How Do Goannas Find Sea Turtle Nests?

Austral Ecology (2017) , – How do goannas ﬁnd sea turtle nests?

JUAN LEI* AND DAVID T. BOOTH School of Biological Science, The University of Queensland, Brisbane, St. Lucia, Queensland 4072, Australia (Email: [email protected])

Abstract Squamate reptiles rely heavily on visual and chemical cues to detect their prey, so we expected yellow-spotted goannas (Varanus panoptes) which are predators of sea turtle nests on mainland beaches in northern Australia would use these cues to ﬁnd sea turtle nests. Ghost crabs (Ocypode ceratophthalmus and Ocypode cordimanus) are also common on Australian sea turtle nesting beaches and frequently burrow into sea turtle nests. However, the potential for ghost crab burrowing activity at sea turtle nests to signal the location of a nest to goannas has not been investigated. Here, we used camera traps and presence of tracks at nests to record goanna activity around selected nests during the incubation period and 10 days after hatchling turtles emerged from their nests. We also recorded the number of ghost crab burrows around nests to evaluate ghost crab activity. Our results indicated that nest discovery by goannas was independent of nest age, but that the nest visitation rate of goannas and crabs increased signiﬁcantly after a nest had been opened by a goanna or after hatchlings had emerged from the nest. There was no apparent connection between ghost crab burrows into a nest and the likelihood of that nest being predated by goannas.

Key words: ghost crab, predation, sea turtle nest, yellow-spotted goanna.

INTRODUCTION is are detected (Burghardt 1964; Cooper 1981; Nico- letto 1985). However, olfaction can also be impor- Understanding interspeciﬁc relationships is an tant, particularly in species that hunt ‘hidden prey’ important part of ecological research, particularly buried in leaf litter or soil which are not visible to a relationships between predators and prey, and inter- lizard moving along the substrate’s surface (Milstead actions between predators that prey on the same 1957; Pianka 1970; Mitchell 1979; Vitt & Cooper species (Krebs 1972). When different predators 1986). prey on the same species, one predator species may Autarchoglossan lizards such as Anguidae, Lacer- provide a cue signalling the location of prey to the tidae, Teiidae, Scincidae and Varanidae have a well- other predator species, particularly when food developed olfactory sensory system that is used in sources become sparse (Hebshi et al. 2008). For prey detection (Burghardt 1973; Auffenberg 1981). example, some scavenging mammals such as hyae- Teiidae and Varanidae lizards have slender forked nas (subfamily Hyaeninae) watch the activities of tongues which are ﬂicked in and out of the mouth to vultures (family Accipitridae) and run towards the sample chemical cues which are transferred to the areas where they see vultures descending and then specialized chemosensitive Jacobson’s organ located take over the carcass (Houston 1974). In another in the roof of the mouth which completes a vomero- example, human hunters follow honeyguide birds nasal olfactory system (Vitt & Cooper 1986; Cooper (genus Prodotiscus) to locate and open beehives 1994; Cooper et al. 2000). Some of these lizards are (Spottiswoode et al. 2016). However, we do not able to locate buried prey using this system to detect know of any studies describing this signalling phe- prey odours emanating through the substrate (Bogert nomenon between different predators that involves & Martın del Campo 1956; Auffenberg 1984; Vitt & reptiles. Cooper 1986). Varanid lizards are active foragers and Prey detection by lizards has been extensively stud- adept at detecting olfactory cues using their vomero- ied (Nicoletto 1985; Vitt & Cooper 1986; Cooper nasal olfactory system (Blamires & Guinea 1998; 1989a,b; Cooper 1994; Cooper et al. 2000; Hoare King & Green 1999; Vincent & Wilson 1999) and et al. 2007; Martin & Lopez 2010), and the major presumably use this system to locate hidden prey. senses used to detect prey are visual and olfactory For example, varanid lizards can be voracious preda- (Cooper 1989a,b). In diurnally active insectivorous tors of sea turtle eggs which are buried 20–80 cm species, movement by prey is the major way in which below the soil surface (Blamires 2004; Maulany 2012). *Corresponding author. At Wreck Rock beach in south-eastern Queens- Accepted for publication November 2017. land, Australia, a varanid lizard, the yellow-spotted

© 2017 Ecological Society of Australia doi:10.1111/aec.12568 2 J.LEIANDD.T.BOOTH goanna (Varanus panoptes), is the most common METHODS predator of loggerhead turtle (Caretta caretta) nests when introduced red fox (Vulpes vulpes) predation is Study site and nest monitoring controlled (Lei & Booth 2017a). Nests can be detected and attacked by goannas at any time during This study was conducted along the beach for 2 km to the the incubation period (Lei & Booth 2017a). At sea north and south of Wreck Rock at Deepwater National turtle nesting beaches, yellow-spotted goannas also Park, south-eastern Queensland (24°18058″S, 151°57055″E) consume ghost crabs (Ocypode spp.) (Blamires 2004). (Fig. 1a). The beach was monitored nightly by personnel Ghost crabs are the most common crabs found on from Turtle Care Volunteers Queensland Inc. who tropical and semitropical ‘ocean-exposed’ sandy bea- recorded the location of freshly constructed loggerhead ches and are considered a significant predator of sea turtle nests using a hand-held GPS (Garmin eTrex 30, Kansas, USA). turtle nests (Le Buff 1990; Thompson 1995; Wither- Once a nest was located, it was visited daily throughout ington 1999; Trocini et al. 2009). They are impor- the incubation period, and at each visit, the presence of tant bioturbators of beaches and form an important goanna tracks and ghost crab burrows on top of it was ecological link in the food webs of seashore ecosys- recorded. If a nest was predated by goannas, nest monitor- tems (Lucrezi & Schlacher 2014). Although several ing continued until 10 days after the predation event. Nest studies have reported that ghost crabs burrow into visitation rate by goannas and burrow activity of ghost crabs and predate sea turtle nests (Le Buff 1990; Thomp- was quantified by dividing the number of days fresh tracks/ son 1995; Witherington 1999; Trocini et al. 2009), borrows were found at a nest by the total number of nest there is no information about the connections, if any, inspection days (nest inspection days = total number of between these decapods and other sea turtle nest times a nest was inspected during the season until hatch- predators. lings emerged from the nest or 10 days after the nest was predated). When burrowing into sea turtle nests, ghost crabs may release odours from the eggs or hatchlings in the nest to the atmosphere and thus attract the attention of predators such as goannas that use olfaction to Camera traps track down potential food sources. Alternatively, fi goannas that predate ghost crabs by digging up their Camera traps (Reconyx Hyper re HC600; Holmen, Wis- burrows may fortuitously discover a sea turtle nest if consin, USA) were set up to capture images of predators visiting a subsample of monitored nests for a period of the ghost crab burrow is associated with a nest. In 30 days after a nest was constructed and for 10 days after these ways, ghost crabs may signal the location of sea the first hatchlings had left a nest. All camera traps were turtle nests to goannas. triggered by motion sensors, could be triggered 24 h per In this study, we were interested in discovering day and were set to take three still images within 5 s when when and how yellow-spotted goannas find sea tur- triggered by the motion sensor. Camera traps were posi- tle nests and tested three hypotheses. First, we tioned 50 cm behind the selected turtle nests, at least hypothesized that the rate of goanna predation on 30 cm above-ground. Each camera trap had a 1 m2 field of sea turtle nests would increase as the nesting season view over the nest insuring that any nest visitation by progressed because as the number of nests predators was recorded. This enabled information on the increases, more goannas in the area would become frequency of predator visits, time of day of predator visits and the species of predator to be collected. To compare the aware that this seasonal food source has become relative activity of goannas visiting nests before hatching available. This hypothesis would be refuted if the and after hatching, we quantified nest visitation rate for nest predation rate remained constant throughout camera trap-monitored nests by calculating the ratio of the sea turtle nesting season. Second, we hypothe- independent images (images taken at least 20 min apart sized predation of nests would be greatest immedi- from each other) of goannas recorded at nests to the num- ately after nests are constructed or after nests have ber of camera trap days. hatched but hatchlings are yet to escape the nest Data are reported as means SE, and statistical com- because cues (visual and olfactory at nest construc- parisons were made using Students t-tests assuming signifi- tion, and olfactory at the end of incubation) are cance if P < 0.05. most obvious at these times. This hypothesis would be refuted if goanna nest predation rate does not change with the time since the nest was con- RESULTS structed. Third, we hypothesized that ghost crabs burrowing into sea turtle nests could alert goannas to a nest’s location. This hypothesis would be Nest monitoring refuted if there is no clear relationship between when a ghost crab burrows into a nest, and if and During the 2014–2015 nesting season (05- when that nest is predated by a goanna. December-2014 until 28-February-2015), 52 doi:10.1111/aec.12568 © 2017 Ecological Society of Australia GOANNAS FIND TURTLE NESTS 3

145º 150º -10º a b Road

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Study site -25º

Brisbane

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Sydney 1 km

Fig. 1. Location of study site, Wreck Rock beach in Deepwater National Park, Queensland, Australia. Shaded grey area indicates the section of beach monitored in this study. The locations of loggerhead turtle nests that were predated are indicated by diamonds, and nonpredated nests are indicated by triangles. The data for both nesting seasons (2014–2015 and 2015–2016) are combined. loggerhead turtle nests were monitored and Ghost crab burrows at nests 57.7% of these nests were predated by goannas as indicated by goanna burrows dug into the nest The ghost crab burrow appearance rate at undis- egg chamber. During the 2015–2016 nesting sea- turbed nests averaged 0.21 burrows per nest per day, son (07-December-2015 until 28-February-2016), but the burrow appearance rate increased fourfold 46 nests were monitored and 17.4% of these (P = 0.05) to 0.81 burrows per nest per day once a nests were predated by goannas. Ten predated nest had been open by a goanna (Fig. 2b). All of the nests were monitored for 10 days after the preda- goanna-predated nests had ghost crabs burrow into tion event during the 2014–2015 season, and them (from one to 19 burrows) before they were pre- eight predated nests were monitored during the dated by goannas, and these ghost crab burrows 2015–2016 season. appeared between one and 56 days before the goanna predation event. Only four of 38 predated nests had ghost crabs burrow into them the day before the Goanna tracks at nests goanna predation event. Nongoanna-predated nests also had ghost crabs burrow into them (from 0 to The goanna visitation rate in undisturbed nests (i.e. 38) before hatchlings emerged. before they were predated by goannas or hatched) averaged 0.13 tracks per nest per day, but the visitation rate increased threefold (P < 0.01) to 0.40 tracks Camera traps per nest per day once a nest had been opened by a goanna (Fig. 2a). Goanna nest predation rate did not A sample of 13 nonpredated loggerhead turtle nests change during the monitored period, that is the num- were monitored by camera traps in the second nesting ber of nests predated for the ﬁrst time on any partic- season (between 01-December-2015 and 27-Febru- ular day did not change between December and ary-2016). Images from camera traps showed that two March (Fig. 3a). Goanna predation activities goanna species, yellow-spotted goannas and lace mon- occurred at all stages of the incubation period, with itors (Varanus varius), visited nests. The visitation rate no particular stage experiencing higher rates of pre- of these two species increased signiﬁcantly (yellow- dation (Fig. 3b). spotted goanna P < 0.01; lace monitor P = 0.03) after

1.4 DISCUSSION 1.2 a There were three signiﬁcant ﬁndings from our study. 1.0 First, goanna predation rate on sea turtle nests did not increase with time as nests were laid. Second, the 0.8 likelihood of a nest being predated by goannas was 0.6 independent of the age of the nest. Third, ghost crab burrows do not appear to assist goannas to locate sea 0.4 turtle nests. 0.2

Tracks per nest per day 0.0 Timing of goanna predation of sea turtle nests

Our observations indicated that the frequency of Before After goanna attacks on sea turtle nests did not increase as the nesting season progressed and the number of sea turtle nests incubating increased. This suggests that 5 the number of goannas predating nests remained b stable and that these goannas did not increase the 4 intake of sea turtle eggs in their diet from the beginning to end of the sea turtle nesting season. Only 3 large male yellow-spotted goannas opened nests and these individuals may exclude others from the beach 2 potentially limiting the number of goannas able to forage on the beach (Lei & Booth 2017b), and this 1 may explain why nest predation rate did not increase as the sea turtle nesting season progressed. 0 fi Burrows perBurrows nest per day The nding that the likelihood of a nest being attacked by a goanna was independent of nest age was surprising. We expected two peaks in nest preda- Before After tion. The first peak was expected immediately after a clutch was laid because goannas could use sand dis- Fig. 2. (a) Whisker–box plot of the number of ghost crab burrows appearing in loggerhead turtle nests (n = 18) turbance associated with nest construction as a visual before and after the nest was opened by a goanna or the cue and olfactory cues left in the sand by female tur- nest had had some hatchlings escape from it. (b) Whisker– tles to locate nests. The second peak was expected box plot of the number of goanna tracks appearing on top just before hatchling nest emergence once the of loggerhead turtle nests (n = 18) before and after the nest embryos had hatched from their eggs and released was opened by a goanna or the nest had had some hatch- egg fluids, the odour of which might be detectable lings escape from it. Dots = data range, Whiskers = 10% & 90% percentiles, Boxes = 25% & 75% percentiles, Hori- on the sand surface that could attract goannas. Fur- zontal line within box = median. thermore, the observation that goannas could crawl over the top of nests numerous times over several weeks before suddenly attacking the nest is puzzling the first hatchlings had left a nest (Fig. 4). Before pre- because the cue(s) used to the detect the nest after dation, visitation rate of yellow-spotted goannas (0.05 the first week of incubation are most likely to be visits per nest per day) and lace monitors (0.02 visits olfactory in nature, and logic implies that such cues per nest per day) was similar (P = 0.12), while after would have been present since the nest was con- hatching visitation rate by yellow-spotted goannas structed. This lead us to hypothesize that other cues (0.26 visits per nest per day) was higher than the lace such as the appearance of ghost crab burrows into a monitor (after: 0.07 visits per nest per day P < 0.01). nest may signal the presence of a nest to goannas. Yellow-spotted goannas were seen to open nests, but lace monitors were never seen to open nests. Nine of 13 (69%) hatched turtle nests were dug into by yellow- The interaction between yellow-spotted goannas spotted goannas, and three of these nests were also vis- and ghost crabs ited by lace monitors. Although lace monitors visited hatched nests before these nests had been dug into by Ghost crabs regularly burrow into sea turtle nests yellow-spotted goanna, lace monitors were never and are known to eat eggs and hatchlings (Le Buff observed to dig out a nest. 1990; Thompson 1995; Witherington 1999; Trocini doi:10.1111/aec.12568 © 2017 Ecological Society of Australia GOANNAS FIND TURTLE NESTS 5

Fig. 3. (a) The nest predation during the 2014–2015 (diamonds) and 2015–2016 (triangles) seasons. (b) Days between lay- ing and ﬁrst predation event from the 2014–2015 (diamonds) and 2015–2016 (triangles) seasons.

0.7 burrows, a yellow-spotted goanna may fortuitously 0.6 discover a sea turtle nest while digging out a ghost crab if the ghost grab burrow was constructed into a 0.5 nest. However, our observations do not support a 0.4 close association between the appearance of ghost crab burrows into a sea turtle nest and the subse- 0.3 quent predation of that nest by goannas. Although 0.2 numerous ghost crab burrow entrances were observed above sea turtle nests, these burrows 0.1 appeared anywhere between one and 56 days before Visits per nest per dayVisits 0.0 the nest was predated by a goanna, and further, numerous other nests had ghost crab burrows constructed into them without being attacked by goan- Yellow before Yellow after Lace before Lace after nas. Indeed, in only four of the 38 goanna-predated Fig. 4. Whisker–box plot of the number of goanna visits nests we monitored did a ghost crab burrow appear as recorded by camera traps to loggerhead turtle nests the day before the goanna predation event. Taken (n = 13) before and after the nest was opened by a goanna together, these observations indicate that ghost crab or the nest had had some hatchlings escape from it. Yel- burrows into sea turtle nests do not lead to the dis- low = yellow-spotted goanna, Lace = lace monitor. covery of the nest by goannas. Dots = data range, Whiskers = 10% & 90% percentiles, Boxes = 25% & 75% percentiles, Horizontal line within box = median. The range = 90% percentile in cases where dots are absent from plots. The influence of predated and hatched turtle nest on goanna activity at nests et al. 2009). Such burrow construction may alert the Our data show that goanna predation activities location of sea turtle nests to goannas by two mecha- occurred at all stages of the incubation period with nisms. First, the burrow into the nest could facilitate no peaks at the beginning or end of incubation. the release of odours from the incubating eggs into However, turtle nests were visited more often and the atmosphere above the nest and thus attracted a material (eggs, egg remains after hatching) taken goanna’s attention. Second, because on numerous from the nest once a nest was opened or hatched, occasions we observed yellow-spotted goannas feed- indicating that goannas were attracted to the odour ing on ghost crabs by digging them out of their of the opened nest, and/or the visual cue of the open © 2017 Ecological Society of Australia doi:10.1111/aec.12568 6 J.LEIANDD.T.BOOTH hole at the nest site. Goannas probably also remem- those nests that are attacked during middle or late ber the location of these nests which allows them to incubation that have been crawled over numerous visit the same nest numerous time on subsequent times earlier on in incubation by goannas before they days to access the food source (Ward-Fear et al. were attacked. Clearly, more work needs to be done 2016). Curiously, some goanna-predated nests did to discover that cues goannas and for that matter, not have all of their eggs consumed even though they ghost crabs, use to find sea turtle nests. We still think were visited on multiple occasions over several days, the most likely cues will be olfactory in nature, and and these nests managed to produce some hatchlings perhaps the next experimental step might be to bury (Lei & Booth 2017c). The reason why not all eggs eggs at different depths below the sand surface to see were consumed remains a mystery. At a single visit, a whether goannas and ghost crabs find shallowly bur- goanna may become sated after eating several eggs ied eggs more easily than deeper buried eggs. and these eggs may take a day or two to digest, but given that predated nests were generally visited over multiple days, satiation does not appear to be an ACKNOWLEDGEMENTS explanation for this phenomenon. Ghost crab burrows were numerous all over the This work was supported by a grant from the Nest to beach dune area, and we did not assess whether bur- Oceans Turtle Protection Program, a programme row density above a nest in undisturbed nests was jointly funded by the Australian and Queensland greater than burrow density in adjacent areas where Governments and would not have been possible with- no nest existed. A future study should address this out the help of Nev and Bev McLachlan’s Turtle Care point because it is of interest to know whether ghost Volunteers organization, the Burnett Mary Regional crabs actively seek out sea turtle nests in order to Group and WWF Australia. All work was approved by prey on eggs and hatchlings, or discover sea turtle a University of Queensland Animal Ethics Committee nests by accident as they randomly construct burrows (permit #SBS/352/EHP/URG) and conducted under into the sand. The facts that (i) numerous studies Queensland Government scientific permit # WITK have reported ghost crabs predating eggs and hatch- 15315614. lings within nests (Le Buff 1990; Thompson 1995; Witherington 1999; Trocini et al. 2009) and (ii) the current study’s observation that ghost crab burrowing activity at sea turtle nests increases when nests have REFERENCES been opened by a goannas suggest ghost crabs actively seek out sea turtle nests and that they may Auffenberg W. 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