Wednesday, 24 July 2013

Fish Are Animals Who Do Things

If you find it hard to believe that fish feel pain, consider this!

Cognition—the ability to think—was an important factor in the establishment of whether fish could feel pain, and it happened that in the same year as Rose's article was published, Bshary, Wickler, and Fricke published a review of the findings on the cognitive capabilities of fish (Bshary et al 2002). Here are a few examples:
Recognition of others as individuals has long been established in many varieties of fish, both visually and acoustically (Myrberg and Riggio 1985). It forms the first step towards complex social lives, in which cognition is often most evident. I documented relationships among reef sharks for years. They, too, relate to each other individually.
Social learning is illustrated by the migrations of the surgeon fish (Acathurus nigrofuscus), described in detail by Arthur A. Myrberg Jr. in 1998. These fish leave their territories all over the lagoon, and travel in single file through paths in the coral to their traditional spawning grounds. They go and return along the same paths each night at precisely the same time, as I saw in the local lagoon, year after year. Their spawning ground was the only place along the lagoon's border where the outflowing current was exactly balanced by the incoming surge, so that the huge cloud of spawn that they left in the gathering night, stayed in place. These short term migrations had been shown to be the result of social learning; each generation of fish learned from its elders where to go to spawn, and when.
Triggerfish (Balistidae) often feed on sea urchins. Usually, they try to blow them onto their side to get access to the unprotected body parts beneath. Hans Fricke (1971) observed at Eilat how five different individuals of Balistapus undulatus sucessfully hunted sea urchins by first biting off the spines, which allowed them to grab the urchin and take it to the surface. They fed on the unprotected parts underneath while the urchin slowly sank. In spite of decades of observations, Fricke never saw this behaviour anywhere else. It appeared to be the result of social learning.
Intertidal gobies (Gobius soporator), live in tide pools, and during low tide they can jump from one to another, without being able to see their target pool at the beginning of the jump. Experimentation showed that the fish had memorized the lay of the land around the home pool by swimming over it when the tide was in, so were referring to a three dimensional memory to navigate when the outgoing tide left them only a labyrinth of pools. (Aronson 1951, 1956).
With the exception of humans, fish are more skillful than primates at nest building. At least 9000 fish species build some sort of nest, either for egg laying or for protection.
The male minnow Exoglossum selects more than three hundred stones, all of the same size, from over 5 m distance, to build a spawning mound 35 cm wide and 10 cm high (van Duzer 1939). Another fish builds dome-shaped nests from 10,000 pebbles (Lachner 1952).
The jawfish, (Opistognathus aurifrons), collects stones of various sizes to build a wall, leaving a hole just big enough to pass through. This involves repeated rearrangement of the stones. In between, the fish searches for new stones that might better fit the available space than the ones it has already collected, using flexible behaviour depending on the circumstances (Kacher 1963; Colin 1972, 1973).
Another example showing surprising flexibility of behaviour is the ability of the ten-spined stickleback (Pygosteus pungitius), to build his nest around the eggs if the female has already laid them, though he usually builds the nest first (Leiner 1931). Great care is required, and a different technique has to be used to avoid damaging the eggs. Since those eggs do hatch, the males achieve their goal. (Morris 1958)
Redouin Bshary (2002), described seeing cooperative hunting between red sea coral groupers (Plectropomus pessuliferus), or lunartail groupers (Variola louti), and giant moray eels (Gymnothorax javanicus):
These two large species of groupers were observed regularly approaching the eels that were resting in a coral cave, and shaking their bodies in exaggerated movements, usually at less than 1 m distance to the moray eel.... In 7 of 14 observations, the moray eel left its cave and the two predators would swim next to each other, searching for prey. The groupers would often come so close that the two predators touched each other at their sides. While the moray eels sneaked through holes, the groupers waited above the corals for escaping fish.
Another unusual form of cooperation among different species is seen in cleaning symbiosis. Cleaner fish come from many different fish families, and depend on cleaning for their diet to varying degrees. They clean the dead skin and ectoparasites from their clients in return for a meal. Full time cleaners may have about 2,300 interactions per day, with clients belonging to 100 different species! (Grutter 1995)
According to the evidence, cleaners have their hundred client species categorized as those who only come to their local cleaner, and those whose home ranges include the territories of other cleaners. For the latter, they have competition, so give them priority over the locals, who have no choice of cleaner.
Cleaners sometimes “cheated” by feeding off the client's healthy flesh as well as doing the usual cleaning job, and the clients with no choice of cleaner punished the cleaner by aggressively chasing it, and inflicting a bite or two, as they saw fit. (Clutten-Brock and Parker 1995). But these clients benefited in the future, because the cleaner fish were seen to give them, but not others who visited in the meantime, a better-than-average cleaning service on the next visit! Apparently cleaners can distinguish more than 100 individual clients belonging to various species.
Cleaners will hover above the client and touch it with their fins, in an effort to influence its decision to come for a cleaning. This touching tactic is also used to try to reconcile with a client whom they have cheated as described above. Cleaners even exploit the presence of a third party in an attempt to make aggressive clients stop chasing them by going to a nearby predator and caressing it, so that the client dares not continue the chase!
Cleaners will behave altruistically toward their clients if they are being watched by potential new clients—but only those who could visit another cleaning station. Since clients will emulate the behaviour of the former client, the sight of another being treated very well by the cleaner, is more likely to convince it to come for servicing than seeing another client being chased or eaten! This tactic suggests a short term image, or social prestige (Alexander 1987; Zahavi 1995; Nowak and Sigmund 1998; Roberts 1998), that determines their success in attracting new clients.
Such complex social behaviour—cheating, reconciliation, altruism, species recognition, individual recognition, punishment, social prestige, and bookkeeping, displayed by full-time cleaners 50 to 100 times per day, is generally considered to indicate consciousness when displayed in primates.
A similar example of social judgement is given by predator inspection, in which different individuals take turns to lead others away from the school to look over a predator. Fish who don't take their turn cooperatively, will not be trusted by their partners in the future. In other words, the fish make an evaluation of the behaviour of another individual, remembers it, and takes it into account in future decisions. (Milinski et al. 1990b; Dugatkin and Wilson 1993)

At the end of the review of cognition in fish, Bshary wrote: “We are aware of only one experimentally shown qualitative difference in mechanisms between primates and fish, and this difference is the ability to imitate.”

References

Alexander RD (1987) The biology of moral systems. Aldine de Gruiter, New York
Aronson LR (1951) Orientation and jumping behavior in the goby fish Bathygobius soporator. Am Mus Novitates 1486
Aronson LR (1956) Further studies on orientation and jumping behaviour in the goby fish Bathygobius soporator. Anat Rec 125:606
Bshary R, Wickler W, Fricke H (2002) Fish cognition: a primate's eye view. Animal Cognition (2002) 5 : 1-13
Colin PL (1972) Daily activity patterns and effects of environmental conditions on the behaviour of the yellowhead jawfish Opistognathus aurifrons, with notes on its ecology. Zoologica 57:137-169
Colin PL (1973) Burrowing behaviour of the yellowhead jawfish, Opistognathus aurifrons. Copeia 1973:84-90
Barber TX (1993) The Human Nature of Birds. Bookman Press, Melbourne
Clutten-Brock TH, Parker GA (1995) Punishment in animal societies. Nature 373:209-215
Chandroo KP, Yue S, and Mocci RD (2004) An evaluation of current perspectives on consciousness and pain in fishes. Fish and Fisheries 5. 281-295
Chapman, CR and Nakamura Y (1999) A passion of the soul: an introduction to pain for consciousness researchers. Consciousness and Cognition 8. 391-422
Dugatkin LA, Wilson DS (1993) Fish behaviour, partner choice, and cognitive ethology. Rev Fish Biol Fish 3:368-372
Duzer EM van (1939) Observations on the breeding habits of the cut-lip minnow, Exoglossum maxillingua. Copeia 1939:65-75
Fricke H (1971) Fische als Feinde tropischer Seeigel. Mar Biol 9:328-338
Edelman GM and Tononi G (2000)A Universe of Consciousness. Basic Books, New York, NY
Glynn I. (1999) An Anatomy of Thought: The Origin and Machinery of the Mind. Wiedenfield and Nicholson
Geiger W (1956) Quantitative Untersuchungen über das Gehirn der Knochenfische, mit besonderer Berücksichtigung seines relativen Wachstums, I Acta Anat 26: 121-163
Grandin T. and Deesing M. American Board of Veterinary Practitioners - Symposium 2002 May 17, 2002, Special Session Pain, Stress, Distress and Fear. Emerging Concepts and Strategies in Veterinary Medicine
Griffin DR (1998) Animal Minds. The University of Chicago Press.
Grutter AS 1995 Relationships between cleaning rates and ectoparasite loads in coral reef fishes. Mar Ecol Prog Ser 118:51-58
Harmes CA, Lewbart GA, Swanson CR, Kishimori JM, Boylan SM (2005) Behavioural and Clinical Pathology Changes in Koi Carp (Cyprinus carpio) Subjected to Anaesthesia and Surgery with and without Intra-Operative Analgesics. Comparative Medicine Vol. 55 No. 3 221-226
Kacher H (1963) Opithognathus aurifrons (Opisthognathidae) Graben einer Wohnhöhle, Wallbau Film E514, Encyclopaedia Cinematographica. Institut für den wissenschaftlichen Film, Göttingen
Lachner A (1952) Studies of the biology of the cyprinid fish of the chub genus Nocomis of northeastern United States. Am Midl Nat 48:433-466
Laureys S., Faymonville ME, Luxon A, Lamy M, Franck G, and Maquet P (2000) Restoration of thalamocortical connectivity after recovery from persistent
Lovibond PF , Shanks DR (2002) The role of awareness in Pavlovian conditioning: empirical evidence and theoretical implication. Journal of Experimental Psychology 28 3-26
Maren S (2001) Neurobiology of Pavlovian fear conditioning. Annual Review of Neuroscience 24. 897-931
Marino L (2002) Convergence of complex cognitive abilities in cetaceans and primates. Brain, Behaviour and Evolution 59. 21-32
Milinski M, Pfluger D, Külling D, Kettler R (1990b) Do sticklebacks cooperate repeatedly in reciprocal pairs? Behav Ecol Sociobiol 27:17-21
Morris D (1958) The reproductive behaviour of the ten-spined stickleback (Pygosteus pungitius L.). Behaviour [Suppl] 6:1-154
Myrberg AA, Riggio RJ (1985) Acoustically mediated individual recognition by a coral reef fish (Pomacentrus portitus)
Myrberg AA, Montgomery WL, Fishelson L (1988) The reproductive behaviour of Acanthurus nigrofuscus (Forskal) and other surgeon fishes (Fam. Acanthuridae) of Eilat, Israel (Gulf of Aqaba, Red Sea). Ethology 79:31-61
Nowak MA, Sigmund K (1998) Evolution of indirect reciprocity by image scoring. Nature 393:573-577
Overmier JB, Hollis KL (1990) Fish in the think tank: learning, memory, and integrated behaviour. Neurobiology of Comparative Cognition (eds Kesner RP, Olson DS), Lawrence Erlbaum, Hillsday, NJ. pp. 205-236
Roberts G (1998) Competitive altruism: from reciprocity to the handicap principle. Proc R Soc Lond B 265:427-431
Rose, JD 2002 The neurobehavioural nature of fishes, and the question of awareness and pain. Rev. Fish. Sci. 10:1-38
Sneddon, LU 2003. The evidence for pain in fish: The use of morphine as an analgesic. Applied Animal Behavior Science. 83:153-162.

Zahavi A (1995) Altruism as a handicap—the limitations of kin selection and reciprocity. J Avian Biol 26:1-3

No comments: