Pain in fish
Whether fish feel pain is controversial. Pain is a complex state, with a distinct perceptual quality but also associated with suffering, which is an emotional state. Because of this complexity, the presence of pain in an animal, or another human for that matter, cannot be determined unambiguously using observational methods, but the conclusion that animals experience pain is often inferred on the basis of likely presence of phenomenal consciousness which is deduced from comparative brain physiology as well as physical and behavioural reactions.
Animal protection advocates have raised concerns about the possible suffering of fish caused by angling. In light of recent lobbying by animal rights groups, some countries, like Germany, have banned specific types of fishing.
The idea that animals might not feel pain as human beings feel it traces back to the 17th-century French philosopher, René Descartes, who argued that animals do not experience pain and suffering, because they lack consciousness. Bernard Rollin of Colorado State University, the principal author of two U.S. federal laws regulating pain relief for animals, writes that researchers remained unsure into the 1980s as to whether animals experience pain, and veterinarians trained in the U.S. before 1989 were simply taught to ignore animal pain. In his interactions with scientists and other veterinarians, Rollin was regularly asked to "prove" that animals are conscious, and to provide "scientifically acceptable" grounds for claiming that they feel pain. Carbone writes that the view that animals feel pain differently is now a minority one. Academic reviews of the topic are more equivocal, noting that although the argument that some animals (most likely higher vertebrates) have at least simple conscious thoughts and feelings has strong support; some critics continue to question how reliably animal mental states can be determined.
Veterinary medicine uses, for actual or potential animal pain, the same analgesics and anesthetics used in humans, because these chemicals act on the nociceptive pathways, blocking signals to the brain where emotional responses to the signals are further processed by certain parts of the brain found in higher vertebrates. There is a great deal of research on anaesthesia and analgesia in fish, however relatively little is known about their effects - for example, in her studies Sneddon found rainbow trout survived levels of morphine an order of magnitude higher than those known to be lethal to birds or small mammals.
Experiments by William Tavolga provide evidence that fish respond to potentially noxious stimuli. For instance, in Tavolga’s experiments, toadfish grunted when electrically shocked, and over time they came to grunt at the mere sight of an electrode. Additional tests conducted at the Roslin Institute and University of Edinburgh, in which bee venom and acetic acid was injected into the "lips" of rainbow trout, resulted in fish rubbing their "lips" along the sides and floors of their tanks, which the researchers believed was an effort to relieve themselves of pain. Several researchers argue about the definition of pain used in the studies, as the behavioural observations recorded were contradictory, non-validated and non-repeatable by other researchers. Since this initial work Lynne Sneddon and her co-workers have characterised alleged pain responses in rainbow trout, common carp and zebrafish. However, when these experiments were replicated by Newby and Stevens without anaesthetic, rocking and rubbing behaviour was not observed, suggesting that some of the alleged pain responses observed by Sneddon and co-workers were likely to be due to recovery of the fish from anaesthesia.
In a 2009 paper, Janicke Nordgreen from the Norwegian School of Veterinary Science, Joseph Garner from Purdue University, and others, published research which claimed that goldfish do feel pain and that their reactions to pain are much like those of humans. "There has been an effort by some to argue that a fish's response to a noxious stimulus is merely a reflexive action, but that it didn't really feel pain," Garner said. "We wanted to see if fish responded to potentially painful stimuli in a reflexive way or a more clever way." The fish were divided into two groups, one given morphine and the other saline. They were then subjected to unpleasant temperatures. The fish that were given saline subsequently acted with defensive behaviours, indicating anxiety, wariness and fear, whereas those given morphine did not. Nordgreen said that the behavioural differences they found showed that fish feel both reflexive and cognitive pain. "The experiment shows that fish do not only respond to painful stimuli with reflexes, but change their behavior also after the event," Nordgreen said. "Together with what we know from experiments carried out by other groups, this indicates that the fish consciously perceive the test situation as painful and switch to behaviors indicative of having been through an aversive experience." In 2013 Rose and others reviewed this and further studies which concluded that pain had been found in fish. They concluded that the results from such research are due to poor design and misinterpretation, and that the researchers were unable to distinguish unconscious detection of injurious stimuli (nociception) from conscious pain.
In 2003 a research team lead by Sneddon at the University of Edinburgh concluded that the brains of rainbow trout fire neurons in the same way human brains do when experiencing pain. Rose from the University of Wyoming criticized the study, claiming it was flawed, mainly since it did not provide proof that fish possess "conscious awareness, particularly a kind of awareness that is meaningfully like ours". Rose, and more recently Brian Key from the University of Queensland, argue that, since the fish brain is very different from ours, fish are probably not conscious in the manner humans are, and while fish may react in a way similar to the way humans react to pain, the reactions in the case of fish have other causes. In 2002 Rose had published a scientific review arguing that fish cannot feel pain because they lack the appropriate neocortex in the brain. Studies indicating that fish can feel pain were confusing nociception (responding to threatening stimulus) with feeling pain, says Rose. "Pain is predicated on awareness. The key issue is the distinction between nociception and pain. A person who is anaesthetised in an operating theatre will still respond physically to an external stimulus, but he or she will not feel pain." According to Rose and Key, the literature relating to the question of consciousness in fish is prone to anthropomorphisms and care is needed to avoid erroneously attributing human-like capabilities to fish. Sneddon suggests it is entirely possible that a species with a different evolutionary path could evolve different neural systems to perform the same functions, as studies on the brains of birds have shown. Key agrees that phenomenal consciousness is likely to occur in mammals and birds, but not in fish.  Animal behaviourist Temple Grandin argues that fish could still have consciousness without a neocortex because "different species can use different brain structures and systems to handle the same functions." Sneddon proposes that to suggest a function suddenly arises without a primitive form defies the laws of evolution. Other researchers also believe that animal consciousness does not require a neocortex, but can arise from homologous subcortical brain networks.
Nociception is the unconscious detection by the nervous system that damage is occurring somewhere. Nociceptors are sensory receptors that respond to potentially damaging stimuli by sending nerve signals to the spinal cord and brain. In 2003 Lynne Sneddon was able to demonstrate the presence of nociceptors on the face and snout of the trout. The receptors responded to touch, heat and chemical stimulation by sending an electrical signal through the trigeminal nerve to the brain.
However, a 2012 review by Rose and others points out that a typical human cutaneous nerve contains 83% C type trauma receptors (the type responsible for excruciating pain in humans), but the same nerves in people with congenital insensitivity to pain only have 24-28% C type fibres. Sneddon showed that rainbow trout on the other hand have only around 5% C type fibres, while sharks and rays have 0%  Fishes resume "normal feeding and activity immediately or soon after surgery", and the absence of C type fibres indicates that signalling leading to pain perception is likely to be impossible for sharks and rays, and the low numbers (5% C fibres) suggest this is also highly unlikely for fish. Rose concludes there is little evidence that sharks and rays possess the nociceptors required to initiate pain detection in the brain, and bony fish are evolutionarily little more advanced than sharks in this respect. The more thickly sheaved delta A type fibres, which rapidly conduct information about noxious stimuli, are common in fish though they have not been found in sharks or rays. Their function is likely to trigger avoidance reactions. Sharks and bony fish have survived well in an evolutionary sense without the full range of nociception typical of humans or other mammals, probably because it would otherwise be disadvantageous to their survival in the aquatic environment.
The Norwegian Research Council is funding a three-year research project, scheduled to end in December 2011, into whether cod can feel pain. The researchers will use fMRI and EEGs to study how the cod brain works. The aim of the study is to identify the parts of the cod brain that activate when cod are exposed to potentially painful stimuli, and how those signals are processed. Early results from these investigations have found significant difference in behaviour of fish exposed to acetic acid injections and fishing hooks compared to control fish which were similarly handled and injected with saline.
Zebrafish, native to the streams of the south eastern Himalayan region, are commonly used as a model organism in studies of vertebrate development and gene function. Zebrafish are used to study development, toxicology and toxicopathology, because the body of a young zebrafish is nearly transparent, providing unique visual access to their internal anatomy. Another extensively used model organism is the medaka, which is much sturdier than the traditional zebrafish. Medakas are easy to rear in the laboratory because of their prolific reproduction rates and short generation times. The short-lived ram cichlid is also used in laboratory studies because of its ease of breeding and predictable pattern of ageing. Sticklebacks have traditionally been used as model organism in the study of fish behaviour.
The extent to which animal research causes pain to laboratory animals is the subject of much debate. Marian Stamp Dawkins defines "suffering" in laboratory animals as the experience of one of "a wide range of extremely unpleasant subjective (mental) states." The United States Department of Agriculture defines a "painful procedure" in an animal study as one that would "reasonably be expected to cause more than slight or momentary pain or distress in a human being to which that procedure was applied."
- Abbott, Frances V.; Franklin, Keith B. J.; Westbrook, R. Frederick (January 1995). "The formalin test: scoring properties of the first and second phases of the pain response in rats". Pain 60 (1): 91–102. doi:10.1016/0304-3959(94)00095-V. PMID 7715946.
- Key, Brian (2014) "Fish do not feel pain and its implications for understanding phenomenal consciousness". Biology & Philosophy, December 2014, 1-17. doi:10.1007/s10539-014-9469-4 Full text
- Carbone, Larry (2004) What Animal Want: Expertise and Advocacy in Laboratory Animal Welfare Policy Oxford University Press, p. 149.
- The Ethics of research involving animals Nuffield Council on Bioethics, Accessed 27 February 2008 Archived February 27, 2008 at the Wayback Machine
- Talking Point on the use of animals in scientific research, EMBO reports 8, 6, 2007, pp. 521–525
- Rollin, Bernard. The Unheeded Cry: Animal Consciousness, Animal Pain, and Science. New York: Oxford University Press, 1989, pp. xii, 117-118, cited in Carbone 2004, p. 150.
- Griffin DR, Speck GB (2004). "New evidence of animal consciousness". Anim. Cogn. 7 (1): 5–18. doi:10.1007/s10071-003-0203-x. PMID 14658059.
- Allen C (1998). "Assessing animal cognition: ethological and philosophical perspectives" (PDF). J. Anim. Sci. 76 (1): 42–47. PMID 9464883.
- Viñuela-Fernández I, Jones E, Welsh EM, Fleetwood-Walker SM (September 2007). "Pain mechanisms and their implication for the management of pain in farm and companion animals". Vet. J. 174 (2): 227–39. doi:10.1016/j.tvjl.2007.02.002. PMID 17553712.
- Sneddon, Lynne U. (2012) "Clinical Anesthesia and Analgesia in Fish." Journal of Exotic Pet Medicine 21, 32-43
- Rose JD, R Arlinghaus, SJ Cooke, BK Diggles, W Sawynok, ED Stevens and CDL Wynne (2012) "Can fish really feel pain?" Fish and Fisheries, 15 (1): 97–133. doi:10.1111/faf.12010
- Dunayer, Joan, "Fish: Sensitivity Beyond the Captor's Grasp," The Animals' Agenda, July/August 1991, pp. 12-18
- Brown, Vantressa. "Fish Feel Pain, British Researchers Say," Agence France-Presse, 1 May 2003.[dead link]
- Sneddon LU, Braithwaite VA and Gentle MJ (2003) "Do fish have nociceptors: Evidence for the evolution of a vertebrate sensory system" Proceedings of the Royal Society: Biological Sciences, 270 (1520)
- Sneddon L.U. (2009) "Pain and Distress in Fish." ILAR J. 50 (4), 338-342.
- Newby, N.C. and Stevens, E.D. (2008) "The effects of the acetic acid "pain" test on feeding, swimming and respiratory responses of rainbow trout (Oncorhynchus mykiss)." Applied Animal Behavior Science 114, pp. 260–269
- Newby, N.C. and Stevens, E.D. (2009) "The effects of the acetic acid "pain" test on feeding, swimming, and respiratory responses of rainbow trout (Oncorhynchus mykiss): a critique on Newby and Stevens (2008)— response." Applied Animal Behaviour Science 116, pp. 97–99.
- Nordgreen J, Joseph P, Garner JP, Janczak AM, Ranheim B, Muir WM and Horsberg TE (2009) "Thermonociception in fish: Effects of two different doses of morphine on thermal threshold and post-test behaviour in goldfish (Carassius auratus)" Applied Animal Behaviour Science, 119(1-2): 101–107.
- "Fish may actually feel pain and react to it much like humans," Purdue University, 29 April 2009.
- "Fish do feel pain, scientists say". BBC News. 30 April 2003. Retrieved 20 May 2010.
- Grandin, Temple; Johnson, Catherine (2005). Animals in Translation. New York, New York: Scribner. pp. 183–184. ISBN 0-7432-4769-8.
- Rose, J.D. (2003) A Critique of the paper: "Do fish have nociceptors: Evidence for the evolution of a vertebrate sensory system" In: Information Resources on Fish Welfare 1970-2003, Animal Welfare Information Resources No. 20. H. E. Erickson, Ed., U. S. Department of Agriculture, Beltsville, MD. Pp. 49-51.
- Rose, James D. (2002) "The neurobehavioral nature of fishes and the question of awareness and pain" Reviews in Fisheries Science, 10 (1): 1–38.
- Rose, James D. "Do Fish Feel Pain?", 2002. Retrieved September 27, 2007.
- "Fish lack the brains to feel pain, says the latest school of thought" The Telegraph, February 10, 2003.
- Rose, J.D. (2007). "Anthropomorphism and ‘mental welfare’ of fishes." Diseases of Aquatic Organisms 75, pp. 139–154.
- Sneddon, Lynne U. " Pain perception in fish: Why critics cannot accept the scientific evidence for fish pain?" August 28, 2012.
- Sneddon, Lynne U. (2012) "Pain Perception in fish: Evidence and Implications for the Use of Fish." Journal of Consciousness Studies, 18, pp. 209–229
- The Cambridge Declaration on Consciousness 7 July 2012. Written by Philip Low and edited by Jaak Panksepp, Diana Reiss, David Edelman, Bruno Van Swinderen, Philip Low and Christof Koch. University of Cambridge.
- Sneddon L.U. (2003) "Trigeminal somatosensory innervation of the head of the rainbow trout with particular reference to nociception." Brain Res., 972, pp. 44–52.
- L. U. Sneddon, V. A. Braithwaite, M. J. Gentle (2003) "'Do fish have nociceptors? Evidence for the evolution of a vertebrate sensory system'," Proceedings of the Royal Society of London Series B 270, pp. 1115–1121.
- Snow P.J., Plenderleith M.B. and Wright L.L. (1993) "Quantitative study of primary sensory neurone populations of three species of elasmobranch fish." Journal of Comparative Neurology 334, pp. 97–103.
- "Nociception and potential pain perception in Atlantic cod (Gadus morhua)" Norwegian Research Council project, 1 August 2008 to 31 December 2011.
- "Can fish feel pain?" Aquatic Community, December 11, 2008.
- Eckroth JR, Aas Hansen, O, Sneddon LU, Bichao H, Doving KB (2014). Physiological and behavioural responses to Noxious stimuli in the Atlantic cod (gadus morhua). PLOS One 9(6): e100150 http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0100150
- Lewbart, Greg (2001) "Anesthesia, Analgesia, and Surgery in Pet Fish" Proceedings of the Atlantic Coast Veterinary Conference.
- Mayden, Richard L.; Tang, Kevin L.; Conway, Kevin W.; Freyhof, Jörg; Chamberlain, Sarah; Haskins, Miranda; Schneider, Leah; Sudkamp, Mitchell; Wood Robert M.; Agnew, Mary; Bufalino, Angelo; Sulaiman, Zohrah; Miya, Masaki; Saitoh, Kenji; He, Shunping (2007). "Phylogenetic relationships of Danio within the order Cypriniformes: a framework for comparative and evolutionary studies of a model species". J. Exp. Zool. (Mol. Dev. Evol.) 308B (5): 642–654. doi:10.1002/jez.b.21175. PMID 17554749.
- Spitsbergen JM, Kent ML (2003). "The state of the art of the zebrafish model for toxicology and toxicologic pathology research—advantages and current limitations". Toxicol Pathol 31 (Suppl): 62–87. doi:10.1080/01926230390174959. PMC 1909756. PMID 12597434.
- Herrera M and Jagadeeswaran P (2004) "Annual Fish as a Genetic Model for Aging" The Journals of Gerontology Series A: Biological Sciences and Medical Sciences 59:B101-B107.
- Froese, Rainer and Pauly, Daniel, eds. (2009). "Cynolebias nigripinnis" in FishBase. July 2009 version.
- Tinbergen, N. (1951) The Study of Instinct. Oxford University Press, New York.
- Duncan IJ, Petherick JC. "The implications of cognitive processes for animal welfare", J. Anim. Sci, volume 69, issue 12, 1991, pp. 5017–22. pmid 1808195; Curtis SE, Stricklin WR. "The importance of animal cognition in agricultural animal production systems: an overview", J. Anim. Sci.. volume 69, issue 12, 1991, pp. 5001–7. PMID 1808193
- Stamp Dawkins, Marian. "Scientific Basis for Assessing Suffering in Animals," in Singer, Peter. In Defense of Animals: The Second Wave. Blackwell, 2006. p. 28.
- Animal Welfare; Definitions for and Reporting of Pain and Distress", Animal Welfare Information Center Bulletin, Summer 2000, Vol. 11 No. 1-2, United States Department of Agriculture.
- Ashley P.J., Sneddon L.U. & McCrohan C.R. (2006) "Properties of corneal receptors in a teleost fish." Neurosci. Letts. 410, 165-168.
- Ashley P.J., Sneddon L.U. & McCrohan C.R. (2007) "Nociception in fish: stimulus–response properties of receptors on the head of trout Oncorhynchus mykiss." Brain Res. 1166, 47-54.
- Ashley P.J., Ringrose S., Edwards K.L., Wallington E., McCrohan C.R. & Sneddon L.U. (2009) "Which is more important in fish: pain, anti-predator responses or dominance status?" Anim. Behav. 77, 403-410.
- Braithwaite, VA (2010) Do Fish Feel Pain? Oxford University Press. ISBN 978-0-19-955120-0
- Braithwaite VA and Boulcott P (2007) "Pain perception, aversion and fear in fish" Diseases of aquatic organisms, 75(2): 131-138. Download
- Chandroo K, Yue S, and Moccia R (2004) "An evaluation of current perspectives on consciousness and pain in fishes" Fish and Fisheries, 5(4): 281-295. Download
- Cooke S.J. & Sneddon L.U. (2007) "Animal welfare perspectives on recreational angling." Appl. Anim. Behav. Sci. 104, 176-198.
- Cottee, Stephanie Yue (2012) "Are fish the victims of 'speciesism'? A discussion about fear, pain and animal consciousness" Fish Physiology and Biochemistry, 38 (1): 5–15. doi:10.1007/s10695-010-9449-9
- Eckroth JR, Aas Hansen, O, Sneddon LU, Bichao H, Doving KB (2014). Physiological and behavioural responses to Noxious stimuli in the Atlantic cod (gadus morhua). PLOS One 9(6): e100150 http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0100150.
- Grandin, Temple and Deesing, Mark (2003 update) Distress in Animals: Is it Fear, Pain or Physical Stress? American Board of Veterinary Practitioners - Symposium 2002.
- Henriksen S, Vaagland H, Sundt-Hansen L, May R and Fjellheim A (2003) "Consequences of pain perception in fish for catch and release, aquaculture and commercial fisheries" Kurs i dyreforsøkslære ZO 8091, Høsten .
- Huntingford FA, C Adams, VA Braithwaite, S Kadri, TG Pottinger, P Sandøe and JF Turnbull (2006) "Review paper: Current issues in fish welfare" Journal of fish biology, 68 (2): 332–372. doi:10.1111/j.0022-1112.2006.001046.x
- Jalmlöv, Maria; Stéen, Margareta; and Röcklinsberg, Helena (2010) "Kan fiskar känna smärta och/eller uppleva lidande?" Swedish Centre for Animal Welfare. Translation: "Can fish feel pain and/or experience suffering?"
- Key B. (2015) "Fish do not feel pain and its implications for understanding phenomenal consciousness." Biology and Philosophy DOI 10.1007/s10539-014-9469-4 http://link.springer.com/article/10.1007%2Fs10539-014-9469-4#page-1.
- Mettam J.J., McCrohan C.R. & Sneddon L.U. (2011) "Characterisation of chemosensory trigeminal receptors in the rainbow trout (Oncorhynchus mykiss): responses to irritants and carbon dioxide." J. Exp. Biol., 215, 685-693.
- Mettam J.J., Oulton L.J., McCrohan C.R. & Sneddon L.U. (2011) "The efficacy of three types of analgesic drugs in reducing pain in the rainbow trout, Oncorhynchus mykiss." Appl. Anim. Behav. Sci. 133, 265–274.
- Newby, N.C. and Stevens, E.D. (2008) "The effects of the acetic acid "pain" test on feeding, swimming and respiratory responses of rainbow trout (Oncorhynchus mykiss)." Applied Animal Behavior Science 114, 260–269.
- Newby, N.C. and Stevens, E.D. (2009) "The effects of the acetic acid "pain" test on feeding, swimming, and respiratory responses of rainbow trout (Oncorhynchus mykiss): a critique on Newby and Stevens (2008)— response." Applied Animal Behaviour Science 116, 97–99.
- Roques JAC, Abbink W, Geurds F, van de Vis H and Flik G (2010) "Tailfin clipping, a painful procedure: Studies on Nile tilapia and common carp" Physiology & Behavior, 101 (4): 533–540.
- Rose JD "Do fish feel pain". Undated essay, University of Wyoming.
- Rose, J.D. (2007). "Anthropomorphism and ‘mental welfare’ of fishes." Diseases of Aquatic Organisms 75, 139–154.
- Rose J.D., Arlinghaus R., Cooke S.J., Diggles B.K., Sawynok W., Stevens E.D., Wynne C.D.L. (2013). "Can fish really feel pain?" Fish and Fisheries DOI: 10.1111/faf.12010
- Reilly S.C., Quinn J.P., Cossins A.R. & Sneddon L.U. (2008) "Novel candidate genes identified in the brain during nociception in common carp." Neuro. Sci. Letts. 437, 135-138.
- Reilly S.C., Quinn J.P., Cossins A.R. & Sneddon L.U. (2008) "Behavioural analysis of a nociceptive event in fish: comparisons between three species demonstrate specific responses." Appl. Anim. Behav. Sci. 114, 248-249.
- Schultz, Nora (2007) "When fish get emotional" New Scientist.
- Smith JLB, Smith MM and Heemstra PC (2003) Smiths' Sea fishes Page 9–10, Struik. ISBN 978-1-86872-890-9. – a classic angler's argument that fish do not feel pain.
- Sneddon L.U. (2002) "Anatomical and electrophysiological analysis of the trigeminal nerve of the rainbow trout, Onchorynchus mykiss." Neurosci. Letts., 312, 167-171.
- Sneddon L.U. Braithwaite V.A. & Gentle M.J. (2003) "Novel object test: examining pain and fear in the rainbow trout." J. Pain, 4, 431-440.
- Sneddon LU (2003) "The evidence for pain in fish: the use of morphine as an analgesic" Applied Animal Behaviour Science, 83(2):153-162.
- Sneddon L.U. (2004) "Evolution of nociception in vertebrates: comparative analysis of lower vertebrates." Brain Res. Rev. 46, 123-130.
- Sneddon L.U. (2006) "Ethics and welfare: Pain perception in fish." Bull. Eur. Assoc. Fish. Pathol. 26, 7-11.
- Sneddon L.U. (2011) "Cognition and Welfare in Fish." In Fish Cognition and Behaviour (ed. Brown et al.), Elsevier.
- Sneddon L.U. (2011) "Responses to Nociception or Pain in Fish." In Encyclopaedia of Fish Biology, Elsevier.
- Sneddon L.U. & Wolfenden D.C.C. (2012) "How do large-scale fisheries affect fish: Pain perception in fish?" In Sea The Truth, Nicholas G. Pierson Foundation.
- Sneddon L.U. (2012) "Pain in trout." In Trout: from physiology to conservation, Nova Publishers.
- Scientists Tip the Scales Against Anglers Der Spiegel, November 2011.
- Nociception and pain in fish, a tough question