Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-08T10:27:38.719Z Has data issue: false hasContentIssue false
  • English
  • Français

Can Invertebrates Suffer? or, How Robust is Argument-By-Analogy?

Published online by Cambridge University Press:  11 January 2023

C M Sherwin
C M Sherwin*
Affiliation:
Division of Animal Health and Husbandry, Department of Clinical Veterinary Science, Langford House, University of Bristol, Bristol BS40 5DU, UK
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

It is a popular notion that, compared to vertebrates, invertebrates have a reduced capacity to experience suffering. This is usually based on arguments that invertebrates show only simple forms of learning, have little memory capacity, do not show behavioural responses to stimuli that would cause ‘higher’ vertebrates to exhibit responses indicative of pain, and have differences in their physiology that would preclude the capacity for suffering. But, how convincing is this ‘evidence’ of a reduced capacity to suffer? Suffering is a negative mental state - a private experience - and, as such, it cannot be measured directly. When assessing the capacity of an animal to experience suffering, we often compare the similarity of its responses with those of ‘higher’ animals, conceptualized in the principle of argument-by-analogy. By closely examining the responses of invertebrates, it can be seen that they often behave in a strikingly analogous manner to vertebrates. In this paper, I discuss published studies that show that invertebrates such as cockroaches, flies and slugs have short- and long-term memory; have age effects on memory; have complex spatial, associative and social learning; perform appropriately in preference tests and consumer demand studies; exhibit behavioural and physiological responses indicative of pain; and, apparently, experience learned helplessness. The similarity of these responses to those of vertebrates may indicate a level of consciousness or suffering that is not normally attributed to invertebrates. This indicates that we should either be more cautious when using argument-by-analogy, or remain open-minded to the possibility that invertebrates are capable of suffering in a similar way to vertebrates.

Keywords

animal welfareargument-by-analogyinvertebratespainsuffering
Type
Research Article
Information
Animal Welfare , Volume 10 , Issue S1: Consciousness, Cognition and Animal Welfare: Proceedings of the UFAW Symposium, Zoological Society of London, 11-12 May 2000 , February 2001 , pp. S103 - S118
Copyright
© 2001 Universities Federation for Animal Welfare

References

Balaban, P 1993 Behavioural neurobiology of learning in terrestrial snails. Progress in Neurobiology 41: 1–19CrossRefGoogle ScholarPubMed
Balaban, P M and Maksimova, O A 1993 Positive and negative brain zones in the snail. European Journal of Neuroscience 5: 768–774CrossRefGoogle ScholarPubMed
Beugnon, G, Pastergue-Ruiz, I, Schatz, B and Lachaud, J P 1996 Cognitive approach of spatial and temporal information processing in insects. Behavioural Processes 35: 55–62CrossRefGoogle Scholar
Biederman, G B and Davey, V A 1993 Social learning in invertebrates. Science 259: 1627–1628CrossRefGoogle ScholarPubMed
Carducci, J P and Jakob, E M 2000 Rearing environment affects behaviour of jumping spiders. Animal Behaviour 59: 39–46CrossRefGoogle ScholarPubMed
Carew, T J and Sahley, C L 1986 Invertebrate learning and memory: from behavior to molecules. Annual Review of Neuroscience 9: 435–487CrossRefGoogle ScholarPubMed
Caubet, Y, Jaisson, P and Lenoir, A 1992 Preimaginal induction of adult behaviour in insects. Quarterly Journal of Experimental Psychology 44B: 165–178Google Scholar
Clatworthy, A L 1996 A simple systems approach to neural-immune communication. Comparative Biochemistry and Physiology 115A: 1–10Google Scholar
Cook, R T, Bailey, S E R, McCrohan, C R, Nash, B and Woodhouse, R M 2000 The influence of nutritional status on the feeding behaviour of the field slug, Deroceras reticulatum (Muller). Animal Behaviour 59: 167–176CrossRefGoogle ScholarPubMed
Danbury, T C, Weeks, C A, Chambers, J P, Waterman-Pearson, A E and Kestin, S C 2000 Self-selection of the analgesic drug carprofen by lame broiler chickens. Veterinary Record 146: 307–311CrossRefGoogle ScholarPubMed
Dethier, V G 1964 Microscopic brains. Science 143: 1138–1145CrossRefGoogle ScholarPubMed
Dickel, L, Chichery, M P and Chichery, R 1998 Time differences in the emergence of short- and long-term memory during post-embryonic development in the cuttlefish, Sepia. Behavioural Processes 44: 81–86CrossRefGoogle Scholar
Durst, C, Eichmuller, S and Menzel, R 1994 Development and experience lead to increased volume of subcompartments of the honeybee mushroom body. Behavioral and Neural Biology 62: 259–263CrossRefGoogle ScholarPubMed
Eisemann, C H, Jorgensen, W K, Merritt, D J, Rice, M J, Cribb, B W, Webb, P D and Zalucki, M P 1984 Do insects feel pain? - A biological view. Experentia 40: 164–167CrossRefGoogle Scholar
Eisenstein, E M, Carlson, A D and Harris, J T 1997 A ganglionic model of ‘learned helplessness’. Integrative Physiological and Behavioral Science 32: 265–271CrossRefGoogle ScholarPubMed
Eisner, T and Camazine, S 1983 Spider leg autotomy induced by prey venom injection: an adaptive response to ‘pain’? Proceedings of the National Academy of Sciences, USA 80: 3382–3385CrossRefGoogle ScholarPubMed
Fiorito, G 1985 Behavioral influence of pain situations in several invertebrates. Paper contributed to the Italian Society of Experimental Psychology Conference, Ravello, Italy, September 1985Google Scholar
Fiorito, G 1986 Is there ‘pain’ in invertebrates? Behavioural Processes 12: 383–388CrossRefGoogle ScholarPubMed
Fiorito, G and Scotto, P 1992 Observational learning in Octopus vulgaris. Science 256: 545–547Google ScholarPubMed
Fresquet, N and Medioni, J 1993 Effects of ageing on visual discrimination learning in Drosophila melanogaster. The Quarterly Journal of Experimental Psychology 46B: 399–412Google Scholar
GB Parliament 1986 Animals (Scientific Procedures) Act. HMSO: London, UKGoogle Scholar
Geissler, T G and Rollo, C D 1987 The influence of nutritional history on the response to novel food by the cockroach, Periplaneta americana (L.). Animal Behaviour 35: 1905–1907CrossRefGoogle Scholar
Gelperin, A 1975 Rapid food aversion learning by a terrestrial mollusc. Science 189: 567–570CrossRefGoogle Scholar
Giurfa, M, Eichmann, B and Menzel, R 1996 Symmetry perception in an insect. Nature 382: 458–461CrossRefGoogle Scholar
Greenberg, M J and Price, D A 1983 Invertebrate neuropeptides: native and naturalized. Annual Review of Physiology 45: 271–288CrossRefGoogle ScholarPubMed
Greggers, U and Menzel, R 1993 Memory dynamics and foraging strategies of honeybees. Behavioral Ecology and Sociobiology 32: 17–29CrossRefGoogle Scholar
Hammer, M and Menzel, R 1995 Learning and memory in the honeybee. Journal of Neuroscience 15: 1617–1630CrossRefGoogle ScholarPubMed
Heyes, C M and Galef, B G (eds) 1996 Social Learning in Animals: the Roots of Culture. Academic Press: California, USAGoogle Scholar
Horridge, G A 1962 Learning of leg position by the ventral nerve cord in headless insects. Proceedings of the Royal Society, London B156: 33–52Google Scholar
Hoyle, G 1979 Mechanisms of simple motor learning. Trends in Neurosciences 2: 153–159CrossRefGoogle Scholar
Jackson, R R and Wilcox, R S 1993a Observations in nature of detouring behaviour by Portia fimbriata, a web-invading aggressive mimic jumping spider from Queensland. Journal of Zoology, London 230: 135–139CrossRefGoogle Scholar
Jackson, R R and Wilcox, R S 1993b Spider flexibly chooses aggressive mimicry signals for different prey by trial and error. Behaviour 127: 21–36CrossRefGoogle Scholar
Kisch, J and Erber, J 1999 Operant conditioning of antennal movements in the honey bee. Behavioural Brain Research 99: 93–102CrossRefGoogle ScholarPubMed
Krasne, F B and Glanzman, D L 1995 What we can learn from invertebrate learning. Annual Review of Psychology 46: 585–624CrossRefGoogle Scholar
Kream, R M, Zukin, R S and Stefano, G B 1980 Demonstration of two classes of opiate binding sites in the nervous tissue of the marine mollusc Mytilus edulis. Positive homotropic cooperativity of lower affinity binding sites. Journal of Biological Chemistry 255: 9218–9224CrossRefGoogle ScholarPubMed
Lee, Y and Bitterman, M E 1990 Learning in honeybees as a function of amount of reward: control of delay. Animal Learning and Behavior 18: 377–386CrossRefGoogle Scholar
Lukowiak, K and Syed, N 1999 Learning, memory and a respiratory central pattern generator. Comparative Biochemistry and Physiology - Part A: Molecular and Integrative Physiology 124: 265–274CrossRefGoogle Scholar
Menzel, R 1993 Associative learning in honey-bees. Apidologie 24: 157–168CrossRefGoogle Scholar
Menzel, R, Geiger, K, Joerges, J, Muller, U and Chittka, L 1998 Bees travel novel homeward routes by integrating separately acquired vector memories. Animal Behaviour 55: 139–152CrossRefGoogle ScholarPubMed
Miller, R R and Berk, A M 1977 Retention over metamorphosis in the African claw-toed frog. Journal of Experimental Psychology, Animal Behaviour Processes 3: 343–356CrossRefGoogle Scholar
Nunez, J, Maldonado, H, Miralto, A and Balderrama, N 1983 The stinging response of the honeybee: effects of morphine, naloxone and some opioid peptides. Pharmacology, Biochemistry and Behaviour 19: 921–924CrossRefGoogle ScholarPubMed
Papini, M R and Bitterman, ME 1991 Appetitive conditioning in Octopus cyanea. Journal of Comparative Psychology 105: 107–114CrossRefGoogle Scholar
Pickup, H E, Cassidy, A M, Danbury, T C, Weeks, C A, Waterman, A E and Kestin, S C 1997 Self selection of an analgesic by broiler chickens. British Poultry Science 38: 512–513Google Scholar
Punzo, F 1997 Leg autotomy and avoidance behaviour in response to a predator in the wolf spider Schizocosa avida (Aranea Lycosidae). Journal of Arachnology 25: 202–205Google Scholar
Rohrseitz, K and Tautz, J 1999 Honey bee dance communication: waggle run direction coded in antennal contacts? Journal of Comparative Physiology A - Sensory Neural and Behavioral Physiology 184: 463–470CrossRefGoogle Scholar
Sahley, C L 1995 What we have learned from the study of learning in the leech. Journal of Neurobiology 27: 434–445CrossRefGoogle Scholar
Sahley, C L, Gelperin, A and Rudy, J W 1981 One-trial associative learning modifies odor preferences of a terrestrial mollusc. Proceedings of the National Academy of Sciences, USA 78: 640–642Google ScholarPubMed
Seeley, T D and Buhrman, S C 1999 Group decision making in swarms of honey bees. Behavioral Ecology and Sociobiology 45: 19–31CrossRefGoogle Scholar
Seyfarth, E A, Hergenroder, R, Ebbes, H and Barth, F G 1982 Idiothetic orientation of a wandering spider: compensation of detours and estimates of goal distance. Behavioral Ecology and Sociobiology 11: 139–148CrossRefGoogle Scholar
Shillito, D L, Gallup, G C, Gallup, J R and Beck, B B 1999 Factors affecting mirror behaviour in western lowland gorillas, Gorilla gorilla. Animal Behaviour 57: 999–1004CrossRefGoogle ScholarPubMed
Smith, B H, Abramson, C I and Tobin, T R 1991 Conditional withholding of proboscis extension in honeybees (Apis mellifera) during discriminative punishment. Journal of Comparative Psychology 105: 345–356CrossRefGoogle ScholarPubMed
Stefano, G B and Scharrer, B 1981 High affinity binding of an enkephalin analog in the cerebral ganglion of the insect Leucophaea maderae (Blattaria). Brain Research 225: 107–114CrossRefGoogle ScholarPubMed
Stefano, G B, Salzet, B and Fricchione, G L 1998 Enkelytin and opioid peptide association in invertebrates and vertebrates: immune activation and pain. Immunology Today 19: 265–268CrossRefGoogle ScholarPubMed
Suboski, M D, Muir, D and Hall, D 1993 Social learning in invertebrates. Science 259: 1628–1629CrossRefGoogle ScholarPubMed
Tarsitano, M S and Jackson, R R 1992 Influence of prey movement on the performance of simple detours by jumping spiders. Behaviour 123: 106–120Google Scholar
Tarsitano, M S and Jackson, R R 1994 Jumping spiders make predatory detours requiring movement away from prey. Behaviour 131: 65–73CrossRefGoogle Scholar
Ugolini, A and Chiussi, R 1996 Astronomical orientation and learning in the earwig Labidura riparia. Behavioural Processes 36: 151–161CrossRefGoogle ScholarPubMed
Varner, G 1999 How facts matter - on the language condition and the scope of pain in the animal kingdom. Pain Forum 8: 84–86CrossRefGoogle Scholar
Walker, S E, Marshall, S D, Rypstra, A L and Taylor, D H 1999 The effects of hunger on locomotory behaviour in two species of wolf spider (Araneae, Lycosidae) Animal Behaviour 58: 515–520CrossRefGoogle ScholarPubMed
Weidenmuller, A and Seeley, T D 1999 Imprecision in waggle dances of the honeybee (Apis mellifera) for nearby food sources: error or adaptation. Behavioral Ecology and Sociobiology 46: 190–199CrossRefGoogle Scholar
Wigglesworth, V B 1980 Do insects feel pain? Antenna 4: 8–9Google Scholar
Wustenberg, D, Gerber, B and Menzel, R 1998 Long-but not medium-term retention of olfactory memory in honeybees is impaired by actinomycin D and anisomycin. European Journal of Neuroscience 10: 2742–2745CrossRefGoogle Scholar
Yamada, A, Sekiguchi, T, Suzuki, H and Mizukami, A 1992 Behavioral analysis of internal memory states using cooling-induced retrograde amnesia in Umax flavus. The Journal of Neuroscience 12: 729–735CrossRefGoogle ScholarPubMed
Zabala, N A, Miralto, A, Maldonado, H, Nunez, J, Jaffe, K and Caderon L de, C 1984 Opiate receptor in praying mantis, effect of morphine and naloxone. Pharmacology, Biochemistry and Behaviour 20: 683687CrossRefGoogle ScholarPubMed