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Within this context we describe a series of unusual observations of C. caretta, found dead or dying in eastern Australia (southeast Queensland and northern New South Wales) during 2000 with porcupine fish, Family Diodontidae, lodged in their posterior buccal cavities (Figure 1). Prior to this, records of marine turtles ingesting porcupine fish have been scarce and the death of marine turtles in eastern Australia resulting from ingestion of natural prey species has been considered a rare event. The reasons for the increased incidence of this previously rare event are not clear, nor are there apparent reasons for the cessation of this type of mortality after 2000.

Tagging-recapture studies of C. caretta in eastern Australian foraging areas began in 1974 (Limpus 1985; Limpus et al. 1994) with associated observations on feeding behaviour. In Queensland and northern New South Wales stranded marine turtles are systematically recorded and, in many cases, necropsied to assess causes of death and gather biological data including diet information. Records of moribund and dead marine turtles in Queensland are summarised in STRANDNET, the Marine Wildlife Stranding and Mortality Database managed by the Queensland Parks and Wildlife Service (QPWS) (Haines et al. 2000). The present study summarises information regarding ingestion of porcupine fish contained in the QPWS tagging research database and STRANDNET. Individual turtles are identified by tag number or STRANDNET identification number (prefix plus numeral). The standard measurements of turtles in these studies are the midline curved carapace length (CCL) and the length of the extended tail from tip to the midline rear of the carapace (TLC), measured with a flexible tape. Sex and maturity of turtles was determined by gonad examination or on tail measurements (Limpus et al. 1994).

Since the commencement of capture-tagging studies in eastern Australian foraging areas in 1974, no turtle has been observed attempting to eat a porcupine fish. However, an adult male C. caretta was captured on Wistari Reefs (23.483°S, 151.883°E, southern Great Barrier Reef) in 1977 with the spine of a porcupine fish (Diodon sp.) embedded in the roof of its mouth (Moodie, 1979). There was nothing unusual noted for the behaviour of this turtle when it was captured. Prior to 2000 there had been only one record of C. caretta ingesting porcupine fish (Limpus et. al. 2001) among the hundreds of stranded C. caretta examined by necropsy in eastern Australia:

20 July 1996: An adult male C. caretta (X10778: CCL =96.0 cm) stranded dead in western Moreton Bay (27.183°S, 153.366°E). At necropsy it was found to have a 21cm long porcupine fish (Diodon liturosus) in the stomach and lacerations to the oesophagus and anterior stomach thought to have been caused by the fish spines. Throughout the remainder of the digestive tract, the food remains were mostly of crabs (Eucrates dorsalis and Galene bispinosa), some mantis shrimp (Squilla sp.) and minor amounts of swimming crab (Portunus sanguinolartus) and other fish.

During 2000, six cases of dead or moribund C. caretta with porcupine fish lodged in their mouths and throat were reported to STRANDNET from southeast Queensland and northern New South Wales of eastern Australia:

22 January 2000: An immature C. caretta (K10525: CCL=84.7 cm, TLC=1.6 cm) was behaving abnormally, swimming at the surface in the mouth of Tallebudgera Creek (28.10°S, 153.467°E) on the Gold Coast, south Queensland. On capture it was found to have no recent external injuries but to have a porcupine fish (Diodon sp.) tightly lodged in the back of the mouth and anterior oesophagus. The fish was obstructing its feeding and breathing. On removal of the porcupine fish, the turtle’s tongue was quite swollen. The turtle was retained in rehabilitation and fed squid and small fish but not medicated. It regained its normal swimming behaviour within 24 hr and was released to the wild on 8 February 2000.

25 February 2000: An immature male C. caretta (Z4034: CCL=86.0cm, TLC=5.0cm) was stranded dead with no recent external injuries at Broadbeach (28.027°S, 153.435°E) on the Gold Coast, south Queensland. At necropsy it had a porcupine fish (Diodon sp.; length ~15 cm) stuck in the back of the mouth; stomach contents included a pipefish (Syngnathidae) and a lizardfish (Synodontidae); small intestine contained a large volume of swimmer crab remains (Portunus); and large intestine contained a piece of porcupine fish skin with spines, a large volume of crab remains and some small fish bones.

27 February 2000: An adult male C. caretta (Z4039: CCL=94.0 cm, TLC=19.0 cm) was stranded dead with no recent external injuries at New Brighton (28.50°S, 153.55°E), via Brunswick Heads, northern New South Wales. At necropsy it was found to have an inflated porcupine fish (D. liturosus) stuck in the posterior buccal cavity and to have “thousands” of spines from the same species of porcupine fish in several clumps plus some crab remains in the intestine. This turtle had good body condition with respect to muscle and fat development.

29 March 2000: A pre-pubescent immature male C. caretta (Z4654: CCL=85.5 cm, TLC=-2.2 cm) was stranded dead with no recent external injuries but with a “swollen” throat area and bleeding freely from the mouth at Kirra Beach (28.1683°S, 153.5357°E), Gold Coast. At necropsy it was found to have a deflated porcupine fish (D. liturosus) stuck in the posterior buccal cavity; two spider crabs in the anterior stomach; and a large quantity of fragments of several species of crab, including Portunus sp., and the remains of two porcupine fish Diodon sp. in the intestine. This turtle had good body condition with respect to muscle and fat development.

11 April 2000: A pubescent immature male C. caretta (Z4764: CCL=92.5 cm, TLC=16.5 cm) was stranded dead at Narrow Neck (27.988°S, 153.429°E), Gold Coast. It had no recent external injuries but had a “swollen” throat area. A rope, not recently tied, was partly constricting the proximal humeral area of the right front flipper. At necropsy it was found to have an inflated porcupine fish (D. liturosus) lodged firmly in the posterior buccal cavity (Fig. 1). At stranding, this turtle had good body condition with respect to muscle and fat development.

Figure 1. Porcupine fish (Diodon liturosus) lodged in the posterior buccal cavity of a freshly dead, stranded loggerhead turtle, Caretta caretta (Z4764), Gold Coast, Australia, 11 April 2000.

23 December 2000: An adult female C. caretta (T23923: CCL=101.0 cm) was stranded dead with no external injuries at Fingal Beach, Tweed Heads (28.2013°S, 153.5696°E), northern New South Wales. At necropsy it was found to have an ~10 cm diameter porcupine fish, Diodon sp., embedded in the back of the throat and some crab remains in the intestine. She had been previously recorded breeding at the Moore Park rookery (24.733°S, 152.333°E) in south Queensland during three breeding seasons in 1985-1986, 1989-1990 and 1994-1995. This female had no enlarged ovarian follicles at the time of her death and hence was not in the Tweed Heads area for breeding. She was presumably there for feeding.

There were no signs to indicate that anything other than the ingestion of porcupine fish had been the primary cause of death or debilitation for these turtles.

In a South African study, Hughes (1974) reported one C. caretta killed by a porcupine fish, Diodon sp., “jammed in the oesophagus”. In his extensive review of C. caretta prey taxa, Dodd (1988) listed no other reference to Diodon sp. in C. caretta diet. Worldwide, C. caretta do not normally capture live fish but feed primarily on invertebrates (Dodd, 1988). In contrast, within inshore waters of southeast Queensland during the late 1990s, C. caretta have been recorded repeatedly preying on fish among discarded trawl bycatch (Limpus et al. 2001). In the present study, the Moreton Bay (X10778) and Broadbeach (Z4034) specimens each had a total gut content that was consistent with the turtle having scavenged on discarded trawl bycatch.

It has not been possible to identify any natural increases in populations of porcupine fish in inshore waters of southeast Queensland to account for the increased incidence of porcupine fish induced mortality among C. caretta during 2000. However, C. caretta in this area are known to feed on fish carcasses floating at or near the water surface (Limpus et al. 2001). Inflated porcupine fish will float at the surface. If porcupine fish were among discarded bycatch from the trawlers that operated in the area, most of the bycatch would sink, resulting in a concentration of porcupine fish at the surface. This could result in a situation in which individual C. caretta could repeatedly access porcupine fish. There had been a progressive introduction of turtle excluder devices (TEDs) and other bycatch reduction devices into the trawl fisheries of southeast Queensland since 1999 until the compulsory regulation of TED use by prawn trawlers in April 2000. However, there is no recognised association between the use of these bycatch reduction devices (BRDs) and an increased accessibility to porcupine fish for foraging turtles.

Given the low incidence of porcupine fish in past diet records of C. caretta in Australia (Conway 1994; Limpus et al. 2001; Moodie 1979) and overseas (Dodd 1988), it is unlikely that C. caretta capture healthy, actively swimming porcupine fish on a regular basis. However, if they are ingested alive it appears that the porcupine fish can lodge in the back of the buccal cavity or upper oesophagus and inflate, as is a characteristic of these “pufferfish”. Under such circumstances, the turtle would be unable to swallow the fish. With the spines of the distended fish embedded in the soft tissue at the rear of the buccal cavity, the turtle would be unable to easily remove the fish from its mouth and the turtle could be expected to die from asphyxiation.

Fish of the Order Tetraodontiformes, including porcupine fish, produce the potent toxin, tetrodotoxin, in their flesh and organs (Sutherland 1983). However, given that three of the turtles (Z4034, Z4039, Z4654) had ingested and digested specimens of Diodon sp. previously without fatality, it is unlikely that these C. caretta died from tetrodotoxin poisoning. However, the possibility that these turtles were poisoned as a result of having damaged specimens of these toxic fish in their mouths cannot be discounted totally.

Z4039, during days or weeks prior to its death, had been feeding primarily on Diodon sp. Such prey selectivity is not expected when these turtles feed on discarded trawl bycatch. While there is a high probability that the C. caretta in this study accessed porcupine fish as food items while scavenging on dead and/or debilitated fish, presumably resulting from discarded trawl bycatch, there remains the possibility that some individuals selectively feed on porcupine fish, perhaps even in the absence of fishing activities.

C. caretta has a severely depleted population in eastern Australia. It is listed as an endangered species in Queensland and Australia (Queensland Nature Conservation Act, 1992; Endangered Species Act, 1992). Any repetitive source of C. caretta mortality from anthropogenic sources is undesirable from a conservation perspective. If it is assumed that these deaths of C. caretta that fed on porcupine fish in eastern Australia were not entirely natural and are tentatively linked to turtles feeding on discarded fisheries bycatch, then the incidence of porcupine fish in trawl bycatch and the behaviour of the fish in response to BRDs warrant further study. In addition, the continued monitoring of stranded turtle carcasses to determine cause of death and to collect associated biological data remain the most effective method for detecting changes in mortality factors operating on turtle populations in coastal waters.

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