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Motivational trade-offs and potential pain experience in hermit crabs
Abstract
One criterion of pain experience is that the emotional response to pain may be traded-off against other motivational requirements. This was tested in hermit crabs, housed in either preferred or unpreferred species of shells, by subjecting their abdomens to electric shocks of gradually increasing intensity. The first observable response was not affected by shell species but those in preferred shells evacuated at a higher shock level than those in poor quality shells. Thus, they seem to trade-off the requirement to retain a high quality shell with that of avoidance of the noxious stimulus. Some crabs returned to their shells and those that got back into the preferred species did so with less probing of the aperture before getting in and subsequently thrust their abdomen in and out less often in further investigation, thus confirming their shell species preference. Not all crabs returned to the vicinity of the shell and some attempted to climb the wall of the experimental chamber. Others engaged in shell rapping as if in a fight and grooming of the abdomen was noted. These findings are consistent with the idea of a pain experience rather than a nociceptive reflex.
... Altered motivation regarding access to or use of resources is expected. Further, pain might cause the animal to give up important resources, but the costs of giving up a resource should be balanced against the benefit of avoiding the pain [21,22]. That is, we expect pain to have marked effects on behaviour in ways that the animal can best cope with the tissue damage and promote subsequent survival [8,12,23]. ...
... Swift escape from noxious stimuli might appear to be a nociceptive reflex, however, it might be more complex than that [37]. This possibility was tested by assessing if tradeoffs occurred between escape responses and other motivational requirements [21,22]. The rationale was that if these immediate responses to a noxious stimulus were influenced by other factors, then the animal must have integrated information from other sources with that from nociceptors, resulting in an adaptive decision rather than an inflexible reflex [9,16]. ...
... Swift escape from noxious stimuli might appear to be a nociceptive reflex, however, it might be more complex than that [37]. This possibility was tested by assessing if trade-offs occurred between escape responses and other motivational requirements [21,22]. The rationale was that if these immediate responses to a noxious stimulus were influenced by other factors, then the animal must have integrated information from other sources with that from nociceptors, resulting in an adaptive decision rather than an inflexible reflex [9,16]. ...
Pain in response to tissue damage functions to change behaviour so that further damage is minimised whereas healing and survival are promoted. This paper focuses on the behavioural criteria that match the function to ask if pain is likely in the main taxa of arthropods. There is evidence consistent with the idea of pain in crustaceans, insects and, to a lesser extent, spiders. There is little evidence of pain in millipedes, centipedes, scorpions, and horseshoe crabs but there have been few investigations of these groups. Alternative approaches in the study of pain are explored and it is suggested that studies on traumatic mating, agonistic interactions, and defensive venoms might provide clues about pain. The evolution of high cognitive ability, sensory systems, and flexible decision-making is discussed as well as how these might influence the evolution of pain-like states.
... However, the crabs trade-off escaping from the shock with other requirements, and thus show that the response is a decision rather than reflex. For example, crabs emerged from the less preferred species of shell at a lower voltage than they did from the preferred species (Appel and Elwood 2009a). Furthermore, when the voltage was kept constant, they were more likely to abandon the less preferred species (Elwood and Appel 2009). ...
... It would thus have similarities to the repeated minor electric shocks to the abdomen that can cause the crab to get out of the shell. The probability and timing of getting out of the shell are traded-off against the shell quality when electric shocks are applied (Appel and Elwood 2009a;Elwood and Appel 2009), and thus is like trade-offs in shell fights (Dowds and Elwood 1983;Arnott and Elwood 2007). That is, the better the shell for the defender, the longer it resists eviction. ...
... Assessing if pain occurs in animals depends on various criteria being fulfilled (Sneddon et al. 2014), some of which have been directly tested with hermit crabs. For example, we see trade-offs between avoidance of noxious stimuli and other motivational requirements (Appel and Elwood 2009a;Elwood and Appel 2009;Magee and Elwood 2016), direction of attention toward the afflicted site (Appel and Elwood 2009a), and long-term motivational change as shown by the increased motivation to move shells if shocked within a shell (Elwood and Appel 2009;Appel and Elwood 2009b), and these are consistent with pain. There is also evidence from a range of other decapod species, which includes physiological stress responses (Fossat et al. 2014;Elwood and Adams 2015), rapid avoidance learning (Okada et al. 2021;Magee and Elwood 2013), reduced risk-taking (Fosssat et al. 2014(Fosssat et al. , 2015, and local anaesthetics reducing responses (Barr et al. 2008). ...
Hermit crabs have an intimate relationship with gastropod shells and show numerous activities by which they locate, select, and change shells in different contexts. They gather information about new shells and update information about their existing shells. This involves integration of different sensory modalities, memory-formation, and comparison of the overall value of each shell. Crabs also fight to get shells from other crabs, and again they gather information about the shell qualities and the opponent. Attacking crabs monitor their fight performance, and defenders are influenced by attacker activities, and both crabs are influenced by the gain or loss that might be made by swapping shells. Swapping shells involves the defender being naked for a short period. Leaving a shell also occurs if the shell is experimentally fixed in place or buried in sand or if small electric shocks are applied to the abdomen, and the quality of the current shell is traded-off against escaping possible asphyxiation or the aversive shocks. Hermit crabs show remarkable abilities, involving future planning, with respect to recognizing the shape and size of shells, and how they limit their passage through environmental obstructions. They also assess if shells might become available and wait for that to happen. Groups of crabs arrange themselves in size order so that orderly transfer of shells might occur down a line of crabs. These observations are discussed in the light of complex perceptual and cognitive abilities, and the possibility of sentience and awareness is discussed.
... To explore this possibility, Appel & Elwood (2009a) asked: if electric shocks are administered to the crabs when they are in the shells, will the crabs leave regardless of the quality of the shell, or will they be more reluctant to leave a high-quality shell than a low-quality shell? The latter would suggest that the disvalue of a noxious stimulus is weighed against other preferences. ...
... They compared the mean voltage required to induce a crab to leave a high-quality shell (Littorina) with the mean voltage required to induce a crab to leave a low-quality shell (Gibbula). They found that "hermit crabs in Littorina shells left the shells at significantly higher voltages than those in Gibbula shells" (Appel & Elwood, 2009a). The mean voltage required to induce a crab to leave a Littorina shell was 17.7V, compared with 15.0V for Gibbula. ...
... They did not find any difference in the mean voltage to evacuate between crabs exposed to this odour and crabs that were not. This can be considered an unsuccessful conceptual replication (but not a direct replication) of Appel and Elwood (2009a). What they did find, however, was that crabs exposed to an odour were substantially more likely to remain in their shells, even when given 25V shocks, than those exposed to no odour. ...
Sentience is the capacity to have feelings, such as feelings of pain, pleasure, hunger, thirst, warmth, joy, comfort and excitement. It is not simply the capacity to feel pain, but feelings of pain, distress or harm, broadly understood, have a special significance for animal welfare law.
Drawing on over 300 scientific studies, we have evaluated the evidence of sentience in two groups of invertebrate animals: the cephalopod molluscs or, for short, cephalopods (including octopods, squid and cuttlefish) and the decapod crustaceans or, for short, decapods (including crabs, lobsters and crayfish). We have also evaluated the potential welfare implications of current commercial practices involving these animals.
... Dyuzen et al. [58] injected formalin into an appendage of the crab, Hemigrapsus sanguineus, which then shook and rubbed the specific appendage, and reduced its use. Hermit crabs, Pagurus bernhardus, that had received electric shocks on the abdomen and had abandoned their shell showed grooming of the abdomen [59], and brown crabs that had one claw removed by twisting it off (as in fishery practice) picked at the wound and held their remaining claw over the wound when confronted by an intact crab [60]. Thus, decapods attend to the area of the body that received the noxious stimulation in a similar manner to that shown by mammals; (ii) Trade-offs between avoidance responses and other motivational requirements. ...
... Such motivational trade-offs were observed by Elwood and Apple [62] in hermit crabs (Pagurus bernardus) that were more likely to abandon a poor-quality shell after electric shock than one of high quality. They also emerged from low-quality shells at a lower intensity shock than did those in high quality shells [59]. Similarly, hermit crabs were less likely to leave their shells after electric shock if the odor of a predator was present in the surrounding water [63]. ...
... This was seen in hermit crabs that got out of their shell when the abdomen was shocked. Some crabs then moved away from the shell and some attempted to climb the wall of the observation chamber [59]. Whilst many hermit crabs reentered the shell, often after a prolonged investigation within, some remained naked for the 15 min observation period. ...
Decapod crustaceans are widely used as experimental models, due to their biology, their sensitivity to pollutants and/or their convenience of collection and use. Decapods have been viewed as being non-sentient, and are not covered by current legislation from the European Parliament. However, recent studies suggest it is likely that they experience pain and may have the capacity to suffer. Accordingly, there is ethical concern regarding their continued use in research in the absence of protective measures. We argue that their welfare should be taken into account and included in ethical review processes that include the assessment of welfare and the minimization or alleviation of potential pain. We review the current use of these animals in research and the recent experiments that suggest sentience in this group. We also review recent changes in the views of scientists, veterinary scientists and animal charity groups, and their conclusion that these animals are likely to be sentient, and that changes in legislation are needed to protect them. A precautionary approach should be adopted to safeguard these animals from possible pain and suffering. Finally, we recommend that decapods be included in the European legislation concerning the welfare of animals used in experimentation. View Full-Text
... However, shell evacuation has been shown to be traded-off against other, competing, motivational requirements. Hermit crabs were less likely to evacuate their shells if the odour of a predator was present [7], and those subjected to the increasing intensity of shock abandoned shells of a preferred species at a higher intensity than did those in poor quality shells [8]. If subjected to shocks of a single intensity hermit crabs were more likely to abandon shells of a less preferred species [9]. ...
... This behaviour was not seen if just seawater was applied [6]. Also, shore crabs, Carcinus maenas, use their claws to scratch at their mouthparts if that is brushed with acetic acid [12] and hermit crabs, shocked on the abdomen, groom at the site of the shock, an activity not seen without the noxious stimulus [8,13]. Furthermore, edible crabs, Cancer pagurus, that have had a clawed appendage twisted off in the manner used in some fisheries [14] held their remaining claw over the wound during a competitive interaction. ...
... But, even with short-term responses, there are indications that reflexes may not always account for the nature of the behaviour. We see this with the motivational trade-off between shock avoidance and other motivational requirements, which indicates that the response is owing to a behavioural decision rather than reflex [8,9]. There are also prolonged complex activities involving rubbing, grooming and wound guarding directed to the specific area [11,12,14]. ...
Animals have quick-acting nociceptive reflexes that protect them from tissue damage. Some taxa have also evolved the capacity for pain. Pain appears to be linked to long-term changes in motivation brought about by the aversive nature of the experience. Pain presumably enhances long-term protection through behaviour modification based, in part, on memory. However, crustaceans have long been viewed as responding purely by reflex and thus not experiencing pain. This paper considers behavioural and physiological criteria that distinguish nociception from potential pain in this taxon. These include trade-offs with other motivational systems and prolonged motivational change. Complex, prolonged grooming or rubbing demonstrate the perception of the specific site of stimulus application. Recent evidence of fitness-enhancing, anxiety-like states is also consistent with the idea of pain. Physiological changes in response to noxious stimuli mediate some of the behavioural change. Rapid avoidance learning and prolonged memory indicate central processing rather than mere reflexes. Thus, available data go beyond the idea of just nociception. However, the impossibility of total proof of pain described in ways appropriate for our own species means that pain in crustaceans is still disputed. Pain in animals should be defined in ways that do not depend on human pain experience.
This article is part of the Theo Murphy meeting issue ‘Evolution of mechanisms and behaviour important for pain’.
... A potential inconvenience to removing the crabs from their shell via heating is that individuals could place different values on different shells, and therefore be willing to endure a more noxious stimulus to retain it (Appel & Elwood 2009b). For instance, the hermit crab (Pagurus bernhardus) shows a motivational trade-off associated with the shell quality; individuals in the preferred shell abandoned it at a higher shock intensity than those in poor quality shells (Appel & Elwood 2009b;Elwood & Appel 2009). ...
... A potential inconvenience to removing the crabs from their shell via heating is that individuals could place different values on different shells, and therefore be willing to endure a more noxious stimulus to retain it (Appel & Elwood 2009b). For instance, the hermit crab (Pagurus bernhardus) shows a motivational trade-off associated with the shell quality; individuals in the preferred shell abandoned it at a higher shock intensity than those in poor quality shells (Appel & Elwood 2009b;Elwood & Appel 2009). However, in C. californiensis the temperature endured by the individuals was not related to the shell quality, at least in terms of shell fit. ...
Hermit crabs (Paguroidea; Latreille 1802) offer great opportunities to study animal behaviour and physiology. However, the animals’ size and sex cannot be determined when they are inside their shell; information crucial to many experimental designs. Here, we tested the effects of the two most common procedures used to make crabs leave their shells: heating the shell apex and cracking the shell with a bench press. We compared the effects of each of the two procedures on the metabolic rate, hiding time, and duration of the recovery time relative to unmanipulated hermit crabs. The hermit crabs forced to abandon their shell through heating increased their respiratory rate shortly after the manipulation (1 h) and recovered their metabolic rate in less than 24 h, as occurs in individuals suddenly exposed to high temperatures in the upper-intertidal zone. Hermit crabs removed from their shells via cracking spent more time hiding in their new shells; this effect was evident immediately after the manipulation and lasted more than 24 h, similar to responses exhibited after a life-threatening predator attack. Both methods are expected to be stressful, harmful, or fear-inducing; however, the temperature required to force the crabs to abandon the shell is below the critical thermal maxima of most inhabitants of tropical tide pools. The wide thermal windows of intertidal crustaceans and the shorter duration of consequences of shell heating compared to cracking suggest heating to be a less harmful procedure for removing tropical hermit crabs from their shells.
... Research has shown that fish experience pain [1,2], suffering, and distress and respond to stressful and noxious stimuli just as other phylogenetically "higher" animals, and this applies for adult fish [3,4], fish larvae [5,6], as well as other invertebrate aquatic animals [7][8][9][10][11]. Furthermore, the administration of analgesic substances with known effects in mammals also modulates responses to painful stimuli in aquatic species [5,7,10,12,13]. Nociception is a useful and necessary capability for self-protection and unquestionable for survival for most creatures. Studies have also suggested affective state and learning abilities for both vertebrate [14] and invertebrate aquatic animals [13,15]. ...
... Nociception is a useful and necessary capability for self-protection and unquestionable for survival for most creatures. Studies have also suggested affective state and learning abilities for both vertebrate [14] and invertebrate aquatic animals [13,15]. ...
Fish and other aquatic animals represent a significant number of species with diverse physiology, size, and housing condition needs. Anesthesia may be necessary for several husbandry procedures as well as treatment of diseases, surgery, or experimental procedures. Choice of drugs and detailed procedures for anesthesia must be adapted to the species in question—there is no “one size fits all” solution. However, there are some basic principles that apply for good anesthetic practice of all animals. These principles include the preparations of animals, personnel, facilities and equipment, monitoring animals under anesthesia, as well as post-anesthetic care to be sure that animals are not lost in the recovery phase. Good anesthesia practice also includes the competence and commitment of personnel involved. Based on professional judgement, key factors will be the focus of this text.
... We used a motivational trade-off paradigm, where animals must flexibly trade-off two competing motivations. For example, hermit crabs require higher voltages of electric shock to evacuate their preferred shell species than for a less preferred one (5,6). Shock avoidance is traded off against shell preference. ...
... Bumblebees avoided noxiously heated feeders less when these dispensed higher sucrose concentrations than unheated feeders. Unlike trade-offs described in other invertebrates (5,6,9), this trade-off relied on associative memories, rather than direct experience of the stimuli. Bees' ability to trade-off heat avoidance against sucrose preference indicates that conditioned motivational stimuli can influence nocifensive behavior, and the trade-off is mediated in the central nervous system (10,11). ...
Insects are traditionally thought to respond to noxious stimuli in an inflexible manner, without the ability to modulate their behavior according to context. We investigated whether bumblebees’ attraction to high sucrose solution concentrations reduces their avoidance of noxious heat. Bees were given the choice between either unheated or noxiously heated (55 °C) feeders with different sucrose concentrations and marked by different colors. Bees avoided noxious feeders when the unheated feeders contained high sucrose concentrations, but progressively increased feeding from noxious feeders when the sucrose concentration at unheated feeders decreased. This shows a motivational trade-off of nociceptive responses. Bees used learned color cues for their decisions, and thus the trade-off was based on processing in the brain, rather than just peripheral processing. Therefore, bees can use contextual information to modulate nociceptive behavior. This ability is consistent with a capacity for pain experiences in insects.
... The behavioural criteria for pain, and experiments designed to test those in decapods, have been reviewed extensively [4,20,[22][23][24] and here we aim to be brief. Hermit crabs show a trade-off of shock avoidance with other motivational requirements, indicating that rapid shell-evacuation is the result of a decision that requires central processing rather than reflex [25][26][27]. Shore crabs rapidly learn to avoid entering a dark shelter associated with electric shock and will pay a cost to avoid the shock [28]. Hermit crabs show long-term changes in behaviour following a shock within their shell and become less motivated to retain that shell [27,29,30], a shift that lasts for at least a day [31]. ...
... It seems that consumers are not concerned about the possibility of suffering in small animals. This, however, is one of public opinion rather than a reaction to evidence because many of the studies that indicate possible pain have been conducted on small decapods, such as glass prawns [12] and hermit crabs [26][27][28]31]. Furthermore, prawns and shrimps are more likely to be dead (fresh, frozen, or boiled) when purchased, so consumers are not faced with the problem of killing them humanely. ...
Vast numbers of crustaceans are produced by aquaculture and caught in fisheries to meet the increasing demand for seafood and freshwater crustaceans. Simultaneously, the public is increasingly concerned about current methods employed in their handling and killing. Recent evidence has shown that decapod crustaceans probably have the capacity to suffer because they show responses consistent with pain and have a relatively complex cognitive capacity. For these reasons, they should receive protection. Despite the large numbers of crustaceans transported and slaughtered, legislation protecting their welfare, by using agreed, standardized methods, is lacking. We review various stunning and killing systems proposed for crustaceans, and assess welfare concerns. We suggest the use of methods least likely to cause suffering and call for the implementation of welfare guidelines covering the slaughter of these economically important animals.
... Similar experiments have been done on iguanas (Iguana iguana) [33] and hermit crabs (Pagurus bernhardus) [34,35], with similar results. What is lacking, so far, is interspecies comparisons of the sophistication of the evaluations being made by different species and investigations of how sophisticated the evaluations need to be to indicate conscious affect. ...
... [24,27] E-richness Motivational trade-off Does the animal weigh different needs against each other in a 'common currency' to make flexible decisions? [30,[33][34][35] Outcome devaluation and revaluation ...
How does consciousness vary across the animal kingdom? Are some animals ‘more conscious’ than others? This article presents a multidimensional framework for understanding interspecies variation in states of consciousness. The framework distinguishes five key dimensions of variation: perceptual richness, evaluative richness, integration at a time, integration across time, and self-consciousness. For each dimension, existing experiments that bear on it are reviewed and future experiments are suggested. By assessing a given species against each dimension, we can construct a consciousness profile for that species. On this framework, there is no single scale along which species can be ranked as more or less conscious. Rather, each species has its own distinctive consciousness profile.
... Crayfish oriented away from the escape door never learned to avoid the shock, showing that avoidance learning was context dependent. Appel and Elwood (2009a) reported motivational trade-offs in hermit crabs (Pagurus bernhardus) exposed to electric shocks as evidence of a "potential pain experience". They found crabs first reacted to electric shock at the same voltage (9.0-9.1 V) regardless of shell type, but it took more voltage on average to evacuate a more preferred shell type (Littorina, 17.7 V) compared with a less preferred shell type (Gibbula, 14.9 V). ...
... Given that crustaceans and other arthropods also commonly and naturally exhibit behaviours such as autotomy [loss and regrowth of entire claws and limbs (Maruzzo et al., 2005;Patterson et al., 2007, Appel andElwood, 2009a;Kotsyuba et al., 2010;Dyuizen et al., 2012;Magee and Elwood, 2013], this brings the validity of many of the criteria presented by Sneddon et al. (2014) into serious question if the word pain (as used and understood by humans) is to be applied to crustaceans. Certainly, it is difficult to understand what adaptive advantage an ability to "feel pain" would confer to a crustacean that spontaneously sacrifices appendages by autotomy during normal development or when under stress (Patterson et al., 2007;Kotsyuba et al., 2010), only for those appendages to be grown back in later moults (Maruzzo et al., 2005). ...
The scientific literature on the subject of welfare and pain in crustaceans is immature. It is based largely on a few dubious and disputed studies done on a small number of decapod species in instances where nociception was not confirmed, laboratory artefacts occurred, all variables that potentially influence the results were not fully controlled, and interpretations of results were questionable or contradictory. The proposed criteria for pain being applied to crustaceans since 2014 has set the "evidential bar" for pain so low it is impossible to have confidence that the behaviours observed in many experiments are even due to nociception, extinguishing scientific confidence that these behaviours are in any way analogous to how the word pain is defined, used, and understood by humans. Given the critical flaws in design and interpretation of several crustacean "pain" studies, acceptance of claims of pain for these animals, even as a precautionary measure, represents acceptance of a much lower evidential bar than is usually dictated by normal scientific standards. This may lead to circumstances whereby the precautionary principle, underpinned by weak science, is used by decision makers to justify unnecessary constraints on scientific research or other uses of crustaceans, imparting significant costs to scientific programs (and potentially food production industries), which are likely to exceed any benefits from changes in welfare status that may (or may not) accrue to these animals.
... However, this position was disputed by the UK Bioscience Sector on the grounds that reliable evidence of pain and sentience had not been scientifically established at that time (Bioscience Sector 2009; Birch 2017c) since it relied on studies such as those in crabs that associated a reduction in defensive responses with a specific analgesic effect of morphine (Lozada et al. 1988;Bergamo et al. 1992) when this may have been due to general non-responsiveness (Barr and Elwood 2011). Although more substantial evidence of pain and sentience subsequently became available (as described later in this paper) (Barr et al. 2008;Appel and Elwood 2009) crustaceans were excluded from the European Union Directive 2010/63/EU on the protection of animals used for scientific purposes (European Parliament and of the Council 2010). ...
... Hermit crabs (Pagurus bernhardus) exposed to an electric shock are less likely to evacuate their shells as the concentration of predator odour escalates (Magee and Elwood 2016) or when housed in a preferred vs non-preferred species of shell (Appel and Elwood 2009). This is known as motivational trade-off, because the preference to avoid noxious stimuli is weighed against a requirement such as shelter. ...
Decapod crustaceans are faceless animals with five pairs of legs, an external skeleton and multiple nerve centres (ganglia) rather than a single brain (as in vertebrates). They include common seafood species such as crayfish, crabs, lobsters, prawns and shrimp. These characteristics make them difficult to empathise with and consequently legal protection of decapods ranges from strong (Norway and New Zealand), through circumstantial (Australia and Italy) to non-existent (in many other countries). Whether they are capable of experiencing pain depends on definitions and the requirement for absolute proof of an inherently subjective psychological experience. Yet like other animals, decapods fulfil neuroanatomical, pharmacological and behavioural criteria that are consistent with a pain response. Whether they experience stress, harm and distress is less controversial because these conditions are more measurable than the pain response. To balance animal welfare concerns with scientific merit whilst providing confidence for the growing public awareness of crustacean welfare, use of decapod crustaceans in research should require ethical review.
... The third class of neurons, the motor neurons, comprise approximately one third of the nematode nervous system (Altun and Hall 2011;Hobert et al. 2016) and are directly responsible for executing motor behaviours. There are distinct pools of motor neurons that contribute to forward and reversal movements (Zhen and Samuel 2015). ...
Deciphering the neural basis of subjective experience remains one of the great challenges in the natural sciences. The structural complexity and the limitations around invasive experimental manipulations of the human brain have impeded progress towards this goal. While animals cannot directly report first-person subjective experiences, their ability to exhibit flexible behaviours such as motivational trade-offs are generally considered evidence of sentience. The worm Caenorhabditis elegans affords the unique opportunity to describe the circuitry underlying subjective experience at a single cell level as its whole neural connectome is known and moreover, these animals exhibit motivational trade-offs. We started with the premise that these worms were sentient and then sought to understand the neurons that were both necessary and sufficient for a motivational trade-off involving the rewarding experience of food and the negative experience of an aversive odour. A simple hierarchical network consisting of two chemosensory neurons and three interneurons was found to produce an output to motoneurons that enabled worms to respond in a contextually appropriate manner to an aversive odour according to the worm's hunger state. Given that this circuitry is like that found in the human spinal cord, retina, and primary visual cortex, three regions which are neither necessary nor sufficient for subjective experience, we conclude that motivational trade-offs are not a criterion for subjective experience in worms. Furthermore, once the neural substrate for a behaviour is described, we question the explanatory role of subjective experience in behaviour.
... Consequently, an increase in sensitivity is often observed after injury referred to as sensitization. Clearly, decapod crustaceans show nociceptive behaviour [46][47][48], but primary nociceptors have only recently been described in one species [49]. It should be noted that, in contrast to Drosophila, crayfsh do not respond to nocigenic chemicals such as capsaicin [49], isothiocyanate [49] or extreme pH [50]. ...
Despite the growing concern on animal welfare in crustacean farming, both from legislative bodies as well as the common public, studies on welfare are limited and transfer to routine farming is missing. While biocertification schemes such as the Aquaculture Stewardship Council (ASC) involve a welfare dimension, these dimensions cannot be communicated to the consumer in a scientifically sound manner. Animal welfare is recognized as integral part of sustainability due to the losses associated with bad animal welfare standards and is considered highly relevant by consumers around the world. On the other hand, increasing animal welfare is also required for the optimisation of aquaculture technology. Behaviour of the animals suggests that decapod crustaceans experience nociception and there are several indications of pain perception as well. Also, distress has rarely been evaluated under routine aquaculture conditions and markers for chronic stress detection need to be identified. Indeed, most work on welfare of crustaceans focuses on cellular, oxidative stress only. Here, a comprehensive assessment of chronic stress should be carried out to optimize rearing technology in nurseries, during ongrowing, harvesting, anesthesia, transportation, and humane slaughter in terms of a good aquaculture practise.
... In the animal sentience literature, motivational trade-off behavior, i.e., behavior which flexibly trades off between rewards and punishments and their respective strengths (e.g., the strength of an electric shock and a food reward), is standardly seen as credible evidence of sentience (Appel and Elwood 2009;Gibbons et al. 2022;Millsopp and Laming 2008). In fact, all five of the overview papers listed above mention this paradigm explicitly. ...
... In arthropods, cognitive studies of fear or aversive conditioning that operate with the innate fear-like response to aversive stimuli have been used to evaluate behavioral and physiological components of emotional responses in insects. Aversive stimuli, electric shocks, social stress and molting have been applied to show the induction of anxiety-like behaviors in crayfish, amphipods and crabs (Appel and Elwood, 2009;Bacqué-Cazenave et al., 2017, 2019Fossat et al., 2014Fossat et al., , 2015Hamilton et al., 2016;Perrot-Minnot et al., 2017). The associative memory paradigm studied here is based on an association between the context presentation and the visual danger stimulus. ...
The interactions between memory processes and emotions are complex. Our previous investigations in the crab Neohelice led to an adaptation of the Affective Extension of Sometimes Opponent Processes (AESOP) model. The model proposes that emotions generate separate emotive memory traces, and that the unfolding of emotional responses is a crucial component of the behavioral expression of reactivated memories. Here, we show that an aversive conditioning, that uses changes in an innate escape response to an aversive visual stimulus, induced an emotional behavior that endured beyond the stimuli: an aversive memory training built an anxiety-like state evaluated in a dark/light plus-maze. We found that, after training session, crabs displayed aversion to maze light areas, and an increased time immobilized in the dark zones of the maze, an anxiety-like behavior induced by stressors or physiological conditions in other crustaceans. The training-dependent anxiety-like behavior was blocked by pretraining administration of fluoxetine, suggesting an underlying serotonin-dependent phenomenon. We hypothesize that this training-induced anxiety-like state generates a separate emotive memory trace that is reinstated and crucial for the modulation of memory expression once the memory is reactivated.
... Such a sensitivity can be characterized as a simple form of self-sensitivity which is prior to mirror selfrecognition (Wittek et al., 2021). 12 Another experimental paradigm stressed by Birch et al. is motivational trade-off which has been detected in fish (Millsopp & Laming, 2008), hermit crabs (Appel & Elwood, 2009) and bees (Gibbons, Versace, Crump, Baran, & Chittka, 2022). ...
The science of animal consciousness investigates (i) which animal species are conscious (the distribution question) and (ii) how conscious experience differs in detail between species (the quality question). We propose a framework which clearly distinguishes both questions and tackles both of them. This two-tier account distinguishes consciousness along ten dimensions and suggests cognitive capacities which serve as distinct operationalizations for each dimension. The two-tier account achieves three valuable aims: First, it separates strong and weak indicators of the presence of consciousness. Second, these indicators include not only different specific contents but also differences in the way particular contents are processed (by processes of learning, reasoning or abstraction). Third, evidence of consciousness from each dimension can be combined to derive the distinctive multi-dimensional consciousness profile of various species. Thus, the two-tier account shows how the kind of conscious experience of different species can be systematically compared.
... My example of the application of the desiderata is trade-off behavior in response to noxious stimuli which has been taken as evidence of consciousness by many authors (e.g., Sneddon et al., 2014;Tye, 2017). Motivational trade-off behavior has been found in fish (Millsopp & Laming, 2008), hermit crabs (Appel & Elwood, 2009) and bees (Gibbons et al., 2022). In the experiment of Millsopp and Laming (2008), goldfish reduced their feeding attempts in a part of an aquarium where they received a shock. ...
Which animals have conscious experiences? Many different, diverse and unrelated behaviors and cognitive capacities have been proposed as tests of the presence of consciousness in an animal. It is unclear which of these tests, if any, are valid. To remedy this problem, I develop a list consisting of eight desiderata which can be used to assess putative tests of animal consciousness. These desiderata are based either on detailed analogies between consciousness-linked human behavior and non-human behavior, on theories of consciousness or on methods from human consciousness science. If a test or set of tests satisfies more of these desiderata, passing it provides stronger evidence of consciousness. Moreover, one can design future tests of animal consciousness with the intention of satisfying these desiderata to ensure their evidential strength.
... 10 Yet whereas Godfrey-Smith wants to deny evaluative experience in insects, he grants it to crustaceans, where wound tending has been firmly established. The work of Elwood and his collaborators (Appel and Elwood 2009;Elwood et al. 2012) has studied the evaluative trade-offs crustaceans are engaged in, particularly decapod crustaceans (shrimps, crabs, and the like). Hermit crabs have shown, for instance, that they are making state-based decisions on whether or not to leave their shell when receiving electric shocks, dependent upon both the predicted presence of predators and the shell value. ...
In order to develop a true biological science of consciousness, we have to remove humans from the center of reference and develop a bottom-up comparative study of animal minds, as Donald Griffin intended with his call for a “cognitive ethology.” In this article, I make use of the pathological complexity thesis (Veit 2022a, b, c) to show that we can firmly ground a comparative study of animal consciousness by drawing on the resources of state-based behavioral life history theory. By comparing the different life histories of gastropods and arthropods, we will be able to make better sense of the possible origins of consciousness and its function for organisms in their natural environments.
... Further, recent evidence demonstrating sentience-linked cognitive abilities in some insects supports this idea, as well as studies indicating pain perception in other invertebrates (e.g. [84][85][86]). Figure 4. An example pathway for the putative insect descending nociception controls in the Drosophila melanogaster adult. ...
Modulation of nociception allows animals to optimize chances of survival by adapting their behaviour in different contexts. In mammals, this is executed by neurons from the brain and is referred to as the descending control of nociception. Whether insects have such control, or the neural circuits allowing it, has rarely been explored. Based on behavioural, neuroscientific and molecular evidence, we argue that insects probably have descending controls for nociception. Behavioural work shows that insects can modulate nocifensive behaviour. Such modulation is at least in part controlled by the central nervous system since the information mediating such prioritization is processed by the brain. Central nervous system control of nociception is further supported by neuroanatomical and neurobiological evidence showing that the insect brain can facilitate or suppress nocifensive behaviour, and by molecular studies revealing pathways involved in the inhibition of nocifensive behaviour both peripherally and centrally. Insects lack the endogenous opioid peptides and their receptors that contribute to mammalian descending nociception controls, so we discuss likely alternative molecular mechanisms for the insect descending nociception controls. We discuss what the existence of descending control of nociception in insects may reveal about pain perception in insects and finally consider the ethical implications of these novel findings.
... 10 Yet whereas Godfrey-Smith wants to deny evaluative experience in insects, he grants it to crustaceans, where wound tending has been firmly established. The work of Elwood and his collaborators (Appel and Elwood 2009;Elwood et al. 2012) has studied the evaluative trade-offs crustaceans are engaged in, particularly decapod crustaceans (shrimps, crabs, and the like). Hermit crabs have shown, for instance, that they are making state-based decisions on whether or not to leave their shell when receiving electric shocks, dependent upon both the predicted presence of predators and the shell value. ...
In order to develop a true biological science of consciousness, we have to remove humans from the centre of reference and develop a bottom-up comparative study of animal minds as Donald Griffin intended with his call for a ‘cognitive ethology’. In this article, I make use of the pathological complexity thesis (Veit 2022a,c,b) to show that we can firmly ground a comparative study of animal consciousness by drawing on the resources of state-based behavioral life-history theory. By comparing the different life histories of gastropods and arthropods, we will be able to make better sense of the possible origins of consciousness and its function for organisms in their natural environments.
... Indeed, many animals have been demonstrated to make trade-offs regarding their own welfare -for example hermit crabs (Appel and Elwood, 2009), rats (Cabanac and Johnson, 1983), and iguanas (Balasko and Cabanac, 1998). This aligns with most accounts of the evolution of valenced subjective experience that take it to function as a common currency when making decisions between competing motivations requiring trade-offs (Cabanac, 1992;Ginsburg and Jablonka, 2019;Gygax, 2017;Spruijt, van den Bos and Pijlman, 2001). ...
One of the most challenging questions surrounding subjective animal welfare is whether these states are measurable: that is, is subjective welfare an appropriately quantifiable target for scientific enquiry and ethical and deliberative calculation? The availability of several different types of measurement scale raises important questions regarding whether subjective experience has the right properties to be meaningfully represented on the types of scale required for different applications. This methodological question has so far received scant attention in the animal welfare literature. In this paper, I address this omission by examining the types of measurement scale we can reasonably expect to apply to animal welfare measurements, and which we will actually need for our applications. I argue that our different applications will require variously ordinal, interval, and ratio scales, and that we have sufficient reason to believe that subjective welfare is a target with the appropriate characteristics to justify the practice of representing it using each of these types of scales.
... We used a motivational trade-off paradigm, where animals must flexibly trade-off two competing motivations. For example, hermit crabs require higher voltages of electric shock to evacuate preferred Littorina shells than non-preferred Gibbula shells (10,11). Shock avoidance is traded off against shell preference. ...
Mammals can supress their nociceptive responses to prioritise other important responses via endogenous modulation from the brain. It is well established that insects display nociception, but not whether the insect brain can modulate nociceptive processing. To address this question, we investigated whether bumblebees′ ( Bombus terrestris ) attraction to higher sucrose solution concentrations reduces their avoidance of noxious heat. Bees were given the choice between either unheated or noxiously-heated (55°C) feeders with different sucrose concentrations. The feeders were associated with colour stimuli to act as conditioned cues. Bees fed more from higher sucrose concentration heated feeders than lower sucrose concentration unheated feeders. Further, bees′ ″testing out″ of feeders (landing but not feeding) reduced as the experiment progressed, demonstrating that conditioned colour cues informed the bees′ behaviour. Therefore, bees trade off competing conditioned motivational stimuli to modulate nocifensive behaviour, suggesting a form of pain perception.
... It is assumed that EMFs may affect crab and lobster behavior, but no laboratory experiment has demonstrated significant trauma or differences in survival between exposed and control settings [48]. In addition, crustaceans are known to experience pain and stress [49] but the extent to which EMFs, underwater noise, or any other interactions with marine energy devices may increase stress-related hormones in crabs and lobsters, which may lead to reproductive failure, remains unknown. ...
Marine energy devices harness power from attributes of ocean water to form a sustainable energy source. Knowledge gaps remain about whether marine energy systems can affect the environment, adding another threat to animal populations and habitats already under pressure from climate change and anthropogenic activities. To date, potential environmental effects have been studied under the scope of stressor–receptor interactions, where moving parts of, or emissions from, a system could harm the animals, habitats, and natural processes. While crucial for understanding effects and identifying knowledge gaps, this approach misses a holistic view of what animals may experience in the presence of marine energy systems. We look at six biological consequences and forces that drive the health of an animal population and the effects expected from marine energy development: success of early life stages; changes in competitive capabilities; growth and survival based on food availability; susceptibility to predators; injury or death; and reproductive success. We use case studies to develop this approach, focusing on a variety of marine animals. An approximate level of risk is assigned for each interaction based on the biological consequences. This work highlights the need to examine the effects of marine energy development on animal populations within their natural habitats.
... The snakes also received two different behavioural tests (emergence test and reverse emergence test) in which they were given the opportunity to select between two potentially conflicting motivations: to stretch out or to use a shelter (Balasko and Cabanac, 1998;Millsopp and Laming, 2008;Appel and Elwood, 2009). A long opaque arena was constructed out of polycarbonate sheets measuring 200 × 40 cm. ...
There is much evidence in mammals and birds demonstrating the importance of providing sufficient space to allow captive animals to exhibit natural behaviours, however, little such evidence exists for reptiles. The aim of this study was to ascertain whether enclosure size impacted on the behaviour and welfare of captive corn snakes (Pantherophis guttatus). Snakes (N=12) were housed in enclosures that were either 2/3 their length (small) or longer than the length of the snake (large) for c.32 days. Their welfare was assessed through observations of the animals in their enclosure and behavioural tests; after completing these tests, each animal was switched to the other housing condition (order counterbalanced across individuals) and received the same welfare assessment. Following the second set of behavioural tests, all animals received a preference test. When housed in large enclosures, snakes were found to be more active and spent time stretched out - a behaviour that was not possible in the small enclosure. The behavioural tests revealed few effects of space provision; however, when given a choice, snakes showed a clear preference for the large enclosure whilst active, although this preference was not observed while resting. These findings suggest that providing a larger enclosure is beneficial to the behaviour and welfare of captive snakes. Not providing sufficient space to allow snakes to fully elongate appears to thwart a behavioural need and thus impacts negatively on their welfare. We therefore recommend that captive snakes be kept in an enclosure longer than their body length.
... Long-term changes in behavior after noxious stimuli have also been shown in hermit crabs (Pagurus bernhardus) (24,25). Crabs were given shocks on their abdomen within their gastropod shells whereas control crabs were not shocked. ...
I review studies that examined the possibility of pain experience in fish and note how they provided guidance on general methods that could be applied to other animals such as decapod crustaceans. The fish studies initially reported the occurrence of prolonged rocking movements in trout and rubbing of their lips if they were injected with acetic acid. Subsequent studies examined the role of morphine in reducing these activities and examined shifts in attention when responding to noxious stimuli. Various studies take up these themes in decapods. The results reported for the two taxonomic groups are remarkably similar and indicate that responses of both go beyond those expected of mere nociceptive reflex. Thus, the idea of pain cannot be dismissed by the argument that fish and decapods respond only by reflex. The responses of both clearly involve central processing, and pain experience, although not proven for either, is a distinct possibility. These studies have been the subjects of highly critical opinion pieces and these are examined and rebutted. The conclusion is that both fish and decapods should be awarded consideration for their welfare.
... (p. 18) This was doubly misleading, since there had not at that time been "extensive studies" of decapod sentience (indeed, it is still the case that the topic is under-explored), and the most recent studies available in May 2009 (e.g., Barr et al. 2008;Appel and Elwood 2009) had in fact yielded scientific evidence of sentience. But this too is unsurprising, given the bioscience sector's obvious interest in minimizing regulation of scientific research. ...
... It may also have arisen from an understanding that natural selection might have shaped emotions more for survival than for prosperity, there being many more 'threats' than 'treats' in the environment [134]. Indeed, pain and other putative aversive stimuli have been major foci of affect-centred research designed to explore the question of sentience in less-studied taxa including fishes [118,119,135], as well as cephalopods [56,[128][129][130], decapods [136][137][138][139][140] and other invertebrates [50]. ...
The focus of this opinion is on the key features of sentience in animals which can experience different states of welfare, encapsulated by the new term ‘welfare-aligned sentience’. This term is intended to exclude potential forms of sentience that do not enable animals in some taxa to have the subjective experiences which underlie different welfare states. As the scientific understanding of key features of sentience has increased markedly during the last 10 to 15 years, a major purpose here is to provide up-to-date information regarding those features. Eleven interconnected statements about sentience-associated body functions and behaviour are therefore presented and explained briefly. These statements are sequenced to provide progressively more information about key scientifically-supported attributes of welfare-aligned sentience, leading, in their entirety, to a more comprehensive understanding of those attributes. They are as follows: (1) Internal structure–function interactions and integration are the foundations of sentience; (2) animals posess a capacity to respond behaviourally to a range of sensory inputs; (3) the more sophisticated nervous systems can generate subjective experiences, that is, affects; (4) sentience means that animals perceive or experience different affects consciously; (5) within a species, the stage of neurobiological development is significant; (6) during development the onset of cortically-based consciousness is accompanied by cognitively-enhanced capacities to respond behaviourally to unpredictable postnatal environments; (7) sentience includes capacities to communicate with others and to interact with the environment; (8) sentience incorporates experiences of negative and positive affects; (9) negative and positive affective experiences ‘matter’ to animals for various reasons; (10) acknowledged obstacles inherent in anthropomorphism are largely circumvented by new scientific knowledge, but caution is still required; and (11) there is increasing evidence for sentience among a wider range of invertebrates. The science-based explanations of these statements provide the foundation for a brief definition of ‘welfare-aligned sentience’, which is offered for consideration. Finally, it is recommended that when assessing key features of sentience the same emphasis should be given to positive and negative affective experiences in the context of their roles in, or potential impacts on, animal welfare.
Appropriate responses to real or potential damaging stimuli to the body (nociception) are critical to an animal's short- and long-term survival. The initial goal of this study was to examine habituation of withdrawal reflexes (whole-body and local shortening) to repeated mechanical nociceptive stimuli (needle pokes) in the medicinal leech, Hirudo verbana, and assess whether injury altered habituation to these nociceptive stimuli. While repeated needle pokes did reduce shortening in Hirudo, a second set of behaviors changes was observed. Specifically, animals began to evade subsequent stimuli by either hiding their posterior sucker underneath adjacent body segments or by engaging in locomotion (crawling). Animals differed in terms of how quickly they adopted evasion behaviors during repeated stimulation, exhibiting a multi-modal distribution for early, intermediate, and later evaders. Prior injury had a profound effect on this transition, decreasing the time frame in which animals began to carry out evasion and increasing the magnitude of these evasion behaviors (more locomotory evasion). The data indicate the presence in Hirudo of a complex and adaptive defensive arousal process to avoid noxious stimuli that is influenced by differences in internal states, prior experience with injury of the stimulated areas, and possibly learning-based processes.
This goal of this thesis in the philosophy of nature is to move us closer towards a true biological science of consciousness in which the evolutionary origin, function, and phylogenetic diversity of consciousness are moved from the field’s periphery of investigations to its very centre. Rather than applying theories of consciousness built top-down on the human case to other animals, I argue that we require an evolutionary bottomup approach that begins with the very origins of subjective experience in order to make sense of the place of mind in nature. To achieve this goal, I introduce and defend the pathological complexity thesis as both a framework for the scientific investigation of consciousness and as a lifemind continuity thesis about the origins and function of consciousness.
The entomology literature has historically suggested insects cannot feel pain, leading to their exclusion from ethical debates and animal welfare legislation. However, there may be more neural and cognitive/behavioural evidence for pain in insects than previously considered. We use Birch et al. 's (2021) eight criteria for sentience to critically evaluate the evidence for pain in insects. We assess six orders (Blattodea, Coleoptera, Diptera, Hymenoptera, Lepidoptera, and Orthoptera) in at least two life stages (adult and first instar juveniles, as well as other instars where relevant data are found). Other insect orders have not received enough research effort to be evaluated. According to the Birch et al. framework, adult Diptera (flies and mosquitoes) and Blattodea (cockroaches and termites) satisfy six criteria, constituting strong evidence for pain. Adults of the remaining orders (except Coleoptera, beetles) and some juveniles (Blattodea and Diptera, as well as last instar Lepidoptera [butterflies and moths]) satisfy 3–4 criteria, or “substantial evidence for pain”. We found no good evidence that any insects failed a criterion. However, there were significant evidence gaps, particularly for juveniles, highlighting the importance of more research on insect pain. We conclude by considering the ethical implications of our findings where insects are managed in wild, farmed, and research contexts.
Decapod crustaceans (crabs, hermit crabs, lobsters, crayfish, shrimps, prawns) are sentient beings, not only responding to noxious stimuli but also being capable of feeling pain, discomfort, and distress. General anaesthesia aims at producing analgesia, immobilization, and unconsciousness, while sedation reduces consciousness, stress, and anxiety, though without analgesia. Anaesthesia is recommended to ensure animal welfare and suppress nociception, pain, and suffering in painful and distressing practice that impairs decapods’ welfare. These include long term restrain, surgical procedures, pain control, examination, diagnostic, sampling, treatment, transportation, and euthanasia. The necessary anaesthetic depth, from sedation to surgical anaesthesia, depends on the procedure type. Anaesthetic bath and injection are commonly used, besides inhalation, local anaesthesia, and intracardiac injection. Agents used for the anaesthetic bath include eugenol, isoeugenol, lidocaine, halothane, and essential oils of lemon balm, lemongrass, lemon verbena, and sandalwood. While alphaxalone, eugenol, ketamine-xylazine, lidocaine, morphine, procaine, tiletamine-zolazepam, and xylazine can be used as injectable agents administered on the arthrodial membrane or intramuscular injection. Halothane can be used on inhalation anaesthesia. Local anaesthetics include lidocaine and benzocaine. Notwithstanding, many others are detrimental or ineffective to decapods, thus discouraged. They include but not limited to hypothermia, carbon dioxide, chlorpromazine, chloroform, ethanol, ether, magnesium salts, tricaine methanesulfonate (MS-222), mint and lavender essential oils, passionflower extract, and valerian. Decapods’ welfare, protection, and veterinary attention should not be neglected, but they must receive ethical treatment, including the best of our knowledge and available tools to ensure they are free of pain and discomfort whenever we deal with them.
We consider the relationship between neural and behavioural evidence for animal consciousness. We critically examine two recent studies: one neural and one behavioural. The first, on crows, finds different neural activity depending on whether a stimulus is reported as seen or unseen. However, to implicate this neural activity in consciousness, we must assume that a specific conditioned behaviour is a report of conscious experience. The second study, on macaques, records behaviours strikingly similar to patterns of conscious and unconscious perception in humans. However, confounds are only ruled out in human subjects, presupposing substantial neural similarity between humans and macaques. Taken together, the two studies reveal a sense in which neural and behavioural research rely on each other. Looking ahead, these two types of evidence could prove to be either mutually reinforcing or mutually undermining. The science of animal consciousness needs both neural and behavioural evidence, ideally obtained as part of a single coordinated programme.
Do animals, including invertebrates, have felt emotions and does this morally matter?
‘Sentience’ sometimes refers to the capacity for any type of subjective experience, and sometimes to the capacity to have subjective experiences with a positive or negative valence, such as pain or pleasure. We review recent controversies regarding sentience in fish and invertebrates and consider the deep methodological challenge posed by these cases. We then present two ways of responding to the challenge. In a policy‐making context, precautionary thinking can help us treat animals appropriately despite continuing uncertainty about their sentience. In a scientific context, we can draw inspiration from the science of human consciousness to disentangle conscious and unconscious perception (especially vision) in animals. Developing better ways to disentangle conscious and unconscious affect is a key priority for future research.
This chapter considers euthanasia to be the process of ending an animal's life using methods that minimize and preferably prevent or eliminate pain and distress. Methods employed for the euthanasia of economically less prominent phyla, including sponges, coelenterates, helminths, annelids, echinoderms, and tunicates, are often an extension of the standard techniques used to immobilize and preserve the specimen for scientific study. The euthanasia protocol should be developed and implemented in such a way that stress and agitation are avoided. Euthanasia of gastropods, particularly those with an external shall large enough to enclose all of the animal's soft parts, may be challenging, especially if the end goal is pathological or other scientific examination of the carcass. Euthanasia techniques must address the presence of a decentralized nervous system and affect all aspects of the central nervous system to be considered humane.
This chapter deals with the conventional separation of crustaceans and insects. A number of crustaceans are maintained as pets and display animals in marine aquaria, especially shrimp. There are six classes within the subphylum Crustacea: Cephalocarida, Branchiopoda, Ostracoda, Remipedia, Maxillopoda, and Malacostraca. The types of diseases affecting crustaceans are in many cases similar to those affecting aquatic vertebrates and terrestrial mammals. Gas bubble disease is a noninfectious condition in aquatic organisms caused by supersaturated levels of total dissolved gas in water. Shell disease is a common term for areas of erosion and melanization in the exoskeleton in crustaceans. White spot disease is caused by white spot syndrome virus, the only member of the genus Whispovirus . Necrotizing hepatopancreatitis is a newly emerging disease caused by infection with the pathogenic agent Hepatobacter penaei . Hematodiniosis is a fatal disease of crustaceans caused by parasitic dinoflagellates of the genus Hematodinium .
The future of the native European crayfish Austropotamobius pallipes depends on accurate conservation management. The goal of this paper is to attempt an investigation of the major ethical conflicts that can emerge in the conservation of this endangered crayfish threatened by invasive competitors, introduced diseases, and landscape alteration. To assess this issue, we will employ the Ethical Matrix, in a version explicitly tailored for its use in conservation. The filled Ethical Matrix will highlight several potential conflicts between values such as environmental protection, social and economic interests, animal welfare, cultural and aesthetic value, etc. We will discuss these conflicts, alongside some potential mitigating strategies present in the literature. We will stress in particular the need to take into account the ethical principle of fairness when assessing the economic and recreational value of invasive species, especially concerning the unfair distribution of costs. Moreover, we will assert the importance of conservation of A. pallipes both for its existence value and for its role as an umbrella and keystone species. Beyond its focus on A. pallipes , the Ethical Matrix here discussed might also provide insights on the value conflicts relative to analogous in situ conservation efforts involving a native species threatened by invasive alien competitors.
Graphic abstract
Pain is a negative affective state arising from tissue damage or inflammation. Because pain is aversive and its relief is innately rewarding, animals may learn to avoid a context in which pain is experienced, and prefer one where pain relief occurs. It is generally accepted that vertebrate animals experience pain, however, there is currently inconclusive evidence that the affective component of pain occurs in any invertebrate. Here we show that octopuses, the most neurologically complex invertebrates, exhibit cognitive and spontaneous behaviors indicative of affective pain experience. In conditioned place preference assays, octopuses avoided contexts in which pain was experienced, preferred a location in which they experienced relief from pain, and showed no conditioned preference in the absence of pain. Injection site grooming occurred in all animals receiving acetic acid injections, but this was abolished by local anesthesia. Thus, octopuses are likely to experience the affective component of pain.
In human conscious experience, many features are present in combination: objects are presented through the senses, information from different sensory modalities is integrated, events are marked with value, and we have a sense of our own location and state. Which of these might come before others in plausible evolutionary trajectories, or do they form a tight package of correlated features that cannot readily be dissociated? I take a comparative approach to these questions, focusing on a distinction between sensory and evaluative aspects of experience and looking at the distribution of subjectivity-relevant features in a range of invertebrate animals.
All animals face hazards that cause tissue damage, and most have nociceptive reflex responses that protect them from such damage. However, some taxa have also evolved the capacity for pain experience, presumably to enhance long-term protection through behaviour modification based on memory of the unpleasant nature of pain. In this review, I consider various criteria that might help to distinguish nociception from pain. Because nociceptors are so taxonomically widespread, simply demonstrating their presence is not sufficient. Further, investigation of the central nervous system provides limited clues about the potential to experience pain. Opioids and other analgesics might indicate a central modulation of responses, but often, peripheral effects could explain the analgesia. Thus, reduction of responses by analgesics and opioids does not allow clear discrimination between nociception and pain. Physiological changes in response to noxious stimuli or the threat of a noxious stimulus might prove useful, but, to date, application to invertebrates is limited. Behaviour of the organism provides the greatest insights. Rapid avoidance learning and prolonged memory indicate central processing rather than mere reflexes and are consistent with the experience of pain. Complex, prolonged grooming or rubbing may demonstrate an awareness of the specific site of stimulus application. Trade-offs 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. Recent evidence of fitness enhancing, anxiety-like states is also consistent with the idea of pain. Thus, available data go beyond the idea of just nociception, but the impossibility of total proof of pain means they are not definitive. Nevertheless, more humane care for invertebrates is suggested.
Pain is an aversive sensation and feeling associated with actual or potential tissue
damage. A pain system involving receptors, neural pathways and analytical centres in
the brain exists in many kinds of animals. The fact that there is rather similar
evidence of physiological responses, direct behavioural responses and ability to learn
from such experiences so that they are minimised or avoided in future, suggests the
existence of feelings of pain in many species. Indeed the feelings are likely to be an
important part of the biological mechanism for coping with actual or potential
damage. The advantages of pain are that action can be taken when damage occurs,
consequent learning allows the minimising of future damage and, where the pain is
chronic, behaviour and physiology can be changed to ameliorate adverse effects.
Species differ in their responses to painful stimuli because different responses are
adaptive in different species but it is likely that the feeling of pain is much less
variable than the responses. The first steps in the evolution of pain must have
involved cell sensitivity and localised responses but substantial changes in efficacy
could occur once efficient communication within the individual and sophisticated
brain analysis could occur. Changes in the pain system, once there was a moderately
complex brain may well have been slight. Pain is an old system which has probably
changed rather little during vertebrate evolution and pain may be a greater problem in
animals with less cognitive ability. The distinction between pain and nociception
does not seem to be useful.
Pain is an aversive sensation and feeling associated with actual or potential tissue damage. A pain system involving receptors, neural pathways and analytical centres in the brain exists in many kinds of animals. Feelings of pain in many species are indicated by physiological responses, direct behavioural responses and ability to learn from such experiences so that they are minimised or avoided in future. Species differ in their responses to painful stimuli because different responses are adaptive in different species but the feeling of pain is probably much less variable. In early evolution, pain must have involved cell sensitivity and localised responses but efficacy would have improved with efficient communication within the individual and sophisticated brain analysis. Pain systems have probably changed rather little during vertebrate evolution. Pain may be a greater problem for animals with less cognitive ability. The distinction between pain and nociception does not seem to be useful.
The morphologies of the cerebral ganglia (brains) of three infraorders of the decapod crustaceans (Astacura-crayfish; Brachyura-crabs; Palinura-spiny lob- sters) are described. A common nomenclature is proposed for homologous nerve roots, brain regions, tracts, com- missures, neuropils, and cell body clusters.
This chapter discusses the different kinds of feelings and considers the origin and possible function of each feeling. Each of these feelings has a biological role that complements various other anatomical, physiological, and behavioral mechanisms. All have some potential for improving fitness and most are likely to have been the subject of considerable selection pressure, but some aspects of feelings are likely to be just epiphenomena of neural mechanisms. With this view that most aspects of feelings have evolved like other biological mechanisms and that they help significantly in coping and responding, a single view of welfare as the state of an individual as regards its attempts to cope with its environment becomes clearer. Feelings are an important part of the welfare of an individual and should be assessed as well as possible. Other coping procedures and effects of the environment on the individual should also be assessed. An effect on an individual that is adverse in the long term is categorized as stress. Programs for trying to evaluate and improve welfare should combine the use of experiments to assess what is important to the individual by measuring the strengths of preferences, with monitoring studies in which feelings and other aspects of welfare are assessed more directly.
Nociception is the detection of a noxious tissue-damaging stimulus and is sometimes accompanied by a reflex response such as withdrawal. Pain perception, as distinct from nociception, has been demonstrated in birds and mammals but has not been systematically studied in lower vertebrates. We assessed whether a fish possessed cutaneous nociceptors capable of detecting noxious stimuli and whether its behaviour was sufficiently adversely affected by the administration of a noxious stimulus. Electrophysiological recordings from trigeminal nerves identified polymodal nociceptors on the head of the trout with physiological properties similar to those described in higher vertebrates. These receptors responded to mechanical pressure, temperatures in the noxious range (more than 40 degrees C) and 1% acetic acid, a noxious substance. In higher vertebrates nociceptive nerves are either A-delta or C fibres with C fibres being the predominating fibre type. However, in the rainbow trout A-delta fibres were most common, and this offers insights into the evolution of nociceptive systems. Administration of noxious substances to the lips of the trout affected both the physiology and the behaviour of the animal and resulted in a significant increase in opercular beat rate and the time taken to resume feeding, as well as anomalous behaviours. This study provides significant evidence of nociception in teleost fishes and furthermore demonstrates that behaviour and physiology are affected over a prolonged period of time, suggesting discomfort.
Field observations showed orb-weaving spiders (Argiope spp.) to undergo leg autotomy if they are stung in a leg by venomous insect prey (Phymata fasciata). The response occurs within seconds, before the venom can take lethal action by spread to the body of the spiders. Autotomy is induced also by honeybee venom and wasp venom, as well as by several venom components (serotonin, histamine, phospholipase A(2), melittin) known to be responsible for the pain characteristically elicited by venom injection in humans. The sensing mechanism by which spiders detect injected harmful chemicals such as venoms therefore may be fundamentally similar to the one in humans that is coupled with the perception of pain.
It is of scientific and practical interest to consider the levels of cognitive ability in animals, which animals are sentient, which animals have feelings such as pain and which animals should be protected. A sentient being is one that has some ability to evaluate the actions of others in relation to itself and third parties, to remember some of its own actions and their consequences, to assess risk, to have some feelings and to have some degree of awareness. These abilities can be taken into account when evaluating welfare. There is evidence from some species of fish, cephalopods and decapod crustaceans of substantial perceptual ability, pain and adrenal systems, emotional responses, long- and short-term memory, complex cognition, individual differences, deception, tool use, and social learning. The case for protecting these animals would appear to be substantial. A range of causes of poor welfare in farmed aquatic animals is summarised.
Part 1 Assessments, decisions and hermit crabs: assessments and decisions the behavioural ecology of hermit crabs "pagurus bernhardus" in Northern Ireland. Part 2 Non-competitive assessment: assessment of unoccupied shells assessment and motivational change. Part 3 Competitive assessment: agonistic behaviour assessments during shell fights assessment strategies and the duration of fights motivational change during aggressive encounters.
In Pagurus bernhardus, the relative sizes of the crabs and shell quality of the larger crab influenced the probability of occurrence of a shell fight. These two factors along with the quality of the smaller crab's shell influenced the probability of an escalated fight occurring. During a shell fight, the attacker was able to assimilate information concerning the defender's shell and to compare it with the shell in possession. On the basis of this comparison the attacker decided whether or not to evict the defender and effect a shell change. The defending crab did not have access to information about the attacker's shell and therefore could only estimate the quality of its own shell. This asymmetry of information experienced by the crabs ensured that the attacker decided the outcome of a shell fight.-from Authors
Factors which influence decisions by hermit crabs concerning whether to approach, investigate and enter another shell have been investigated by systematically varying the size of the shell in possession and the size of the shell being offered. The probability that a crab will approach or enter the shell depends on both variables. Investigation after contact, however, depends only on the size of the shell in possession. Durations of each stage of the sequence are negatively correlated with the numbers of crabs in each experimental group performing the next stage. For the final sequence of aperture investigatory activities, the fewer crabs entering the offered shell, the greater the number of investigatory acts performed by those crabs. In addition to variation in number of acts and duration of investigation, specific use of appendages varies according to the experimental situation. Thus naked crabs use the minor cheliped to investigate shells in preference to the major cheliped, which is normally used by housed crabs, with the major cheliped being reserved for defence by naked crabs. These data are discussed in terms of information collection and decisions made on the basis of that information.
Previous work showed that goldfish learn to avoid a region of an aquarium where they receive a discrete shock to the flank. This avoidance is reduced if another fish is present next to the shock zone, suggesting fish trade-off avoidance against a tendency to associate [Dunlop, R., Millsopp, S., Laming, P., 2006. Avoidance learning in goldfish (Carassius auratus) and trout (Oncorhynchus mykiss) and implications for pain perception. App. Anim. Behav. Sci. 97 (2–4), 255–271]. Only shock intensity was adjusted in those experiments, here we report results where a requirement for food was also altered.Fish were trained to feed at a region of the aquarium where subsequently they would receive a discrete shock to the flank. One experimental group had different shock intensities applied, whereas in the other group shock intensity was consistent but food deprivation was varied.We show the number of feeding attempts and time spent in the feeding/shock zone decreased with increased shock intensity and with increased food deprivation the number and the duration of feeding attempts increased as did escape responses as this zone was entered. These data suggest that goldfish balance their need for food against avoidance of an acute noxious stimulus.
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.
Shell fighting behaviour of the hermit crab Pagurus bernhardus was investigated. Analysis of fights between crabs in which there was little or no asymmetry in potential benefit for the two crabs from a shell exchange suggested that the duration of the fight increased as the potential benefit increased. Further experiments indicated that a naked crab was capable of evicting a housed crab by a process of direct aggression. Analysis of fights in which there was a slight asymmetry in potential gains from shell exchange indicated that the result of the fight was primarily determined by the large of the two crabs. These results are contrary to the proposal of Hazlett (1978) that the interactions represent a process of negotiation rather than aggression.
The occurrence of empty gastropod shells and those occupied by the hermit crab, Pagurus bernhardus, was examined on the shore. This survey suggested that small crabs prefer L. littoralis shells to those of Gibbula species and this was confirmed by preference tests in the laboratory. Crabs removed from these small shells show an initial preference for Nucella shells to those of L. littorea. However, medium sized crabs collected in either Nucella or L. littorea prefer the species in which they were collected. This preference is still apparent when the size of the test shells is varied. These data provide the first clear evidence for a modification of shell preferences after experience of particular shell species.
An experiment was conducted to compare the influence of sex and rearing conditions on two measures of shock-elicited aggression rats. The results indicated that shock-elicited fighting and shock-elicited biting were differentially affected by both raising rats in isolation and the sex of the animals.
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.
Hermit crabs offer unique opportunities in studying the underlying motivational mechanisms involved in resource assessment. In particular, when assessing shells, the information gathered must influence the motivational state and the processes of motivational change may be elucidated by experimentation in two main ways. First, by stopping the sequence of assessment, either by blocking the shell aperture with cement or by sticking the shell, aperture down, to the substrate. This enables the duration for which the crab persists in assessing the shell to be measured. Second, by presenting a novel, potentially startling, stimulus at some point in the assessment and measuring the duration of the startle response. With the first method persistence time should show a positive correlation with motivation to acquire the new shell, whereas, with the second method, the duration of the startle response should be negatively correlated with that motivational state. Because the motvational state must reflect the information the crab has at any moment, these two methods provide independent ways of probing the acquisition of information. The fact that shell assessment is easily observed and quantified in the laboratory and that the resource (shell) may be experimentally modified in numerous ways, makes these crabs the ideal subjects with which to develop a general model of resource assessment.
1.Game theoretical models of animal contests assume that animals attempt to maximize individual fitness during contests with nonrelatives. The asymmetric war of attrition takes into account the probability that the ratio of cost to benefit for each opponent will be different, but the information that each contestant has about its relative cost to benefit ratio, in comparison to that of its opponent, is unlikely to be perfect. The sequential assessment model suggests that the accuracy of this information increases with each performance of the agonistic activity in question. Recent models, however, such as the energetic war of attrition, assume that aggressive signals are performed repeatedly because they accumulate to give a signal of stamina.2.Hermit crabs interact in pairs in apparently agonistic encounters over the ownership of gastropod shells. The key activity during these interactions is “shell rapping,” where the attacker brings its shell rapidly and repeatedly into contact with that of the defender in a series of bouts. At the end of an encounter the attacker may evict the defender from its shell and permanently occupy, the new, empty shell. The evicted defender is then free to occupy the shell discarded by the attacker and the crabs are said to have “exchanged shells.” Under certain circumstances both crabs may benefit from these interactions.3.This possibility of mutual gain from shell exchanges has lead to the hypothesis that crabs negotiate over the ownership of shells during these interactions. The negotiation model suggests that the function of shell rapping is to provide the nonrapping crab with information about the shell of the attacker. The defender would then be able to make a decision about whether to release its own shell on the basis of the change in shell quality that this would entail. Under the aggression model, however, it is expected that any information transferred by shell rapping concerns either the fighting ability of attackers, their motivation to continue, or a combination of these two factors. In addition, shell rapping might incur some direct detrimental effect on defenders.4.The shell selection process in nonagonistic situations has been used to provide a model of information gathering and motivational change. A threshold model of motivational change during shell investigation relates two causal factors, the quality of the shell currently occupied and the quality of the potential new shell, to the decisions available to the crab: continue investigating the new shell, enter the new shell, or reject the new shell. This model allows various trajectories of motivational change to be calculated, which relate investigation time to the likely decision of the crab, for different scenarios defined by the quality of the crab's original shell and that of the empty shell under investigation. This model was tested by probing the motivational state of crabs during shell investigation by (1) preventing adequate investigation and measuring persistence times and (2) using a novel stimulus to startle the crabs during shell investigation and measuring the time taken to return to investigatory behavior. Experiments conducted using these techniques confirmed that crabs use the two sources of information predicted by the model.5.Motivational state is expected to vary in attackers during shell fights. An indication of this is provided by the duration of contests where attackers give up, but the majority of fights end in an eviction of the defender, hence there are too few data to test attacker motivation in this way. The novel stimulus technique was thus used to probe the motivational state of attackers during fights. It was found that the duration of the startle response was related to the potential gain, with those with the greater potential improvement in shell quality showing the shortest startle durations. Furthermore, attackers that were eventually victorious were shown to have a higher motivational state during the early escalated phase of the fight than those that did not evict the opponent. Surprisingly, the motivation of attackers did not appear to be related to the size difference between the two crabs.6.The key determinants of the outcome of encounters are the power of the impact of the raps, the duration of the pauses between bouts of rapping, and the mean number of raps performed in each bout, with powerful and vigorous attackers being more likely to evict the opponent. Differences in vigor are also associated with the potential gain available to the attacker and with the relative size difference between the two crabs. Vigor also varies during the course of the fight: at the start of the fight the duration of pauses increases such that the vigor is de-escalated, however, at the end of the fight successful attackers increase the rate of rapping prior to evicting the opponent, whereas those that give up decrease the rate of rapping before doing so. The only game theoretical model of fighting that allows both increase and decrease in the rate of signaling during the contest is the energetic war of attrition. According to this model the function of repeated signals is to provide information about the stamina of receivers. That the rate of rapping is mediated by fatigue was confirmed by staging fights with crabs that had been preexposed to hypoxic water and by analysis of lactic acid concentration in the hemolymph, following fights. We conclude that hermit crab shell fights represent a useful model of animal contests that involve communication between the two participants. First, the value of the resource in question and the relative fighting ability of the crabs can be easily manipulated. Second, unlike other signaling systems, the roles of attacker and defender are fixed throughout the fight such that the decision rules used by signalers and receivers can be examined separately.
Animals are routinely subjected to painful procedures, such as tail docking for puppies, castration for piglets, dehorning for dairy calves, and surgery for laboratory rats. Disease and injury, such as tumours in mice and sole ulcers on the feet of dairy cows, may also cause pain. In this paper we describe some of the ways in which the pain that animals experience can be recognized and quantified. We also describe ways in which pain can be avoided or reduced, by reconsidering how procedures are performed and whether they are actually required. Ultimately, reducing the pain that animals experience will require scientific innovation paired with changed cultural values, and willingness to address regulatory, technological and economic constraints. # 2006 Published by Elsevier B.V.
Littoral hermit crabs, Pagurus bernhardus, show a strong preference for Littorina obtusata shells rather than those of Gibbula species. The fitness consequences, in terms of fecundity, for this shell preference is examined for female crabs. Females in the preferred species produced eggs earlier in the season, produced more eggs in the first brood, and produced a second brood more often than did females in the less preferred species. The smaller brood for Gibbula spp. was not a consequence of egg loss from the pleopods due to an unfavourable shape of shell, but rather reflected lower egg production. It is not clear, however, if this differential reproduction is due to direct costs of carrying an unfavourable shell, i.e. the shell impedes reproduction, or whether crabs compete aggressively for favoured shells so that only crabs of low quality inhabit lowquality shells.
Nociception is the ability to perceive a noxious stimulus and react in a reflexive manner and occurs across a wide range of taxa. However, the ability to experience the associated aversive sensation and feeling, known as pain, is not widely accepted to occur in nonvertebrates. We examined the responses of a decapod crustacean, the prawn, Palaemon elegans, to different noxious stimuli applied to one antenna to assess reflex responses (nociception) and longer-term, specifically directed behavioural responses that might indicate pain. We also examined the effects of benzocaine, a local anaesthetic, on these responses. Noxious stimuli elicited an immediate reflex tail flick response, followed by two prolonged activities, grooming of the antenna and rubbing of the antenna against the side of the tank, with both activities directed specifically at the treated antenna. These responses were inhibited by benzocaine; however, benzocaine did not alter general swimming activity and thus the decline in grooming and rubbing is not due to general anaesthesia. Mechanical stimulation by pinching also resulted in prolonged rubbing, but this was not inhibited by benzocaine. These results indicate an awareness of the location of the noxious stimuli, and the prolonged complex responses indicate a central involvement in their organization. The inhibition by a local anaesthetic is similar to observations on vertebrates and is consistent with the idea that these crustaceans can experience pain.
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 cheliped probes within the aperture prior to moving in. Thus the experience of the shock altered future behaviour 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.
The value of contested resources (shells) in hermit crab fights depends on the sizes of the crabs relative to the sizes of the resources. Thus when relative contestant size is the main experimental variable, motivational factors associated with shell size will also be an experimental problem. Two experiments are described that together overcome this problem. Relative crab size influences all stages of shell fights including pre-fight display, escalation, eviction and examination of the opponent's shell by the victor both before and after eviction of the loser. Shell fights occur more often between disparately-sized animals than between those similar in size. This apparent contradiction of recent theory (Maynard-Smith & Parker 1976) is probably due to the high cost of being without a shell and the small chance that an escalated fight will result. Relative crab size influences the time taken in resource assessments and thus the effectiveness of these assessments is also probably influenced. Causal factors influencing each of the major decisions in shell fights are described and although these fights are more complex than most they are in general agreement with theory on animal contests.
The process by which animals gather the information required to make a decision on whether or not to accept a resource was examined. A motivational model was developed to predict how information changes levels of causal factors and the model was tested by experiments on hermit crabs investigating shells. A prediction of the model is that, when there is a high utility in accepting the resource, each stage of the assessment procedure will be rapid, whereas if the utility is low the assessment will be prolonged. If the resource is not available for some reason, for example if a shell has the aperture blocked, the animal will persevere for longer if the initial stages of assessment indicated a high-quality resource than if it had indicated a low-quality resource. These and other predictions of the model were upheld in experiments in which the information available to hermit crabs at each stage of assessment was varied.
This paper investigates spatially cued behavioural responses of two species of fish to an acute noxious stimulus and demonstrates response elasticity. Typical avoidance responses to a nociceptive stimulus were used to test (1) if fish learn to avoid spatial areas associated with a potentially noxious stimulus, (2) learning and memory improves with increased stimulus intensity and (3) a supposedly innate reflex behavioural responses change depending on the circumstances. Electric shocks with two different intensities, low (2.5 V and 3 V for trout and goldfish, respectively) and high (25 V and 30 V for trout and goldfish, respectively), were administered directly to the skin to stimulate cutaneous nociceptors. Goldfish (n = 8) demonstrated spatially cued shock avoidance and an increase in stimulus voltage, significantly improved shock-avoidance learning and memory. However, trout (n = 8) demonstrated shock-avoidance learning but no significant stimulus discrimination and little information retention. The presence of a conspecific significantly changed this behavioural response to a noxious stimulus. Trout were willing to remain in the vicinity of the conspecific while being subjected to low intensity shock stimuli previously shown to elicit avoidance. Goldfish tended to leave this area yet remain in the mid-tank area, adjacent to the stimulating zone, rather than at the end of the tank. These results suggest that shock avoidance in fish is not purely a reflex action. Fish were prepared to change the supposedly innate avoidance reaction according to a change in circumstances, an important concept in the ongoing debate on pain perception in fish. (c) 2005 Elsevier B.V. All rights reserved.
Shell exchanges between hermit crabs may occur after a period of shell rapping, when the initiating or attacking crab brings its shell rapidly and repeatedly into contact with the shell of the non-initiator or defender, in a series of bouts. There are two opposing models of hermit crab shell exchange and the function of shell rapping. The negotiation model views shell exchange as a mutualistic activity, in which the initiator supplies information about the quality of its shell via the fundamental frequency of the rapping sound. The aggression model views shell rapping as either detrimental to the defending crab, or as providing it with information about the initiator's ability or motivation to continue, or both. The negotiation model makes no predictions about the temporal pattern of rapping, but under the aggression model it would be expected that crabs that rapped more vigorously would be more likely to effect an exchange. Repeating the signal could be expected under either model. Crabs that achieve an exchange rap more vigorously, rapping is more persistent when a clear gain in shell quality may be achieved, and the vigour is greater when the relative resource-holding potential (or 'fighting ability') is high. These findings support the aggression model rather than the negotiation model. Contrary to the predictions of game theory, crabs that do not effect an exchange appear to signal that they are about to give up. The data suggest that rapping is performed repeatedly because the accumulation of all of the performances acts as a signal of stamina.
The number of pecks delivered by birds to an attractive visual stimulus was measured before and again 6, 26 and 32 h after partial beak amputation. There was a significant reduction in the number of pecks by birds 26 h after amputation but not at 6 h after. This reduction was considered to be a quantitative measure of pain related guarding behaviour. The results indicated the presence of a pain-free period immediately following amputation which may last in some birds for as long as 26 h.
Male crabs Chasmagnathus granulatus were trained by means of a method similar to the standard inhibitory avoidance technique widely used in vertebrates. Each crab was placed in the dark compartment (DC) of a double-chamber device, allowed to move towards the light compartment (LC) and latency to enter measured. Experimental crabs received a shock in LC, but controls were not punished. After 1 min, both experimental and control crabs were free to return to DC. On completion of 1, 2, 3 or 24 hr intertrial interval in DC a retention test was administered and latency to enter LC was measured. A single trial was proven enough to establish a LC-shock association that was detected up to 3 hr later, but no retention was proved after 24 hr. Memory was disrupted when crabs were removed from the apparatus during the 3 hr intertrial interval. Similarities and differences between the passive avoidance method used with crabs and that used with vertebrates are discussed.
Male crabs (Chasmagnathus granulatus) exhibited a defensive response (DR) to an electric shock (8 V, 50 Hz, 1 sec). The DR so elicited was used as a model for studying the antinociceptive effect of morphine. Injections of morphine-HCl (MP) (25, 50, 100 and 150 micrograms/g) were administered and the DR was examined at 2, 7.5, 15, 30, 45 and 75 min post-injection. (a) MP produced a dose-dependent reduction of the crab's sensitivity to the nociceptive stimulus. (b) A 100 micrograms/g dose of MP caused a 50% response inhibition with an injection-shock interval of 30 minutes, but no inhibition occurred when the same dose was administered with 1.6 micrograms/g of naloxone-HCl, suggesting that MP acts through an opiate receptor. (c) The ED50 at 2 min post-injection was roughly 33 micrograms/g and the threshold dose was estimated to be 6.8 micrograms/g. These doses are lower than ED50 values reported for other arthropods (90 to 930 micrograms/g) and approach those of vertebrates. (d) The peak MP effect was reached quickly, within 2 min post-injection. The duration of the MP effect was calculated to be 45.0-75.0 min depending on the dose, and an indirect estimate of half-life elimination was 15.7 min. These values are remarkably lower than those reported for vertebrates. The shorter duration of the MP peak effect is attributable to a greater permeability of the arthropod blood-brain barrier as compared to that of vertebrates.
Analgesics are often not provided to amphibians because the presence and severity of pain may not be recognized in these animals. In addition, there is little information on the mechanism of action of analgesic agents in amphibians. However, amphibians possess appropriate neurologic components for transmitting pain from peripheral receptors to the central nervous system and antinociceptive mechanisms to modulate pain. They are capable of displaying behavioral and physiologic modification of pain systems in response to analgesic pharmacologic agents. Therefore, pain perception in amphibians is likely analogous to that in mammals and invasive, potentially painful procedures should be accompanied by appropriate analgesia and anesthesia. Although specific doses have not been established in clinical trials, basic research into the mechanisms and regulation of endogenous opioid systems demonstrates the potential clinical benefit for the use of opioids in these animals. Other analgesics such as alpha2-agonists, ketamine, and tricaine methanesulfonate have also demonstrated analgesic potential.
This review summarizes the work from our laboratory investigating mechanisms of opioid analgesia using the Northern grass frog, Rana pipiens. Over the last dozen years, we have accumulated data on the characterization of behavioral effects after opioid administration on radioligand binding by using opioid agonist and antagonist ligands in amphibian brain and spinal cord homogenates, and by cloning and sequencing opioid-like receptor cDNA from amphibian central nervous system (CNS) tissues. The relative analgesic potency of mu, delta, and kappa opioids is highly correlated between frogs and other mammals, including humans. Radioligand binding studies using selective opioid agonists show a similar selectivity profile in amphibians and mammals. In contrast, opioid antagonists that are highly selective for mammalian mu, delta, and kappa opioid receptors were not selective in behavioral and binding studies in amphibians. Three opioid-like receptor cDNAs were cloned and sequenced from amphibian brain tissues and are orthologs to mammalian mu, delta, and kappa opioid receptors. Bioinformatics analysis of the three types of opioid receptor cDNAs from all vertebrate species with full datasets gave a pattern of the molecular evolution of opioid receptors marked by the divergence of mu, delta, and kappa opioid receptor sequences during vertebrate evolution. This divergence in receptor amino acid sequence in later-evolved vertebrates underlies the hypothesis that opioid receptors are more type-selective in mammals than in nonmammalian vertebrates. The apparent order of receptor type evolution is kappa, then delta, and, most recently, the mu opioid receptor. Finally, novel bioinformatics analyses suggest that conserved extracellular receptor domains determine the type selectivity of vertebrate opioid receptors.
Nociception is an important sensory system of major fundamental and clinical relevance. The nociceptive system of higher vertebrates is well studied with a wealth of information about nociceptor properties, involvement of the central nervous system and the in vivo responses to a noxious experience are already characterised. However, relatively little is known about nociception in lower vertebrates and this review brings together a variety of studies to understand how this information can inform the evolution of nociception in vertebrates. It has been demonstrated that teleost fish possess nociceptors innervated by the trigeminal nerve and that these are physiologically similar to those found in higher vertebrates. Opioid receptors and endogenous opioids are found in the brain and spinal cord of the fishes and morphine blocks avoidance learning using electric shock as well as reducing nociceptive behavioural and physiological responses to noxious stimulation. Comparative analysis of the fishes and higher vertebrates show that fish possess less C fibres than higher vertebrates. The electrophysiological properties of fish nociceptors are almost identical to those found in higher vertebrates suggesting the evolution of these properties occurred before the emergence of the fish groups.
Information gathering during agonistic and non agonistic shell aquistion by hermit crabs
- Elwood
Elwood, R.W., Briffa, M., 2001. Information gathering during agonistic and non agonistic shell aquistion by hermit crabs. Adv. Study Behav. 30, 53–97.