De centrale vraag bij ongewervelde dieren zoals kreeften en krabben is of ze pijn kunnen voelen. Ze reageren wel op prikkels zoals electrische stroomstoten, maar binnen het wetenschappelijk onderzoek vraagt men zich vervolgens af of die reacties gelijkstaan met reflexen die zonder pijnervaring plaatsvinden of dat die reacties toch gepaard gaan met het ervaren van pijn. Een belangrijke vraag want als er sprake is van pijn, dan dient er bij de vangst en verwerking van deze dieren – het gaat om astronomische aantallen – wel rekening mee gehouden te worden, net zoals we dat, ook in wetgeving, doen met gewervelde dieren, die qua lichaamsbouw dichterbij de mens staan.

Er is de jaren laatste voortdurend onderzoek gedaan bij kreeften en krabben waarbij deze vraag centraal staat. Zo is bijvoorbeeld uitvoerig onderzocht of en hoe krabben reageren op een stroomstoot die hen in hun veilige schuilplaats wordt toegediend. Ze blijken net zoals de dichterbij de mens staande gewervelde dieren die stroomstoten als pijn te ervaren en hierop niet louter te reageren met een reflex die niet gepaard gaat met een pijnervaring.

De onderzoekers hebben voor het ervaren van pijn – in tegenstelling tot reflexen – een aantal criteria vastgesteld. Belangrijke criteria zijn dat de dieren de pijnervaring in hun geheugen opslaan, ze vervolgens proberen te vermijden, en hierbij de voor- en nadelen van het opgeven van hun schuilplaats voor een andere plek afwegen (trade-off). In de toonaangevende studies van de afgelopen jaren wordt steevast de conclusie getrokken dat de reactie van de ongewervelde dieren voldoet aan de wetenschappelijke criteria voor pijn. Er wordt echter geregeld ook door de onderzoekers bij gezegd dat daarmee nog niet definitief het definitieve bewijs is geleverd dat de ongewervelde dieren pijn kunnen lijden.

Dit voorbehoud begint onder druk van het vele bewijsmateriaal voor het ervaren van pijn echter ook de onderzoekers zelf steeds meer te knellen. Dat is begrijpelijk wanneer ieder onderzoek weer het resultaat oplevert dat bijvoorbeeld de ongewervelde dieren pijn hebben ervaren of die juist hebben vermeden, dat ze over leervermogen beschikken, in staat zijn om tussen sterke en zwakkere tegenstanders onderscheid te maken en in het algemeen in tal van opzichten precies zo reageren als gewervelde dieren. In een aantal recente artikelen wordt op dit probleem door de onderzoekers ook ingegaan.
In de eerste plaats wijzen zij er op dat hun onderzoeksresultaten voor degenen die ongewervelde dieren gebruiken (vangen, verhandelen en eten) aanleiding moeten zijn om ze op een humane, diervriendelijke manier te behandelen, overeenkomstig de wijze waarop gewervelde dieren moeten worden behandeld op grond van wet- en regelgeving.
Verder stellen zij steeds duidelijker dat het niet aangaat om identieke reacties van gewervelde en ongewervelde dieren op pijnprikkels steevast voor de ongewervelde dieren als ongeldig te verklaren. Een van de toonaangevende onderzoekers, R.W. Elwood, spreekt in dit verband van een vooroordeel bij de onderzoekers tegenover ongewervelde dieren: ‘A taxonomic bias is evident in the evaluation of experimentel data’. Een zware uitspraak in de wereld van de wetenschap.
Het duidelijkst spreken zich een viertal onderzoekers (Kelsey Horvath, Dario Angeletti, Giuseppe Nascetti en Claudio Carere) in een artikel uit 2013 hierover uit, zoals al uit de titel blijkt: Invertebrate welfare: an overlooked issue. (Ann Ist Super Sanità 2013 | Vol. 49, No. 1: 9-17).
Zij stellen dat de huidige onderzoeksresultaten het aannemelijk maken dat ongewervelde dieren, zo niet alle, kunnen lijden onder de wijze waarop er met deze dieren worden behandeld, waarbij er kennelijk van uitgegaan wordt dat deze dieren geen pijn en stress kunnen ervaren en niet over enig bewustzijn beschikken. Zij spreken de hoop of verwachting uit dat wetenschappen en educatie hierin verandering zullen kunnen aanbrengen.

Hieronder een lijst van de belangrijkste wetenschappelijke artikelen met hun abstract en soms een passage uit het artikel. Toegevoegd is nog een abstract van het in dit verband interessante artikel van C.M. Sherwin, Can invertebrates suffer? waarin deze al betrekkelijk vroeg, in 2001, stelt dat er wat pijnbeleving en bewustzijn betreft, op basis van dezelfde onderzoeksresultaten geen discriminerend onderscheid gemaakt mag worden tussen gewervelde dieren en ongewervelde dieren.

R.W. Elwood and M. Appel, Pain experience in hermit crabs? Animal Behaviour 77 (2009) 1243-1246.

Abstract
Pain may be inferred when the responses to a noxious stimulus are not reflexive but are traded off
against other motivational requirements, the experience is remembered and the situation is avoided in
the future. To investigate whether decapods feel pain we gave hermit crabs,
Pagurus bernhardus, small electric shocks within their shells.
Only crabs given shocks evacuated their shells indicating the aversive nature of the stimulus, but fewer crabs evacuated from a preferred species of shell indicating a motivational trade-off. Some crabs that evacuated attacked the shell in the manner seen in a shell fight. Most crabs, however, did not evacuate at the stimulus level we used, but when these were subsequently offered a new shell, shocked crabs were more likely to approach and enter the new shell.
Furthermore, they approached that shell more quickly, investigated it for a shorter time and used fewer cheeped probes within the aperture prior to moving in. Thus the experience of the shock altered future behavior in a manner consistent with a marked shift in motivation to get a new shell to replace the one occupied. The results are consistent with the idea of pain in these animals.

R.W. Elwood, S. Barr and L. Patterson, Pain and stress in crustaceans? Applied Animal Behaviour Science 118 (2009) 128-136.

Abstract
We consider evidence that crustaceans might experience pain and stress in ways that are analogous to those of vertebrates. Various criteria are applied that might indicate a potential for pain experience: (1) a suitable central nervous system and receptors, (2) avoidance learning, (3) protective motor reactions that might include reduced use of the affected area, limping, rubbing, holding or autotomy, (4) physiological changes, (5) trade-offs between stimulus avoidance and other motivational requirements, (6) opioid receptors and evidence of reduced pain experience if treated with local anaesthetics or analgesics, and (7) high cognitive ability and sentience. For stress, we examine hormonal responses that have similar function to glucocorticoids in vertebrates. We conclude that there is considerable similarity of function, although different systems are used, and thus there might be a similar experience in terms of suffering. The treatment of these animals in the food industry and elsewhere might thus pose welfare problems.

R.W. Elwood (2011), Pain and suffering in invertebrates? Institute for Laboratory Animal Research (ILAR) Journal 52 (2011) 175-184.

Rapid avoidance learning and prolonged memory indicate central processing rather than simple reflex and are consistent with the experience of pain. Complex, prolonged grooming or rubbing may demonstrate an awareness of the specific site of stimulus application. Tradeoffs with other motivational systems indicate central processing, and an ability to use complex information suggests sufficient cognitive ability for the animal to have a fitness benefit from a pain experience.Availlable data are consistent with the idea of pain in some invertebrates and go beyond the idea of just nociception but are not not definitive. In the absence of conclusive data, more humane care for invertebrates is suggested.
Slot: While awaiting there results of further relevant studies, perhaps all who use invertebrates should consider the possibility that at least some might suffer pain and, as a precaution, ensure humane care for these animals.

R.W. Elwood, Evidence for pain in decapods crustaceans? Animal Welfare 21 Suppl. 2 (2012) 23-27.

Abstract
Vast numbers of decapods are used in human food and currently subject to extreme treatments and there is concern that they might experience pain. If pain is indicated then a positive change in the care afforded to this group has the potential to produce a major advance in animal welfare. However, it is difficult to determine pain in animals. The vast majority of animal phyla have a nociceptive ability that enables them to detect potential or actual tissue damage and move away by a reflex response. In these cases there is no need to assume an unpleasant feeling that we call pain. However, various criteria have been proposed that might indicate pain rather than simple nociception. Here, with respect to decapod crustaceans, four such criteria are discussed: avoidance learning, physiological responses, protective motor reactions and motivational trade-offs. The evidence from various experiments indicates that all four criteria are fulfilled and the data are thus consistent with the idea of pain. The responses cannot be explained by nociception alone but, it is still difficult to state categorically that pain is experienced by decapods. However, the evidence is as strong for this group as it is for fish but the idea that fish experience pain has broader acceptance than does the idea of decapod pain. A taxonomic bias is evident in the evaluation of experimental data.

Barry Magee and Robert W. Elwood, Shock avoidance by discrimination learning in the shore crab (Carcinus maenad) is consistent with a key criterion for pain. The Journal of Experimental Biology 216 (2013) 353-358.

Abstract
Nociception allows for immediate reflex withdrawal whereas pain allows for longer-term protection via rapid learning. We examine here whether shore crabs placed within a brightly lit chamber learn to avoid one of two dark shelters when that shelter consistently results in shock. Crabs were randomly selected to receive shock or not prior to making their first choice and were tested again over 10 trials. Those that received shock in trial 2, irrespective of shock in trial 1, were more likely to switch shelter choice in the next trial and thus showed rapid discrimination. During trial 1, many crabs emerged from the shock shelter and an increasing proportion emerged in later trials, thus avoiding shock by entering a normally avoided light area. In a final test we switched distinctive visual stimuli positioned above each shelter and/or changed the orientation of the crab when placed in the chamber for the test. The visual stimuli had no effect on choice, but crabs with altered orientation now selected the shock shelter, indicating that they had discriminated between the two shelters on the basis of movement direction. These data, and those of other recent experiments, are consistent with key criteria for pain experience and are broadly similar to those from vertebrate studies.

Slot: In conclusion, the data from this and other studies (e.g. Elwood, 2012) go beyond the idea of crustaceans responding to noxious stimuli simply by nociceptive reflex. Instead, long-term motivational change that enables discrimination learning has been demonstrated. Perhalps such motivational changes and learning can arise without any an unpleasant experience, although that is doubted by Gentle (Gentle, 2011) for birds. However, if we accept that possibility for invertebrates, we should also accept the same possibility for at least some vertebrates.

Kelsey Horvath, Dario Angeletti, Giuseppe Nascetti en Claudio Carere), Invertebrate welfare: an overlooked issue. Annali dell’Istituto Superiore di Sanità 2013 49 (2013) No. 1: 9-17.

Abstract
While invertebrates make up the majority of animal species, their welfare is overlooked compared to the concern shown to vertebrates. This fact is highlighted by the near absence of regulations in animal research, with the exception of cephalopods in the European Union. This is often justified by assumptions that invertebrates do not experience pain and stress while lacking the capacity for higher order cognitive functions. Recent research suggests that invertebrates may be just as capable as vertebrates in experiencing pain and stress, and some species display comparable cognitive capacities. Another obstacle is the negative view of invertebrates by the public, which often regards them as pests with no individual personalities, gastronomic entities, or individuals for scientific experimentation without rules. Increasingly, studies have revealed that invertebrates possess individual profiles comparable to the personalities found in vertebrates. Given the large economic impact of invertebrates, developing certain attitude changes in invertebrate welfare may be beneficial for producers while providing higher welfare conditions for the animals. While the immense number and type of species makes it difficult to suggest that all invertebrates will benefit from increased welfare, in this review we provide evidence that the topic of invertebrate welfare should be revisited, more thoroughly investigated, and in cases where appropriate, formally instituted.

C.M. Sherwin, Can invertebrates suffer? Or how robust is argument-by-analogy? Animal Welfare 10 (2001) 103-118.

Abstract
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.