Introduction

Marine turtles are caught and slaughtered for consumption as part of traditional indigenous community harvest in Australia as well as in many other countries in which marine turtles can be found.

In early March 2012, a story aired on Australian national television that questioned the traditional hunting practices and illegal trade of turtles and dugongs; two iconic species of conservation concern (http://www.abc.net.au/7.30/content/2012/s3448943.htm). The result was a public backlash causing the state of Queensland Government’s Animal Care and Protection Act 2001 to be changed to remove the exemption from animal welfare obligations that existed for Aboriginal and Torres Strait Islander people acting according to their 4000-year old Islander custom. An offence exemption is now included to ensure that these animals when killed in the exercise of Aboriginal tradition or Island custom are killed in a way that causes as little pain as is reasonable. By definition, this change of wording elevated the slaughter of marine turtles to require elements of euthanasia in alignment with modern abattoir practices. Slaughter is the killing of animals for preparation of meat for human consumption, whereas euthanasia (Gk “good death”) is an easy or painless death [1].In response to this change in legislation, the Torres Strait Regional Authority (TSRA), under guidance from the Great Barrier Reef Marine Park Authority (GBRMPA) and Queensland Department of Environment and Heritage Protection (EHP), determined that a humane alternative to current traditional hunting practices to slaughter marine turtles was warranted. Such an alternative would permit hunters to continue traditional practices within the rules of the legislation.

Conventional methods for the slaughter of livestock for human consumption includes captive bolt and gunshot, electric stunning and electrocution, carbon dioxide stunning, decapitation and cervical dislocation, and ritual slaughter. Captive bolt and gunshot requires the penetration of a projectile through the skull into the brain. Non-penetrating projectiles, such as mushroom guns only deliver concussive forces and do not achieve euthanasia alone. Electric stunning and electrocution induce instantaneous unconsciousness that allow for euthanasia via exsanguination. Carbon dioxide stunning involves holding groups of animals in chambers where gas is injected to displace the oxygen resulting in anaesthetising and asphyxiation. Decapitation and cervical dislocation involve the separation of the head from the body and/or the breaking of the spinal cord to prevent sensory stimulation of the body to the brain. Ritual slaughter involves exsanguination by cutting the throat [2, 3]. In many Torres Strait Island communities, ethically-acceptable euthanasia solutions (e.g. lethal injection drugs, such as sodium pentobarbitone) and weapons, including firearms, captive bolt guns and stun guns, are restricted without special licenses and risk harm to those using them or eating meat from animals killed this way. Consequently, conventional methods are not readily available to indigenous hunters.

The right to hunt a marine turtle by Indigenous Australians is considered an earned cultural privilege within communities and only allowed when a high level of skill is achieved after years of training by elder hunters. For many of the sea faring communities, turtles and dugongs are totem animals, for which the slaughter of these animals is done with great respect. Consequently, hunters are attuned to determining a live, unconscious and dead animal as well as show a high level of empathy with their totem animal. Traditional Owner methods of slaughter vary between communities. In general, the turtle is placed on its carapace and (1) a sharp blow is delivered to the rostrum or the top of the head by a large stone when the turtle’s head is extended clear of the carapace (“stone method”); or (2) a palm frond is taken and stripped of leaves to create a sharp probe that is inserted through the nasal cavity (“broom stick method”). Both methods are simple and use freely available resources. To keep with the practicality and acceptance of these methods, a simple device with minimal moving parts was required for a viable alternative.

The proposed device would need to stabilise the skull and restrict head movement for the reliable direction of a sharp probe through the hindbrain (by ‘pithing’- the destruction of the central nervous system) and severing of the spinal cord ensuring death and ablation of any sensation or nervous communication between the body and the brain. Ablation of the hindbrain by pithing, including severing of the spine, is considered successful in achieving rapid painless death by replicating pithing and decapitation in a single function. Pithing and decapitation causing destruction of the brain and spinal cord is recommended by the American Veterinary Medical Association’s Guidelines on Euthanasia [4] as an acceptable combination method for the euthanasia of reptiles of all sizes.

Work and Balazs [5] demonstrated a sharp blow to the head with a pointed probe can effectively penetrate the skull in a small Hawaiian green turtle (Chelonia mydas). Considerations that need to be taken into account when using this principle to dispatch a large reptile with a solid exoskeleton are (1) the mobility of a healthy green turtle even if placed on its carapace or restrained; (2) the elasticity of the skull to percussive insults; (3) reliably being able to position the probe to ablate the hindbrain from a dorsal approach (as turtle forebrain insults are seldom fatal); (4) the need for a ‘single blow’ slaughter method to cause rapid death; (5) indigenous community restrictions; (6) indigenous and wider community perception; and (7) the need for a durable device with few moving parts that will not wear out or fail with prolonged exposure to marine elements.

The aim of this project was to establish an alternative option for the humane slaughter of marine turtles by meeting the following objectives:

1. Develop a euthanasia harness device for testing;
2. trial the harness in a step-wise manner on carcasses through to live healthy marine turtles;
3. engage the indigenous communities in trialling the device and providing feedback to its effectiveness and suitability as an alternative option to current practices.

Materials and Methods

The University of Queensland Animal Ethics Committee Approval number: SVS/382/13/TSRA; The University of Queensland Behavioural and Social Sciences Ethical Review Project Number: 2012000895; Field Permit: Department of Environment and Heritage Protection Permit Number: WISP1199511.

Device development

There were four device iterations (Device 1–4) developed and tested from the first prototype in July 2012 through to the device left among the communities at the conclusion of the project between May and November 2015 (Fig 1). Each followed the same principle of penetrating the hindbrain and severing the spinal cord by introduction of a 9 mm diameter × 240 mm long probe perpendicularly through the dorsal surface of the skull at the caudal aspect of the frontoparietal scale to penetrate at least 140 mm into the adult skull to ensure severing of the spinal cord after passing through the hindbrain. Each device positioned and secured the probe with a guide placed above the frontoparietal scale, which was either a head brace, such as used in Device 1, or a head plate and strap, such as used in Device 4. Each device had an interchangeable 9 mm stainless steel probe sharpened to a rounded or chisel point at one end and a strike plate for the sledgehammer welded on the other end. As such, devices were considered the same with respect to testing the effectiveness of its use as a tool to kill marine turtles. Modifications throughout the trial were to create a more robust product and encourage community acceptance of the device. Device 4 was developed post Community feedback and was considered the most likely device to be adopted by hunters. Probe deployment was made by a single blow from a 5 kg sledgehammer “dropped” with moderate hand-operated downward force directly vertically from approximately 50 cm above the strike plate.

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Fig 1. Device evolution throughout the project.

All conform to the same mechanism of action.

https://doi.org/10.1371/journal.pone.0167849.g001

Device 1 was a frame prototype of a proposed enclosed box that would contain the turtle’s head and discourage movement. A head brace maintained the caudal frontoparietal scale under the probe for a range of head sizes. This maintained the strike site in the same place.

Devices 2 and 3 created a small head plate and probe guide that could be affixed to the head of the turtle immediately above the frontoparietal plate. A strap affixed the device in place.

Device 4 refined the previous devices, following trials with each device, by shortening the probe and curving the head plate to better fit the skull and stay in position.

Results

Carcasses

For the 11 carcasses on which the devices were deployed, this method was considered successful for nine carcasses (81%, 9/11; 95% CI 48.2–97.7; Fig 2). For the two failures, in both cases the probe did not penetrate the cranial case, rather deflected off to the side within the skull.

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Fig 2. Device deployment, path of insertion and resultant destruction of the brain and spinal cord.

Typical (A) presentation for correct penetration of the device through the skull at the caudal aspect of the frontoparietal scale; (B) longitudinal section showing passage of probe (encircled) with severed spinal cord (green) and ablated hindbrain with fore (yellow) and mid (red) brain intact; (C) gross appearance of a brain that has successfully had the device deployed where the hindbrain is ablated (large circle) and spinal cord (small circle) is severed; and (D) the resultant histology showing separation of the spinal cord (arrows) and the disrupted architecture of the hindbrain.

https://doi.org/10.1371/journal.pone.0167849.g002

Live turtles

Five turtles were anaesthetised prior to device deployment and two were slaughtered by local indigenous hunters in country while the researcher was present as part of the device trails. In all cases, deployment was measured as successful with an average of 96.7 seconds (10 seconds to 180 seconds) from deployment to confirmed death (Table 1). Where gross examination and histology were performed on the brain, findings were consistent with those reported for probe deployment on the carcasses.

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Table 1. Duration from deployment of device to confirmed death of the turtle in live turtles.

https://doi.org/10.1371/journal.pone.0167849.t001

Death was confirmed by absence of respiration, deep pain reflex and palpebral reflex. Heart beat was considered a secondary assessment tool.

Discussion

This research met the aim to establish an alternative option for the humane slaughter of marine turtles for the participating Torres Strait Island Communities. It also met each of its three objectives: (1) We developed an effective euthanasia harness device; (2) We trialled the harness in a step-wise manner on carcasses through to live healthy marine turtles to ensure a robust effective design that repeatedly ablated the hindbrain and severed the spinal cord when deployed correctly; (3) We engaged the indigenous communities in developing and trialling the device through visits and feedback in an attempt to develop a device with indigenous input, ownership and thus optimise the likelihood of community acceptance.

Over 3.5 years of testing, we built on the preliminary study conducted by our colleagues in Hawaii [5] and developed a device capable of penetrating the skull using a 9 mm stainless steel probe over the caudal aspect of the frontoparietal scale. When correctly positioned and deployed with sufficient force, the probe was able to pass through the caudal aspect of the brain and effectively ablate the hindbrain and sever the spinal cord (Fig 1), rendering death. In reptiles, it is inherently difficult to confirm death. We employed the loss of palpebral reflex, menace response, jaw tone, spontaneous respiration, deep pain and cardiac activity as indicators of death. It is common for cardiac function to cease and spontaneously regenerate several minutes later in many reptile species under duress or persist in reptiles even after removal from the body. As such, presence or absence of a heart beat was not considered conclusive in death. Cellular death (vs prolonged loss of consciousness) is facilitated by pithing [4], which the device tested in these trials achieves by the probe ablating the hindbrain. Traditional Owner slaughter practice also facilitates this process of death as turtles are immediately fully bled (achieving exsanguination) so the blood can be collected before it congeals, and the carcass butchered.

In this study, histology was limited to confirming that target structures had been destroyed and the extent of destruction (Fig 2d). From the live animals that were successfully euthanized while under anaesthesia, it was shown that death occurred even if only 50% of the hindbrain and spinal cord was disrupted. Minimal tissue destruction requirements were not determined, but at least 50% disruption is fatal.

The device successfully achieved euthanasia via two mechanisms. (1) Ablating the hindbrain and (2) severing the spinal cord. Ablation is the equivalent of pithing which is the destruction of neural tissue rendering the recipient to have no cognitive function or feel pain [1]. Severing the spinal cord is the nervous equivalent to decapitation (removal of the head) [1], whereby the organs are deprived of all involuntary functions. Ablation (pithing) and decapitation comply with international standards for humane euthanasia in a large reptile [4].

These methods should be suitable for use in food animals, with minimal production and systemic dissemination of brain emboli, and rapid achieving of death. Although pithing is not recommended in animals intended for human consumption due to risk of embolism of brain tissue containing specified risk material into the lungs or muscles that are eaten [9], there is no known specified risk material (e.g. bovine spongiform encephalitis prions in cattle) in a wild caught healthy marine turtles of the Torres Strait. When deployed on live animals, the device was effective in causing death between 10 seconds and 3 minutes (Table 1). This is within acceptable timeframes identified in slaughter of livestock [2].

Although capture, restraint and traditional slaughter were untested in this research, traditional slaughter methods may have merit as a humane hunting practice. The alternatives to this proposed device are the stone and broomstick methods. These methods have been long used by hunters within the Torres Strait communities and are reported to be effective methods of slaughter. They may cause shock to the cranial and peripheral nerves associated with the head causing a sensory overload to the brain and result in loss of consciousness allowing for slaughter to be humanely performed by exsanguination. In this respect, these methods may be a variance of the standard electrical stunning that results in instantaneous loss of consciousness and tonic-clonic muscular movement. These practices are used in a range of species of different sizes in abattoirs throughout the world [2].

Limitations to this device were noted during the carcass and live turtle phases. For successful deployment of the device, it needed to be positioned correctly, both over the right place on the skull but also deployed at the right angle (perpendicular to the top of the skull in both planes). To maintain this position, time was required to fit the device correctly. When this was not achieved, the probe missed the hindbrain and spinal cord. While device fitting was easily achieved under laboratory conditions, it was more of a challenge in healthy, active animals and a negative experience for indigenous hunters. Better design to secure the device such as a head-clamp is required. If the device misfires and does not achieve hindbrain ablation and spinal cord severing in one percussive blow, it is recommended the device be immediately redeployed. Alternative traditional methods may be of use under these circumstances, but cannot be recommended until they are tested. Improvements to the device design could include a single fitting piece that secures the head plate to the skull such as a flexible clamp and a handle to allow control of the head once the device is secured. Any modifications should be done in consultation with communities and consider the harshness of the marine environment to moving parts and durability.

Other negative feedback from the communities were concerns about the need and design of the device including usability in country and concerns over loss of traditional practice, repercussions of project outcomes and preference to use their traditional methods over the device. Hunters felt traditional methods were equally humane and more than one person was required to use the device. However, they expressed a willingness to continue to trial and refine the device to create an agreeable design that can be used by a single hunter to humanely slaughter a marine turtle in a quick and effective manner and comply with changing legislation.

An objective of this project was not to develop a device to replace existing traditional methods, but to provide an alternative method for optional adoption. The next step in this investigation should include ongoing work with the communities to produce a device that is acceptable to the hunters and encourage adoption. Once this has been achieved, support for use by managers and use by government staff as an ancillary tool for marine turtle euthanasia may benefit the wider community. Consultation is needed to define the requirements for endorsement by government and veterinary officials, including acceptance as part of standard reptile euthanasia guidelines and slaughter guides [3, 4]; although this device has so far met the standards outlined by welfare guides.

Conclusion

The device developed severs the spinal cord and ablates the hindbrain in a manner that is in accordance with recommendations by the AVMA Guidelines on euthanasia for reptiles and would achieve the requirements of the Animal Care and Protection Act 2001 to cause as little pain as is reasonable. Indigenous communities were supportive of the device although there will be much needed roll-out, including modification, further trialling and extensive communication, before the alternative device is preferred to traditional hunting practices. There is no governmental requirement to investigate currently-used traditional hunting methods or for hunters to use the device we present here.

Supporting Information

Acknowledgments

The authors wish to thank the Torres Strait Regional Authority staff for all of their help, guidance, and organisation throughout this project; The University of Queensland Animal Ethics Committee for constructive feedback for each stage of this project; the Steering Committee formed to advise on this project with experts from the Torres Strait Regional Authority, Queensland Department of Environment and Heritage Protection, Great Barrier Reef Marine Park Authority, Royal Society for the Prevention of Cruelty to Animals Queensland, James Cook University, Department of Agriculture and Fisheries- Animal Welfare unit, Australian Institute of Aboriginal and Torres Strait Islander Studies, and Australian Fisheries Monitoring Authority; external advisers including Dr. Col Limpus (Department of Environment and Heritage Protection), Mr. George Balazs (National Oceanic and Atmospheric Administration) and Dr. Thierry Work (United States Geological Survey); and the Torres Strait Island communities of Masig, Badu, Mabuiag, and Moa Islands.

All animal research was performed under Scientific Purposes Permit (through DEHP-WISP11995112) and Animal Ethics Number (through UQ- SVS/342/12/TSRA). All interactions with indigenous communities was performed under Human Ethical Clearance Number (through UQ- 2012000895).