What capacity do invertebrates and fish have to suffer?

Until relatively recently it was assumed that the absence of a neocortex in invertebrates meant that they could neither feel pain nor comprehend the world past simple internal and external cues [9], but relied on the simplest forms of cognitive processes [10]. This has since been disputed [11, 12, 13] and it has been argued that the neocortex is not indicative of the ability to suffer if analogous structures are present; for example, macaques have no prefrontal cortex yet the presence of subcortical and cortical structures allow them to efficiently problem solve with a potential awareness of their memory ability [14, 15]. Sneddon [13] found that when testing behaviour changes following exposure to noxious stimuli in trout, it resulted in decreased feeding motivation, rocking whilst on substrate surface, and rubbing their snouts on tank walls, indicating aversive and abnormal behavioral reactions related to pain [15]. Studies in cephalopods (molluscs) [16] and decapod crustaceans (i.e. shrimps, crabs) [17] have observed an avoidance of stimuli that could be associated with pain.

The concept of suffering is not merely restricted to pain but also involves the assessment of cognitive ability when considering the impact of behavioral deprivation. Several species of fish have exhibited complex learning behavior, such as the ability to generate internal map-like representations; seen by Aronson [18] in a rock pool gobiid fish who relied on knowledge of escape routes and topography. Observational learning can even be seen in species such as fighting fish, who will observe victors of previous fights and avoid conflicts with them subsequently [19]. Examples exist of both aquatic vertebrates [20] and cephalopods [21] which have exhibited tool use and the ability to modify their behavior to achieve a more beneficial outcome, suggesting a cognitive ability similar to that of terrestrial vertebrates [20]. Feld et al. [22] recognized an advanced cognitive ability in decapod crustaceans, whereby information could be stored for several days and complex learning was displayed. This was supported by studies into crabs who consistently avoided a structure similar to where they had previously received a ‘painful’ electric shock [23, 17].

Is live prey feeding necessary?

Live prey feeding to animals kept in captivity is seen as necessary by some to promote behaviours that occur naturally in the wild [8] and therefore may have beneficial impacts on the animals’ behavior, general health and lifespan [24]. Live prey feeding may, however, may be detrimental to the wellbeing of the predator due to injury risk when hunting and killing [25] and energy expenditure [26] in an unnatural and/or finite enclosure, cage or tank. A key argument by opponents to live feeding is the suggestion that well-designed environmental enrichment can essentially replace the behavioral opportunities that would otherwise be lost. For example, Quirke et al. [27] documented comparable speeds attained by a cheetah exposed to a ‘cheetah run’ device whereby a lure is followed to simulate hunting. However, not all attempts at enrichment are successful in recreating experiences afforded by the presence of live prey, as demonstrated by Skibiel et al [28] in their provision of raw bones to captive large felids. A brief review of positive and negative aspects of live prey feeding can be seen in Table 1.

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Table 1. A brief list of examples of positive and negative aspects of live prey feeding.

https://doi.org/10.1371/journal.pone.0216777.t001

Assessments on behavior changes of aquatic animals’ dependent on a live prey diet are few in comparison to terrestrial mammalian studies [36]. Despite fewer studies of the effects in aquatic species there is evidence to justify live prey feeding amongst them. Cuttlefish (i.e. Sepia officinalis), for example, exhibit greater growth and survival rates when fed live instead of frozen shrimp [37]. A similar pattern is seen in seahorses; and prohibiting a live prey diet can even have fatal consequences on developing fry [31]. Conversely, this health benefit is lost if the damage caused by hunting prey is significant, which can happen in small tanks (Cooke pers.obs) as some common captive aquatic predators (e.g. cephalopods) damage easily in captivity [31]. Regardless of potential harm, learned predatory behaviour may be a necessary skill for fish to obtain if they were to be re-released for conservation goals [38]. Trout with predatory experience were seen to be significantly more skilled than those without, which had a substantial effect on their growth, mortality, reproduction and health when released [24]. Cox and Pankhurst [39] recognize this as a reluctance of inexperienced trout to feed on novel prey.

Feeding fish to shark

‘Fish’ is a relatively vague term that covers a variety of species, meaning that participants could be varied in their interpretation of this question. Visitors of the aquarium had seen a fish recently, but had no contact with a shark, potentially indicating why they were opposed to this scenario both on and off show if they had built empathy with fish. This theory would not, however, be supported by answers from UK professionals, who found this scenario most acceptable of all groups surveyed as they are likely to be familiar with fish; especially those working with them. This pattern emerges in many of the scenarios, both on and off show.

Feeding crab to cuttlefish

The aquarium did not house any cuttlefish and only one species of crab (hermit crab) at the time of the survey, yet this scenario was significantly opposed by zoo and aquarium visitors as well as US professionals. UK professionals, again, were significantly more accepting of this.

Crab is a popular meat in the UK, especially in coastal regions (such as Paignton, where the surveys were taken), so it may be expected that this would influence scores of zoo and aquarium visitors into finding this more acceptable, yet the opposite is seen.

These findings may question whether an empathic response has been built from the learning style in zoos and aquariums that is generalized to aquatic life, a response which is individual to these establishments as UK professionals, who are likely to be educated well within their field, do not exhibit this.

Feeding fish to fish

This scenario went against some of the previous patterns, with UK professionals being the most opposed when on show and US professionals and aquarium visitors finding it significantly acceptable if it is off show. This variation does raise, again, the reliability of this question if participants are considering a range of fish in their answers. Especially by using ‘fish’ both as prey and predator it could imply to a participant that the same species was being used on both roles, potentially eliciting concern of disease spread (such as a minor outbreak of Botulism in April 2017 in US).

Feeding shrimp to fish

This scenario saw US consistently finding this scenario more acceptable, both on and off show. This may be expected due to the popularity of shrimp meat in the US. Aquarium visitors, however, also found this scenario more acceptable when off show. Whilst it could be argued that due to the lack of shrimp at the aquarium there was more of an empathic response to the predating fish in this question, when looking at responses to feeding ‘live crab to cuttlefish’, this did not seem to significantly impact the responses.

Feeding fish to cuttlefish

This scenario saw UK professionals being significantly more accepting than any other group. The repetition of finding live prey feeding where a cuttlefish is the predator may stem from a higher empathic response from those who work with fish towards cuttlefish, as research about their higher cognitive abilities and electroreception is emerging. It would, however, then be expected that US professionals would follow this pattern, yet here it is seen that they, like the zoo and aquarium visitors, do not find this ethically acceptable; on or off show.

Feeding octopus to shark

This scenario did evoke a different response, with responses being much less separated dependent on group. UK professionals were most opposed to this on show yet found it more acceptable when off show. Zoo and aquarium visitors found this more ethically acceptable than many other scenarios they had responded to.

This could stem from an excitement of seeing the hunting and feeding behavior and a recognition of ‘it is what happens on the wild’ that may be wanted within an education of the aquarium or zoo.

The responses from UK professionals finding this less acceptable than many other given scenarios within the survey may be, as assumed with cuttlefish, due to an empathic response to octopus. As cephalopods, octopi are regarded as more intelligent than many other aquatic species which may cause empathy from participants due to a presumed level of cognition closer to theirs and an attributed mental state. Fish, as a broad term, may be interpreted in many ways; all of which holding more emotional attachment of compassion than a shrimp or crab, which are commonly consumed in both the UK and US.

Similarly, the feeding behavior of sharks, whilst exciting to the public, may not be seen as an appropriate behavior for the public to view due to their representation in the media. This may be through reports of shark attacks and the subsequent pressures on local governments to prevent future attacks by means of public announcements [59]. This fear and negative association can be seen in a more subconscious suggestion in background music to televised shark scenes [60], which is a common accompaniment and can provoke fear in viewers.

On and off show

The largest difference in responses seen was from UK professionals when feeding live octopus to sharks. It is considered that zoo and aquarium visitors as well as US professionals were, on average, less accepting of live prey feeding and therefore may not have changed their answers to even lower when the scenario was off-show.

Whilst zoo and aquarium visitors did score lower on the survey, the lack of change in response to live prey feeding on and off show may be due to the recent exposure to many of the species and feeling an involvement, therefore if the practices were to take place, participants may assume that they would not feel too differently whether they saw it or not. Despite a potential wariness of allowing children to see feeding, it seems to be more important to the visitors that they learn about ‘natural habits’ of the animals–including hunting and feeding. This could be a desire for seeing exciting things when they visit or from an educational point of view and understanding what happens; even teaching children there about how animals live.

Professional participants

UK professionals were often in agreement on many scenarios, with UK non-aquarist professionals finding scenarios slightly more acceptable. US professionals, however, did not follow similar patterns often finding scenarios to be less ethically acceptable. These differences are not seen to be due to a separate variable as all professional surveys were completed online.

This is surprising, as it contradicts legislation in each country. It would be expected that UK professionals would adhere beliefs towards what the EU Directive has set out, and US professionals to be more willing to accept live prey feeding due to the lack of legislation directly prohibiting the act.

Gender as an effect on ethical acceptability of live prey feeding

In previous studies [1, 2], females were more likely to find live prey feeding of terrestrial animals ‘slightly unacceptable’, yet the findings from this data did not reflect that, instead showing no significant differences between males and females. Due to a smaller sample size of males it is possible that this data is unreliable, however, there may also be explanations for the similarities.

The lack of difference in response based on gender varies from previous research from Ings [2], Cottle [1] and Ormandy and Schuppli [55]. Ormandy and Schuppli state that women are more likely to object to issues implicating animal rights as they are more likely to attribute mental states with animals. This may still be the case, however the mental state of the cuttlefish and sharks as predators may be a less imminent factor than it is with terrestrial animals.

The difference in fish and terrestrial animals with responses from the female demographic are defined by Panagiotarakou [56]. She states that whilst aretic (i.e. spiritual and totalitarianist), feminist-inspired ethics are suited to companion animal ethics they are not to endangered or ‘unlovable’ species. As discussed earlier, the decrease of emotion felt towards aquatic animals may be a reason why female opinions will be less predictable when discussing ‘unlovable’ animals.

It must also be considered that there are likely cultural changes from the results collected by Ings in 1997, both due to geography and the time difference. This may be one of the most significant reasons for the contrast in results based on gender.

Experience of participant as an effect on the ethical acceptability of live prey feeding

Expectancy of differences between those that had recently visited a zoo or aquarium were that they would be more like professionals, due to zoos’ and aquariums’ long-term educational goals [57]. The data showed visitors that had just been to the zoo or aquarium were more opposed to live prey feeding than US aquarists and UK non-aquarists.

Potential reasons for this divide could be the immediate contact that participants had with the species. The survey was completed as zoo and aquarium visitors were leaving the establishments so, with help from species exposure and educational tools (such as posters, interactive games and talks), a short-term ‘ethic of care’ may have been created [58].

This same ethical opposition is seen less in professionals, especially within the UK. This may be due to a habituation to some species, meaning that this ‘ethic of care response’ is reduced. Due to the large variation of work completed in the profession, even just in the aquarist participants, it is unknown which other variables would affect this.

Previous studies [1, 2] have seen the demographic of participants with a higher education correlating with a higher acceptance of finding live prey feeding ethically acceptable. It is invalid to suggest that the UK and US professionals will all possess a higher level of education than zoo or aquarium participants, however it is much more likely that their education will be specific to animals; if not aquatic life particularly. This would imply that they are more familiar with welfare and husbandry regulations. This may be the reason that explains why there is such a difference in UK professionals and other groups’ responses.