1 How do goannas find sea turtle nests?
2 Juan Lei 1,* and David T. Booth1
3 1 School of Biological Science, The University of Queensland, Brisbane, St. Lucia, QLD 4072,
4 Australia
5 * Corresponding author. Email: [email protected]
6 Phone: 0411565518
7 Address: School of Biological Science, The University of Queensland, Brisbane, St. Lucia,
8 QLD 4072, Australia
9
10 Acknowledgements
11 This work was supported by a grant from the Nest to Oceans Turtle Protection Program, a
12 program jointly funded by the Australian and Queensland Governments and would not have
13 been possible without the help of Nev and Bev McLachlan’s Turtle Care Volunteers
14 organization, the Burnett Mary Regional Group and WWF Australia. All work was approved
15 by a University of Queensland Animal Ethics Committee (permit #SBS/352/EHP/URG) and
16 conducted under Queensland Government scientific permit # WITK15315614. Author Manuscript
This is the author manuscript accepted for publication and has undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as doi: 10.1111/AEC.12568
This article is protected by copyright. All rights reserved
1
2 MR. JUAN LEI (Orcid ID : 0000-0002-4324-7500)
3
4
5 Article type : Original Article
6
7
8 How do goannas find sea turtle nests?
9
10 Abstract
11 Squamate reptiles rely heavily on visual and chemical cues to detect their prey, so we
12 expected yellow spotted goannas (Varanus panoptes) which are predators of sea turtle nests
13 on mainland beaches in northern Australia would use these cues to find sea turtle nests. Ghost
14 crabs (Ocypode ceratophthalmus and Ocypode cordimanus) are also common on Australian
15 sea turtle nesting beaches and frequently burrow into sea turtle nests. However, the potential
16 for ghost crab burrowing activity at sea turtle nests to signal the location of a nest to goannas
17 has not been investigated. Here we used camera traps and presence of tracks at nests to record
18 goanna activity around selected nests during the incubation period and 10 days after hatchling
19 turtles emerged from their nests. We also recorded the number of ghost crab burrows around
20 nests to evaluate ghost crab activity. Our results indicated that nest discovery by goannas was
21 independent of nest age, but that the nest visitation rate of goannas and crabs increased
22 significantly after a nest had been opened by a goanna or after hatchlings had emerged from
23 the nest. There was no apparent connection between ghost crab burrows into a nest and the
24 likelihood of that nest being predated by goannas.
25
26 Keywords Yellow-spotted goanna; Ghost crab; Sea turtle nest; Predation
27 Author Manuscript
28
29
30 Introduction
This article is protected by copyright. All rights reserved
31 Understanding interspecific relationships is an important part of ecological research,
32 particularly relationships between predators and prey, and interactions between predators that
33 prey on the same species (Krebs 1972). When different predators prey on the same species,
34 one predator species may provide a cue signaling the location of prey to the other predator
35 species, particularly when food sources become sparse (Hebshi et al. 2008). For example,
36 some scavenging mammals such as hyaenas (subfamily Hyaeninae) watch the activities of
37 vultures (family Accipitridae) and run towards the areas where they see vultures descending
38 and then take over the carcass (Houston 1974). In another example, human hunters follow
39 honey-guide birds (genus Prodotiscus) to locate and open beehives (Spottiswoode et al. 2016).
40 However, we do not know of any studies describing this signaling phenomenon between
41 different predators that involves reptiles.
42
43 Prey detection by lizards has been extensively studied (Nicoletto 1985; Vitt and Cooper 1986;
44 Cooper 1989; Cooper 1994; Cooper et al. 2000; Hoare et al. 2007; Martin 2010) and the
45 major senses used to detect prey are visual and olfactory (William & Cooper 1989). In
46 diurnally active insectivorous species, movement by prey is the major way in which prey are
47 detected (Burghardt 1964; Cooper 1981; Nicoletto 1985). However, olfaction can also be
48 important, particularly in species that hunt ‘hidden prey’ buried in leaf litter or soil which are 49 not visible to a lizard moving along the substrate’s surface (Milstead 1957; Pianka 1970; 50 Mitchell 1979; Vitt & Cooper 1986).
51
52 Autarchoglossan lizards such as Anguidae, Lacertidae, Teiidae, Scincidae and Varanidae have
53 a well-developed olfactory sensory system that is used in prey detection (Burghardt 1973;
54 Auffenberg 1981). Teiidae and Varanidae lizards have slender forked tongues which are
55 flicked in and out of the mouth to sample chemical cues which are transferred to the
56 specialized chemosensitive Jacobson’s organ located in the roof of the mouth which
57 completes a vomeronasalAuthor Manuscript olfactory system (Vitt & Cooper 1986; Cooper 1994; Cooper et al.
58 2000). Some of these lizards are able to locate buried prey by using this system to detect prey
59 odors emanating through the substrate (Bogert & Del Campo 1956; Auffenberg 1984; Vitt &
60 Cooper 1986). Varanid lizards are active foragers and adept at detecting olfactory cues using
This article is protected by copyright. All rights reserved
61 their vomeronasal olfactory system (Blamires & Guinea 1998; King & Green 1999; Vincent
62 & Wilson 1999) and presumably use this system to locate hidden prey. For example, varanid
63 lizards can be voracious predators of sea turtle eggs which are buried 20-80 cm below the soil
64 surface (Blamires 2004; Maulany 2012).
65
66 At Wreck Rock beach in southeastern Queensland, Australia, a varanid lizard, the
67 yellow-spotted goanna (Varanus panoptes), is the most common predator of loggerhead turtle
68 (Caretta caretta) nests when introduced red fox (Vulpes vulpes) predation is controlled (Lei &
69 Booth 2017a). Nests can be detected and attacked by goannas at any time during the
70 incubation period (Lei & Booth 2017a). At sea turtle nesting beaches, yellow-spotted goannas
71 also consume ghost crabs (Ocypode spp.) (Blamires 2004). Ghost crabs are the most common
72 crabs found on tropical and semitropical ‘ocean-exposed’ sandy beaches and are considered a
73 significant predator of sea turtle nests (Le Buff 1990; Thompson 1995; Witherington 1999;
74 Trocini et al. 2009). They are important bioturbators of beaches and form an important
75 ecological link in the food webs of seashore ecosystems (Lucrezi & Schlacher 2014).
76 Although several studies have reported that ghost crabs burrow into and predate sea turtle
77 nests (Le Buff 1990; Thompson 1995; Witherington 1999; Trocini et al. 2009), there is no
78 information about the connections, if any, between these decapods and other sea turtle nest
79 predators.
80
81 When burrowing into sea turtle nests, ghost crabs may release odors from the eggs or
82 hatchlings in the nest to the atmosphere and thus attract the attention of predators such as
83 goannas that use olfaction to track down potential food sources. Alternatively, goannas that
84 predate ghost crabs by digging up their burrows may fortuitously discover a sea turtle nest if
85 the ghost crab burrow is associated with a nest. In these ways ghost crabs may signal the
86 location of sea turtle nests to goannas. Author Manuscript 87
88 In the current study we were interested in discovering when and how yellow-spotted goannas
89 find sea turtle nests and tested three hypotheses. First, we hypothesized that the rate of goanna
This article is protected by copyright. All rights reserved
90 predation on sea turtle nests would increase as the nesting season progressed because as the
91 number of nests increases more goannas in the area would become aware that this seasonal
92 food source has become available. This hypothesis would be refuted if the nest predation rate
93 remained constant throughout the sea turtle nesting season. Second, we hypothesized
94 predation of nests would be greatest immediately after nests are constructed or after nests
95 have hatched but hatchlings are yet to escape the nest because cues (visual and olfactory at
96 nest construction, and olfactory at the end of incubation) are most obvious at these times. This
97 hypothesis would be refuted if goanna nest predation rate does not change with the time since
98 the nest was constructed. Third, we hypothesized that ghost crabs burrowing into sea turtle
99 nests could alert goannas to a nest’s location. This hypothesis would be refuted if there is no 100 clear relationship between when a ghost crab burrows into a nest, and if and when that nest is
101 predated by a goanna.
102
103 Methods
104 Study site and nest monitoring
105 This study was conducted along the beach for 2 km to the north and south of Wreck Rock at
106 Deepwater National Park, Southeast Queensland (24°18’ 58” S, 151°57’ 55” E) (Fig. 1a). The 107 beach was monitored nightly by personnel from Turtle Care Volunteers Queensland Inc. who
108 recorded the location of freshly constructed loggerhead turtle nests using a handheld GPS
109 (Garmin eTrex 30, Kansas, USA).
110
111 Once a nest was located it was visited daily throughout the incubation period and at each visit
112 the presence of goanna tracks and ghost crab burrows on top of it recorded. If a nest was
113 predated by goannas, nest monitoring continued until 10 days after the predation event. Nest
114 visitation rate by goannas and burrow activity of ghost crabs was quantified by dividing the
115 number of days fresh tracks/borrows were found at a nest by the total number of nest
116 inspection days (nestAuthor Manuscript inspection days = total number of times a nest was inspected during the
117 season until hatchlings emerged from the nest or 10 days after the nest was predated).
118
119 Camera traps
This article is protected by copyright. All rights reserved
120 Camera traps (Reconyx Hyperfire HC600, Holmen, Wisconsin, USA) were set up to capture
121 images of predators visiting a sub-sample of monitored nests for a period of 30 days after a
122 nest was constructed and for 10 days after the first hatchlings had left a nest. All camera traps
123 were triggered by motion sensors, could be triggered 24 h per day and were set to take three
124 still images within 5 seconds when triggered by the motion sensor. Camera traps were
125 positioned 50 cm behind the selected turtle nests, at least 30 cm above ground. Each camera
126 trap had a 1 m2 field of view over the nest insuring that any nest visitation by predators was
127 recorded. This enabled information on the frequency of predator visits, time of day of
128 predator visits and the species of predator to be collected. To compare the relative activity of
129 goannas visiting nests before hatching and after hatching, we quantified nest visitation rate for
130 camera trap monitored nests by calculating the ratio of independent images (images taken at
131 least 20 minutes apart from each other) of goannas recorded at nests to the number of camera
132 trap days.
133
134 Data are reported as means ± SE, and statistical comparisons were made using Students
135 T-tests assuming significance if P<0.05.
136
137 Results
138 Nest monitoring
139 During the 2014-2015 nesting season (05-Dec-2014 until 28-Feb-2015), 52 loggerhead turtle
140 nests were monitored and 57.7% of these nests were predated by goannas as indicated by
141 goanna burrows dug into the nest egg chamber. During the 2015-2016 nesting season
142 (07-Dec-2015 until 28-Feb-2016), 46 nests were monitored and 17.4% of these nests were
143 predated by goannas. Ten predated nests were monitored for 10 days after the predation event
144 during the 2014-2015 season and 8 predated nests were monitored during the 2015-2016
145 season.
146 Author Manuscript
147 Goanna tracks at nests
148 The goanna visitation rate in undisturbed nests (i.e. before they were predated by goannas or
149 hatched) averaged 0.13 tracks per nest per day but the visitation rate increased 3-fold (P <
This article is protected by copyright. All rights reserved
150 0.01) to 0.40 tracks per nest per day once a nest had been opened by a goanna (Fig. 2a).
151 Goanna nest predation rate did not change during the monitored period, i.e. the number of
152 nests predated for the first time on any particular day did not change between December and
153 March (Fig 3a). Goanna predation activities occurred at all stages of the incubation period,
154 with no particular stage experiencing higher rates of predation (Fig 3b).
155
156 Ghost crab burrows at nests
157 The ghost crab burrow appearance rate at undisturbed nests averaged 0.21 burrows per nest
158 per day but the burrow appearance rate increased 4-fold (P = 0.05) to 0.81 burrows per nest
159 per day once a nest had been open by a goanna (Fig. 2b). All of the goanna predated nests had
160 ghost crabs burrow into them (from one to 19 burrows) before they were predated by goannas
161 and these ghost crab burrows appeared between one and 56 days before the goanna predation
162 event. Only four out of 38 predated nests had ghost crabs burrow into them the day before the
163 goanna predation event. Non-goanna predated nests also had ghost crabs burrow into them
164 (from 0 to 38) before hatchlings emerged.
165
166 Camera traps
167 A sample of 13 non-predated loggerhead turtle nests were monitored by camera traps in the
168 second nesting season (between 01-Dec-2015 and 27-Feb-2016). Images from camera traps
169 showed that two goanna species, yellow-spotted goannas and lace monitors (V. varius) visited
170 nests. The visitation rate of these two species increased significantly (yellow-spotted goanna
171 P<0.01; lace monitor P=0.03) after the first hatchlings had left a nest (Fig 4). Before predation
172 visitation rate of yellow-spotted goannas (0.05 visits per nest per day) and lace monitors (0.02
173 visits per nest per day) was similar (P=0.12), while after hatching visitation rate by
174 yellow-spotted goannas (0.26 visits per nest per day) were higher than the lace monitor (after:
175 0.07 visits per nest per day P<0.01). Yellow-spotted goannas were seen to open nests, but lace
176 monitors were neverAuthor Manuscript seen to open nests. Nine of 13 (69%) hatched turtle nests were dug into
177 by yellow-spotted goannas, and three of these nests were also visited by lace monitors.
178 Although lace monitors visited hatched nests before these nests had been dug into by
179 yellow-spotted goanna, lace monitors were never observed to dig out a nest.
This article is protected by copyright. All rights reserved
180
181 Discussion
182 There were three significant findings from our study. First, goanna predation rate on sea turtle
183 nests did not increase with time as nests were laid. Second, the likelihood of a nest being
184 predated by goannas was independent of the age of the nest. Third, ghost crabs burrows do
185 not appear to assist goannas to locate sea turtle nests.
186
187 Timing of goanna predation of sea turtle nests
188 Our observations indicated that the frequency of goanna attacks on sea turtle nests did not
189 increase as the nesting season progressed and the number of sea turtle nests incubating
190 increased. This suggests that the number of goannas predating nests remained stable, and that
191 these goannas did not increase the intake of sea turtle eggs in their diet from the beginning to
192 end of the sea turtle nesting season. Only large male yellow-spotted goannas opened nests,
193 and these individuals may exclude others from the beach potentially limiting the number of
194 goannas able to forage on the beach (Lei & Booth 2017b) and this may explain why nest
195 predation rate did not increase as the sea turtle nesting season progressed.
196
197 The finding that the likelihood of a nest being attacked by a goanna was independent of nest
198 age was surprising. We expected two peaks in nest predation. The first peak was expected
199 immediately after a clutch was laid because goannas could use sand disturbance associated
200 with nest construction as a visual cue and olfactory cues left in the sand by female turtles to
201 locate nests. The second peak was expected just before hatchling nest emergence once the
202 embryos had hatched from their eggs and released egg fluids, the odor of which might be
203 detectable on the sand surface that could attract goannas. Furthermore, the observation that
204 goannas could crawl over the top of nests numerous times over several weeks before suddenly
205 attacking the nest is puzzling because the cue(s) used to the detect the nest after the first week
206 of incubation are mostAuthor Manuscript likely to be olfactory in nature, and logic implies that such cues would
207 have been present since the nest was constructed. This lead us to hypothesize that other cues
208 such as the appearance of ghost crab burrows into a nest may signal the presence of a nest to
209 goannas.
This article is protected by copyright. All rights reserved
210
211 The interaction between yellow-spotted goannas and ghost crabs
212 Ghost crabs regularly burrow into sea turtle nests and are known to eat eggs and hatchlings
213 (Le Buff 1990; Thompson 1995; Witherington 1999; Trocini et al. 2009). Such burrow
214 construction may alert the location of sea turtle nests to goannas by two mechanisms. First,
215 the burrow into the nest could facilitate the release of odors from the incubating eggs into the
216 atmosphere above the nest and thus attracted a goanna’s attention. Second, because on 217 numerous occasions we observed yellow-spotted goannas feeding on ghost crabs by digging
218 them out of their burrows, a yellow-spotted goanna may fortuitously discover a sea turtle nest
219 while digging out a ghost crab if the ghost grab burrow was constructed into a nest. However,
220 our observations do not support a close association between the appearance of ghost crab
221 burrows into a sea turtle nest and the subsequent predation of that nest by goannas. Although
222 numerous ghost crab burrow entrances were observed above sea turtle nests, these burrows
223 appeared anywhere between one and 56 days before the nest was predated by a goanna, and
224 further, numerous other nests had ghost crab burrows constructed into them without being
225 attacked by goannas. Indeed, in only four of the 38 goanna predated nests we monitored did a
226 ghost crab burrow appear the day before the goanna predation event. Taken together, these
227 observations indicate that ghost crabs burrows into sea turtle nests do not lead to the
228 discovery of the nest by goannas.
229
230 The influence of predated and hatched turtle nest on goanna activity at nests.
231 Our data show that goanna predation activities occurred at all stages of the incubation period
232 with no peaks at the beginning or end of incubation. However, turtle nests were visited more
233 often and material (eggs, egg remains after hatching) taken from the nest once a nest was
234 opened or hatched, indicating that goannas were attracted to the odor of the opened nest,
235 and/or the visual cue of the open hole at the nest site. Goannas probably also remember the
236 location of these nestsAuthor Manuscript which allows them to visit the same nest numerous time on subsequent
237 days to access the food source (Ward-Fear et al. 2016). Curiously, some goanna predated
238 nests did not have all of their eggs consumed even though they were visited on multiple
239 occasions over several days, and these nests managed to produce some hatchlings (Lei &
This article is protected by copyright. All rights reserved
240 Booth 2017c). The reason why not all eggs were consumed remains a mystery. At a single
241 visit a goanna may become sated after eating several eggs and these eggs may take a day or
242 two to digest, but given that predated nests were generally visited over multiple days, satiation
243 does not appear to be an explanation for this phenomenon.
244
245 Ghost crab burrows were numerous all over the beach dune area and we did not assess if
246 burrow density above a nest in undisturbed nests was greater than burrow density in adjacent
247 areas where no nest existed. A future study should address this point because it is of interest to
248 know if ghost crabs actively seek out sea turtle nests in order to prey on eggs and hatchlings,
249 or discover sea turtle nests by accident as they randomly construct burrows into the sand. The
250 facts that (1) numerous studies have reported ghost crabs predating eggs and hatchlings within
251 nests (Le Buff 1990; Thompson 1995; Witherington 1999; Trocini et al. 2009) and (2) the
252 current study’s observation that ghost crab burrowing activity at sea turtle nests increase when 253 nests have been opened by a goannas suggest ghost crabs actively seek out sea turtle nests and
254 that they may use olfactory cues to aid them in this task.
255
256 Conclusion
257 We set out to test three hypotheses about how and when yellow-spotted goannas discover sea
258 turtle nests and the evidence we collected during our study does not support any of these
259 hypotheses. First, we hypothesized that the rate of goanna predation on sea turtle nests would
260 increase as the nesting season progressed as more nests became available for predation, but
261 we found the daily number of nests attached was constant throughout the nesting season.
262 Second, we hypothesized predation of nests would be greatest immediately after nests are
263 constructed or after nests have hatched but hatchlings, but we found the likelihood of a sea
264 turtle nest being depredated was independent of nest age. Third, we hypothesized that ghost
265 crabs burrowing into sea turtle nests could alert goannas to a nest’s location, but we found no
266 evidence of a relationshipAuthor Manuscript between ghost crab burrowing activity at nests and the likelihood of
267 goanna nest predation. Hence, we do not know the mechanism used by goannas to find sea
268 turtle nests, particularly those nests that are attacked during middle or late incubation that
269 have been crawled over numerous times earlier on in incubation by goannas before they were
This article is protected by copyright. All rights reserved
270 attacked. Clearly, more work needs to be done to discover that cues goannas and for that
271 matter, ghost crabs, use to find sea turtle nests. We still think the most likely cues will be
272 olfactory in nature, and perhaps the next experimental step might be to bury eggs at different
273 depths below the sand surface to see if goannas and ghost crabs find shallowly buried eggs
274 more easily than deeper buried eggs.
275
276 References
277 Auffenberg W. (1981) The behavioral ecology of the Komodo monitor. University of Florida
278 Press, Gainesville, Florida.
279
280 Auffenberg W. (1984) Notes on feeding behaviour of Varanus bengalensis (Sauria: Varanidae).
281 J Bombay Nat Hist Soc. 80, 286-302.
282
283 Blamires S. J. & Guinea M. L. (1998) Implications of nest site selection on egg predation at
284 the sea turtle rookery at Fog Bay. In: Proceedings of Marine Turtle Conservation and
285 Management in Northern Australia Workshop. (eds R. Kennett, A. Webb, G. Duff, M. L.
286 Guinea, G. J. E. Hill) pp. 20-24. Darwin, Australia.
287
288 Blamires S. J. (2004) Habitat Preferences of Coastal Goannas (Varanus panoptes): Are They
289 Exploiters of Sea Turtle Nests at Fog Bay, Australia? Copeia. 2, 370-377.
290
291 Bogert C. M. & Campo MDel. (1956) The gila monster and its allies: the relationships, habits,
292 and behavior of the lizards of the family Helodermatidae. Bull. Am Mus Nat Hist. 109, 1-238.
293
294 Burghardt G. M. (1964) Effects of prey size and movement on the feeding behavior of the
295 lizards Anolis carolinensis and Eumneces fasciatus. Copeia. 1964, 576-578.
296 Author Manuscript
297 Burghardt G. (1973) Chemical release of prey attack: extension to naive newly hatched
298 lizards, Eumeces fasciatus. Copeia. 1973, 178-181.
299
This article is protected by copyright. All rights reserved
300 Cooper WEJr. (1981) Visual guidance of predatory attack by a scincid lizard, Eumeces
301 laticeps. Anim Behav. 29, 1127-1136.
302
303 Cooper WEJr. (1989) Absence of prey odor discrimination by iguanid and agamid lizards in
304 applicator tests. Copeia. 1989, 472–478. 305
306 Cooper WEJr. (1994) Chemical discrimination by tongue-flicking in lizards: a review with
307 hypothesis on its origin and its ecological and phylogenetic relationships. J Chem Ecol. 20,
308 439–487. 309
310 Cooper WEJr., Paulissen M. A. & Habegger J. J. (2000) Discrimination of prey, but not plant,
311 chemicals by actively foraging, insectivorous lizards, the lacertid Takydromus sexlineatus and
312 the teiid Cnemidophorus gularis. J Chem Ecol. 26, 1623–1634. 313
314 Hebshi A. J, Duffy D. C & Hyrenbach K. D. (2008) Associations between seabirds and
315 subsurface predators around Oahu, Hawaii. Aquat Biol. 4, 89-98.
316
317 Hoare J. M, Pledger S. & Nelson N. J. (2007) Chemical discrimination of food, conspecifics
318 and predators by apparently visually oriented diurnal geckos, Naultinus manukanus.
319 Herpetologica. 63. 184–192. 320
321 Houston D. C. (1974) Food searching in griffon vultures. Afr J Ecol. 12, 63-77.
322
323 Krebs C. J. (1972) Ecology: the experimental analysis of distribution and abundance. Harper
324 and Row, New York.
325
326 King D. & Green Author Manuscript B. (1999) Monitor: the biology of varanid lizards. NSW University Press,
327 Sydney.
328
329 Le Buff CRJr. (1990) The Loggerhead Turtle in the Eastern Gulf of Mexico. Caretta Research,
This article is protected by copyright. All rights reserved
330 Inc, Sanibel, Florida.
331
332 Lei J. & Booth D. T. (2017a) Who are the important predators of sea turtle nests at Wreck
333 Rock beach? PeerJ. 5:e3515; DOI 10.7717/peerj.3515.
334
335 Lei J. & Booth D. T. (2017b) Spatial ecology of yellow-spotted goannas adjacent to a sea
336 turtle nesting beach. Aust J Zool. http://dx.doi.org/10.1071/ZO17006
337
338 Lei J. & Booth D. T. (2017c) How best to protect the nests of the endangered loggerhead
339 turtle Caretta caretta from monitor lizard predation? Chelonian Conserv Biol (in press)
340
341 Lucrezi S. & Schlacher T. A. (2014) The ecology of ghost crabs. Oceanogr Mar Biol Annu
342 Rev. 52, 201–256. 343
344 Maulany R. I. (2012) The Nesting Biology, Ecology, and Management of the Olive Ridley
345 Turtle (Lepidochelys olivacea) in Alas Purwo National Park, Banyuwangi (East Java),
346 Indonesia. A thesis submitted for the degree of Doctor of Philosophy, The University of
347 Queensland, Australia
348
349 Martin J. & Lopez P. (2010) Condition-dependent pheromone signaling by male rock lizards:
350 more oily scents are more attractive. Chem Senses. 35, 253–262. 351
352 Milstead W. W. (1957) Some aspects of competition in natural populations of whiptail lizards
353 (genus Cnemidophorus). Texas J Sci. 9, 410- 447.
354
355 Mitchell J. C. (1979) Ecology of southeastern Arizona whiptail lizards (Cnemidophorus:
356 Teiidae): populationAuthor Manuscript densities, resource partitioning, and niche overlap. Can J Zool. 57,
357 1487-1499.
358
359 Nicoletto P. F. (1985) The relative roles of vision and olfaction in prey detection by the
This article is protected by copyright. All rights reserved
360 ground skink, Scincella lateralis. J Herpetol. 19, 411–415. 361
362 Pianka E. R. (1970) Sympatry of desert lizards (Ctenotus) in western Australia. Ecology 50,
363 1012-1030.
364
365 Spottiswoode C. N., Begg K. S. & Begg C. M. (2016) Reciprocal signaling in
366 honeyguide-human mutualism. Science. 353, 387–389. 367
368 Thompson M. S. (1995) The effect of ghost crab predation on the survival rate of loggerhead
369 sea turtle eggs. In: Proceedings of the 15th Annual Symposium on Sea Turtle Biology and
370 Conservation (eds D. A. Keinath, D. E. Barnard, J. A. Musick, B. A. Bell) pp. 323–324. 371 NOAA Technical Memo. NMFS-SEFSC-387.
372
373 Trocini S, Robertson I. & Bradley S. (2009). Crime scene investigation on a loggerhead turtle
374 nesting beach: who ate the eggs? In: Proceedings of the 29th Annual Symposium on Sea Turtle
375 Biology and Conservation. International Sea Turtle Society, Brisbane, Australia
376
377 Vincent M. & Wilson S. (1999) Australian goannas. New Holland Publishers Pty Ltd,
378 Sydney, NSW.
379
380 Vitt L. J. & Cooper WEJr. (19860 Foraging and diet of a diurnal predator (Eumeces laticeps)
381 feeding on hidden prey. J Herpetol. 20, 408–415. 382
383 Ward-Fear G., Pearson D. J., Brown G. P., Balanggarra Rangers, & Shine R. (2016)
384 Ecological immunization: in situ training of free-ranging predatory lizards reduces their
385 vulnerability to invasive toxic prey. Bio Lett. 12, 20150863.
386 Author Manuscript
387 William E. & Cooper, Jr. (1989) Absence of prey odor discrimination by iguanid and agamid
388 lizards in applicator tests. Copeia. 2, 472-478.
389
This article is protected by copyright. All rights reserved
390 Witherington B. E. (1999) Reducing threats to nesting habitat. In: Research and Management
391 Techniques for the Conservation of Sea Turtles (eds K. L Eckert, K. A Bjorndal, F. A
392 Abreu-Grobois, M. Donelly) pp. 179–183. IUCN/SSC Marine Turtle Specialist Group 393 Publication 4.
394
395 Figure 1. Location of study site, Wreck Rock beach in Deepwater National Park, Queensland,
396 Australia. Shaded grey area indicates the section of beach monitored in this study. The
397 locations of loggerhead turtle nests that were predated are indicated by diamonds, and
398 non-predated nests are indicated by triangles. The data for both nesting seasons (2014-2015
399 and 2015-2016) are combined.
400
401 Figure 2. a. Whisker-box plot of the number of ghost crab burrows appearing in loggerhead
402 turtle nests (n=18) before and after the nest was opened by a goanna or the nest had had some
403 hatchlings escape from it. b. Whisker-box plot of the number of goanna tracks appearing on
404 top of loggerhead turtle nests (n=18) before and after the nest was opened by a goanna or the
405 nest had had some hatchlings escape from it. Dots = data range, Whiskers = 10% & 90%
406 percentiles, Boxes = 25% & 75% percentiles, Horizontal line within box = median.
407
408 Figure 3. a. The nest predation during the 2014-2015 (diamonds) and 2015-2016 (triangles)
409 seasons. b. Days between laying and first predation event from the 2014-2015 (diamonds) and
410 2015-2016 (triangles) seasons.
411
412 Figure 4. Whisker-box plot of the number of goanna visits as recorded by camera traps to
413 loggerhead turtle nests (n=13) before and after the nest was opened by a goanna or the nest
414 had had some hatchlings escape from it. Yellow = yellow spotted goanna, Lace = lace
415 monitor. Dots = data range, Whiskers = 10% & 90% percentiles, Boxes = 25% & 75%
416 percentiles, HorizontalAuthor Manuscript line within box = median. The range = 90% percentile in cases where
417 dots are absent from plots.
This article is protected by copyright. All rights reserved 145º 150º -10º a b Road
-15º Coral Sea Coral Sea
Cairns
-20º Townsville Wreck Rock
Study site -25º
Brisbane
-30º
N
Sydney 1 km
aec_12568_f1.eps Author Manuscript
This article is protected by copyright. All rights reserved 1.4
1.2 a ay
d 1.0
0.8 0.6
0.4 0.2
Tracks per nest Tracks per 0.0
Before After
5 b 4
3
2 Author Manuscript 1
0 Burrows Burrows per nest per day
This article is protected by copyright. All rights reserved Before After
aec_12568_f2.eps aec_12568_f3.eps Author Manuscript
This article is protected by copyright. All rights reserved 0.7
0.6
0.5
0.4
0.3
0.2
0.1 Visits per nestVisits per day 0.0
Yellow before Yellow after Lace before Lace after
aec_12568_f4.eps Author Manuscript
This article is protected by copyright. All rights reserved