Protecting nests of the Critically Endangered South Pacific loggerhead turtle Caretta caretta from goanna Varanus spp. predation

Page created by April Figueroa
 
CONTINUE READING
Protecting nests of the Critically Endangered South
           Pacific loggerhead turtle Caretta caretta from goanna
           Varanus spp. predation
                                      CHRISTINE A. MADDEN HOF, GABRIELA SHUSTER, NEV MCLACHLAN
                        BEV      M C L A C H L A N , S A R A N N E G I U D I C E , C O L I N L I M P U S and T O M O H A R U E G U C H I

           Abstract The South Pacific subpopulation of the loggerhead                            Supplementary material for this article is available at
           turtle Caretta caretta is categorized as Critically Endangered                        https://doi.org/./S
           on the IUCN Red List because of significant population de-
           clines. Five Queensland beaches support high-density nesting
           of this subpopulation, but egg and hatchling survival are low
                                                                                                 Introduction
           at some beaches because of feral and native terrestrial preda-
           tors. We quantified predation of loggerhead turtle eggs by
           two species of goanna, Varanus panoptes and Varanus varius,
           at Wreck Rock beach, one of the turtle’s major nesting bea-
                                                                                                 T     here is one genetic subpopulation for the loggerhead
                                                                                                       turtle Caretta caretta in the South Pacific Ocean
                                                                                                 (Bowen et al., ; Limpus et al., ; Boyle et al., )
           ches. In addition, we conducted an experiment to determine                            and most breeding females from this subpopulation nest on
           the efficacy of a nest protection device. Predation rates at                          beaches in eastern Australia and New Caledonia (Limpus &
           Wreck Rock beach were .% for treatment and .% for                               Limpus, ; Limpus, ). Post-hatchlings emerging at
           non-treatment clutches during the – nesting season.                           these beaches undertake trans-Pacific migrations to the
           A higher probability of predation (%) was predicted for the                         west coast of South America, reaching the coastal waters
           northern beach. Although nests were only partially predated                           of Peru and Chile (Kelez et al., ; Boyle et al., ;
           (.% of the total number of eggs), nest loss to predators and                       Donoso & Dutton, ; Alfaro-Shigueto et al., ).
           beach erosion (caused by a cyclone) was .%. If left unman-                         Along the east coast of Australia, sandy beaches in Queens-
           aged, the cumulative impact of predation and other threats,                           land support the majority of nesting, with c. % occurring
           including those exacerbated by climate change, can cause                              at five beaches: Wreck Island, Woongarra Coast, Tryon
           unsustainable loss of loggerhead turtle nests. This study                             Island, Erskine Island and Wreck Rock (Limpus, ;
           provides one of the first quantitative data sets on rates of                          Limpus & Casale, ).
           loggerhead turtle clutch predation in the South Pacific. It                               Despite its protected status and several decades of
           enhances our understanding of goanna predation impacts                                conservation effort, particularly in Queensland, the South
           and identifies an efficient predator exclusion device for                             Pacific subpopulation of the loggerhead turtle continues to
           mitigating the effects of terrestrial predators at Wreck Rock                         decline (Limpus et al., ; Limpus & Casale, ) and was
           beach, and for protecting marine turtle nests across northern                         categorized as Critically Endangered on the IUCN Red List
           Australia and globally.                                                               in  (Limpus & Casale, ). In recent years, although
           Keywords Automated cameras, Caretta caretta, eastern                                  the number of nesting loggerhead turtles has been increas-
           Australia, feasibility study, goanna predation, loggerhead                            ing (Limpus et al., ), the escalated mortality of post-
           turtle, predator exclusion device, Varanus                                            hatchlings from synthetic debris ingestion in the first
                                                                                                 few months after leaving the nesting beaches (Boyle &
                                                                                                 Limpus, ) and bycatch mortality of large post-
                                                                                                 hatchlings caught in long-line fisheries in Peru and Chile
           CHRISTINE A. MADDEN HOF (Corresponding author) and GABRIELA SHUSTER World
           Wide Fund for Nature Australia, Level 1, 17 Burnett Lane, Brisbane, QLD 4000,
                                                                                                 (Donoso & Dutton, ; Alfaro-Shigueto et al., ) have
           Australia. E-mail chof@wwf.org.au                                                     hampered population recovery.
           NEV MCLACHLAN and BEV MCLACHLAN TurtleCare Volunteers Queensland Inc.,                    In this context, reducing mortality from other causes at
           Buderim, Australia                                                                    nesting beaches could support population growth. Such
           SARANNE GIUDICE Burnett Mary Regional Group for Natural Resource                      causes include the predation of eggs and hatchlings by
           Management, Bundaberg, Australia                                                      introduced and native predators, the hatchling loss asso-
           COLIN LIMPUS Queensland Department of Environment and Science, Brisbane,              ciated with light pollution, and beach degradation caused
           Australia
                                                                                                 by anthropogenic and natural events (Limpus, ; Berry
           TOMOHARU EGUCHI Marine Mammal and Turtle Division, Southwest Fisheries                et al., ; Limpus & Casale, ).
           Science Center, National Marine Fisheries Service, National Oceanic and
           Atmospheric Administration, La Jolla, USA                                                 Increasing hatchling production by reducing clutch pre-
           Received  August . Revision requested  October .                          dation is a recommended and common practice for marine
           Accepted  December . First published online  November .                   turtles (Mroziak et al., ; Engeman et al., , ;

           Oryx, 2020, 54(3), 323–331 © 2019 Fauna & Flora International doi:10.1017/S0030605318001564
Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 23 Aug 2021 at 21:32:30, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms
. https://doi.org/10.1017/S0030605318001564
324         C. A. Madden Hof et al.

             O’Connor et al., ). Native and feral predators include                            within and adjacent to various land tenure (Fig. ). With a
             the red fox Vulpes vulpes, raccoon Procyon lotor and pig                              coastline exposed to onshore winds and largely unprotected
             Sus scrofa. Strategies to reduce depredation of marine turtle                         by the reef, the coastal dunes are a naturally dynamic eco-
             eggs have been used with varying levels of success; e.g.                              system characterized by coastal scrubs, eucalypt woodlands,
             predator control through shooting or baiting, deployment                              wet heaths and sedge lands. Delineated by camp and beach
             of exclusion devices (fencing, cages) and scent deterrents,                           access points, Wreck Rock beach is divided into north and
             and clutch relocation (Stancyk et al., ; Addison &                                south beach sectors and marked every  m with timber
             Henricy, ; Addison, ; Ratnaswamy et al., ; Yerli                          pegs. Pegs on the north beach sector are numbered –
             et al., ; Blamires & Guinea, ; Baskale & Kaska, ;                         and on the south beach sector –. The north beach is
             Norris et al., ; Kurz et al., ; Engeman et al., ;                         located adjacent to Deepwater National Park. There are
             Lamarre-DeJesus & Griffin, ). However, there are few                              two public access campsites (Middle Rock and Wreck
             in situ studies examining the effectiveness of these strategies                       Rock) within the Park (Fig. ).
             for loggerhead turtles (Schroeder, ; Macdonald et al.,
             ; Yerli et al., ; O’Connor et al., ).                                     Methods
                 Wreck Rock beach supports the second largest number of
             loggerhead turtles nesting on the eastern Australian main-                            Data collection
             land, with c.  nests per season (Limpus, ). Clutch
             loss on Wreck Rock beach results from two primary sources:                            The Wreck Rock Turtle Research Team, under the guid-
             storm surge erosion and flooding of nests, which varies                               ance of the Queensland Government’s Queensland Turtle
             widely between years (C.J. Limpus, , pers. comm.),                                Research Programme, has monitored the Wreck Rock
             and depredation by goannas Varanus spp., which may                                    beach study site for loggerhead turtle nesting activity for
             now have the greatest impact on hatchling production at                               more than  years, since . During the – nest-
             this beach (McLachlan et al., ). Historically, predation                          ing season ( December – March ), in addition to
             by feral foxes was a major threat, with predation levels                              carrying out the standard nesting and hatchling emergence
             reaching c. –% of clutches laid prior to the mid s                            census for all turtle species (loggerhead, green Chelonia
             (Limpus, ). A baiting programme was introduced in                                 mydas and flatback Natator depressus turtles), we moni-
              and led to the near-complete elimination of clutch pre-                          tored predator activity at  experimental loggerhead turtle
             dation by foxes. Although clutch loss to native goannas was                           clutches ( treatment and  control) daily. Following ovi-
             considered negligible historically, anecdotal evidence now                            position, we marked each nest with flagging tape during the
             suggests reduced fox numbers have shifted the balance of                              night patrol, and designated them for control or treatment
             predator–prey interactions, resulting in increased goanna                             plots (with an exclusion device installed at the latter) the
             predation of turtle nests at Wreck Rock beach. Although                               following day. Treatment and control nests were spread
             goannas have long been known to consume marine turtle                                 throughout the study area to ensure sufficient representa-
             eggs (Marquez, , p. ), their predation rates on logger-                         tion of both on the north (control = , treatment = )
             head turtle clutches at Wreck Rock beach remained un-                                 and south beaches (control = , treatment = ; Fig. ). It
             quantified (Lei & Booth, a). In addition, there is a                              was not possible to place control and treatment plots
             dearth of information on varanid ecology, behaviour and                               randomly in space and time.
             predation cues to develop effective goanna management                                     We constructed predator exclusion devices, modelled
             strategies for this region.                                                           after those developed and deployed successfully on the
                 Here we report on the outcome of experiments that suc-                            Sunshine Coast (O’Connor et al., ), from interlocking
             cessfully reduced goanna predation on loggerhead turtle                               aluminium mesh panels. We chose aluminium mesh be-
             clutches at Wreck Rock beach. We quantify goanna predation                            cause it has been used successfully in previous studies and
             rates, provide an effective method to decrease predation and                          is unlikely to disrupt the hatchlings’ magnetic imprinting
             present alternative management interventions to reduce the                            (Irwin & Lohmann, ). Each exclusion device (cage)
             threat of goanna predation on clutches, which can be applied                          consisted of a  m top panel and four side flaps of – cm
             widely at nesting beaches in northern Australia and globally.                         width (Supplementary Plate ). The mesh size of  mm was
                                                                                                   sufficiently large to allow hatchlings to emerge, but small
             Study area                                                                            enough to prevent access by varanid and mammalian
                                                                                                   predators. We placed predator exclusion devices at a
             The study site at Wreck Rock (Fig. ) comprises  km of                              depth of c.  cm below the sand surface over  treatment
             east-facing beaches from Broadwater Creek to Red Rock.                                nests and left  control nests unprotected.
             The site lies at the southern end of the Great Barrier Reef                               We conducted predator activity surveys of the treatment
             Coast Marine Park (Queensland State Government) and                                   and control plots during daylight hours at low tide using a
             Great Barrier Reef Marine Park (Commonwealth), situated                               pro-forma datasheet. For reasons of practicality, data were

                                                                                        Oryx, 2020, 54(3), 323–331 © 2019 Fauna & Flora International doi:10.1017/S0030605318001564
Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 23 Aug 2021 at 21:32:30, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms
. https://doi.org/10.1017/S0030605318001564
Protecting loggerhead turtle nests                 325

                                                                                                 recorded within a . cm (total length of the measuring
                                                                                                 tape used) radius from each marked nest centre as a stand-
                                                                                                 ard measure and distance of likely plot predation. We
                                                                                                 collected the following data: sand disturbance or predator
                                                                                                 tracks (species identified as goanna, fox, dog, ghost crab);
                                                                                                 attempted predation (holes had been dug but no empty egg
                                                                                                 shells were found); predation: holes dug, number of empty
                                                                                                 egg shells (if greater than half a shell) and number of un-
                                                                                                 developed or unhatched eggs on sand surface; and the dis-
                                                                                                 tance between the nest centre and the egg remains farthest
                                                                                                 away from it. After recording the data, we manually re-
                                                                                                 moved signs of predator activity using footwear, so as to
                                                                                                 minimize human scent at the nest site.
                                                                                                    In addition, we monitored  nests ( treatment and two
                                                                                                 control nests) for predator activity throughout the incuba-
                                                                                                 tion period, using infrared wildlife motion-sensor cameras
                                                                                                 (Reconyx Hyperfire HC, Reconyx, Holmen, USA).
                                                                                                 Cameras were secured onto timber marker posts using bun-
                                                                                                 gee cords and positioned to aim at the centre of each nest.
                                                                                                 The cameras recorded ambient air temperatures and still
                                                                                                 images whenever movement was detected. If a camera-
                                                                                                 monitored nest was destroyed by predators, we moved the
                                                                                                 camera to another nest. We identified species that visited
                                                                                                 the clutches from the recorded camera images. Goannas
                                                                                                 were not individually identified and we assumed a new
                                                                                                 visitation event after  s of no recording.
                                                                                                    We excavated the clutches when the hatchlings emerged,
                                                                                                 or after  days of incubation, to determine hatching suc-
                                                                                                 cess. We calculated hatching success using data from the
                                                                                                 unpredated clutches and the following equation:
                                                                                                    Hatching success = (no. of empty shells)/(no. of un-
                                                                                                 hatched eggs + no. of undeveloped eggs + no. of empty
                                                                                                 shells). We then used the median hatching success to esti-
                                                                                                 mate the total hatchling production of the beach throughout
                                                                                                 the nesting season.

                                                                                                 Statistical analysis

                                                                                                 We calculated clutch loss as the proportion of clutches lost
                                                                                                 to all causes (predation and erosion) out of the total number
                                                                                                 of control clutches. Predation rates were computed as the
                                                                                                 proportion of clutches lost to predation out of the total
                                                                                                 number of control clutches. Nest monitoring was inter-
                                                                                                 rupted during  January– February  because a cyclone
                                                                                                 made landfall nearby. Therefore, we calculated loss of nests
           FIG. 1 Study site at Wreck Rock beach, land tenure and location                       in two distinct periods: before (quantified predation rate)
           of camp sites. Markers pegs – are on the north beach and                           and after (quantified predation + cyclone-caused nest loss)
           – on the south beach. C and D indicate the numbers of                            the cyclone event.
           control and treatment (deployment of a predator exclusion
                                                                                                    To determine the effectiveness of the exclusion devices
           device) loggerhead turtle Caretta caretta clutches, respectively,
           on a stretch of beach between the marker pegs shown. The size                         on loggerhead turtle clutches, we considered five logistic re-
           of the circles represents the total nesting activity, including                       gression models, using three predictor variables: days since
           failed nesting attempts, per year on the respective beach                             the beginning of the experiment (Days), location of the nests
           stretches.                                                                            measured by the peg numbers (Location), and treatment

           Oryx, 2020, 54(3), 323–331 © 2019 Fauna & Flora International doi:10.1017/S0030605318001564
Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 23 Aug 2021 at 21:32:30, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms
. https://doi.org/10.1017/S0030605318001564
326         C. A. Madden Hof et al.

             with a predator exclusion device (Treatment; Table ). We                             % CI = .–.%) than after the cyclone (.%,  of 
             compared models using the Akaike information criterion                                control plots depredated; % CI = .–.%). The major-
             (AIC; Akaike, ). Using the best model from the analysis                           ity of predation of control nests occurred on the northern
             on the effectiveness of the treatment, we predicted the prob-                         beach (/ = %; % CI = .–.%).
             ability of predation at all observed nest locations along the                             Exclusion devices appeared to be effective in reducing
             entire beach.                                                                         clutch predation. With exclusion devices deployed at 
                To determine whether the exclusion device delayed pre-                             nests, only one hatchling became entrapped during emer-
             dation, we compared the mean number of days from laying                               gence. Compared with the control plots ( of  control
             to predation between control and treatment plots using a                              nests; .%; % CI = .–.%), fewer treatment plots
             Bayesian t test. We hypothesized that the mean number of                              were depredated during the nesting season ( of  treatment
             days between laying and predation would be greater for the                            nests; .%; % CI = .–.%). The point estimate of pre-
             treatment plots than for the control plots.                                           dation with exclusion devices was % (/; % CI = .–
                To estimate the total number of hatchlings on the entire                           .%) prior to the cyclone, and % (/; % CI = .–
             beach, we used a parametric bootstrap procedure. For all                              .%) after the cyclone. Although the point estimate was
             observed clutches at the nesting beach, we estimated the                              greater for the treatment plots than control (.% vs
             probability of predation using the logistic regression models.                        .%), the binomial % CI overlapped (.–.% vs .–
             The median nest size and median hatching success rate were                            .%). Because of the large uncertainties associated with
             used to compute the total number of hatchlings for the                                small sample sizes, they were not statistically different.
             unpredated nests. We repeated this process , times to                                 Amongst the models used to determine the effects of the
             obtain the uncertainty in the estimate from the predation                             exclusion device on the predation of loggerhead turtle
             probability.                                                                          clutches, Model  had the smallest AIC value, although dif-
                We conducted all statistical analyses in R .. (R Core                           ferences in AIC values between the top  models were , ,
             Team, ) with packages ggplot (Wickham, ) and                                 indicating that these models were not substantially different
             gamm (Wood & Scheipl, ). Bayesian computations                                   (Table ). In the following analyses, we use the best model,
             were conducted using jags .. (Plummer, ) through                               which included treatment, location, and their interactions.
             rjags (Plummer, ) in R.                                                               The interaction term was significant at α = . (Table ),
                                                                                                   indicating that the effectiveness of the treatment varied sig-
                                                                                                   nificantly along the beach. This can be seen in Fig. , where
             Results                                                                               the predicted probability of predation decreases with in-
                                                                                                   creasing peg number (i.e. from north to south along the
             During the – nesting season ( December –
                                                                                                   beach) for the control plots, but increases for the treatment
             March ) we recorded  loggerhead,  green and 
                                                                                                   clutches. However, because of the small sample sizes in the
             flatback turtles laying one or more clutches at Wreck Rock
                                                                                                   area farthest from the field station, on the south beach,
             beach (Supplementary Table ). Of the loggerhead turtles,
                                                                                                   confidence intervals are wide in this area. For the area
              were new recruits and  were recaptures from previous
                                                                                                   with larger sample sizes, on the north beach, the predicted
             nesting seasons. During the nesting season, we recorded 
                                                                                                   probability of predation was smaller for the treatment than
             loggerhead nesting activities, with  successful nests and
                                                                                                   for the control plots.
              failed attempts. Of the  successful nesting events, 
                                                                                                       The main effect of the exclusion device was also signifi-
             clutches were laid on the north and  on the south beach.
                                                                                                   cant at α = . (Table ), indicating that the devices signifi-
             We used  of the  successfully laid nests in our study,
                                                                                                   cantly reduced the predation of loggerhead turtle clutches.
             deployed exclusion devices on  treatment clutches and
                                                                                                   This is supported by the percentage of predated clutches
             used  as control. During the study,  plots (eight treat-
                                                                                                   in control vs treatment plots (. vs .%, respectively).
             ment and  controls) were lost to erosion when cyclone
             Dylan made landfall near Wreck Rock beach on 
             January .
                                                                                                   Hatching success

             Clutch loss                                                                           The mean clutch size was . ± SE . (n = ; median )
                                                                                                   and the mean hatching success was . ± SE .
             During the – season,  of  control clutches were                           (n = ; median .). Using the most parsimonious logis-
             depredated (mean = .%, % CI = .–.%), an add-                               tic regression model (Model ) from the previous analysis,
             itional  were lost to erosion. In total, clutch loss to preda-                      we predicted the probability of predation at all observed nest
             tors and erosion events (exacerbated by a cyclone) was .%                          locations; i.e. extrapolated to the entire beach (Fig. ). Using
             (% CI = .–.%). The predation rate was greater prior                           the probability of predation, median hatching success,
             to the cyclone (.%,  of  control plots depredated;                            median clutch size, and a parametric bootstrap analysis,

                                                                                        Oryx, 2020, 54(3), 323–331 © 2019 Fauna & Flora International doi:10.1017/S0030605318001564
Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 23 Aug 2021 at 21:32:30, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms
. https://doi.org/10.1017/S0030605318001564
Protecting loggerhead turtle nests                 327

           TABLE 1 Logistic regression models used to determine the effective-                   TABLE 2 Estimated linear model coefficients of the best-performing
           ness of predator exclusion devices on loggerhead turtle Caretta ca-                   model (Model ), with standard deviations and P values.
           retta clutches, showing predictor variables and difference in Akaike                  The model was Predation * Intercept + Treatment + Location +
           information criterion values from best-performing model (ΔAIC).                       Treatment × Location.

           Model                   Variables1                                        ΔAIC        Parameter                               Estimate                            P
           Model 4                 Treatment × Location                              0.00        (Intercept)                             −1.40 ± SE 0.38                     0.00
           Model 3                 Treatment                                         0.57        Treatment                               −0.64 ± SE 0.37                     0.08
           Model 2                 Treatment + Location                              1.22        Location                                −0.16 ± SE 0.41                     0.70
           Model 1                 Treatment + Location + Days                       3.12        Treatment:Location                       0.71 ± SE 0.40                     0.08
           Model 5                 Treatment × Days                                  4.45
           
            Days, days since the beginning of the experiment; Location, location of
           the nests measured by the peg numbers along the beach; Treatment, clutch              on emerging hatchlings at Wreck Rock beach. On several
           treatment with a predator exclusion device.                                           occasions we observed predation on nests adjacent to
                                                                                                 control plots (i.e. on nests not included in this study).
                                                                                                    We recorded  goanna visitation events to  logger-
           we estimated the total number of hatchlings produced at
                                                                                                 head turtle nests monitored by automated cameras. The
           Wreck Rock beach during the nesting season to be ,
                                                                                                 yellow spotted monitor was found most frequently (
           with a % CI of ,–, (Supplementary Fig. ).
                                                                                                 recorded visits) followed by the lace monitor ( visits). Of
           Some loggerhead turtle clutches were only partially pre-
                                                                                                 the  monitored clutches,  were visited multiple times by
           dated. Although sample sizes were small, the mean number
                                                                                                 the same species on  occasions ( times by yellow spotted
           of predated eggs per nest was c.  ± SE . (.%, n = ).
                                                                                                 monitors and  times by lace monitors). The remaining
           Undeveloped eggs (unhatched eggs with no obvious em-
                                                                                                 four nests were visited once by one goanna species, and at
           bryo) also accounted for % of the total eggs in nests.
                                                                                                 two of these nests the second species continued to visit
              The Bayesian equivalent of a two-sampled t test
                                                                                                 multiple times after the first species had visited.
           indicated there was no significant difference in the tim-
                                                                                                    Ambient air temperature during goanna visits to the
           ing of predation between treatment and control nests
                                                                                                 clutches was – °C. We found differences between the
           (Supplementary Fig. ). Further, the % posterior interval
                                                                                                 mean temperatures at visits by the two goanna species and
           (Gelman et al., ) of the contrast coefficient (control vs
                                                                                                 other species (birds and mammals; Supplementary Fig. )
           treatment effects) included zero (−., .). For both
                                                                                                 Lace monitors visited turtle nests at a lower ambient tem-
           control and treatments, however, predation seemed to
                                                                                                 perature (mean = . ± SE . °C, n = ) than yellow
           occur either in the early or late stages of incubation
                                                                                                 spotted monitors (. ± SE . °C, n = ).
           (Supplementary Fig. ).

           Predation                                                                             Discussion

           With individual cameras operating for – days, the total                           As the South Pacific loggerhead turtle subpopulation con-
           camera-trapping time was , hours over a period of                                tinues to decline, it requires renewed attention to decrease
            days. Species recorded by automatic cameras included                               mortality at all life history stages. Nest predation by terres-
           hares Lepus sp., kites Milvus sp., cats Felis sp., foxes                              trial predators may significantly reduce recruitment and
           Vulpes sp., emus Dromaius sp., pied butcherbirds Cracticus                            could lead to additional declines in the already depleted
           nigrogularis and wallabies Macropus sp. The two species                               population (CMS, ). This study provides new infor-
           of goannas recorded near turtle nests were the yellow                                 mation about goanna depredation and demonstrates that
           spotted or Argus monitor Varanus panoptes and the lace                                exclusion devices effectively reduce predation. We also pro-
           monitor Varanus varius (A. Amey, , pers. comm.). A                                vide a recent estimate of the predation rate on loggerhead
           third goanna Varanus gouldii may be present, but the                                  turtle clutches at a major nesting beach in the South
           species identification could not be confirmed. As expected,                           Pacific.
           goanna activity tended to occur during daylight hours                                     The predation rate of loggerhead turtle clutches (.%)
           (.–.).                                                                         at Wreck Rock beach was lower than that reported at
              Based on tracks, predation at both treatment and control                           other nesting beaches. For example, % of flatback turtle
           plots was carried out by goannas, with only one incidence of                          clutches were predated at Fog Bay (Blamires, ; Blamires
           fox predation recorded, at a treatment plot. On one occa-                             & Guinea, ), –% of flatback turtle clutches at
           sion, more than six goannas were observed predating on                                Pennefather beach (J. Doherty and Cape York Peninsula
           loggerhead turtle hatchlings as they emerged from a nest.                             Development Association, unpubl. data in Whytlaw et al.,
           This was the first recorded observation of goanna predation                           ), –% of green and loggerhead turtle clutches in

           Oryx, 2020, 54(3), 323–331 © 2019 Fauna & Flora International doi:10.1017/S0030605318001564
Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 23 Aug 2021 at 21:32:30, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms
. https://doi.org/10.1017/S0030605318001564
328         C. A. Madden Hof et al.

             FIG. 2 Predicted probability of loggerhead turtle nest predation                      FIG. 3 Predicted predation probabilities with respect to beach
             as a function of location on the beach and control vs predator                        marker pegs (location) and time since the beginning of the
             exclusion device treatment. Shaded areas correspond to %                            experiment (days). The size of the points corresponds to the
             confidence intervals.                                                                 probabilities.

             Turkey (Macdonald et al., ), and –% of loggerhead                             Repos (mean % loss of entire clutches from natural causes,
             turtle clutches in North America (Stancyk et al., ;                               range .–.%; Limpus, ), clutches are regularly
             Engeman et al., ). During the – and –                                 lost to natural erosion and flooding at Wreck Rock beach
              nesting seasons at Wreck Rock beach, Lei & Booth                                 (N. McLachlan, unpubl. data). These events will continue
             (a) reported .% and .% of clutches predated by                              to be exacerbated with severe cyclones, floods and storms
             goannas, respectively. However, their study was confined to                           predicted to increase in frequency with climate change
             a -km stretch of beach, whereas we monitored the entire                              (IPCC, ). During the study, a natural tide storm surge
             -km stretch. The difference in results may be a result of                           and wind additionally exposed turtle nests to predation and
             this spatial difference in sampling effort and the heterogen-                         increased the total number of clutches lost. This loss was
             eity of predation across a rookery (Blamires, ). It is also                       greater for the treatment nests, probably because the exclu-
             possible that predation is temporally variable because of                             sion devices provided visual cues for the predators. In add-
             fluctuations in predator and prey density.                                            ition, hatchlings are affected by light pollution associated
                In recent years, as also evidenced in Lei & Booth (a),                         with coastal development. Overall, Wreck Rock beach
             goannas have been the primary predators of turtle eggs and                            grossly exceeds a sustainable level of annual clutch loss of
             hatchlings at Wreck Rock beach. For the first time, we ob-                            c. % (CMS, ). Consequently, it is important to
             served predation of hatchlings by multiple goannas. Foxes                             develop ongoing predator management (cognizant of the
             are now minor predators of loggerhead turtle clutches, pre-                           threat posed by extreme weather events) as this may be the
             sumably the result of the long-term fox baiting programme.                            only threat that can be addressed effectively in a timeframe
             Yellow spotted and lace monitors were the most promi-                                 that allows the population to recover.
             nent visitors to turtle nests at the study site. A third species,                         The deployment of exclusion devices, although effective,
             Varanus gouldii, is frequently found in close proximity to                            may not be feasible for nesting beaches with moderate to
             yellow spotted monitors (Shine, ; A. Amey, , pers.                            high turtle numbers (e.g. .  turtles per night). Devices
             comm.) but further studies are needed to confirm its                                  may impede nesting attempts (Kurz et al., ), and re-
             presence.                                                                             sources are often limited (Lei & Booth, b; Lei et al.,
                In this study, the aluminium cage predator exclusion                               ). A suite of alternative predator control methods
             devices were effective in reducing predation of loggerhead                            (some of which are already being applied at Wreck Rock
             turtle nests at Wreck Rock beach. With only one entrapped                             beach) should be included in future studies to develop a con-
             hatchling amongst  cage deployments, the devices were                               servation strategy considerate of the main predator species,
             deemed successful for reducing predation and letting                                  habitat and climatic conditions, and budgetary and logistical
             hatchlings pass through. The same conclusion was also                                 constraints. Additional types of predator exclusion devices
             reached by Lei & Booth (b) in subsequent years.                                   that could be deployed include plastic mesh nest protectors
             Given Wreck Rock beach is predicted to produce c. ,                              (Lei & Booth, b) and flat chain link screening or less
             hatchlings per season, the use of these anti-predator devices                         rigid wire mesh cages, if not disruptive to hatchlings
             should result in increased hatchling production.                                      magnetic imprinting (Addison & Henricy, ; Addison,
                The loss of clutches observed in this study (from preda-                           ). The application of scent deterrents such as habanero
             tion and other causes combined) was .%, which is a cause                           powder (see Ratnaswamy et al., ; Lamarre-DeJesus &
             for concern. Historically only quantified for beaches at Mon                          Griffin, ; Lei et al., ), human scent (see Burke

                                                                                        Oryx, 2020, 54(3), 323–331 © 2019 Fauna & Flora International doi:10.1017/S0030605318001564
Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 23 Aug 2021 at 21:32:30, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms
. https://doi.org/10.1017/S0030605318001564
Protecting loggerhead turtle nests                 329

           et al., ), visual disturbance (such as flags, see Burke                           could uncover vital information regarding the timing of pre-
           et al., ), or the use of pheromones (goanna’s own or                              dation (Ferreira, ; Welicky et al., ), repeated visi-
           other species such as cane toads) may be effective in deterring                       tation by predators, and complete (Limpus, ) vs partial
           goannas. Nest relocation (including into hatcheries) should                           clutch loss (Chatto & Baker, ). For example, further re-
           only be trialled as a last resort because it could reduce hatch-                      search could provide insights into why control clutches were
           ling imprinting and success (see Kornaraki et al., ).                             predated less than anticipated, and why nests not included
               Culling of goannas to protect turtle nests is not viable as                       in this study but directly adjacent to control plots were also
           they are protected in Australia. Coastal populations of the                           predated (as per the simulation in Blamires & Guinea,
           yellow spotted monitor may be the species’ last stronghold,                           ). Although the lace monitor was not previously con-
           as many inland populations have declined as a result of                               sidered a predator of turtle eggs, this species accounted for
           a toxic diet of cane toads (Ujvari & Madsen, ; Shine,                             more than one-third of total predation and visited turtle
           ). Because the species is not categorized as threatened                           nests at a lower temperature than the yellow spotted moni-
           on the IUCN Red List, Lei & Booth (b; Lei et al., )                           tor ( vs  °C, respectively).
           suggest the temporary removal of male yellow spotted                                      Until further studies are undertaken, interim manage-
           monitors (the primary predators of turtle eggs) during the                            ment is recommended particularly for the north beach.
           turtle nesting season. However, given the monitor’s eco-                              Camp site usage and waste management should be reviewed
           logical role as a mesopredator, resource managers must                                as a priority to reduce goanna activity in this area. This
           first understand the local predator–prey interactions and                             could be achieved with relatively little effort through educa-
           the ecosystem-level effects of any predator control method                            tion and enforcement. Future site-specific management is
           selected (Prugh et al., ; Welicky et al., ). Studies on                       necessary to maximize hatchling success. The exclusion
           the raccoon Procyon lotor, another mesopredator that tar-                             devices deployed in this study are effective in reducing
           gets marine turtle clutches, showed its removal had no effect                         depredation on marine turtle nesting beaches, but are not
           on mainland clutch depredation (Ratnaswamy et al., ;                              cost-effective for Wreck Rock beach because of high nest-
           Barton & Roth, ). Tsellarius et al. () suggested                              ing numbers and limited resources. An alternative predator
           goannas scent-mark territorial boundaries to keep strangers                           control programme should be explored, to provide the
           out and control local population sizes, so the removal of in-                         most efficient allocation of resources and management. This
           dividual goannas from a local populations could potentially                           will be the most robust strategy to maximize hatchling
           lead to an increase in goanna numbers.                                                production and thus contribute to future recruitment of
               Goanna predation and nest selectivity is probably dri-                            the declining and Critically Endangered South Pacific subpo-
           ven by olfactory and visual cues and influenced by spatial                            pulation of the loggerhead turtle.
           and temporal nest deposition (Blamires & Guinea, ;
           Blamires, ; Welicky et al., ), proximity to urbanized                         Acknowledgements We thank the volunteers of TurtleCare’s
                                                                                                 Wreck Rock Turtle Research Team and the Gidarjil Aboriginal
           areas (Smith & Engeman, ; Blamires & Guinea, ;                                Corporation for their assistance with field work; and Kirsten Wortel
           Prange et al., ) and human and goanna conspecific                                 and the Burnett Mary Regional Group (BMRG) for assistance with
           activity (Ferreira, ). In contrast to Welicky et al. (),                      mapping. We acknowledge funding from WWF-Australia and BMRG.
           predation risk in this study was more probable on the
           north beach in areas heavily utilized by humans, with                                 Author contributions Study design: all authors; data collection:
                                                                                                 CAMH, GS, NM, BM, SG; data analysis: CAMH, GS, TE; writing:
           campsites and food waste. This raises the question of why                             CAMH; revisions: all authors.
           goannas have become more abundant at Wreck Rock beach
           (they were considered uncommon in the s; C. Limpus,                               Conflicts of interest None.
           , pers. comm.) and what drives their behaviour. It is
           possible that the control of apex predators (dingoes and                              Ethical standards This research abided by the Oryx guidelines on
                                                                                                 ethical standards. Research protocols for this study were approved by
           foxes) has altered predator–prey relationships and reduced
                                                                                                 an authorised ethics committee (SA 2015/11/531) and authority under
           competition for goannas. This, together with increased                                the Nature Conservation Act 1994.
           human activity and camp site waste (particularly on the
           north beach), could have increased food availability for
                                                                                                 References
           goannas, supporting them in greater numbers (Prugh et al.,
           ).                                                                                A D D I S O N , D.S. () Galvanized wire cages can protect nest
               Research with a focus on goanna ecology and loggerhead                               depredation. Marine Turtle Newsletter, , –.
           turtle clutch predation could improve management inter-                               A D D I S O N , D.S. & H E N R I C Y , S. () A comparison of galvanized wire
                                                                                                    mesh cages vs flat chain-link screen in preventing Procyon lotor
           ventions for Wreck Rock beach. Such studies should include
                                                                                                    depredation of Caretta caretta nests. NOAA Technical
           research into the biology and behaviour of goannas, exam-                                Memorandum, , .
           ination of long-term predation effects and human impacts                              A K A I K E , H. () A new look at the statistical model identification.
           on predator behaviour. An examination of clutch predation                                IEEE Transactions on Automatic Control, , –.

           Oryx, 2020, 54(3), 323–331 © 2019 Fauna & Flora International doi:10.1017/S0030605318001564
Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 23 Aug 2021 at 21:32:30, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms
. https://doi.org/10.1017/S0030605318001564
330         C. A. Madden Hof et al.

             A L F A R O -S H I G U E T O , J., M A N G E L , J., B E R N E D O , F., D U T T O N , P.H.,       F E R R E I R A , M.B.M.d.S. () Nesting habitat preferences and nest
                S E M I N O F F , J.A. & G O D L E Y , B.J. () Small-scale fisheries of Peru:                   predation of green turtles (Chelonia mydas) in the Bijagós
                a major sink for marine turtles in the Pacific. Journal of Applied                                  Archipelago, Guinea Bissau. MSc thesis, Universidade de Lisboa,
                Ecology, , –.                                                                             Lisbon, Portugal.
             B A R T O N , B.T. & R OT H , J. () Raccoon removal on sea turtle nesting                      G E L M A N , A., C A R L I N , J.B., S T E R N , H.S., D U N S O N , D.B., V E H T A R I , A.
                beaches. The Journal of Wildlife Management, , –.                                         & R U B I N , D.B. () Bayesian Data Analysis. CRC Press, Boca
             B A S K A L E , E. & K A S K A , Y. () Sea turtle nest conservation                                Raton, USA.
                techniques on southwestern beaches in Turkey. Israel Journal                                    I N T E R G OV E R N M E N TA L P A N E L O N C L I M A T E C H A N G E () Climate
                of Zoology , –.                                                                               Change –The Physical Science Basis: Working Group I
             B E R R Y , M., B O O T H , D.C. & L I M P U S , C.J. () Artificial lighting and                   Contribution to the Fourth Assessment Report of the IPCC.
                disrupted sea-finding behaviour in hatchling loggerhead turtles                                     Cambridge University Press, Cambridge, UK.
                (Caretta caretta) on the Woongarra coast, south-east Queensland,                                I R W I N , W.P. & L O H M A N N , K.J. () Magnet-induced disorientation
                Australia. Australian Journal of Zoology, , –.                                              in hatchling loggerhead sea turtles. Journal of Experimental Biology,
             B L A M I R E S , S.J. () Quantifying the impact of predation on sea turtle                        , –.
                nests by varanids at Fog Bay. MSc thesis. Northern Territory                                    K E L E Z , S., M A M R I Q U E , C. & V E L E Z -Z U A Z O , X. () Conservation of
                University, Darwin, Australia.                                                                      Sea Turtles Along the Coast of Peru. Unpublished Report to UNEP/
             B L A M I R E S , S.J. () Habitat preferences of coastal goannas (Varanus                          CMS from Asociación Peruana para la Conservación de la
                panoptes): are they exploiters of sea turtle nests at Fog Bay,                                      Naturaleza y Grupo de Tortugas Marinas—Perú. Https://www.cms.
                Australia? Copeia, , –.                                                                      int/sites/default/files/publication/Tortugas_Peru_informe_final_
             B L A M I R E S , S.J. & G U I N E A , M.L. () Emergence success of flatback                       CMS_En.pdf [accessed  July ].
                Sea turtles (Natator depressus) at Fog Bay, Northern Territory,                                 KORNARAKI, E., M AT O S S I A N , D.A., M A Z A R I S , A.D., M A T S I N O S , Y.G. &
                Australia. Chelonian Conservation and Biology, , –.                                          M A R G A R I T O U L I S , D. () Effectiveness of different conservation
             B O W E N , B.W., K A M E Z A K I , N., L I M P U S , C.J., H U G H E S , G.R., M E Y L A N ,          measures for loggerhead sea turtle (Caretta caretta) nests at
                A.B. & A V I S E , J.C. () Global phylogeography of the loggerhead                              Zakynthos Island, Greece. Biological Conservation, , –.
                turtle (Caretta caretta) as indicated by mitochondrial DNA                                      K U R Z , D.J., S T R A L E Y , K.M. & D E G R E G O R I O , B.A. () Out-foxing
                haplotypes. Evolution, , –.                                                               the red fox: how to best protect the nests of the Endangered
             B O Y L E , M.C. & L I M P U S , C.J. () The stomach contents of                                   loggerhead marine turtle Caretta caretta from mammalian
                post-hatchling green and loggerhead sea turtles in the southwest                                    predation? Oryx, , –.
                Pacific: an insight into habitat association. Marine Biology, ,                              L A M A R R E -D E J E S U S , A.S. & G R I F F I N , C.R. () Use of habanero
                –.                                                                                            pepper powder to reduce depredation of loggerhead sea turtle nests.
             B O Y L E , M.C., F I T Z S I M M O N S , N.N., L I M P U S , C.J., K E L E Z , S.,                    Chelonian Conservation and Biology, , –.
                V E L E Z -Z U A Z O , X. & W E Y C O T T , M. () Evidence for                              L E I , J. & B O O T H , D.T. (a) Who are the important predators of sea
                transoceanic migrations by loggerhead sea turtles in the southern                                   turtle nests at Wreck Rock beach? Peer J, , e.
                Pacific Ocean. Proceedings of the Royal Society B: Biological Sciences,                         L E I , J. & B O O T H , D.T. (b) How best to protect the nests of
                , –.                                                                                     the Endangered loggerhead turtle Caretta caretta from
             BURKE, R.L., S C H N E I D E R , C.M., D O L I N G E R , M.T. () Cues                              monitor lizard predation? Chelonian Conservation and Biology, ,
                used by raccoons to find turtle nests: effects of flags, human                                      –.
                scent, and diamond-backed terrapin sign. Journal of Herpetology,                                L E I , J., B O O T H , D.T. & D W Y E R , R.G. () Spatial ecology of
                , –.                                                                                        yellow-spotted goannas adjacent to a sea turtle nesting beach.
             C H AT T O , R. & B A K E R , B. () The Distribution and Status of Marine                          Australian Journal of Zoology, , –.
                Turtle Nesting in the Northern Territory. Parks and Wildlife Service                            L I M P U S , C.J. () The flatback turtle, Chelonia depressa Garman in
                of the Northern Territory, Palmerston, Australia.                                                   Southeast Queensland, Australia. Herpetologica, , –.
             CMS (C O N V E N T I O N O N T H E C O N S E R VAT I O N O F M I G R AT O R Y                      L I M P U S , C.J. () A Biological Review of Australian Marine
                S P E C I E S O F W I L D A N I M A L S ) () Single Species Action Plan for                     Turtles. . Loggerhead Turtle Caretta caretta (Linneaus). Queensland
                the Loggerhead Turtle, Caretta caretta, in the South Pacific Ocean.                                 Environment Protection Agency, Brisbane, Australia.
                Https://www.cms.int/sites/default/files/document/COP_Doc__                                  L I M P U S , C. & C A S A L E , P. () Caretta caretta (South Pacific
                __Rev_Annex__SSAP_Loggerhead_Turtle_E_.pdf [accessed                                           subpopulation). In The IUCN Red List of Threatened Species :
                 May ].                                                                                       e.TA. Http://dx.doi.org/./IUCN.UK.-
             D O N O S O , M. & D U T T O N , P. () Sea turtle bycatch in the Chilean                           .RLTS.TA.en [accessed  January ].
                pelagic longline fishery in the south-eastern Pacific: opportunities                            L I M P U S , C.J. & L I M P U S , D.J. () Loggerhead turtles in the
                for conservation. Biological Conservation, , –.                                          equatorial and Southern Pacific Ocean: a species in decline.
             E N G E M A N , R.M., M A R T I N , R.E., C O N S TA N T I N , B., N O E L , R. &                      In Loggerhead Sea Turtles (eds A.B. Bolten & B.E. Witherington),
                W O O L A R D ., J. () Monitoring predators to optimize their                                   pp. –. Smithsonian Institution, Washington, DC, USA.
                management for marine turtle nest protection. Biological                                        L I M P U S , C.J., B O Y L E , M. & S U N D E R L A N D , T. () New Caledonian
                Conservation, , –.                                                                         loggerhead turtle population assessment:  pilot study. In Kinan,
             E N G E M A N , R.M., M A R T I N , R.E., S M I T H , H.T., W O O L A R D , J., C R A DY ,             I. Proceedings of Second Western Pacific Sea Turtle Cooperative
                C.K., C O N S T A N T I N , B. et al. () Impact on predation of sea turtle                      Research and Management Workshop. Volume II. North Pacific
                nests when predator control was removed midway through the                                          Loggerhead Sea Turtles, pp. –. Western Pacific Regional
                nesting season. Wildlife Research, , –.                                                     Fisheries Management Council, Honolulu, Hawaii, USA.
             E N G E M A N , R., M A R T I N , R.E., W O O L A R D , J., S T A H L , M., P E L I Z Z A , C.,    L I M P U S , C.J., P A R M E N T E R , C.J. & C H A LO U P K A , M. () Monitoring
                D U F F I N E Y , A. & C O N S T A N T I N , B. () An ideal combination for                     of Coastal Sea Turtles: Gap Analysis . Loggerhead Turtles, Caretta
                marine turtle conservation: exceptional nesting season, with low                                    caretta, in the Port Curtis and Port Alma Region. Report Produced
                nest predation resulting from effective low-cost predator                                           for the Ecosystem Research and Monitoring Program Advisory
                management. Oryx, , –.                                                                      Panel as Part of Gladstone Ports Corporation’s Ecosystem Research

                                                                                                     Oryx, 2020, 54(3), 323–331 © 2019 Fauna & Flora International doi:10.1017/S0030605318001564
Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 23 Aug 2021 at 21:32:30, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms
. https://doi.org/10.1017/S0030605318001564
Protecting loggerhead turtle nests                 331

               and Monitoring Program. Gladstone Ports Corporation, Gladstone,                             R C O R E T E A M () R: a language and environment for statistical
               Australia.                                                                                      computing. R Foundation for Statistical Computing, Vienna,
           M AC D O N A L D , D.W., B R O W N , L., Y E R L I , S. & C A N B O L AT , A-F. ()              Austria.
               Behavior of red foxes, Vulpes vulpes, caching eggs of loggerhead                            S C H R O E D E R , B.A. () Predation and nest success in two species of
               turtles, Caretta caretta. Journal of Mammalogy, , –.                                    marine turtles (Caretta caretta and Chelonia mydas) at Merritt
           M A R Q U E Z , M.R. () Sea Turtles of the World. Vol. . An Annotated                         Island, Florida. Florida Scientist, , .
               and Illustrated Catalogue of Sea Turtle Species Known to Date. Food                         S H I N E , R. () Food habits, habitats and reproductive biology of
               and Agriculture Organisations of the United Nations, Rome, Italy.                               four sympatric species of varanid lizards in tropical Australia.
           M C L AC H L A N , N., M C L AC H L A N , B., H O F , C., G I U D I C E , S., S H U S T E R ,       Herpetologica, , –.
               G., B U N C E , A. & E G U C H I , T. () Predator reduction strategies for              S H I N E , R. () The ecological impact of invasive cane toads
               protecting loggerhead turtle nests at Wreck Rock beach in                                       (Bufo marinus) in Australia. The Quarterly Review of Biology, ,
               Queensland. In: Proceedings of the Second Australian and Second                                 –.
               Western Australian Marine Turtle Symposia, Perth - August                               S M I T H , H.T. & E N G E M A N , R.M. () An extraordinary raccoon
                (compiled by S.D. Whiting & A. Tucker), p. . Science                                     density at an urban park in Florida. Canadian Field Naturalist,
               Division, Department of Parks and Wildlife, Perth, Australia.                                   , –.
           M R O Z I A K , M.L., S A L M O N , M. & R U S E N KO ., K. () Do wire cages                S TA N C Y K , S.E., T A L B E R T , O.R. & D E A N , J.M. () Nesting activity of
               protect sea turtles from foot traffic and mammalian predators?                                  the loggerhead turtle Caretta caretta in South Carolina II. Protection
               Chelonian Conservation Biology, , –.                                                     of nests from raccoon predation by transplantation. Biological
           N O R R I S , A., L O W , T., G O R D O N , I., S A U N D E R S , G., L A P I D G E , S.,           Conservation, , –.
               L A P I D G E , K. et al. () Review of the Management of Feral                          T S E L L A R I U S , A.Y., M E N ’ S H I KOV , Y.G. & T S E L L A R I U S , E.Y. ()
               Animals and their Impact on Biodiversity in the Rangelands: a                                   Spacing pattern and reproduction in Varanus griseus of Western
               Resource to Aid NRM Planning. Pest Animal Control Cooperative                                   Kyzylkum. Russian Journal of Herpetology, , –.
               Research Centre, Canberra, Australia.                                                       U J VA R I , B. & M A D S E N , T. () Increased mortality of naive varanid
           O’C O N N O R , J.M., L I M P U S , C.J., H O F M E I S T E R , K.M., A L L E N , B.L.,             lizards after the invasion of non-native cane toads (Bufo marinus).
               B U R N E T T , S.E. () Anti-predator meshing may provide greater                           Herpetological Conservation and Biology, , –.
               protection for sea turtle nests than predator removal. PLOS ONE,                            W E L I C K Y , R.L., W Y N E K E N , J. & N O O N B U R G , E.G. ()
               , e.                                                                                   A retrospective analysis of sea turtle nest depredation patterns.
           P L U M M E R , M. () rjags: Bayesian Graphical Models using MCMC.                              The Journal of Wildlife Management, , –.
               R package version -. Http://CRAN.R-project.org/package=rjags                             W H Y T L AW , P.A., E D WA R D S , W. & C O N G D O N , B.C. () Marine
               [accessed  May ].                                                                         turtle nest depredation by feral pigs (Sus scrofa) on the Western
           P R A N G E , S., G E H R T , S.D. & W I G G E R S , E.P. () Influences on                      Cape York Peninsula, Australia: implications for management.
               anthropogenic resources on raccoon (Procyon lotor) movements                                    Wildlife Research, , –.
               and spatial distribution. Journal of Mammology, , –.                                W I C K H A M , H. () Ggplot: Elegant Graphics for Data Analysis.
           P R U G H , L.R., S T O N E R , C.J., E P P S , C.W., B E A N , W.T., R I P P L E , W.J.,           Springer, New York, USA.
               L A L I B E R T E , A.S. & B R A S H A R E S , J.S. () The rise of the                  W O O D , S. & S C H E I P L , F. () gamm: Generalized additive mixed
               mesopredator. Bioscience, , –.                                                          models using mgcv and lme. R package version .-. Http://CRAN.
           R A T N A S WA M Y , M.J., W A R R E N , R.J., K R A M E R , M.T. & A D A M , M.D.                  R-project.org/package=gamm [accessed  May ].
               () Comparisons of lethal and nonlethal techniques to reduce                             Y E R L I , S., C A N B O L AT , A.F., B R OW N , L.J. & M AC D O N A L D , D.W. ()
               raccoon depredation of sea turtle nests. The Journal of Wildlife                                Mesh grids protect loggerhead turtle (Caretta caretta) nests from red
               Management, , –.                                                                        fox (Vulpes vulpes) predation. Biological Conservation, , –.

           Oryx, 2020, 54(3), 323–331 © 2019 Fauna & Flora International doi:10.1017/S0030605318001564
Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 23 Aug 2021 at 21:32:30, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms
. https://doi.org/10.1017/S0030605318001564
You can also read