seasons 190
(Ebrahimi et al, 2015). Successfully mated females may stay in same burrows to 191
increase their chance of further mating.
192
A fourth and major result from the current study was the substantial number of 193
lizards that maintained residence in the same burrows for at least two full seasons. It is 194
possible that many of the 26 lizards that we recorded as long term residents had already 195
occupied the same burrows for one or more years before the filming started, or that they 196
continued to occupy those burrows after it stopped. Long term residence of burrow 197
refuges is consistent with the previous suggestion that there is a shortage of high 198
quality, deep burrows (Fellows et al, 2009) and with the previously observed vigorous 199
burrow defence by burrow occupiers against approaching conspecifics (Fenner and 200
Bull, 2011). In our study some resident lizards were lost from one autumn to the next 201
spring. These lizards may have died over the winter. One probable cause of mortality 202
was by drowning as a result of burrows becoming inundated during high winter 203
rainfall (Ebrahimi et al, 2012), or they may have moved late in one season or early in 204
the next season to find a new burrow.
205
Conservation implications 206
9
This study highlights a number of implications for the conservation management 207
of this endangered lizard species. First, within established populations we should expect 208
a relatively stable spatial structure of long-term resident adult lizards with some 209
dispersers from neighbouring locations available to replace any mortality losses.
210
Second, the study emphasises the importance of burrows as a major resource for the 211
lizards. Since they do not dig burrows themselves, maintenance of burrows within 212
population sites should be a high priority. A critical link for the management of pygmy 213
bluetongue lizard populations will be to maintain the spiders that build the burrows. We 214
know little about processes that might threaten the spiders, and currently no protective 215
measures for spiders are in place. Human intervention to construct artificial burrows is 216
possible (Souter et al, 2004), but will be very expensive in time and effort to maintain 217
over the periods required for the long term persistence of this species. It would be better 218
to rely on the natural burrow diggers that can sustain this service over much longer 219
periods of time. The management of grazing by domestic stock is a significant issue 220
that needs to be considered in terms of conserving such sites. Although grazing reduces 221
grass cover to allow lizards easier access to prey (Pettigrew and Bull, 2014), the 222
accompanying trampling and potential burrow destruction need to be monitored and 223
minimised. A third implication relates to the possible use of relocations as a longer term 224
strategy to maintain the species under predicted climate changes (Fordham et al, 2012).
225
An essential component of any relocation program will be to provide adequate 226
abundances of natural or artificial burrow refuges, to encourage individuals to remain 227
close to where they are released (Ebrahimi and Bull, 2014), and to take up long-term 228
residence as lizards do in their natural populations.
229
Acknowledgements 230
10
This research was funded by a grant from the Australian Research Council. We thank 231
the Nature Foundation of South Australia for access to their “Tiliqua” property, and 232
Dale Burzacott for logistic support with the camera set up.
233
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Fig 1. Records of occupancy of burrows by adult pygmy bluetongue lizards over two 332
complete field seasons.
333
