Australian Field Ornithology 2017, 34, 1–9http://dx.doi.org/10.20938/afo34001009

Introduction

Introduced predators are recognised as one of the largest threats to avifauna and a leading cause of decline in bird populations (Atkinson 1996; Clavero & García-Berthou 2005). Introduced mammalian predators in particular prey upon not only eggs and chicks, but also adult birds, which can cause waves of extinctions and reductions in population sizes, both locally and globally (e.g. Nogales et al. 2004; Hilton & Cuthbert 2010). Therefore, identifying predators and understanding their impact on bird populations are crucial and fundamental steps in implementing effective conservation measures (Baker et al. 2002; Croxall et al. 2012). However, many predators are still unknown and their identification often relies on subjective assessments of evidence/signs left at nests or burrows, often producing misleading and inconclusive results because of similarities between activities of different predators, individual variation and multi-predator/scavenger visits (e.g. Lariviėre 1999; Stake & Cimprich 2003; Kawakami & Fujita 2004; reviewed in Lariviėre 1999).

Seabirds are particularly vulnerable to introduced predators because they have long reproductive cycles, slow turnover of generations and high fidelity to their breeding site (Moors et al. 1992; Bried et al. 2002). As a result, many ground-nesting seabird species nest only in areas inaccessible to introduced predators (such as remote islands and cliffs: Barrett 2008; Jovani et al. 2008) and generally lack the adaptations to protect or defend themselves from introduced predators (Moors et al. 1992; Miles et al. 2013). For example, Igual et al. (2007) found that Cory’s Shearwater Calonectris diomedea did not perceive the presence of Black Rats Rattus rattus when selecting burrows, and thus did not assess differences in predation risk and their impacts on breeding success. Similar issues can arise with recently encountered native predators: Leach’s Storm-Petrels Hydrobates leucorhoa showed no predator recognition when presented with

models of Great Skua Stercorarius skua, a major native predator in the Scottish study area (Outer Hebrides in the north-eastern Atlantic) but thought to be a recent colonist, and absent from most of the range of Leach’s Storm-Petrel (Miles et al. 2013).

Here, we focus on the Little Penguin Eudyptula minor, a flightless seabird that nests in burrows close to shore or under dense bushes and shrubs (Klomp et al. 1991; Dann 1994), and thus highly susceptible to terrestrial mammalian predators. Over recent decades, studies have documented population declines in some populations of Little Penguins across Australia and New Zealand (e.g. Dann 1992, 1994, 2013; Dann et al. 2000; Wiebkin 2011). In South Australia, the Little Penguin population on Granite Island has fallen from 1548 individuals in 2001 to only 32 individuals in 2014 (Colombelli-Négrel 2015a; see also Wiebkin 2011). In other areas such as Kangaroo Island, where Little Penguin numbers have either not been monitored or have been considered to be stable, Little Penguin populations are now also showing declines (Natural Resources Kangaroo Island unpubl. data 2014). Many factors have been suggested to explain these declines, including limited prey availability and starvation (Harrigan 1992; Dann et al. 2000; Wiebkin 2011), abundance of parasites (Harrigan 1992; Cannell et al. 2013), the recent increase in Long-nosed Fur Seals Arctocephalus forsteri (Bool et al. 2007; Wiebkin 2011), and predation on land by introduced predators such as the Red Fox Vulpes vulpes, Black Rat, Cat Felis catus and Dog Canis lupus familiaris (Dann 1992; Perriman et al. 2000; Preston 2008; Wiebkin 2011). Evidence from Little Penguin carcasses in the St Vincent Gulf showed that predation on land is one of the major threats causing population declines in this area, with 15–45% of the Little Penguin carcasses found washed up on beaches showing signs of predation (Tomo 2012, 2014). It has been suggested that native Water-rats Hydromys chrysogaster and introduced Black Rats are potential predators on Granite Island (Bool et al. 2007), and feral cats are one of the most likely predators

Identification of terrestrial predators at two Little Penguin colonies in South Australia

Diane Colombelli-Négrel1* and Ikuko Tomo2, 3

1School of Biological Sciences, Flinders University, Adelaide SA 5000, Australia2South Australian Museum, North Terrace, Adelaide SA 5000, Australia

3School of Dentistry, University of Adelaide, Adelaide SA 5005, Australia*Corresponding author. Email: diane.colombelli-negrel@flinders.edu.au

Abstract. Identifying predators and determining their influence on bird population declines can be crucial in the implementation of appropriate conservation measures. In this study, we focus on the Little Penguin Eudyptula minor, a flightless seabird whose numbers have seriously declined in some populations across Australia and New Zealand, for a variety of reasons, some not fully understood. Using a combination of motion-camera monitoring at active burrows and postmortem examinations of carcasses, we present data on the identity, occurrence and impact of terrestrial predators at two colonies in South Australia: Granite Island and Emu Bay (Kangaroo Island). Terrestrial predation varied from 20% for carcasses found on Granite Island to 44% at Emu Bay. There was no evidence for predation at burrows on Granite Island but, at Emu Bay, we identified goannas (Heath Monitor Varanus rosenbergi) as predators of chicks (by using cameras), and Cats Felis catus as predators of chicks and juveniles (from postmortem examination of carcasses). In addition, 45% of the carcasses found at Emu Bay were categorised as chicks. We discuss potential biases in identifying causes of death from carcasses only and the importance of combining both direct and indirect evidence.

2 Australian Field Ornithology D. Colombelli-Négrel & I. Tomo

full colour during daytime or in monochrome at night via a LED infrared illuminator array. Images were stored on SDHC memory cards upon activation of a motion sensor every 10 seconds. Each camera was placed ~1 m away and facing the entrance of the burrow. All cameras were checked every 2 weeks to change the batteries and memory cards.

During each visit, the number of Little Penguin adults, eggs and chicks present in each burrow and the breeding stage were noted. Breeding stages were defined as: eggs [1–2 adult(s) incubating their eggs], young chicks (the guard stage, one adult present with chicks <2–3 weeks old), and older chicks (post-guard stage; chicks older than 3 weeks, no adult present).

Collection and analysis of Little Penguin carcasses

Between May 2011 and November 2014, Little Penguin carcasses and records of death were collected opportunistically from both study sites during the ongoing monitoring of the breeding burrows and from a network of government staff and members of the public. All carcasses examined for this study were found on land, far enough away from the sea that they could not have been washed up, and therefore we are confident that these carcasses originated from the monitored colonies. All carcasses collected were stored in a freezer until the postmortem examinations were conducted. Although the use of frozen bodies can interfere with the interpretation, this was necessary because of the distance between the study sites and the necropsy facility. Only carcasses that were in reasonable condition were examined.

Standard postmortem examination was carried out by IT at the South Australian Museum (Adelaide, South Australia). Carcasses were weighed, photographed and measured using a standard penguin examination procedure (Hocken 2002), and particular attention was paid to potential signs of predation and intentional injury. The condition of the skin and any wounds found were noted, sketched and used to determine the cause of death wherever possible (Ratz et al. 1999). Subcutaneous tissues were examined carefully for penetrating wounds and haemorrhage, and the position, size and severity of these were noted. Skeletons were examined to identify any broken bones. When two penetrating wounds were found close to each other, the distance between them (DPW) was measured using a digital calliper or digimatic caliper NTD12-15CX (Mitutoyo Corporation, Japan) and compared with the inter-canine distances of potential mammalian predators known to occur at the study sites. Inter-canine distances in cats are generally 8.3–20.6 mm (mean 14.7 mm) but in dogs (even small dogs) are no smaller than 20 mm (mean 35.3 mm: Ratz et al. 1999; Cuthbert 2003; Tedeschi-Oliveira et al. 2011). Following advice from experts at the Forensics Odontology Dental School (Adelaide), inter-canine distances for Long-Nosed Fur Seals were estimated from skulls at the South Australian Museum as 20.8–45.6 mm. In addition, adult Long-Nosed Fur Seals have a pair of sharp incisors next to their canines, also capable of making penetrating wounds, which uniquely identifies predation by that species. All results were documented on outline drawings and datasheets, and photographs were taken of any abnormal features, lesions or injuries.

on Kangaroo Island (Masters 2007; Achurch et al. 2013). However, the exact identity of these predators (and their rates of predation) remains to be determined.

In this study, we present data on the identity, occurrence and impact of terrestrial predators at two Little Penguin colonies (Granite and Kangaroo Islands) in South Australia. We used carcasses collected around active burrows and monitoring with cameras that are activated by motion to identify predators. Motion-camera monitoring was also used to identify other intruders and to assess their potential impact on the behaviours of the Little Penguins.

Methods

Study species

Little Penguins breed from May through to January (Reilly & Cullen 1981; Johannesen et al. 2003; Colombelli-Négrel 2015b). During incubation and the first 2 weeks of chick-rearing (the guard stage), the male and female Penguins take turns to forage at sea while the other adult remains in the burrow to incubate the eggs or protect the young chicks (Miyazaki & Waas 2003). After the guard stage, both adults leave to forage during the day, returning at night to feed the chicks (Chiaradia & Kerry 1999). Clutch-size is usually two eggs, and Little Penguins can produce up to two clutches in one breeding season (Kemp & Dann 2001; Johannesen et al. 2003; Colombelli-Négrel 2015a,b). Little Penguin eggs hatch after an incubation period of 33–44 days and chicks fledge after 8–9 weeks (Kemp & Dann 2001; Numata et al. 2004; Chiaradia & Nisbet 2006; Colombelli-Négrel 2015a,b).

Study sites and monitoring with motion cameras

We monitored active burrows for four breeding seasons (2011–2014) between August and January at two locations in South Australia: Granite Island (35°37′S, 138°36′E) near Victor Harbor (2011–2014), and Emu Bay (35°39′E, 137°31′S) on Kangaroo Island (2013–2014). Granite Island is dominated by indigenous grasses with patchy woodlands and shrubs covering the lower areas, and it has a rocky granite coastline. It is accessed by a bridge causeway open to pedestrians from Victor Harbor on the mainland. Emu Bay is on the northern coast of Kangaroo Island, 18 km west of Kingscote. The Little Penguin colony there is located along a sandy beach and rocky coastline, and is close to human habitation.

We visited each colony every 2 weeks during the breeding season (August–January) for each study year (Granite Island: 2011–2014, Emu Bay: 2013–2014) and searched systematically for burrows. To identify potential terrestrial predators, each active burrow, once located, was monitored continuously until the chicks fledged or until reproductive failure or predation occurred. Twelve small motion-sensor-activated cameras were installed at different times at 35 active burrows (25 on Granite Island, 10 at Emu Bay). Two models of camera were used: Scout Guard KG680V Faunatech cameras (Faunatechaustbat, Australia) 140 mm × 102 mm × 74 mm powered by eight internal AA batteries; and Buckeyes Orion 5030-2 XIR cameras (BuckEye Cam, Australia) powered by a single 6V 12A rechargeable battery. Both camera models were weatherproof and captured 3-megapixel images either in

Little Penguin predators 3

Figure 1. Predatory visits by goannas to the Little Penguin colony at Emu Bay, Kangaroo Island, South Australia. (a) Goanna visiting a Penguin burrow with young chicks and adults but without predating it. (b–c) Goannas predating older chicks in their burrows. (d) Goanna scavenging a Little Penguin carcass. Photos: (a–c) from motion cameras, (d) Rochelle Davies

a c

b d

Little Penguins were assigned to three age categories based on size and plumage characteristics (colour of feathers, condition of feet and bill, body length, and weight): chicks (<8 weeks old; individuals that were mainly in or around their burrow at the time of death and had not been to sea, and thus had only had opportunities to encounter terrestrial predators); juveniles (individuals close to adult size, and with bright-blue undamaged feathers, that would have been just on the point of fledging) and adults. Individuals with a body length of ≤36 cm were considered as chicks; body length in juveniles and adults was 37–46 cm (DC-N unpubl. data). When possible, the sex (from examination of reproductive organs) and body condition (which indicates general health) were also assessed. In most cases, when birds are in good condition at the time of death, it is likely that death was acute and sudden.

Each Little Penguin was then assigned to one of the following categories associated with the circumstances of its death: trauma (terrestrial or marine predation), malnutrition, and unknown. This was based on evidence gathered at the time of collection in the field as well as during postmortem examination and subsequent pathology investigations. Sometimes there was more than one potential cause of death, e.g. some carcasses showed evidence of both disease and penetrating wounds

from predation. These penetrating wounds were not attributed to scavenging activity as signs found during the postmortem examinations confirmed that the wounds had occurred premortem.

Statistical analysis

SPSS 18.0 for Windows (SPSS Inc., Chicago, USA) was used for all statistical analyses. Differences in the number of visits by intruders between Little Penguin colonies (Emu Bay, Granite Island), predator/intruder types (rats, possums, cats, goannas) and Little Penguin breeding stages (eggs, young and older chicks) were tested using analyses of variance (ANOVA). The number of visits in relation to Little Penguin breeding stages was analysed separately for each predator/intruder type.

Results

Monitoring with motion cameras

Thirty-five active Little Penguin burrows were monitored, 25 on Granite Island (2011–2014) and 10 at Emu Bay (2013–2014). Twenty-one burrows were recorded during the incubation stage (Emu Bay 9, Granite Island 12) and 20 during the chick stage (Emu Bay 5, Granite Island 15). We analysed a total of c. 25 043 h of video images for

4 Australian Field Ornithology D. Colombelli-Négrel & I. Tomo

Figure 2. Intruder visits to Little Penguin colonies by cats (a–b), a Water-rat (c) and a Common Brushtail Possum (d), recorded by motion cameras at the study sites in South Australia. (a–b) Cats were seen only at Emu Bay (Kangaroo Island). (c) A Water-rat enters a Little Penguin burrow during the incubation phase on Granite Island. (d) Possums visited Little Penguin burrows significantly more often than any other intruder did and were observed looking inside burrows and smelling the immediate area a long time after chicks had left their burrows. Photos: from motion cameras

a c

b d

evidence of predatory behaviour or disturbance activity at burrows, and recorded a total of 422 visits from five species of intruders and potential predators: Goannas Varanus rosenbergi, feral cats, Black Rats, Water-rats, and Common Brushtail Possums Trichosurus vulpecula. There were significantly more intruder/predator visits on Granite Island than at Emu Bay (F1, 121 = 12.42, P = 0.001), and possums visited Little Penguin burrows significantly more often than did any other intruder/predator (F1, 121 = 4.75, P = 0.004). Of the 422 visits, only two resulted in predation, and both of these involved predation of Little Penguin chicks aged c. 6–7 weeks by goannas at Emu Bay during daytime (Figure 1b–c).

Goannas and feral cats were seen at Emu Bay but not on Granite Island, and no cats have been observed or reported on Granite Island during the study years (DC-N pers. obs.). We recorded a total of 11 goanna visits at six Little Penguin burrows and nine cat visits at four burrows (Figures 1, 2a–b). Goannas were also seen scavenging on fresh Little Penguin carcasses around active burrows (Figure 1d). There were significantly more goanna visits at burrows with chicks (young and older chicks) than at burrows with eggs (F2, 16 = 5.86, P = 0.01; Figure 3). There

was no significant difference in cat visits across Little Penguin breeding stages (F2, 16 = 0.08, P = 0.92; Figure 3). No interaction was seen between adult Little Penguins and cats or goannas.

Black Rats and Common Brushtail Possums were seen on Granite Island and at Emu Bay, whereas Water-rats were seen only on Granite Island (Figure 2). We recorded a total of 33 visits at 14 Little Penguin burrows by rats (Black Rats and Water-rats combined, as Water-rats were seen on only two occasions), and a total of 369 visits at 20 Little Penguin burrows by possums. There was no significant difference in rat (F2, 43 = 1.53, P = 0.23) or possum (F2, 43 = 0.23, P = 0.79) visits across Little Penguin breeding stages (Figure 3). Only one interaction between an adult Penguin and a Black Rat was observed: the Little Penguin appeared to guard the burrow from the intruding rat until the rat left the burrow area. Adult Penguins that were not protecting eggs or chicks ignored possums foraging around burrows but were cautious if guarding chicks, and retreated back into their burrow if a possum approached too close. Possum activity increased after Little Penguin chicks left their burrows.

Little Penguin predators 5

Penguin carcasses and necropsy

Twenty Little Penguin carcasses were found during this study (Emu Bay 15, Granite Island 5). Most carcasses from Emu Bay were found near the edge of the grassy habitat where Little Penguins can become visible to predators.

Age and body condition

More juvenile carcasses were collected on Granite Island (80%) than at Emu Bay (22%) (Table 1, Figure 4). No carcasses of chicks were found on Granite Island but four

were found at Emu Bay (45%) (Table 1, Figure 4). We confirmed the sex of four Little Penguin carcasses: one male and one female from Granite Island and two males from Emu Bay (Appendix 1). Only six carcasses (Granite Island 2, Emu Bay 4) could be assessed for body condition: all four individuals from Emu Bay had good body condition but only one of the two assessed from Granite Island did (Table 1, Appendix 1).

Principal cause of death

Because of the conditions of the carcasses when found, postmortem examinations could be conducted on only 14 individuals (Emu Bay 9, Granite Island 5: Table 1, Appendix 1). Based on the postmortem examination results, trauma was observed in six of the 14 carcasses. One Little Penguin was euthanased because of serious trauma. One Little Penguin from Granite Island was classified as having died of malnutrition, and for six others the cause of death could not be determined (Granite Island 2, Emu Bay 4: Table 1, Figure 5, Appendix 1). The latter included one Little Penguin from Emu Bay with brain haemorrhage and five (Granite Island 2, Emu Bay 3) for which the evidence was inconclusive.

Among the Little Penguins that had died from trauma, signs of both terrestrial and marine predation were observed. One from Granite Island and four from Emu Bay were suspected to be victims of terrestrial predation, and probable marine predation was noted for one bird from Granite Island and one from Emu Bay (Table 1, Figure 5, Appendix 1). Among the Little Penguins from Emu Bay that are likely to have been killed by a terrestrial predator, the distance between pairs of penetrating wounds (DPW) could be measured for two birds: in one individual, the DPW was 5 mm at the knee joint, and in the other it was 19 mm in the neck region. We attributed the latter to cat predation based on the facts that: (1) the DPW fell within the range of cat inter-canine distances (8.3–20.6 mm), (2) cats were 32-fold more common than dogs at Emu Bay (Achurch et al. 2013) and (3) no dogs have been observed in the colony during the study years (DC-N pers. obs.). For

Granite Island

Emu Bay

Total

Age category Chicks 0 4 4

Juveniles 4 2 6

Adults 1 2 3

Unknown 0 1 1

Body condition Good 1 4 5

Poor 1 0 1

CNBD 3 5 8

Probable cause of death

Malnutrition 1 0 1

Terrestrial predation

1 4 5

Marine predation

1 1 2

CNBD 2 4 6

Total 5 9 14

Table 1. Number of Little Penguin carcasses collected at Granite Island and Emu Bay (Kangaroo Island), South Australia, May 2011–November 2014, and categorised by age (chicks, <8 weeks old; juveniles, recently fledged/point of fledging), body condition, and probable cause of death. CNBD = could not be determined. See text for further details.

Figure 3. Average number of visits (mean ± standard error) per Little Penguin burrow by rats, Common Brushtail Possums, feral cats, and goannas on Granite Island and at Emu Bay (Kangaroo Island), South Australia, in relation to Little Penguin breeding stage. The data showed significantly more goanna visits at burrows with chicks than at burrows with eggs, but there was no significant difference across Little Penguin breeding stages for rat, possum or cat visits.

Figure 4. Little Penguin carcasses found on Granite Island and at Emu Bay (Kangaroo Island), South Australia. Little Penguin age catgories: chick (<8 weeks old), juvenile (recently fledged), adult, and unknown. The data showed that more juvenile carcasses were found on Granite Island (80%) than at Emu Bay (22%) and that no chick carcasses were found on Granite Island.

6 Australian Field Ornithology D. Colombelli-Négrel & I. Tomo

However, as with the study by Achurch et al. (2013), we observed cats checking burrows on Kangaroo Island, with 40% (4/10) of the monitored burrows being visited by cats. In addition, we found one chick carcass showing penetrating wounds interpreted as cat bite marks with an inter-canine distance of 19 mm (i.e. in the known inter-canine distance for cats: Ratz et al. 1999; Cuthbert 2003; Tedeschi-Oliveira et al. 2011). Two of the carcasses classified under probable terrestrial predation had their skin inside out, with one individual showing signs of skin lacerations and the other missing its abdomen and head, again suggestive of predation by cats. Cats often skin their prey, peeling the intact skin with the feathers away from the body, and chew through the sternum to open the thoracic cavity (Cuthbert 2003). Although caution must be exercised as the identity of the predatory species cannot be ascertained without eye-witness or genetic evidence from saliva, predation by cats is more likely than by dogs in this case, particularly because cats were found to be 32 times more common than dogs at this study site (Achurch et al. 2013). This is further supported by a previous study on Kangaroo Island that showed remains of Little Penguins in cat gut contents (Masters 2007). Our study also showed that the wounds found in carcasses had occurred premortem, thus providing evidence of predation rather than scavenging. The lack of detection of cat predation with motion cameras (Achurch et al. 2013; this study) suggests that cats do not prey on Little Penguins sitting inside their burrows; rather, they mainly prey on them when they venture out (thus targeting inexperienced birds such as chicks and juveniles, as demonstrated in this study), which would not be apparent on video monitoring at burrows.

This study also highlighted the role of goannas as predators of Little Penguin chicks, which, to our knowledge, is the first evidence of predatory activity by this reptile at active Little Penguin burrows. Goannas are a prominent species of lizard in Australia that prey on various animals (e.g. insects, smaller lizards, snakes, mammals, birds and eggs) and scavenge dead animals (King & Green 1999). In this study, we recorded two predation events, several visits by goannas before predation, and observed scavenging on carcasses. In addition, we found that goannas visited Little Penguin burrows with chicks more often than during the incubation period, perhaps to check the status of the burrows and for presence of adults. Further study should be considered to fully understand the impact of goannas on breeding success and survival of Little Penguins.

Although we included only carcasses found on land, far enough from the sea to ensure that the carcasses belonged to the monitored colonies, we found two carcasses of Little Penguins killed by probable marine predators, even though the bodies were found in grassland. The carcass found on Granite Island was of an adult bird with clear penetrating abdominal wounds and a DPW of 28.5 mm, suggestive of predation by a Long-Nosed Fur Seal. That at Emu Bay was a very young bird, classified as a recently fledged juvenile, and thus less likely (but not impossible) to have been to sea. Death of this bird was attributed to probable marine predation based on the DPW (43.3 mm) in the caudal abdominal region (suggesting predation by a Long-nosed Fur Seal) and the fact that it was missing most of its organs and had a bruise on its foot. It is possible that these two Little Penguins were predated near the shore, stranded on the beach, and then relocated by a scavenger.

the one Little Penguin on Granite Island probably killed by a terrestrial predator, the DPW (18.6 mm) was within the range of inter-canine distances for terrestrial predators. For the two Little Penguins likely to have been killed by marine predators, the DPWs were 43.3 mm (Emu Bay) and 28.5 mm (Granite Island), which are within the range of inter-canine distances for Long-Nosed Fur Seals. Details of postmortem examinations are presented in Appendix 1.

Discussion

This study is the first to identify terrestrial predators of Little Penguins by combining both motion-camera monitoring at active burrows and postmortem examination of carcasses. In particular, we provide evidence that, at Emu Bay (Kangaroo Island), goannas and cats are predators of chicks and juveniles. At this colony, terrestrial predation was identified for 44% (four of nine) of the carcasses analysed and carcasses of chicks were the most prevalent (representing 45% of all carcasses found).

Although previous studies suggested that Water-rats and Black Rats may have impacted breeding success of Little Penguins on Granite Island in the past (Bool et al. 2007), both motion-camera monitoring and postmortem analyses failed to provide any evidence of predation on Little Penguin chicks on this island. This confirms results of more recent studies that showed no predation at active burrows since 2012 (Colombelli-Négrel & Kleindorfer 2014; Colombelli-Négrel 2015b), most likely as a result of intense rat-baiting on Granite Island during the 2006 breeding season (Bool et al. 2007). On the contrary, most Little Penguin carcasses found (80%, n = 5) were juveniles (or recently fledged Little Penguins), supporting the hypothesis that low return rates of subadults on Granite Island result from high mortality in the first 2 years of life (Colombelli-Négrel 2015b).

Feral cats are recognised predators of adult Little Penguins in Australia (Stahel & Gales 1987; Masters 2007; Stevenson & Woehler 2007). In this study, we found no evidence of cat predation with the motion cameras.

Figure 5. Causes of death assigned to Little Penguins found as carcasses on Granite Island and at Emu Bay (Kangaroo Island), South Australia: malnutrition, trauma (terrestrial predation and marine predation), and unknown. Terrestrial predation varied from 20% of carcasses found on Granite Island to 44% at Emu Bay.

Little Penguin predators 7

Identifying the cause of death from carcasses is not always simple because the conditions of the carcasses when found can be quite complex and misleading (Hocken 2000, 2002). The only way to prove predation is to obtain direct evidence, via observation or video monitoring, but, as demonstrated in this study, this can be difficult because predation events are generally unpredictable both in time and space (see also Robinson & Robinson 2001; Colombelli-Négrel et al. 2009). Body condition at the time of death can be a good indicator for predation because the death of an individual in good body condition is likely to have been sudden and thus most likely to have been caused by predation (especially in conjunction with recognisable teeth marks on the skin or subcutaneously). However, postmortem factors, such as the impacts of scavengers, can mask the real cause of death. For example, goannas tend to swallow live prey whole, but tear up carcasses while shredding their skin and meat (M. Hutchinson pers. comm. 2015), which would mask evidence of any other predators. This study thus clearly highlights the critical importance for researchers to rely on a combination of both direct and indirect evidence to deduce the exact cause of death and to identify potential predators.

Analysis of Little Penguin carcasses in South Australia commenced in 2011, predominantly in Encounter Bay and on Kangaroo Island, and indicated that the dominant cause of death was trauma (particularly probable predation by terrestrial predators on Kangaroo Island: Tomo 2012, 2014). The present study supports these findings, demonstrating the impact of terrestrial predation using both pathology examinations and motion-camera monitoring. Although the sample size was very small (only 14 carcasses analysed and two predation events recorded), it is important to note that population censuses have shown <15 active burrows each year over the last 2 years on Granite Island and that only 18 active burrows were found at Emu Bay in 2014 (Colombelli-Négrel & Kleindorfer 2014; Colombelli-Négrel 2015a). In addition, five (31%) burrows of the 16 monitored on Kangaroo Island during the 2014 breeding season showed evidence of predation during the chick stage (Colombelli-Négrel 2015a), supporting our results showing high predation of chicks on Kangaroo Island. We predict that predation of chicks at such a rate in a small colony would have a significant impact on its long-term population trend. Further monitoring of predation on Kangaroo Island is therefore required to understand its full impact on breeding success and consequent impact on population decline.

AcknowledgementsWe thank the Adelaide and Mt Lofty Ranges Natural Resources Management Board, the Department of Environment, Water and Natural Resources, the Nature Foundation of South Australia, the Lirabenda Endowment Research Fund, and BirdsSA for funding. Special thanks go to Tony Flaherty and Sonia Kleindorfer for their continued support of the project. Thanks also go to Annelise Wiebkin for advice on penguin research, and to Martine Kinloch, Kym Lashmar and Alicia McArdle for their help in monitoring the Little Penguin populations on Kangaroo Island. Many thanks go to Stefan Szwedzinski for preliminary analyses of the video data in 2012 and data collection. Thanks go to Vanessa Owens, Katharina Peters, Anna Koetz, all the volunteers who helped collect the data and the local volunteers who collected the carcasses. Thanks go to Rochelle Davies for the picture of the scavenging activities of the goannas. Many thanks go to Tomoyo Segawa for her help with the postmortem examinations and to

Mark Hutchinson for information on the natural behaviours of the goannas. Many thanks go to Karen Bath, Peter Shaughnessy, Philippa Horton and Mark Hutchinson for helpful comments on the manuscript. This project was approved by the Flinders University Ethics Committee (E388) and is supported by a scientific permit to conduct the research (Y26040).

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Little Penguin predators 9

Record Date (day, month, year) Age Sex Body condition Circumstances of death Evidence for predation

Emu Bay

EM122 8.10.11 C U G Euthanased. Evidence of trauma, possible terrestrial predation

Penetrating wounds. DPW 5 mm

EM127 20.11.11 U U CNBD ? Limited sample

EM243 21.09 11 A M G ? Brain haemorrhaging acute

EM265 23.10.14 J U CNBD Trauma (probable terrestrial predation)

Skin inside out, missing abdomen and head

EM266 23.10.14 A U CNBD ? Limited sample

EM268 24.10.14 C M G Trauma (probable terrestrial predation)

Penetrating wounds. DPW 19 mm

EM269 21.09.14 C U CNBD ? Limited sample

EM270 22.09.14 J U G Trauma (probable marine predation)

Missing abdomen. DPW 43.3 mm

EM273 8.10.14 C U CNBD Trauma (probable terrestrial predation)

Skin laceration, skin inside out

Granite Island

EM84 6.09.11 J F P Malnutrition

EM151 22.05.11 J U CNBD Trauma (probable terrestrial predation)

Penetrating wounds. DPW 18.6 mm

EM157 3.06.12 J U CNBD ?

EM175 9.09.12 A M G Trauma (probable marine predation)

Penetrating wounds. DPW 28.5 mm

EM259 20.10.14 J U CNBD ? Head missing. No other sign of predation.

Appendix 1. Information from results of postmortem examination for Little Penguin carcasses from Emu Bay (Kangaroo Island) and Granite Island, South Australia. Age: A = adult, C = chick, J = juvenile, U = unknown; sex: F = female, M = male, U = unknown; body condition: G = good, P = poor, CNBD = could not be determined; circumstances of death: ? = unknown; evidence for predation: DPW = distance between pairs of penetrating wounds.