Ascribing sentience to animals and case study of the evidence for sentience in cephalopods: Scottish Animal Welfare Commission report

Part 2: Ascribing sentience to cephalopods: a case study

Background

The cephalopods are represented by over 800 exclusively marine living species, including squid, octopus, cuttlefish and nautilus (Jereb and Roper, 2010). The invertebrates show an enormous diversity of species with profound differences in their body plan, nervous organisation and cognitive capacity. The most advanced class among the invertebrates is the Cephalopoda, which possess the largest invertebrate nervous system (Zullo and Hochner, 2011).

Cephalopods are a significant source of food for humans, are popular aquarium exhibits, and have been considered valuable experimental subjects. For example, the squid giant axon enabled the discovery of the basic mechanisms of the action potential (Hodgkin and Huxley, 1952), and fundamental discoveries were also made about mechanisms of neurotransmitter release at the squid giant synapse (Katz and Miledi 1967).

In recent years the question of their sentience and consequent need for legal protection has been the subject of considerable discussion. The cephalopod molluscs and the decapod crustaceans are believed to be the most cognitively developed and intelligent invertebrates (Winlow and Di Cosmo, 2019). They are consequently often used as the "next" taxon to consider for sentience after vertebrates, and therefore an illustrative example of the approach proposed and adopted by the SAWC.

Cephalopod welfare protection in law

As with most animals used as a resource for humans, the need for legal protection in different contexts has begun to be recognised, but this remains limited.

There is currently no general welfare protection for cephalopods in Scotland. Section 16 of the Animal Health and Welfare (Scotland) Act 2006 refers to protected animals as being "vertebrates other than man" and specifically excludes protection for foetuses or embryos. The Act does allow for Scottish Ministers to regulate for the extension of this definition to include invertebrates but only on the proviso that scientific evidence can be found to show that such invertebrates are "capable of experiencing pain or suffering" (Animal Health and Welfare (Scotland) Act 2006, section 16(4)).

Cephalopods have been included in various national codes of practice and legislation covering research in several countries outside the EU, for example: Canada, 1991; New Zealand, 1999; Australia, 2004; Switzerland, 2011; Norway, 2011 (Smith et al., 2013; Fiorito et al., 2014). One species of cephalopod, Octopus vulgaris, was added to the UK Animals [Scientific Procedures] Act 1986) in 1993, while the Animals (Scientific Procedures) Act 1986 Amendment Regulations 2012 extended protection to any living cephalopod, excluding embryonic forms. Humane killing of cephalopods in contexts other than scientific research is not a statutory requirement in any EU member state.

Through Directive 2010/63/EU on the protection of animals used for scientific purposes, cephalopods gained the same EU legal protection as previously afforded only to vertebrates (Fiorito et al., 2014). The Directive, which came into force in 2013, marked a paradigm shift in policy, by including an entire Class of Molluscs.

Much of the evidence for inclusion of cephalopods in the Directive is based upon various aspects of neuroscience research on cephalopods (Fiorito, 2014). In the European Food Safety Authority Opinion on the "Aspects of the biology and welfare of animals used for experimental and other scientific purposes" (EFSA 2005), the Scientific Panel on Animal Health and Welfare (AHAW) concluded that Directive 86/609/EEC relating to the protection of animals used for experimental and other scientific purposes should be revised to include cephalopods. Stopping short of claiming that cephalopods were sentient, the AHAW argued that "cyclostomes, all Cephalopoda and decapod crustaceans fall into the same category of animals as those currently protected" (EFSA 2005). The decision to include cephalopods was based primarily upon the recommendations of a scientific panel which concluded that there was "scientific evidence of their ability to experience pain, suffering, distress and lasting harm" (i.e. Directive 2010/63/EU: Recital 8, European Parliament and Council of the European Union 2010).

Categories of evidence to be considered in relation to sentience

Some authors have stated that proving the ability for experiences is infeasible (Walters, 2018). A counter argument uses the precautionary principle, arguing that certain species should be assumed to be sentient given the current limitations of science (Sneddon et al 2018). We have taken a middle ground of considering the multiple sources of relevant evidence relating to neuroanatomical, behavioural and cognitive functions.

Using the criteria laid out in Table 2 we have considered the evidence in support of pain responses and thus sentience for cephalopods.

1. Phylogenetic "proximity" to sentient species

Cephalopods are, like mammals, classified within Eumetazoa and ParaHoxozoa, but are not very closely related to mammals. However, the evidence of convergent evolution in various cognitive functions suggests this phylogenetic distance is not a sufficient reason to reject ascriptions of sentience based on other categories of evidence. Convergent evidence indicates that many non-human animals, including some cephalopods, possess the capacity for consciousness (Low, 2021)

2. Neuroanatomical functioning

Nociceptors

In both squid and octopus, mechanical force applied to the tentacles or arms results in rapid behavioural responses (withdrawal of the damaged limb), and sensitisation of responses to further stimulation (Crook et al., 2013; Perez et al., 2017). Further examination demonstrates the presence of neurons that only responded to noxious stimuli, and which are more reactive (sensitised) following previous injury (Perez et al., 2017). Interestingly, as seen in mammals, there is evidence that early life injury in squid permanently alters neural excitability to later stimulation (Howard et al., 2019).

Neurological anatomy

In the European Food Safety Authority Journal report 2005 (EFSA 2005), the authors state that there is evidence that 'cephalopods have a nervous system and relatively complex brain, similar to many vertebrates, and sufficient in structure and functioning for them to experience pain.'

Evidence for this includes;

a. they release adrenal hormones in response to situations that would elicit pain and distress in humans

b. they can experience and learn to avoid pain and distress such as avoiding electric shocks

c. they have nociceptors in their skin (EFSA 2005)

Cephalopods have been shown in at least one taxon to have receptors for anaesthetic drugs (Sneddon et al., 2014). Additionally, anaesthesia in octopus and cuttlefish has been demonstrated to act in a similar way to mammals, by providing strong and reversible blockade of afferent and efferent nerve activity (Butler-Struben et al., 2018). These data suggest that cephalopods show loss of consciousness and anaesthesia when treated with drugs that have similar impacts in vertebrates, and that this is not merely immobility when applied to these animals.

3. Behavioural indicators

The complex behavioural and learning capabilities of cephalopods (Hanlon and Messenger 1996; Borrelli and Fiorito 2008; Huffard 2013) correspond to a highly sophisticated nervous system that appears to be correlated with their lifestyle (Nixon and Young 2003; Borrelli 2007 in Fiorito et al 2014).

As noted in EFSA (2005), cephalopods can experience and learn to avoid pain and distress such as avoiding electric shocks, they have significant cognitive ability including good learning ability and memory retention, and they display individual temperaments since some individuals can be consistently inclined towards avoidance rather than active involvement.

Octopus and squid show behavioural sensitisation following injury, involving defensive behaviours (Alupay et al., 2014), which are expressed earlier under threat of predation than in uninjured animals (Crook et al., 2014). These responses could be interpreted as an adaptive response to avoid predation, as fish predators target injured animals over uninjured, and suggest altered behavioural choices or responses.

During periods of stress, Giant Pacific Octopuses may show signs of stereotypy, by pacing around the tank, or sitting under water returns for long periods of time – however these may also be signs of poor health or senescence (BIAZA 2011). Giant Pacific Octopuses react rapidly to environmental changes or external stimuli with physiological consequences that can be relatively long lasting (Fiorito et al, 2015), and signs of stress may include autophagy, non-healing epidermal lesions (Anderson et al, 2002) and reduced epidermal colour change (AITAG 2014).

Cephalopod behaviour and memory may be altered by environmental conditions. An enriched environment can positively influence cephalopod behaviour in cuttlefish (Poirier et al. 2004, 2005; Yasumuro and Ikeda 2016) and octopus (Beigel and Boal, 2006; Yasumuro and Ikeda, 2011, BIAZA, 2011). Memory formation may also be affected (Dickel et al. 2000; Borrelli et al. 2020). Octopus avoid a location previously associated with noxious stimuli (Crook, 2021).

Octopuses demonstrate flexible and varied approaches to feed on different shellfish, finding food in a dynamic environment and navigating predator-prey relationships (Amodio et al., 2019). They can also apply these skills in an artificial laboratory setting by for example opening jars, using methods that are more complex than simple trial and error learning (Amodio et al., 2019).

Many cephalopods live in social groups and hence may have levels of cognitive ability similar to those of vertebrates that have complex social relationships (EFSA 2005). Learning is involved in most signalling and the most elaborate signalling and communication systems occur in cuttlefish and squid that can show rapid emotional colour changes and respond to these changes in other individuals (EFSA, 2005). Deception (possibly indicating they possess a theory of mind) – for example male mourning cuttlefish (Sepia plangon) can simultaneously signal courtship patterns on one half of their body to receptive females and display female patterns to a single rival male on the other, thus preventing the rival from disrupting courtship (Brown et al 2012).

There is some argument that cephalopods show evidence of cognitive abilities including spatial and visual awareness and learning abilities, long and short term memory, higher learning such as discrimination and reversal learning, brain lateralization, learning in response to both visual and tactile cues, and potential domain generality and simple concept formation, awareness of their position, both within themselves and in larger space, including having a working memory of foraging areas in the recent past, and complex spatial problem-solving (Macknick, 2006; Mather, 2008).

Reasons against ascribing sentience to cephalopods

Some of the arguments used by Elwood et al. (2009) to explain why crustacean welfare is overlooked also apply to the cephalopods and include that it might be inconvenient (given that it is considered normal to boil crustaceans alive prior to eating), that they are not held in high regard by the public and that the absence of concrete data to prove that they suffer is used as an excuse to overlook their potential for suffering. There may be conflict between practice and invertebrate welfare (Garrido and Nanetti, 2019). Appeals to the lack of scientific data to refute claims of suffering, which otherwise appears intuitively likely, echo the conclusions of the Brambell report (Brambell, 1965).

Recently, public assumptions are being altered by anecdotes of octopus behaviour, and by several recent popular books on cephalopods behaviour and intelligence (Mather, 2020). Several authors have argued that, although proving that invertebrates suffer requires a different paradigm of data collection and interpretation, the evidence is becoming clear that these animals can suffer and so require further legal protection (Sherwin 2001, Elwood and Appel, 2009).

A specific debate surrounds the design of models based on human and AI studies used to demonstrate whether non-human animals are sentient. For example: Sneddon refutes claims such as those made by Key and Brown (2018) that evidence gathered using an AI-based model demonstrates that cephalopod neuroanatomy is incapable of human like neural processing. Sneddon states: "What is fascinating is that to process all the information, the computers used for AI are powerful and considered very complex. However, animals such as fish, that exhibit a similar range of complex actions without programming, are not considered complex." (Sneddon 2018).

Conclusions and recommendation

The welfare of invertebrate animals has 'begun to matter' to the public and the scientific community (Mather, 2020), and whilst current scientific evidence can never provide absolute proof of the existence of sentience in non-human species (or indeed in anyone other than oneself), the weight of evidence indicates 'that humans are not unique in possessing the neurological substrates that generate consciousness' (Low, 2012). Appreciation of the diverse forms of sentience in the animal world may lead to more inclusive animal ethics (Mikhalevich & Powell, 2020).

The overall weight of scientific evidence discussed in this paper supports the conclusion that cephalopods fulfil the same criteria as other animals that are considered sentient. If we consider that evidence of an ability to feel pain can serve as evidence for sentience, then cephalopods have been shown to have nearly all the capacities defined in Table 2. This, coupled with the additional evidence of behavioural and other abilities as outlined above, is supportive of cephalopods being treated as sentient. It would logically follow that their welfare should be considered within policymaking.

The SAWC therefore recommends that the Scottish Government consider whether the welfare considerations and legal protection that have been afforded to vertebrates should now be extended to cephalopods.