Humane Slaughter of Edible Decapod Crustaceans
Abstract
:Simple Summary
Abstract
1. Introduction
2. Nociception, Pain and Stress in Decapods
3. Legislation Related to Decapod Protection and Welfare at the Time of Killing
4. Stunning and Slaughter Methods
4.1. Electrical Stunning/Slaughter
4.2. Stunning and Slaughter by Cold
4.3. Drowning in Fresh Water
4.4. Salt Baths
4.5. Splitting
4.6. Spiking
4.7. Carbon-Dioxide (CO2) Narcosis
4.8. High-Pressure Killing
4.9. Dismemberment
4.10. Boiling
5. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- Elwood, R.W. Evidence for pain in decapod crustaceans. Anim. Welf. 2012, 21, 23–27. [Google Scholar] [CrossRef]
- Sherwin, C.M. Can invertebrates suffer? Or how robust is argument-by-analogy? Anim. Welf. 2001, 10, S103–S108. [Google Scholar]
- Broom, D.M. Considering animals’ feelings. Anim. Sentience 2016, 5, 1–11. Available online: https://www.wellbeingintlstudiesrepository.org/cgi/viewcontent.cgi?article=1015&context=animsent (accessed on 7 April 2021). [CrossRef]
- Elwood, R.W. Discrimination between nociceptive reflexes and more complex responses consistent with pain in crustaceans. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2019, 11, 374. [Google Scholar] [CrossRef] [PubMed]
- Diggles, B.K. Review of some scientific issues related to crustacean welfare. ICES J. Mar. Sci. 2019, 76, 66–81. [Google Scholar] [CrossRef]
- Sneddon, L.U. Comparative physiology of nociception and pain. Physiology 2018, 33, 63–73. [Google Scholar] [CrossRef]
- Puri, S.; Faulkes, Z. Can crayfish take the heat? Procambarus clarkii show nociceptive behaviour to high temperature stimuli, but not low temperature or chemical stimuli. Biol. Open 2015, 4, 441–448. [Google Scholar] [CrossRef] [Green Version]
- Rose, J.D.; Arlinghaus, R.; Cooke, S.J.; Diggles, B.K.; Sawynok, W.; Stevens, E.D.; Wynne, C.D.L. Can fish really feel pain? Fish Fish. 2014, 15, 97–133. [Google Scholar] [CrossRef]
- Broom, D.M. Cognitive ability and sentience: Which aquatic animals should be protected? Dis. Aquat. Org. 2007, 75, 99–108. [Google Scholar] [CrossRef] [Green Version]
- Elwood, R.W.; Barr, S.; Patterson, L. Pain and stress in crustaceans? Appl. Anim. Behav. Sci. 2009, 118, 128–136. [Google Scholar] [CrossRef]
- Lopez-Bellido, R.; Himmel, N.J.; Gutstein, H.B.; Cox, D.N.; Galko, M.J. An assay for chemical nociception in Drosophila larvae. Phil. Trans. R. Soc. B 2019, 374, 20190282. [Google Scholar] [CrossRef] [Green Version]
- Barr, S.; Laming, P.R.; Dick, J.T.A.; Elwood, R.W. Nociception or pain in a decapod crustacean? Anim. Behav. 2008, 75, 745–751. [Google Scholar] [CrossRef]
- Ali, M.A. Nervous Systems in Invertebrates; Plenum Press: New York, NY, USA, 1987. [Google Scholar]
- Derby, C.D.; Steullet, P. Why do animals have so many receptors? The role of multiple sensors in animal perception. Biol. Bull. 2001, 200, 211–215. [Google Scholar] [CrossRef]
- Cate, H.S.; Derby, C.D. A chemo-mechanosensillum that is ubiquitous on the Caribbean spiny lobster and other lobster species. Soc. Neurosci. Abstr. 2000, 30, 75. [Google Scholar]
- Aggio, J.F.; de Freitas, J.C. Physiological and behavioural effects of chemoreceptors located in different body parts of the swimming crab Callinectes danae. Comp. Biochem. Physiol. A 2007, 146, 653–660. [Google Scholar] [CrossRef]
- Key, B. Why fish do not feel pain. Anim. Sent. 2016, 3, 34. [Google Scholar]
- Langworthy, K.; Helluy, S.M.; Benton, J.; Beltz, B.S. Amines and peptides in the brain of the American lobster: Immunocytochemical localization patterns and implications for brain function. Cell Tissue Res. 1997, 288, 191–206. [Google Scholar] [CrossRef] [PubMed]
- Chittka, L.; Niven, J. Are bigger brains better? Curr. Boil. 2009, 19, R995–R1008. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Elwood, R.W. Pain and suffering in invertebrates? ILAR J. 2011, 52, 175–184. [Google Scholar] [CrossRef] [PubMed]
- Bateson, P. Assessment of pain in animals. Anim. Behav. 1991, 42, 827–839. [Google Scholar] [CrossRef]
- Elwood, R.W. Assessing the potential for pain in crustaceans and other invertebrates. In The Welfare of Invertebrate Animals; Carere, C., Mather, J., Eds.; Springer: Cham, Switzerland, 2019; pp. 147–177. [Google Scholar]
- Sneddon, L.U.; Elwood, R.W.; Adamo, S.A.; Leach, M.C. Defining and assessing animal pain. Anim. Behav. 2014, 97, 201–212. [Google Scholar] [CrossRef] [Green Version]
- Passantino, A.; Elwood, R.W.; Coluccio, P. Why Protect Decapod Crustaceans Used as Models in Biomedical Research and in Ecotoxicology? Ethical and Legislative Considerations. Animals 2021, 11, 73. [Google Scholar] [CrossRef]
- Magee, B.; Elwood, R.W. Trade-offs between predator avoidance and electric shock avoid- ance in hermit crabs demonstrate a non-reflexive response to noxious stimuli consistent with prediction of pain. Behav. Process. 2016, 130, 31–35. [Google Scholar] [CrossRef]
- Appel, M.; Elwood, R.W. Motivational trade-offs and the potential for pain experience in hermit crabs. Appl. Anim. Behav. Sci. 2009, 119, 120–124. [Google Scholar] [CrossRef]
- Elwood, R.W.; Appel, M. Pain in hermit crabs? Anim. Behav. 2009, 77, 1243–1246. [Google Scholar] [CrossRef]
- Magee, B.; Elwood, R.W. Shock avoidance by discrimination learning in the shore crab (Carcinus maenas) is consistent with a key criterion for pain. J. Exp. Biol. 2013, 216, 353–358. [Google Scholar] [CrossRef] [Green Version]
- Elwood, R.W.; Stewart, A. The timing of decisions during shell investigation by the hermit crab, Pagurus bernhardus. Anim. Behav. 1985, 33, 620–627. [Google Scholar] [CrossRef]
- Elwood, R.W. Motivational change during resource assessment in hermit crabs. J. Exp. Mar. Biol. Ecol. 1995, 193, 41–55. [Google Scholar] [CrossRef]
- Appel, M.; Elwood, R.W. Gender differences, responsiveness and memory of a potentially painful event in hermit crabs. Anim. Behav. 2009, 78, 1373–1379. [Google Scholar] [CrossRef]
- McCambridge, C.; Dick, J.T.A.; Elwood, R.W. Effects of autotomy compared to manual declawing on contests between males for females in the edible crab, Cancer pagurus: Implications for fishery practice and animal welfare. Shellfish Res. 2016, 35, 1037–1044. [Google Scholar] [CrossRef] [Green Version]
- Elwood, R.W.; Dalton, N.; Riddell, G. Aversive responses by shore crabs to acetic acid but not to capsaicin. Behav. Process. 2017, 140, 1–5. [Google Scholar] [CrossRef]
- Dyuizen, I.V.; Kotsyuba, E.P.; Lamash, N.E. Changes in the nitric oxide system in the shore crab Hemigrapsus sanguineus (Crustacea, Decapoda) CNS induced by a nociceptive stimulus. J. Exp. Biol. 2012, 215, 2668–2676. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fossat, P.; Bacque-Cazenave, J.; De Deurwaerdere, P.; Delbecque, J.P.; Cattaert, D. Anxiety-like behavior in crayfish is controlled by serotonin. Science 2014, 344, 1293–1297. [Google Scholar] [CrossRef]
- Fossat, P.; Bacque-Cazenave, J.; De Deurwaerdere, P.; Cattaert, D.; Delbecque, J.P. Serotonin, but not dopamine, controls stress response and anxiety-like behavior in crayfish, Procambarus clarkii. J. Exp. Biol. 2015, 218, 2745–2752. [Google Scholar] [CrossRef] [Green Version]
- Broom, D.M.; Johnson, K.G. Stress and Animal Welfare, 2nd ed.; Springer: Berlin, Germany, 2019. [Google Scholar]
- Adamo, S.A. The effects of the stress response on immune function in invertebrates: An evolutionary perspective on an ancient connection. Horm. Behav. 2012, 62, 324–330. [Google Scholar] [CrossRef]
- Chung, J.S.; Zmora, N.; Katayama, H.; Tsutsui, N. Crustacean hyperglycemic hormone (CHH) neuropeptidesfamily: Functions, titer, and binding to target tissues. Gen. Comp. Endocrinol. 2010, 166, 447–454. [Google Scholar] [CrossRef]
- Patterson, L.; Dick, J.T.A.; Elwood, R.W. Physiological stress responses in the edible crab Cancer pagurus to the fishery practice of de-clawing. Mar. Biol. 2007, 152, 265–272. [Google Scholar] [CrossRef]
- Elwood, R.W.; Adams, L. Electric shock causes physiological stress responses in shore crabs, consistent with prediction of pain. Biol. Lett. 2015, 11, 20150800. [Google Scholar] [CrossRef] [Green Version]
- Birch, J. Animal sentience and the precautionary principle. Anim. Sentience 2017, 2, 1–15. [Google Scholar] [CrossRef]
- Horvath, K.; Angeletti, D.; Nascetti, G.; Carere, C. Invertebrate welfare: An overlooked issue. Ann. Ist. Super. Sanita 2013, 49, 9–17. [Google Scholar] [PubMed]
- Rowe, A. Should scientific research involving decapod crustaceans require ethical review? J. Agric. Environ. Ethics 2018, 31, 625–634. [Google Scholar] [CrossRef]
- British Veterinary Association. Welfare of Animals at Slaughter. Available online: https://www.bva.co.uk/take-action/ourpolicies/welfare-of-animals-at-slaughter/ (accessed on 11 February 2021).
- European Union. Council Regulation (EC) No 1099/2009 of 24 September 2009 on the protection of animals at the time of killing. Off. J. Eur. Union 2009, L303, 1–30. Available online: http://data.europa.eu/eli/reg/2009/1099/2019-12-14 (accessed on 11 February 2021).
- Smith, J.A.; Andrews, P.L.R.; Hawkins, P.; Louhimies, S.; Ponte, G.; Dickel, L. Cephalopod research and EU Directive 2010/63/EU: Requirements, impacts and ethical review. J. Exp. Mar. Biol. Ecol. 2013, 447, 31–45. [Google Scholar] [CrossRef]
- Crustaceans Compassion. Available online: https://www.crustaceancompassion.org.uk/the-problem (accessed on 11 February 2021).
- Johnston, C.; Jungalwalla, P. Aquatic Animal Welfare Guidelines: Guidelines on Welfare of Fish and Crustaceans in Aquaculture and/or in Live Holding Systems for Human Consumption. An Initiative of the National Aquaculture Council of Australia (NACA), through Consultation with Aquatic Animal Health Unit, Department of Agriculture, Fisheries and Forestry, Australian Government; National Aquaculture Council of Australia (NACA) Inc.: Curtin, Australia, 2000. [Google Scholar]
- French Ministry of Agriculture, Agrifood and Forestry. Service Note DGAL/SDSSA/N2012-8219, Dated 20 November 2012. Authorisation and Health Inspection of Storage Tanks for Crustaceans and Seawater and Freshwater Fish; French Ministry of Agriculture, Agrifood and Forestry: Paris, France, 2012. [Google Scholar]
- Sullivan, K. Good News! Swiss Gov’t Says Lobsters and Other Crustaceans Can’t Be Boiled Alive. 2018. Available online: https://www.peta.org/blog/switzerland-bans-boiling-lobsters-crustaceans-alive/#:~:text=Switzerland%20has%20made%20it%20illegal,the%20country’s%20animal%2Dprotection%20laws (accessed on 11 February 2021).
- Weineck, K.; Ray, A.J.; Fleckenstein, L.J.; Medley, M.; Dzubuk, N.; Piana, E.; Cooper, R.L. Physiological changes as a measure of crustacean welfare under different standardized stunning techniques: Cooling and electroshock. Animals 2018, 8, 158. [Google Scholar] [CrossRef] [Green Version]
- Conte, F.; Voslarova, E.; Passantino, A. Destinozí korýši: Otázka welfare v souvislosti s jejich využitím jako potraviny [Decapod crustaceans: Some issues related to welfare and their use as food]. Maso 2018, 7, 51–54. [Google Scholar]
- Murray-Ragg, N. Boiling Lobsters Alive Has Now Been Made Illegal in Switzerland. 2018. Available online: https://www.livekindly.co/boiling-lobsters-alive-illegal-switzerland/ (accessed on 11 February 2021).
- Corte di Cassazione, Sez. III Penale 16 Giugno 2017, Sentenza n. 30177. Available online: https://www.ambientediritto.it/giurisprudenza/corte-di-cassazione-penale-sez-3-16-06-2017-sentenza-n-30177/ (accessed on 11 February 2021).
- Liuzzo, G.; Rossi, R.; Giacometti, F.; Mescolini, G.; Piva, S.; Serraino, A. Analysis of provincial and municipal regulations governing crustacean welfare in Italy. Ital. J. Food Saf. 2017, 6, 54–56. [Google Scholar] [CrossRef] [Green Version]
- Crustaceans as Sentient Beings and Their Mistreatment: Sentence n. 30177/2017 of the Third Criminal Section of Italian Supreme Court. Available online: https://ddd.uab.cat/record/189937 (accessed on 11 February 2021).
- European Union. Council Regulation (EC) No 853/2004 of 29 April 2004 Laying down Specific Hygiene Rules for Food of Animal Origin. Off. J. Eur. Union 2004, L139, 5–205. Available online: https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=celex%3A32004R0853 (accessed on 11 February 2021).
- Conte, F.S. Stress and the welfare of cultured fish. Appl. Anim. Behav. Sci. 2004, 86, 205–223. [Google Scholar] [CrossRef]
- Dawkins, M.S. Why Animals Matter. Animal Consciousness, Animal Welfare, and Human Well-Being; Oxford University Press: Oxford, UK, 2012. [Google Scholar]
- Albalat, A.; Sinclair, S.; Laurie, J.; Taylor, A.; Neil, D.M. Targeting the live market: Recovery of Norway lobsters Nephrops norvegicus (L.) From trawl-capture as assessed by stress-related parameters and nucleotide breakdown. J. Exp. Mar. Biol. Ecol. 2010, 395, 206–214. [Google Scholar] [CrossRef] [Green Version]
- Neil, D.M. Ensuring crustacean product quality in the post-harvest phase. J. Invertebr. Pathol. 2012, 110, 267–275. [Google Scholar] [CrossRef] [PubMed]
- Gardner, C. Options for humanely immobilising and killing crabs. J. Shellfish Res. 1997, 16, 219–224. [Google Scholar]
- Neil, D.; Thompson, J. The Stress Induced by the Crustastun™ Process in Two Commercially Important Decapod Crustaceans: The Edible Brown Cancer pagurus and the European Lobster Homarus gammarus; Project Report; University of Glasgow: Glasgow, UK, 2012. [Google Scholar]
- Roth, B.; Grimsbø, M. Electrical Stunning of Edible Crabs; NOFIMA Report 18/2013; Nofima: Tromsø, Norway, March 2013; Available online: https://www.mitchellcooper.co.uk/content/files/content/Product%20Page%20Additions/Crustastun/Electrical%20stunning%20of%20edible%20crabs%202013%20nofima.pdf (accessed on 11 February 2021).
- Roth, B.; Øines, S. Stunning and killing of edible crabs (Cancer pagurus). Anim. Welf. 2010, 19, 287–294. [Google Scholar]
- Gardner, C. Treating the prawn well on its way to the barbie: Welfare of aquatic crustaceans. In Welfare Underwater: Issues with Aquatic Animals. Proceedings of the 2004 RSPCA Australia Scientific Seminar, Telstra Theatre, Australian War Memorial, Canberra, Australia, 26 February 2004; Jones, B., Ed.; ©RSPCA Australia Inc.: Deakin West, Australia, 2004; pp. 21–24. [Google Scholar]
- Yue, S. The Welfare of Crustaceans at Slaughter. The Humane Society Institute for Science and Policy HSUS REPORTS. 4. 2008. Available online: http://animalstudiesrepository.org/hsus_reps_impacts_on_animals/4 (accessed on 11 February 2021).
- Mood, A. Welfare during Killing of Crabs, Lobsters and Crayfish. Fish Count. 2014. Available online: http://fishcount.org.uk/welfare-of-crustaceans/welfare-during-killing-of-crabs-lobsters-and-crayfish (accessed on 11 February 2021).
- EFSA (European Food Safety Authority). Opinion of the Scientific Panel on Animal Health and Welfare (AHAW) on a request from the Commission related to the aspects of the biology and welfare of animals used for experimental and other scientific purposes. EFSA-Q-2004-105. EFSA J. 2005, 292, 1–46. [Google Scholar]
- The Royal Society for the Prevention of Cruelty to Animals (RSPCA Australia). What Is the Most Humane Way to Kill Crustaceans for Human Consumption? 2016. Available online: https://kb.rspca.org.au/knowledge-base/what-is-the-most-humane-way-to-kill-crustaceans-for-human-consumption/ (accessed on 11 February 2021).
- Fotedar, S.; Evans, L. Health management during handling and live transport of crustaceans: A review. J. Invertebr. Pathol. 2011, 106, 143–152. [Google Scholar] [CrossRef] [PubMed]
- Jury, S.H.; Watson III, W.H. Seasonal and sexual differences in the themal preferences and movements of American lobsters. Can. J. Fish. Aquat. Sci. 2013, 70, 1650–1665. [Google Scholar] [CrossRef]
- Aaser, C. Koking av Hummer; Foreningen til Dyrenes Beskytte1se: Oslo, Norway, 1947. [Google Scholar]
- Baker, J. Experiments on the humane killing of crabs. J. Mar. Biol. Ass. UK 1955, 34, 15–24. [Google Scholar] [CrossRef] [Green Version]
- Gonçalves, A.A.; de Paiva Alves, J. High pressure technology improves the quality and yield in the seafood industry. Infofish Int. 2013, 6, 35–38. Available online: https://www.researchgate.net/publication/267509875_High_pressure_technology_improves_the_quality_and_yield_in_the_seafood_industry (accessed on 28 March 2021).
- HPP Seafood: Shells Away with High Pressure Processing (HPP) Shucking. Available online: https://blog.hiperbaric.com/en/hpp-seafood-shells-away-with-high-pressure-processing (accessed on 28 March 2021).
- Available online: https://www.peta.org.uk/blog/live-lobsters-torn-apart-in-agony-in-shocking-eyewitness-video/ (accessed on 11 February 2021).
- Carroll, J.C.; Winn, R.N. Species Profiles: Life Histories and Environmental Requirements of Coastal Fishes and Invertebrates (Pacific Southwest)-Brown Rock Crab, Red Rock Crab, and Yellow Crab; U.S. Fish and Wildlife Service Biological Report 82 (11.117); TR EL-82-4; U.S. Army Corps of Engineers: Washington, DC, USA, 1989; 16p. [Google Scholar]
- Bergmann, M.; Taylor, A.C.; Moore, P.G. Physiological stress in decapod crustaceans (Munida rugosa and Liocarcinus depurator) discarded in the Clyde Nephrops fishery. J. Exp. Mar. Biol. Ecol. 2001, 259, 215–229. [Google Scholar] [CrossRef]
- Bellchambers, L.M.; Smith, K.D.; Evans, S.N. Effect of Exposure to Ice Slurries on Nonovigerous and Ovigerous Blue Swimmer Crabs, Portunus pelagicus. J. Crustacean Biol. 2005, 25, 274–278. [Google Scholar] [CrossRef] [Green Version]
- Passantino, A. Welfare of animals at slaughter and killing: A new regulation on the protection of animals at the time of killing. J. Verbrauch. Lebensm. 2009, 4, 273–285. [Google Scholar] [CrossRef]
- Esposito, G.; Nucera, D.; Meloni, D. Retail stores policies for marketing of lobsters in Sardinia (Italy) as influenced by different practices related to animal welfare and product quality. Foods 2018, 7, 103. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Browman, H.I.; Cooke, S.J.; Cowx, I.G.; Derbyshire, S.W.G.; Kasumyan, A.; Key, B.; Rose, J.D.; Schwab, A.; Berit Skiftesvik, A.; Don Stevens, E.; et al. Welfare of aquatic animals: Where things are, where they are going, and what it means for research, aquaculture, recreational angling, and commercial fishing. ICES J. Mar. Sci. 2018, 76, 82–92. [Google Scholar] [CrossRef]
Stunning and Killing Methods | Species | Signs of Pain and Distress | Suitable for Humane Slaughter |
---|---|---|---|
Electrical stunning | Lobster, Crab | None | Yes [64,65,66,69] |
Splitting | Lobster | None | Yes |
Spiking | Crab | None | Yes |
Chilling | Large crustaceans | No behavioural signs of distress but a long time to death. Not suitable as calming before boiling. | No * [72] |
Carbon-dioxide (CO2) narcosis | Crab | Aversive behaviour (tearing at their own sternums with their chelae, exposing internal organs) and autotomy. | No [48,63,66,67] |
High-pressure killing | Lobster, Crab, other decapods | More information on the speed of killing and possible suffering are required for a better evaluation | Possibly [69,76,77] |
Drowning | Saltwater species | Aversive behaviour (uncoordinated bodily movements and increased intensity of respiration) and autotomy | No [63] |
Salt baths | Lobster | Abnormal behaviours (retraction of the antennae, stillness, and feeble locomotion in some cases) | No [69] |
Boiling | Crab, Lobster | Physiological shock and autotomy | No [2,67,71] |
Dismemberment | Lobster, Crab | Markedly decreased ability to feed, rapid stress response | No [32,40,80] |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Conte, F.; Voslarova, E.; Vecerek, V.; Elwood, R.W.; Coluccio, P.; Pugliese, M.; Passantino, A. Humane Slaughter of Edible Decapod Crustaceans. Animals 2021, 11, 1089. https://doi.org/10.3390/ani11041089
Conte F, Voslarova E, Vecerek V, Elwood RW, Coluccio P, Pugliese M, Passantino A. Humane Slaughter of Edible Decapod Crustaceans. Animals. 2021; 11(4):1089. https://doi.org/10.3390/ani11041089
Chicago/Turabian StyleConte, Francesca, Eva Voslarova, Vladimir Vecerek, Robert William Elwood, Paolo Coluccio, Michela Pugliese, and Annamaria Passantino. 2021. "Humane Slaughter of Edible Decapod Crustaceans" Animals 11, no. 4: 1089. https://doi.org/10.3390/ani11041089
APA StyleConte, F., Voslarova, E., Vecerek, V., Elwood, R. W., Coluccio, P., Pugliese, M., & Passantino, A. (2021). Humane Slaughter of Edible Decapod Crustaceans. Animals, 11(4), 1089. https://doi.org/10.3390/ani11041089