Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-27T14:34:35.996Z Has data issue: false hasContentIssue false

Considerations for implementing regulation of decapods in science

Published online by Cambridge University Press:  27 November 2024

Adam Powell*
Affiliation:
Department of Life Sciences, Aberystwyth University, Ceredigion SY23 3DA, UK
Ann-Lisbeth Agnalt
Affiliation:
Institute of Marine Research, Nordnesgaten 50, Bergen 5005, Norway
Kevin Heasman
Affiliation:
Cawthron Institute, Nelson, New Zealand
Amaya Albalat
Affiliation:
Institute of Aquaculture, University of Stirling, Stirling FK9 4LA, UK
*
Corresponding author: Adam Powell; Email: [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Decapod crustaceans, commonly utilised for pure or applied scientific research and commercial food production, have generally remained outside ethical debate. However, in the last decade many parts of the world have seen an increase in public interest in the welfare of decapod crustaceans and statutory legal protection has been introduced in several countries. Although still limited to a small number of countries and remaining relatively unharmonised, relevant legislation could be increasingly broadened to include decapods in further jurisdictions. Much existing legislation, originally intended for protecting terrestrial vertebrates during scientific study, might be unsuitable for aquatic invertebrates such as decapods. Indeed, precedence with many fish species and cephalopods suggests detail is lacking with respect to fundamental guidance. Therefore, similar inclusion of decapods into such legislation could make welfare or scientific goals more challenging to achieve unless relevant guidance is available, particularly to animal care practitioners. This horizon paper aims to summarise existing decapod legislation, and the considerations required should decapods be included in current conceptual frameworks and scientific legislation.

Type
Horizon Topic
Creative Commons
Creative Common License - CCCreative Common License - BY
This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0), which permits unrestricted re-use, distribution and reproduction, provided the original article is properly cited.
Copyright
© The Author(s), 2024. Published by Cambridge University Press on behalf of The Universities Federation for Animal Welfare

Introduction

The order Decapoda includes commercially fished and farmed crustaceans, consisting mainly of aquatic species such as crabs, lobsters, crayfish, prawns and shrimp. The increase in human population, living standards and associated longevity have accelerated the demand and commercial production of decapods (Stentiford et al. Reference Stentiford, Neil, Peeler, Shields, Small, Flegel, Vlak, Jones, Morado, Moss, Lotz, Bartholomay, Behringer, Hauton and Lightner2012; Jennings et al. Reference Jennings, Stentiford, Leocadio, Jeffery, Metcalfe, Katsiadaki, Auchterlonie, Mangi, Pinnegar, Ellis, Peeler, Luisetti, Baker-Austin, Brown, Catchpole, Clyne, Dye, Edmonds, Hyder, Lee, Lees, Morgan, O’Brien, Oidtmann, Posen, Santos, Taylor, Turner, Townhill and Verner-Jeffreys2016). More specifically in scientific research, decapods are widely studied in many fields encompassing biotechnological, medical and ecotoxicological research and development (Hamed et al. Reference Hamed, Özogul and Regenstein2016; Vogt Reference Vogt2018; Passantino et al. Reference Passantino, Elwood and Coluccio2021), ecological studies including contemporary issues such as climate change and microplastic pollution (Toh et al. Reference EXP, Gan and Yeo2022; Yin et al. Reference Yin, Li, Craig and Su2022) and teaching (Cooper et al. Reference Cooper, Ambrose and Ventura2022; Wallis Reference Wallis2023).

Globally, human use of vertebrate animals is regulated according to standard veterinary, agricultural and husbandry practices, which as a minimum require basic husbandry and maintenance of animals during commercial operations. Many countries further regulate the use of non-human vertebrates during scientific research procedures (Codecasa et al. Reference Codecasa, Pageat, Marcet-Rius and Cozzi2021). In the UK, for example, the Animal Scientific Procedures Act 1986 (ASPA) regulates the use of protected animals (any living vertebrate other than humans, and any living cephalopod) during experimental procedures that cause pain, suffering, distress or lasting harm (PSDLH), thus impacting physical, mental and social well-being, including disease, injury and physiological or psychological discomfort (UK Government 1986). Decapods have generally been excluded from ethical debate and relevant welfare regulations (Passantino et al. Reference Passantino, Elwood and Coluccio2021; Rowan et al. Reference Rowan, D’Silva, Duncan and Palmer2021).

A landmark review by Birch et al. (Reference Birch, Burn, Schnell, Browning and Crump2021) analysed several criteria which cumulatively attributed evidence of decapod sentience (the capacity to have feelings). Whilst not individually conclusive, criteria included brain morphology, nociception (rapid detection and response to noxious stimuli) and more complex phenomena such as behaviour and learning. In relation to ASPA, frameworks need to clarify whether decapods can perceive PSDLH to help inform relevant legislation, perhaps via studies that investigate longer-term biological phenomena and wider criteria (Passantino et al. Reference Passantino, Elwood and Coluccio2021). Observational studies on behaviour, learning and strategy (e.g. injury-directed activities, motivational changes) are likely to increasingly suggest the ability of decapods to perceive pain (Elwood Reference Elwood2022; Barr & Elwood Reference Barr and Elwood2024). Whilst from a scientific standpoint the debate on sentience continues (Briffa Reference Briffa2022a; Diggles et al. Reference Diggles, Arlinghaus, Browman, Cooke, Cooper, Cowx, Derby, Derbyshire, Hart, Jones, Kasumyan, Key, Pepperell, Rogers, Rose, Schwab, Skiftesvik, Stevens, Shields and Watson2023), a working precautionary approach, alongside changing governmental policy, has meant that several countries (including the UK, under The Animal Welfare [Sentience] Act 2022 [AWSA]), have now recognised decapods as sentient beings (Birch Reference Birch2017; UK Government 2022a; Wickens Reference Wickens2022).

The European Union (EU) also recognised all animals as sentient beings within founding agreements such as the Lisbon Treaty (EU 2007; Rowan et al. Reference Rowan, D’Silva, Duncan and Palmer2021). EU agencies additionally recommended extending scientific legislation to include decapods (European Food Safety Authority [EFSA] 2005). Whilst this remains to be implemented, regulatory precedence has been set outside the EU, with several countries incorporating invertebrates within relevant national legal frameworks. Specifically for decapods, this includes Norway, Switzerland and New Zealand (Smith et al. Reference Smith, Andrews, Hawkins, Louhimies, Ponte and Dickel2013; Passantino et al. Reference Passantino, Elwood and Coluccio2021). Whilst AWSA does not cascade to specific legislation such as ASPA, it mandated the formation of an Animal Sentience Committee, responsible for analysing potential negative welfare impacts on sentient animals that may arise from government policy (UK Government 2022a). Consequently, a consultation process was initiated in 2023 to detail decapod use in science, potentially altering the future scope of UK legislation (UK Government 2022b).

Recent efforts to improve welfare in commercial sectors, for instance optimising husbandry and euthanasia (Albalat et al. Reference Albalat, Zacarias, Coates, Neil and Rey Planellas2022; Neil et al. Reference Neil, Putyora and Albalat2024) are pertinent to decapod use in the research sector. However, consideration of how decapod welfare could be introduced within existing scientific governance frameworks remains lacking. It therefore seems timely to expand the discussion further, firstly by reviewing extant invertebrate legislation and precedence, and secondly, by considering decapod-specific aspects that would be relevant within current vertebrate-centric legislation.

Ethical considerations

No animals were required for this desk study.

Precedence for invertebrates within scientific legislation

Animals are referred to as ‘protected’ under scientific regulation, although this varies between countries or jurisdictions, taxon and life stage (Codecasa et al. Reference Codecasa, Pageat, Marcet-Rius and Cozzi2021). EU Directive 2010/63 (on the protection of animals used for scientific purposes) is arguably the most inclusive and extensive legislation, harmonising scientific use of animals across all EU member states (EU 2010). As with many other legal frameworks, relevant EU and UK law also protects non-human vertebrates and cephalopods from early developmental stages (Codecasa et al. Reference Codecasa, Pageat, Marcet-Rius and Cozzi2021).

Additional, specific inclusion of decapods within welfare legislation exists in several countries (Passantino et al. Reference Passantino, Elwood and Coluccio2021). However, the spectrum of protected taxa varies between neighbouring countries, for example in Asia, with decapod protection during science and teaching mandatory in Thailand and Indonesia (Law of the Republic of Indonesia 2009; Animals for Scientific Purposes Act BE 2558 2015 [Retnam et al. Reference Retnam, Chatikavanij, Kunjara, Paramastri, Goh, Hussein, Mutalib and Poosala2016]; Wallis Reference Wallis2023). Even regionally, protected species may vary, for example, across Australian territories (Victorian Government 1986; Wallis & Katayama Reference Wallis and Katayama2022). Delineation between general commercial and scientific use also varies in legislation. For example, both purposes are contained within the same law in Norway, which protects decapods from the time they start feeding as larvae (Norwegian Government 2009; National Research Ethics Committee 2015). On the other hand, legislation is split across two Regulations and Acts in New Zealand, which protects decapods after larval developmental stages have been completed (NZ Government 1999, 2018). The most detailed legislation, covering both general and scientific governance, is contained within Swiss legislation (Swiss Federal Council 2005, 2008; Eggel & Camendzind Reference Eggel and Camendzind2020; Swiss Federation 2020), although neighbouring Austria stipulates standards for general husbandry only (Austrian Federal Chancellery 2004). In summary, this simple retrospective suggests that decapod protection has proceeded in a relatively piecemeal fashion and is not harmonised according to purpose, practical detail, and protection status.

Furthermore, previous regulatory change has not always been logical. As an example, ASPA amendments in 1993 extended protection (from exclusively vertebrates) to one invertebrate species in the UK, the common octopus (Octopus vulgaris) (UK Government 1993). However, other cephalopod species, including the more prevalent curled octopus (Eledone cirrhosa) (Barrett et al. Reference Barrett, Bradley and Brazier2023) were not protected under ASPA and researchers were not obliged to record and submit numbers enrolled in scientific research. In 2013, the UK transposed EU Directive 2010/63/ into ASPA, which broadened protection to all cephalopod species (EU 2010; Dunn Reference Dunn2021). This demanded swift dissemination of available technical knowledge regarding cephalopod husbandry and associated legal obligations (e.g. Andrews et al. Reference Andrews, Darmaillacq, Dennison, Gleadall, Hawkins, Messenger, Osorio, Smith and Smith2013; Smith et al. Reference Smith, Andrews, Hawkins, Louhimies, Ponte and Dickel2013). Nevertheless, specific, yet fundamental recommendations for cephalopods (for example, husbandry and euthanasia) are not specified in EU Directive 2010/63 (EU 2010).

The 3Rs and decapods

The use of animals in research is driven by internationally established principles of utilitarianism and the 3Rs (Replacement, Reduction and Refinement; Russell & Burch Reference Russell and Burch1959; Anon 2012). The concept is enshrined within ASPA, EU Directive 2010/63 and other national laws which specify animals as non-human vertebrates and cephalopods (UK Government 1986; EU 2010; Codecasa et al. Reference Codecasa, Pageat, Marcet-Rius and Cozzi2021). Prior to discussing specifics of legislation in detail, a more fundamental question is whether the 3Rs approach would remain a suitable platform to promote decapod welfare and improve data integrity.

Replacement promotes alternatives to using protected animals, either partially or fully. The use of in vitro systems and in silico modelling may be useful alternatives to assist Replacement (Liu et al. Reference Liu, Yang, Cai, Cao, Sun, Wang, Li, Liu, Lee and Tang2019; Passantino et al. Reference Passantino, Elwood and Coluccio2021). Whilst some in vitro research has been developed for decapod research, there are no available invertebrate cell lines, due to high taxonomic diversity, fragmented research effort and additional knowledge gaps in cell metabolic requirements (Domart-Coulon & Blanchoud Reference Domart-Coulon, Blanchoud, Ballarin, Rinkevich and Hobmayer2022). Therefore, research is needed in this area to support Replacement within the decapod research field.

Reduction advocates using minimal numbers of animals whilst maintaining worthwhile and robust scientific data. Reduction encompasses universally applicable goals of optimal experimental design, associated robust statistics and avoidance of study duplication (as exemplified by the ARRIVE and PREPARE guidelines; Smith et al. Reference Smith, Clutton, Lilley, Hansen and Brattelid2018; Percie du Cert et al. Reference Percie du Sert, Hurst, Ahluwalia, Alam, Avey, Baker, Browne, Clark, Cuthill, Dirnagl, Emerson, Garner, Holgate, Howells, Karp, Lazic, Lidster, MacCallum, Macleod, Pearl, Petersen, Rawle, Reynolds, Rooney, Sena, Silberberg, Steckler and Würbel2020). In terms of minimising animal numbers at the planning stage, decapods may be well suited. Many species are aggressive, cannibalistic and naturally solitary (Romano & Zheng Reference Romano and Zeng2017). In captivity, the welfare obligation to maintain decapods separately, rather than communally, also creates a powerful (n) number of individual experimental units, promoting robust statistical study design. Although not a widely cultured taxa, modular rearing systems are commercially available for certain decapod groups such as clawed lobsters (Nephropidae) (Hinchcliffe et al. Reference Hinchcliffe, Agnalt, Daniels, Drengstig, Lund, McMinn and Powell2022.

The impact of genetic variation and disease in the study population can also result in weak experimental data and inflate animal numbers to an unnecessary level. Ensuring a high health status and proven genetic lines (within designated breeding establishments) also supports Reduction. This is best achieved by establishing domesticated model species cultured with a closed lifecycle (i.e. full control over successive generations, breeding and health status, with straightforward husbandry requirements in captivity). For aquatic taxa in extant legislation, this only encompasses specifically zebrafish (Danio rerio) (EU 2010). In the case of decapods, whilst there is emerging interest in decapod veterinary care (e.g. Wahltinez et al. 2022), the lack of conventional immune memory in invertebrates (Rowley & Powell Reference Rowley and Powell2007) suggests that preventative measures supporting Reduction, such as vaccination, would confer limited benefit or proven pathogen resistance. Nevertheless, a general biomedical model may lie with crayfish species (Mykles & Hui Reference Mykles and Hui2015; Vogt Reference Vogt2018), whilst hermit crabs have been suggested for behavioural, and indeed sentience research (Briffa Reference Briffa2022b; Elwood Reference Elwood2022).

Refinement demands general and specific technical knowledge to optimise the lived experience of research animals and working to ensure that they have a good life. Additionally, this supports satisfactory data quality during scientific procedures. Refinement includes exemplary husbandry, positive welfare, seeking minimally invasive techniques, humane endpoints, and pain control (Anon 2012). However, our understanding of wild decapods is limited, in terms of maintaining them in their preferred environment in captivity, potentially over long periods of time. For instance, maintaining a robust and commonly studied European decapod (shore crabs [Carcinus maenas]) in captivity for a six-month period had a detrimental effect on their health, despite provision of husbandry and aquarium conditions that were hitherto deemed satisfactory (Wilson et al. Reference Wilson, Wyeth, Spicer and McGaw2022). Encouragingly, behavioural assessment techniques have been adapted to support positive welfare in captive decapods (Narshi et al. Reference Narshi, Free, Justice, Smith and Wolfensohn2022).

Sharing expertise and developing best practice protocols are clearly needed, and transferable knowledge from decapod farming could support Refinement. Recent advances include species-specific operational welfare indicators, for example in abundantly farmed penaeid shrimp (e.g. the Pacific whiteleg shrimp, Penaeus vannamei) (Albalat et al. Reference Albalat, Zacarias, Coates, Neil and Rey Planellas2022; Pedrazzani et al. Reference Pedrazzani, Cozer, Quintiliano, Tavares, da Silva and Ostrensky2023) and continuous remote monitoring systems resulting from the emerging field of precision aquaculture (Browning Reference Browning2023). Nevertheless, there is a lack of available veterinarian expertise, or consensus surrounding aquatic invertebrate health, disease diagnosis, treatment or euthanasia (Wahltinez et al. 2022). There remain several opportunities and needs to establish and improve anaesthesia, ethical killing and less-invasive sampling methods during research (Rottlant et al. Reference Rottlant, Llonch, García Del Arco, Chic, Flecknell and Sneddon2023; Crump et al. Reference Crump, Fischer, Arnott, Birch, Briffa, Browning, Coates, Elwood, Khan, Thanrar and Barrett2024). Refinement will also require further research or ethical debate surrounding detrimental practices, for example claw banding and particularly ‘nicking’ (Johnson et al. Reference Johnson, Coates, Albalat, Todd and Neil2016). While both practices compromise animals displaying normal behaviours, in some cases banding might be required to prevent physical trauma caused by intraspecific aggression.

Whilst there has been some call to revise or redefine the 3Rs for contemporary use (Tannenbaum & Bennett Reference Tannenbaum and Bennett2015; MacArthur-Clarke Reference MacArthur Clark2018), considered use of conceptual frameworks would likely improve the care of decapods when utilised in science and teaching, or at least provide more accountability regarding the use of these animals for research purposes.

Scientific legislation

The following section will discuss the extensive, albeit vertebrate-centric legislation that currently does not protect decapods (EU Directive 2010/63 and ASPA). Cumulatively, regulation of protected animals during research and teaching generally falls within four practical sections (UK Government 1986; EU 2010; Codecasa et al. Reference Codecasa, Pageat, Marcet-Rius and Cozzi2021): Breeding and supply; care and accommodation; procedures that cause pain, suffering, distress or lasting harm; and appropriate euthanasia. There is also increasing emphasis on improving the psychological well-being of research animals (Englund & Cronin Reference Englund and Cronin2023).

Defining when a decapod becomes a protected animal

The age (or, more accurately, life stage) at which aquatic taxa become protected under law is variable. Cephalopods are protected upon hatching while, for fish, it is at the point of independent feeding (EU 2010). Research involving early life stages of fish demand specific knowledge, experience, and awareness that experimental populations may transition into a protected status during a scientific study. Precise timing varies not only between any poikilotherm species but also correlates with culture temperature (degree days), with decapod species being no exception. Decapods possess a range of reproductive strategies, encompassing widely variable fecundity, life stage developmental forms and stage durations. For example, redclaw crayfish (Cherax quadricarinatus) may brood a few hundred embryos which remain attached and develop on the female abdomen, emerging as precocious benthic juveniles (Haubrock et al. Reference Haubrock, Oficialdegui, Zeng, Patoka, Yeo and Kouba2021). In contrast, Pacific whiteleg shrimp (P. vannamei) release several hundred thousand embryos shortly after fertilisation, which following hatching and initial reliance on yolk, develop through twelve larval stages in a pelagic environment, increasingly foraging larger and more active prey (Scott-Quackenbush Reference Scott Quackenbush2001; Food and Agriculture Organisation [FAO] 2007).

Although detailed decapod larval ecology is known for a limited number of species, a precautionary and straightforward approach (cephalopod model – protect upon hatching) could be beneficial and is practiced in Norway (Norwegian Government 2009). Alternatively, the study of larval species that initially lack mouthparts and remain lecithotrophic (nutritionally sustained by yolk reserves) following hatching would more reasonably fall under the fish model (protect upon first feeding). Further targeted scientific review focusing on larval life stages, and subsequent ethical debate, would need to agree on the stage at which decapods are likely sentient, and logically become protected.

Relevant legislation demands accurate records of animal numbers enrolled within project licences to populate publicly available national welfare audits (UK Government 2022c). Should decapods become protected, the potentially immense number of decapod larvae and juveniles could contribute significantly to published values, both for individual establishments and nationally, running contrary to efforts to reduce the numbers of animals in research (UK Government 2014a; Marshall et al. Reference Marshall, Constantino and Seidle2022). Accurate quantification of mortality at these stages will be challenging given the high fecundity and larval mortality associated with aquatic invertebrate reproductive strategies. Nevertheless, this is a known issue within the aquaculture hatchery sector with accurate counting devices under development (e.g. Li et al. Reference Li, Liu, Wang, Zheng, Lv, Fan, Guo and Gao2023).

Decapod supply

Breeders, suppliers and users of animals are regulated within scientific research legislation and are preferentially sourced from licenced breeding facilities (EU 2010) to assist Refinement. Zebrafish have been utilised as a biomedical and genetic model since the early 1980s (Streisinger Reference Streisinger, Walker, Dower, Knauber and Singer1981) and are the only fish species stipulated within EU legislation which must be sourced from a licenced breeding facility (EU 2010). All other fish species and cephalopods can therefore be obtained via alternative means.

Commercial decapod aquaculture has reached a sophisticated technological level for some species, such as penaeid shrimp (Barki et al. Reference Barki, Jones, Karplus, Breithaupt and Thiel2010; Castillo-Juárez et al. Reference Castillo-Juárez, Campos-Montes, Caballero-Zamora and Montaldo2015). Provided the species of interest is farmed, stock can be secured via commercial aquaculture facilities which may possess specific pathogen health status. Often, the quantity required for small-scale research purposes is negligible compared to commercial supplies, and for a minor customer such as a research project manager procurement can be challenging (A Powell, A-L Agnalt, K Heasman, A Albalat, personal observation 2023). However, for most species closure of the lifecycle and genetic manipulation is uncommon.

Although the number of farmed species is very limited in comparison to overall species diversity, it is likely much research will concentrate on fished or farmed decapod species due to their commercial importance. Nevertheless, a significant proportion of research and teaching is likely to focus on species that are not commercially produced. Should they become protected, decapods taken from the wild require an exemption prior to use in science, with an obligation to capture specimens humanely and competently, and stipulations on ‘Setting free’ after use (EU 2010). Additionally, wild caught animals also have an unknown health status and genetic provenance or variation. Although no decapod is currently under CITES protection (Convention on International Trade in Endangered Species of Wild Fauna and Flora [CITES] 2024), national or regional regulations may restrict the species, number, size, location or method of capture; or furthermore, keeping or release of non-native and likely imported species.

For decapods, procurement from the wild could encompass a range of habitats and capture methods, most simply via field collection in person. However, much procurement would need to rely on commercial, wild-capture fisheries, encompassing active or static nets and traps. Varying degrees of physical damage, physiological stress and morbidity can occur depending on capture method and the quality of subsequent husbandry (Fotedar & Evans Reference Fotedar and Evans2011; Stoner Reference Stoner2012). Transportation conditions that are sub-optimal for a particular species can elicit stress and morbidity and associated ethical and welfare concerns (Powell et al. Reference Powell, Barrento, Cowing, Lovrich and Thiel2020). Therefore, general and scientific EU legislation would need to consider if and how to regulate decapod procurement from the wild in a manner that is achievable in practical terms, whilst securing high welfare status before, during and after individual studies. For instance, emersed or iced transport of decapods for any purpose is banned in Switzerland (Swiss Federal Council 2008).

Decapod care and accommodation

For vertebrates and cephalopods, it is a fundamental obligation to ensure satisfactory care and accommodation for stock and experimental populations of animals used in scientific research. This currently includes taxonomic group and species-specific requirements, such as detail on housing dimensions and stocking density for discrete mammalian, avian, reptile and amphibian groups (EU 2010). The legislation additionally states that the care, accommodation needs and characteristics of each species should be addressed, and ideally harmonised and updated as knowledge is developed.

However, legal requirements for fish, combining all species and life stages, are somewhat limited to maintaining ‘adequate’ or ‘appropriate’ aquatic environmental parameters, whilst there is apparently no guidance for cephalopods (EU 2010). Further information may be available via national codes of practice (e.g. UK Government 2014b), however the limited and unharmonised detail on specific animal care within European legislation is a challenge (Marinou & Dontas Reference Marinou and Dontas2023) and adaption of the Five Domains model to aquatic animals remains to be formally established (Perkins Reference Perkins2021). Although it would be unreasonable for such documents to provide detailed specific advice pertinent to every species and life stage and provenance, standardised fundamental requirements for invertebrate care are needed, should decapods be included in future legislation.

Whilst decapods share many similar biological characteristics, the diverse anatomy, physiology and life history inevitably influences husbandry requirements. There are over 17,000 recorded species, inhabiting a range of marine, freshwater and terrestrial habitats (De Grave et al. Reference De Grave, Decock, Dekeyzer, Davie, Fransen, Boyko, Poore, Macpherson, Ahyong, Crandall, de Mazancourt, Osawa, T-Y, Ng, Lemaitre, van der Meij and Santos2023). Conservative estimates suggest that about 50 species are farmed, and generally possess contrasting species- and life stage-specific husbandry requirements (FAO 2022). Therefore, only a very small fraction (circa 0.3%) of known species is understood at a level that would confer knowledge to support care and welfare of decapods in captivity. For cultured species, commercial sensitivities may preclude dissemination of production manuals, although material is available via the public sector, for commonly farmed (e.g. tropical marine and freshwater shrimp; FAO 2002, 2007) and emerging species (e.g. clawed lobsters; Burton Reference Burton2003; Powell et al. Reference Powell, Cowing, Scolding, Shepherd-Waring, Eriksson, Lupatsch, Johnson, Shields and Gowland2015). To the authors’ knowledge, there remains only one specific decapod laboratory handbook available (Ingle Reference Ingle1995; updated, Elwood & Ingle Reference Elwood, Ingle, Richardson and Golledge2024) and a recent guidance document for decapods in research (Crump et al. Reference Crump, Fischer, Arnott, Birch, Briffa, Browning, Coates, Elwood, Khan, Thanrar and Barrett2024).

In addition to care and accommodation requirements, legislation requires adequate staff education, training and competence, encompassing variable responsibilities during scientific management. These include general competencies (designing and carrying out procedures, animal care, culling), and species-specific managerial responsibilities (overseeing procedures, providing species information and training; EU 2010). Furthermore, the requirement for suitable veterinary and unbiased welfare support, alongside competent inspections, would likely demand development of novel training, potentially incorporating basic health checks, husbandry and commonly used procedures. Such knowledge would also support competency within related animal welfare bodies and, indeed, ethical review panels could change or expand markedly (Cooper et al. Reference Cooper, Ambrose and Ventura2022), commensurate with increased quantity, novelty and animal numbers realised in project proposals. External and internal management and governance, which may include training, examination and licencing at many levels, will be challenging to achieve with limited species knowledge and before formal guidelines have been agreed and established. To the authors’ knowledge, Swiss law is unique in that it stipulates a statutory need for decapod-specific training of personnel in correct handling, biology, water quality monitoring and housing (Swiss Federal Council 2008).

Regulated procedures that cause pain, suffering, distress or lasting harm

Whilst planning and performing a regulated procedure, researchers have several pertinent obligations. These include: avoiding death as an endpoint; to classify procedure severity levels using assignment criteria; to reach decisions on continued or re-use of animals; and to report actual rather than predicted severity (EU 2010). In UK legislation, a regulated procedure means any procedure which may have the effect of causing the animal a level of pain, suffering, distress or lasting harm (PSDLH) equivalent to, or higher than, that caused by the introduction of a needle in accordance with good veterinary practices. This definition would also be applicable to decapods, albeit perhaps refined somewhat to reflect the highly calcified exoskeleton of many species. Furthermore, procedures may be assigned across four severity categories, with specific (vertebrate-centric) examples provided in the legislation (EU 2010). For example, procedures defined by an upper limit on blood sample volume, or duration of food withdrawal, would be challenging to apply to decapods, which have an open circulatory system, and are poikilothermic with potentially low energy expenditure.

Nevertheless, general assignment of procedure severity category may occur on a case-by-case basis within specific studies, based on animal life history, the nature and cumulative PSDLH caused by procedures, preventing natural behaviour, and humane endpoints (EU 2010). Should decapods become protected, the assignment process will require good understanding of potential welfare indicators that can be used to evaluate likely severity of any proposed procedure. These may be radically different, or indeed rather subtle, compared to vertebrates (Coates & Söderhäll Reference Coates and Söderhäll2021. For instance, cortisol is often used as a stress biomarker in vertebrates, however decapods rely on an alternative hyperglycaemic response system (Lorenzon Reference Lorenzon2005; Sadoul & Geffroy Reference Sadoul and Geffroy2019) with serum glucose and lactate also likely established indicators of physiological stress (Conneely & Coates Reference Conneely and Coates2024).

Operational welfare indicators are often relatively simple, visual observations that infer the welfare state of an animal or population. Decapods show primary responses to stressors such as behavioural defensive postures, increased locomotion or shelter-seeking (Stoner Reference Stoner2012). Should these fail, the animal can release at least one appendage at a predefined breakage plane in the carapace (autotomy) to promote escape whilst maintaining homeostasis (Fleming et al. Reference Fleming, Muller and Bateman2007). Therefore, autotomy could be used as a welfare indicator during regulated procedures. Alternatively, some behavioural changes have been recorded during the onset of morbidity (e.g. Brown crab [Cancer pagurus]; Barrento et al. Reference Barrento, Marques, Vaz-Pires and Nunes2012). These have been used to define vitality indices and include environmental parameters, creating reflex action mortality predictors (RAMPs) to predict morbidity and mortality (e.g. for the Norway lobster [Nephrops norvegicus] and blue crab [Calinectes sapidus] (Albalat et al. Reference Albalat, Sinclair and Neil2017; Walters et al. Reference Walters, Crowley, Gandy and Behringer2022). Further, decapod integument can change according to infection status, albeit in a limited number of diseases, such as shell disease or Sacculina spp infection (Shields Reference Shields2012). Therefore, efforts could be made to extend these approaches to assist assignment of procedure severity.

Anaesthesia and toward ethical killing

Appropriate methods of anaesthesia and ethical killing are fundamental within animal scientific legislation, encompassing pain control during severe procedures, stock (non-experimental) management, and to euthanase experimental animals during or following experimentation (EU 2010). Satisfactory protection of decapods under scientific legislation would therefore require extension of similar protocols. Whilst historically it has been challenging to confirm efficacious and ethical anaesthesia of decapods, due to their differing neural system anatomy, neurotransmitter repertoire and hard exoskeleton (Belanger Reference Belanger2005; Walters Reference Walters2018), recent reviews of compounds and techniques used for decapod anaesthesia have been published (de Souza Valente Reference de Souza Valente2022; Wahltinez et al. Reference Wahltinez, Stacy, Hadfield, Harms and Lewbart2022) and a decision support tool is now available (Rottlant et al. Reference Rottlant, Llonch, García Del Arco, Chic, Flecknell and Sneddon2023).

Ethical killing of decapods may occur following a scientific procedure, or be termed euthanasia (to end suffering), or slaughter (for consumption) across commercial, domestic and scientific sectors. However, existing methods for stunning and slaughter of decapods are varied (Yue Reference Yue2008; Conte et al. Reference Conte, Voslarova, Vecerek, Elwood, Coluccio, Pugliese and Passantino2021) with many considered inhumane by the EU (EFSA 2005). Under scientific legislation, appropriate euthanasia methods are taxon-specific, require training and are stated plainly for some taxa, such as fish but not cephalopods (EU 2010). Norwegian and New Zealand legislations require decapods to be rendered insensible or stunned before imminent destruction (Norwegian Government 2009; New Zealand Government 2018). Decapod euthanasia under Swiss legislation follows a detailed precautionary approach, demanding training and specifying electrical stunning prior to additional boiling, splitting or spiking, and differentiating the optimal method according to the particular body plans of the decapod group (Swiss Federation 2020). Data so far indicate that electrical stunning might be effective for some species (Roth & Øines Reference Roth and Øines2010; Roth & Grimsbø Reference Roth and Grimsbø2013; Neil et al. Reference Neil, Albalat and Thompson2022, Reference Neil, Putyora and Albalat2024). However, further work is needed in this area, particularly in terms of confirming the level of insensitivity achieved using decapod-equivalent electroencephalogram (EEG) data and defining animal-based indicators that can be used as proxies of insensitivity by operators.

Animal welfare implications

Decapod crustaceans are increasingly becoming the subject of welfare and ethical considerations during scientific research. Recent reviews on this topic have suggested that decapods are sentient beings. Existing legislation, originally designed to protect vertebrates during scientific research, could soon be broadened to include decapods. However, precedence with other aquatic animals and invertebrates (such as cephalopods) shows that inclusion into legislation is poorly supported in terms of fundamental requirements such as general care and euthanasia. Additionally, much of the terminology used in such legislation is not compatible with the general biology of decapods or suffers from a lack of knowledge. This horizon paper considers the challenges of adding decapods into extant scientific legislation, and potential ways forward to practically deliver improved decapod welfare and scientific research.

Conclusion and ways forward

Whilst the concept of the 3Rs is applicable to scientific endeavour and associated welfare of decapods, this horizon paper has highlighted practical issues that could arise should decapods be included within extant legislation regulating animals in science. Whilst there are encouraging practical developments in scientific and veterinary fields (e.g. Refinement; culling) and transferable knowledge from commercial sectors (e.g. operational welfare indicators; precision aquaculture), there are important knowledge gaps remaining and a lack of best code practice from an animal welfare perspective. Indeed, for those countries that do protect decapods, disparity remains (for example, the developmental stage that decapods are protected, husbandry training and requirements, and precise method of euthanasia).

While it is uncertain whether decapods will be incorporated into active legislation, precedence, best practice and experiences from other nations may be worth considering. For example, in one Australian territory, licencing of scientific activities involving animals includes discrete fieldwork activities, such as teaching, in addition to on-premises and breeding licences (Victorian Government Reference Government1986; Timoshanko et al. Reference Timoshanko, Marston and Lidbury2016; Wallis Reference Wallis2023). Further, a scientific code of conduct in Australia aims to harmonise standards, with varying degrees of joint self-regulation and enforced regulation between states. Defined as ‘co-regulation’, this governance approach could be a further method for scientists to reasonably ensure decapod care and welfare (Timoshanko et al. Reference Timoshanko, Marston and Lidbury2016). Research codes of conduct also aim to support ethical research using animals within and between Australia and New Zealand (Ministry for Primary Industries 2022; ANZCART 2024) and Malaysia (Wallis Reference Wallis2023). Decapod science may be considered niche in Norway, however care and welfare aims are supported and underpinned by collaboration between scientists, governing bodies, and the aquaculture sector (Norwegian Government 2009; A Powell, A-L Agnalt, K Heasman, A Albalat, personal observation 2023). Research organisations may also adhere to internal voluntary ethical standards surrounding decapod use which exceed national or territorial statutory laws, such as CSIRO in Australia (Rowe Reference Rowe2022).

From the Discussion in this horizon paper, inclusion of decapod taxa into scientific regulation needs careful thought if the aim is to significantly improve welfare. Collaboration between stakeholders, including scientists, governments and NGOs, will help ensure regulatory practicality and efficacy. This would preferably involve learning from the experience of other nations, and historical precedence, to harmonise any legislation. We hope that this overview underlines the points to consider should decapods be included in extant legislation and encourages government to consider research priorities to ensure maximum impact in any policy changes. This will foster better science whilst optimising animal care and welfare – the ultimate aims of the 3Rs and progressive scientific governance.

Acknowledgements

The authors would like to thank Professor Douglas Neil for his suggestions to the manuscript and no funding is associated with this manuscript.

Competing interest

None.

Footnotes

Author contributions: Conceptualisation: AP, AA; Project administration: AP; Writing – original draft: AP, A-LA, KH, AA; Writing – review & editing: AP, A-LA, KH, AA

References

Albalat, A, Sinclair, S and Neil, D 2017 Validation of a vigour index for trawl-caught Norway lobsters (Nephrops norvegicus) destined for the live market: Underlying links to both physiological condition and survivability. Fisheries Research 191: 2529. https://doi.org/10.1016/j.fishres.2017.02.016CrossRefGoogle Scholar
Albalat, A, Zacarias, S, Coates, CJ, Neil, DM and Rey Planellas, S 2022 Welfare in farmed decapod crustaceans, with particular reference to Penaeus vannamei. Frontiers in Marine Science 9: 886024. https://doi.org/10.3389/fmars.2022.886024CrossRefGoogle Scholar
Andrews, PLR, Darmaillacq, AS, Dennison, N, Gleadall, IG, Hawkins, P, Messenger, JB, Osorio, D, Smith, VJ and Smith, JA 2013 The identification and management of pain, suffering and distress in cephalopods, including anesthesia, analgesia and humane killing. Journal of Experimental Marine Biology and Ecology 447: 4664. https://doi.org/10.1016/j.jembe.2013.02.010CrossRefGoogle Scholar
Anon 2012 Guidelines for the treatment of animals in behavioural research and teaching. Animal Behaviour 83(1): 301309. https://doi.org/10.1016/j.anbehav.2011.10.031CrossRefGoogle Scholar
ANZCCART 2024 Australian and New Zealand Council for the Care of Animals in Research and Teaching. https://www.anzccart.org.nz/ (accessed 16 September 2024).Google Scholar
Austrian Federal Chancellery 2004 Federal Act on the Protection of Animals. https://www.animallaw.info/sites/default/files/statprotection_of_animals.pdf (accessed 16 September 2024).Google Scholar
Barki, A, Jones, C and Karplus, I 2010 Chemical communication and aquaculture of Decapod crustaceans: Needs, problems, and possible solutions. In: Breithaupt, T and Thiel, M (eds) Chemical Communication in Crustaceans. Springer: New York, NY, USA. https://doi.org/10.1007/978-0-387-77101-4_25Google Scholar
Barr, S and Elwood, RW 2024 Effects of acetic acid and morphine in shore crabs, Carcinus maenas: Implications for the possibility of pain in Decapods. Animals 14(11): 1705. https://doi.org/10.3390/ani14111705CrossRefGoogle ScholarPubMed
Barrento, SI, Marques, A, Vaz-Pires, P and Nunes, ML 2012 Physiological changes during simulated live transport of Cancer pagurus and recovery in holding tanks. Aquaculture Research 43: 14151426. https://doi.org/10.1111/j.1365-2109.2011.02943.xCrossRefGoogle Scholar
Barrett, CJ, Bradley, K and Brazier, A 2023 Common, curled or miscellaneous: The need for species-specific recordings of octopuses to inform stock assessments. Marine Policy 153: 105632. https://doi.org/10.1016/j.marpol.2023.105632CrossRefGoogle Scholar
Belanger, JH 2005 Contrasting tactics in motor control by vertebrates and arthropods. Integrative and Comparative Biology 45(4): 672678. https://doi.org/10.1093/icb/45.4.672CrossRefGoogle ScholarPubMed
Birch, J 2017 Animal sentience and the precautionary principle. Animal Sentience 2(16). https://doi.org/10.51291/2377-7478.1200CrossRefGoogle Scholar
Birch, J, Burn, C, Schnell, A, Browning, H and Crump, A 2021 Review of the evidence of sentience in cephalopod molluscs and decapod crustaceans. LSE Consulting, LSE Enterprise Ltd, The London School of Economics and Political Science, London, UK. https://www.lse.ac.uk/News/News-Assets/PDFs/2021/Sentience-in-Cephalopod-Molluscs-and-Decapod-Crustaceans-Final-Report-November-2021.pdf (accessed 13 September 2024).Google Scholar
Briffa, M 2022a Sentience in decapods: an open question. Animal Sentience 7(32): 19. https://doi.org/10.51291/2377-7478.1740CrossRefGoogle Scholar
Briffa, M 2022b When should we ascribe sentience to animals? A commentary on ‘Hermit crabs, shells and sentience’ (Elwood 2022). Animal Cognition 25: 13751380. https://doi.org/10.1007/s10071-022-01633-5CrossRefGoogle ScholarPubMed
Browning, H 2023 Improving welfare assessment in aquaculture. Frontiers in Veterinary Lobster hatcheries and stocking programmes : An introductory manual.Science 10: 1060720. https://doi.org/10.3389/fvets.2023.1060720Google Scholar
Burton, CA 2003 Sea Fish Industry Authority Aquaculture Development Service. Seafish Report, SR552. https://www.seafish.org/document/?id=0121143b-bca6-4b02-980d-6d56f244227f (accessed 16 September 2024).Google Scholar
Castillo-Juárez, H, Campos-Montes, GR, Caballero-Zamora, A and Montaldo, HH 2015 Genetic improvement of Pacific white shrimp (Penaeus [Litopenaeus] vannamei): perspectives for genomic selection. Frontiers in Genetics 6: 93. https://doi.org/10.3389/fgene.2015.00093CrossRefGoogle ScholarPubMed
CITES (Convention on International Trade in Endangered Species of Wild Fauna and Flora) 2024 Species Appendices. https://cites.org/eng/app/appendices.php (accessed 13 September 2024).Google Scholar
Coates, CJ and Söderhäll, K 2021 The stress-immunity axis in shellfish. Journal of Invertebrate Pathology 186: 107492. https://doi.org/10.1016/j.jip.2020.107492CrossRefGoogle ScholarPubMed
Codecasa, E, Pageat, P, Marcet-Rius, M and Cozzi, A 2021 Legal frameworks and controls for the protection of research animals: A focus on the Animal Welfare Body with a French case study. Animals 11(3): 695. https://doi.org/10.3390/ani11030695CrossRefGoogle ScholarPubMed
Conte, F, Voslarova, E, Vecerek, V, Elwood, RW, Coluccio, P, Pugliese, M and Passantino, A 2021 Humane slaughter of edible decapod crustaceans. Animals 11(4): 1089. https://doi.org/10.3390/ani11041089CrossRefGoogle ScholarPubMed
Conneely, EA and Coates, CJ 2024 Meta‐analytic assessment of physiological markers for decapod crustacean welfare. Fish and Fisheries 25(1): 134150. https://doi.org/10.1111/faf.12798CrossRefGoogle Scholar
Cooper, JJ, Ambrose, T and Ventura, BA 2022 Decapods as food, companions and research animals: Legal impact of ascribing sentience. Animal Sentience 32(27). https://doi.org/10.51291/2377-7478.1759Google Scholar
Crump, A, Fischer, B, Arnott, G, Birch, J, Briffa, M, Browning, H, Coates, C, Elwood, R, Khan, N, Thanrar, U and Barrett, M 2024 Guidelines for protecting and promoting decapod crustacean welfare in research. Insect Welfare Research Society. https://irep.ntu.ac.uk/id/eprint/50897/ (accessed 13 September 2024).Google Scholar
De Grave, S, Decock, W, Dekeyzer, S, Davie, PJF, Fransen, CHJM, Boyko, CB, Poore, GCB, Macpherson, E, Ahyong, ST, Crandall, KA, de Mazancourt, V, Osawa, M, T-Y, Chan, Ng, PKL, Lemaitre, R, van der Meij, SET and Santos, S 2023 Benchmarking global biodiversity of decapod crustaceans (Crustacea: Decapoda). Journal of Crustacean Biology 43(3): ruad042. https://doi.org/10.1093/jcbiol/ruad042CrossRefGoogle Scholar
de Souza Valente, C 2022 Anaesthesia of decapod crustaceans. Veterinary and Animal Science 16: 100252. https://doi.org/10.1016/j.vas.2022.100252CrossRefGoogle ScholarPubMed
Diggles, BK, Arlinghaus, R, Browman, HI, Cooke, SJ, Cooper, RL, Cowx, IG, Derby, CD, Derbyshire, SW, Hart, PJB, Jones, B, Kasumyan, AO, Key, B, Pepperell, JG, Rogers, DC, Rose, JD, Schwab, A, Skiftesvik, AB, Stevens, D, Shields, JD and Watson, C 2023 Reasons to be skeptical about sentience and pain in fishes and aquatic invertebrates. Reviews in Fisheries Science and Aquaculture 32: 127150. https://doi.org/10.1080/23308249.2023.2257802CrossRefGoogle Scholar
Domart-Coulon, I and Blanchoud, S 2022 From primary cell and tissue cultures to aquatic invertebrate cell lines: An updated overview. In: Ballarin, L, Rinkevich, B and Hobmayer, B (eds) Advances in Aquatic Invertebrate Stem Cell Research: From Basic Research to Innovative Applications pp 164. MDPI: Basel, Switzerland. https://doi.org/10.3390/books978-3-0365-1635-6Google Scholar
Dunn, R 2021 Brexit: A boon or a curse for animals used in scientific procedures? Animals 11(6): 1547. https://doi.org/10.3390/ani11061547CrossRefGoogle ScholarPubMed
Eggel, M and Camendzind, S 2020 Authorization of animal research projects – a comparison of harm concepts in the Swiss Animal Welfare Act and the European Directive 2010/63/EU. Berlin and Munich Veterinary Weekly 13: 3. https://doi.org/10.2376/0005-9366-19057Google Scholar
EFSA (European Food Safety Authority) 2005 Scientific Panel on Animal Health and Welfare: Opinion on the Aspects of the biology and welfare of animals used for experimental and other scientific purposes. The EFSA Journal 292: 146. https://doi.org/10.2903/j.efsa.2005.292Google Scholar
Elwood, RW 2022 Hermit crabs, shells, and sentience. Animal Cognition 25: 12411257. https://doi.org/10.1007/s10071-022-01607-7CrossRefGoogle ScholarPubMed
Elwood, RW and Ingle, RW 2024 Decapod crustaceans. In: Richardson, C, Golledge, H (eds) The UFAW Handbook on the Care and Management of Laboratory and Other Research Animals, Ninth Edition pp 9931011. Wiley-Blackwell: London, UK.Google Scholar
Englund, MD and Cronin, KA 2023 Choice, control, and animal welfare: definitions and essential inquiries to advance animal welfare science. Frontiers in Veterinary Science 10: 1250251. https://doi.org/10.3389/fvets.2023.1250251CrossRefGoogle ScholarPubMed
EU (European Union) 2007 Treaty of Lisbon – Amending the treaty on European Union and the treaty establishing the European Community. 2007/C 306/01. https://eur-lex.europa.eu/eli/treaty/lis/sign (accessed 13 September 2024).Google Scholar
EU (European Union) 2010 European Parliament and Council of the European Union Directive 2010/63/EU of 22 September 2010 on the protection of animals used for scientific purposes. Office of the Journal of the European Union pp 3379. https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=celex%3A32010L0063 (accessed 13 September 2024).Google Scholar
FAO 2002 Farming freshwater prawns. A manual for the culture of the giant river prawn (Macrobrachium rosenbergii). FAO Fisheries Technical Paper, No 428. FAO: Rome, Italy.Google Scholar
FAO 2007 Improving Penaeus monodon hatchery practices. Manual based on experience in India. FAO Fisheries Technical Paper, No 446. FAO: Rome, Italy.Google Scholar
FAO 2022 The State of World Fisheries and Aquaculture 2022. Towards Blue Transformation. FAO: Rome, Italy.Google Scholar
Fleming, PA, Muller, D and Bateman, PW 2007 Leave it all behind: a taxonomic perspective of autotomy in invertebrates. Biological Reviews 82(3): 481510. https://doi.org/10.1111/j.1469-185X.2007.00020.xCrossRefGoogle ScholarPubMed
Fotedar, S and Evans, L 2011 Health management during handling and live transport of crustaceans: a review. Journal of Invertebrate Pathology 106(1): 143152. https://doi.org/10.1016/j.jip.2010.09.011CrossRefGoogle ScholarPubMed
Hamed, I, Özogul, F and Regenstein, JM 2016 Industrial applications of crustacean by-products (chitin, chitosan, and chitooligosaccharides): A review. Trends in Food Science & Technology 48: 4050. https://doi.org/10.1016/j.tifs.2015.11.007CrossRefGoogle Scholar
Haubrock, PJ, Oficialdegui, F, Zeng, Y, Patoka, J, Yeo, DC and Kouba, A 2021 The red claw crayfish: A prominent aquaculture species with invasive potential in tropical and subtropical biodiversity hotspots. Reviews in Aquaculture 13(3): 14881530. https://doi.org/10.1111/raq.12531CrossRefGoogle Scholar
Hinchcliffe, J, Agnalt, AL, Daniels, CL, Drengstig, AR, Lund, I, McMinn, J and Powell, A 2022 European lobster Homarus gammarus aquaculture: Technical developments, opportunities and requirements. Reviews in Aquaculture 14(2): 919937. https://doi.org/10.1111/raq.12634CrossRefGoogle Scholar
Ingle, RW 1995 UFAW Handbook on the Care and Management of Decapod Crustaceans in Captivity. Universities Federation for Animal Welfare: Wheathampstead, Herts, UK.Google Scholar
Jennings, S, Stentiford, GD, Leocadio, AM, Jeffery, KR, Metcalfe, JD, Katsiadaki, I, Auchterlonie, NA, Mangi, SC, Pinnegar, JK, Ellis, T, Peeler, EJ, Luisetti, T, Baker-Austin, C, Brown, M, Catchpole, TL, Clyne, FJ, Dye, SR, Edmonds, NJ, Hyder, K, Lee, J, Lees, DN, Morgan, OC, O’Brien, CM, Oidtmann, B, Posen, PE, Santos, AR, Taylor, NGH, Turner, AD, Townhill, BL and Verner-Jeffreys, DW 2016 Aquatic food security: insights into challenges and solutions from an analysis of interactions between fisheries, aquaculture, food safety, human health, fish and human welfare, economy and environment. Fish and Fisheries 17(4): 893938. https://doi.org/10.1111/faf.12152CrossRefGoogle Scholar
Johnson, L, Coates, CJ, Albalat, A, Todd, K and Neil, D 2016 Temperature – dependent morbidity of “nicked” edible crab, Cancer pagurus. Fisheries Research 175: 127131. https://doi.org/10.1016/j.fishres.2015.11.024CrossRefGoogle Scholar
Law of the Republic of Indonesia 2009 No 18, Chapter VI, Veterinary Public Health and Animal Welfare; Part 2, Animal Welfare; Articles 66–67. https://faolex.fao.org/docs/pdf/ins98701.pdf (accessed 13 September 2024).Google Scholar
Li, X, Liu, R, Wang, Z, Zheng, G, Lv, J, Fan, L, Guo, Y and Gao, Y 2023 Automatic Penaeus monodon larvae counting via Equal Keypoint Regression with smartphones. Animals 13(12): 2036. https://doi.org/10.3390/ani13122036CrossRefGoogle ScholarPubMed
Liu, L, Yang, H, Cai, Y, Cao, Q, Sun, L, Wang, Z, Li, W, Liu, G, Lee, PW and Tang, Y 2019 In silico prediction of chemical aquatic toxicity for marine crustaceans via machine learning. Toxicology Research 8(3): 341352. https://doi.org/10.1039/c8tx00331aCrossRefGoogle ScholarPubMed
Lorenzon, S 2005 Hyperglycaemic stress response in crustacea. Survival Journal 2: 2.Google Scholar
MacArthur Clark, J 2018 The 3Rs in research: a contemporary approach to replacement, reduction and refinement. British Journal of Nutrition 120(S1): S1S7. https://doi.org/10.1017/S0007114517002227CrossRefGoogle ScholarPubMed
Marinou, KA and Dontas, IA 2023 European Union legislation for the welfare of animals used for scientific purposes: Areas identified for further discussion. Animals 13(14): 2367. https://doi.org/10.3390/ani13142367CrossRefGoogle ScholarPubMed
Marshall, LJ, Constantino, H and Seidle, T 2022 Phase-in to phase-out-targeted, inclusive strategies are needed to enable full replacement of animal use in the European Union. Animals 12(7): 863. https://doi.org/10.3390/ani12070863CrossRefGoogle ScholarPubMed
Ministry for Primary Industries 2022 Good Practice Guide for the use of animals in research, testing and teaching. https://www.mpi.govt.nz/dmsdocument/33585-Good-Practice-Guide-for-the-use-of-animals-in-research-testing-and-teaching (accessed 13 September 2024).Google Scholar
Mykles, DL and Hui, JHL 2015 Neocaridina denticulata: A Decapod crustacean model for functional Genomics. Integrative and Comparative Biology 55(5): 891897. https://doi.org/10.1093/icb/icv050CrossRefGoogle ScholarPubMed
Narshi, TM, Free, D, Justice, WSM, Smith, SJ and Wolfensohn, S 2022 Welfare assessment of invertebrates: Adapting the Animal Welfare Assessment Grid (AWAG) for zoo decapods and cephalopods. Animals 12(13): 1675. https://doi.org/10.3390/ani12131675CrossRefGoogle ScholarPubMed
Neil, DM, Albalat, A and Thompson, J 2022 The effects of electrical stunning on the nervous activity and physiological stress response of a commercially important decapod crustacean, the brown crab Cancer pagurus L. Plos One 17(7): e0270960. https://doi.org/10.1371/journal.pone.0270960CrossRefGoogle ScholarPubMed
Neil, DM, Putyora, E and Albalat, A 2024 Towards the humane slaughter of decapod crustaceans: identifying the most effective indicators of insensibility following electrical stunning. Frontiers in Animal Science 5. https://doi.org/10.3389/fanim.2024.1378350CrossRefGoogle Scholar
Norwegian Government 2009 Animal Welfare Act. https://www.regjeringen.no/en/dokumenter/animal-welfare-act/id571188/ (accessed 13 September 2024).Google Scholar
National Research Ethics Committee 2015 Research ethical guidelines for natural sciences and technology. https://www.forskningsetikk.no/retningslinjer/nat-tek/forskningsetiske-retningslinjer-for-naturvitenskap-og-teknologi/ (accessed 13 September 2024).Google Scholar
New Zealand Government 1999 Animal Welfare Act. Parliamentary Counsel Office: Wellington, New Zealand. https://www.legislation.govt.nz/act/public/1999/0142/latest/whole.html#DLM50284Google Scholar
New Zealand Government 2018 Animal Welfare (Care and Procedures) Regulations. NZ Government: Wellington, New Zealand https://www.legislation.govt.nz/regulation/public/2018/0050/latest/whole.html (accessed 16 September 2024).Google Scholar
Passantino, A, Elwood, RW and Coluccio, P 2021 Why protect decapod crustaceans used as models in biomedical research and in ecotoxicology? Ethical and legislative considerations. Animals 11(1): 73. https://doi.org/10.3390/ani11010073CrossRefGoogle ScholarPubMed
Pedrazzani, AS, Cozer, N, Quintiliano, MH, Tavares, CPDS, da Silva, UDAT and Ostrensky, A 2023 Non-invasive methods for assessing the welfare of farmed white-leg shrimp (Penaeus vannamei). Animals 13(5): 807. https://doi.org/10.3390/ani13050807CrossRefGoogle ScholarPubMed
Percie du Sert, N, Hurst, V, Ahluwalia, A, Alam, S, Avey, MT, Baker, M, Browne, WJ, Clark, A, Cuthill, IC, Dirnagl, U, Emerson, M, Garner, P, Holgate, ST, Howells, DW, Karp, NA, Lazic, SE, Lidster, K, MacCallum, CJ, Macleod, M, Pearl, EJ, Petersen, OH, Rawle, F, Reynolds, P, Rooney, K, Sena, ES, Silberberg, SD, Steckler, T and Würbel, H 2020 The ARRIVE guidelines 2.0: Updated guidelines for reporting animal research. PLoS Biology 18(7): e3000410. https://doi.org/10.1177/0271678X20943823CrossRefGoogle ScholarPubMed
Perkins, K 2021 Can aquatic invertebrates within public aquaria fit the Five Domain Welfare Model? Journal of Applied Animal Ethics Research 3(2): 181204. https://doi.org/10.1163/25889567-bja10025CrossRefGoogle Scholar
Powell, A, Barrento, S and Cowing, DM 2020 Management and handling of commercial crustaceans. In: Lovrich, G and Thiel, M (eds) The Natural History of the Crustacea: Fisheries and Aquaculture pp 495523. Oxford University Press: Oxford, UK.Google Scholar
Powell, A, Cowing, DM, Scolding, JWS, Shepherd-Waring, T, Eriksson, SP, Lupatsch, I, Johnson, ML, Shields, RJ and Gowland, D 2015 Nephrops norvegicus: Hatchery Handbook. Patent Application Number: GB1509666.2. https://www.researchgate.net/publication/337110913_Nephrops_norvegicus_Hatchery_handbook (accessed 13 September 2024).Google Scholar
Retnam, L, Chatikavanij, P, Kunjara, P, Paramastri, YA, Goh, YM, Hussein, FN, Mutalib, AR and Poosala, S 2016 Laws, Regulations, Guidelines and Standards for Animal Care and Use for Scientific Purposes in the Countries of Singapore, Thailand, Indonesia, Malaysia, and India. ILAR Journal 57(3): 312323. https://doi.org/10.1093/ilar/ilw038Google ScholarPubMed
Romano, N and Zeng, C 2017 Cannibalism of decapod crustaceans and implications for their aquaculture: a review of its prevalence, influencing factors, and mitigating methods. Reviews in Fisheries Science & Aquaculture 25(1): 4269. https://doi.org/10.1080/23308249.2016.1221379CrossRefGoogle Scholar
Roth, B and Grimsbø, E 2013 Nofima Report 18/2013 Electrical Stunning of Edible Crabs. https://nofima.brage.unit.no/nofima-xmlui/handle/11250/284020 (accessed 13 September 2024).Google Scholar
Roth, B and Øines, S 2010 Stunning and killing of edible crabs (Cancer pagurus). Animal Welfare 19(3): 287294. https://doi.org/10.1017/S0962728600001676CrossRefGoogle Scholar
Rottlant, G, Llonch, P, García Del Arco, JA, Chic, Ò, Flecknell, P and Sneddon, LU 2023 Methods to induce analgesia and anesthesia in crustaceans: A supportive decision tool. Biology 12(3): 387. https://doi.org/10.3390/biology12030387CrossRefGoogle Scholar
Rowan, AN, D’Silva, JM, Duncan, IJH and Palmer, N 2021 Animal sentience: history, science, and politics. Animal Sentience 31(1). https://doi.org/10.51291/2377-7478.1697Google Scholar
Rowe, A 2022 Why should scientific research involving decapod crustaceans require ethical review? ANZCCART 2022 Conference; 26–28 July 2022; Melbourne, VIC, Australia.Google Scholar
Rowley, AF and Powell, A 2007 Invertebrate immune systems-specific, quasi-specific, or nonspecific? Journal of Immunology 179: 72097214. https://doi.org/10.4049/jimmunol.179.11.7209CrossRefGoogle ScholarPubMed
Russell, WMS and Burch, RL 1959 The Principles of Humane Experimental Technique. Methuen: London, UK.Google Scholar
Sadoul, B and Geffroy, B 2019 Measuring cortisol, the major stress hormone in fishes. Journal of Fish Biology 94(4): 540555. https://doi.org/10.1111/jfb.13904CrossRefGoogle ScholarPubMed
Scott Quackenbush, L 2001 Yolk synthesis in the marine shrimp Penaeus vannamei. American Zoologist 41(3): 458464. https://doi.org/10.1093/icb/41.3.458Google Scholar
Shields, JD 2012 The impact of pathogens on exploited populations of decapod crustaceans. Journal of Invertebrate Pathology 110(2): L 211224. https://doi.org/10.1016/j.jip.2012.03.011CrossRefGoogle ScholarPubMed
Smith, AJ, Clutton, RE, Lilley, E, Hansen, KEA and Brattelid, T 2018 PREPARE: guidelines for planning animal research and testing. Laboratory Animals 52(2): 135141. https://doi.org/10.1177/0023677217724823CrossRefGoogle ScholarPubMed
Smith, JA, Andrews, PLR, Hawkins, P, Louhimies, S, Ponte, G and Dickel, L 2013 Cephalopod research and EU Directive 2010/63/EU: Requirements, impacts and ethical review. Journal of Experimental Marine Biology and Ecology 447: 3145 https://doi.org/10.1016/j.jembe.2013.02.009CrossRefGoogle Scholar
Stentiford, GD, Neil, DM, Peeler, EJ, Shields, JD, Small, HJ, Flegel, TW, Vlak, JM, Jones, B, Morado, F, Moss, S, Lotz, J, Bartholomay, L, Behringer, DC, Hauton, C and Lightner, DV 2012 Disease will limit future food supply from the global crustacean fishery and aquaculture sectors. Journal of Invertebrate Pathology 110(2): 141157. https://doi.org/10.1016/j.jip.2012.03.013CrossRefGoogle ScholarPubMed
Streisinger, G, Walker, C, Dower, N, Knauber, D and Singer, F 1981 Production of clones of homozygous diploid zebra fish (Brachydanio rerio). Nature 291: 293296. https://doi.org/10.1038/291293a0CrossRefGoogle ScholarPubMed
Stoner, AW 2012 Assessing stress and predicting mortality in economically significant crustaceans. Reviews in Fisheries Science 20(3): 111135. https://doi.org/10.1080/10641262.2012.689025CrossRefGoogle Scholar
Swiss Federal Council 2005 Animal Welfare Act. https://www.fedlex.admin.ch/eli/cc/2008/414/en (accessed 13 September 2024).Google Scholar
Swiss Federal Council 2008 Animal Protection Ordinance. https://www.blv.admin.ch/blv/en/home/tiere/tierschutz.html (accessed 13 September 2024).Google Scholar
Swiss Federation 2020 Animal Welfare Technical Information no. 16.8. Correct euthanasia of decapods. https://www.blv.admin.ch/blv/en/home/tiere/tierschutz/heim-und-wildtierhaltung.html (accessed 13 September 2024).Google Scholar
Tannenbaum, J and Bennett, BT 2015 Russell and Burch’s 3Rs then and now: the need for clarity in definition and purpose. Journal of the American Association for Laboratory Animal Science 54(2): 120132.Google ScholarPubMed
Timoshanko, AC, Marston, H and Lidbury, BA 2016 Australian regulation of animal use in science and education: A critical appraisal. ILAR Journal 57(3): 324332. https://doi.org/10.1093/ilar/ilw015CrossRefGoogle ScholarPubMed
EXP, Toh, Gan, LX, Yeo, DCJ 2022 A global overview of climate change impacts on freshwater decapods: substantial research gaps across taxa and biogeographic regions Journal of Crustacean Biology 42(1). https://doi.org/10.1093/jcbiol/ruab088Google Scholar
UK Government 1986 Animals (Scientific Procedures) Act 1986. https://www.legislation.gov.uk/ukpga/1986/14/contents (accessed 13 September 2024).Google Scholar
UK Government 1993 The Animals (Scientific Procedures) Act (Amendment) Order 1993. http://www.legislation.gov.uk/uksi/1993/2103/made (accessed 13 September 2024).Google Scholar
UK Government 2014a Working to reduce the use of animals in scientific research. https://assets.publishing.service.gov.uk/media/5a7c79b1e5274a559005a1ee/bis-14-589-working-to-reduce-the-use-of_animals-in-research.pdf (accessed 13 September 2024).Google Scholar
UK Government 2014b Code of practice for the housing and care of animals bred, supplied or used for scientific purposes. https://www.gov.uk/government/publications/code-of-practice-for-the-housing-and-care-of-animals-bred-supplied-or-used-for-scientific-purposes (accessed 13 September 2024).Google Scholar
UK Government 2022a Animal Welfare (Sentience) Act 2022. https://www.legislation.gov.uk/ukpga/2022/22/enacted (accessed 13 September 2024).Google Scholar
Vogt, G 2018 Investigating the genetic and epigenetic basis of big biological questions with the parthenogenetic marbled crayfish: a review and perspectives. Journal of Bioscences 43: 189223. https://doi.org/10.1007/s12038-018-9741-xCrossRefGoogle ScholarPubMed
Wahltinez, SJ, Stacy, NI, Hadfield, CA, Harms, CA, Lewbart, GA, Newton A and Nunamaker EA 2022 Perspective: Opportunities for advancing aquatic invertebrate welfare. Frontiers in Veterinary Science 9: 973376. https://doi.org/10.3389/fvets.2022.973376CrossRefGoogle Scholar
Wallis, R 2023 Animal ethics in biology teaching and research in selected Asian countries. Jurnal Pendidikan Biologi Indonesia 9(2): 115121. https://doi.org/10.22219/jpbi.v9i2.25263Google Scholar
Wallis, R and Katayama, N 2022 Using live animals in biology teaching and research–a comparison between Australia and Japan. The Asian Journal of Biology Education 14: 816. https://doi.org/10.57443/ajbe.14.0_8Google Scholar
Walters, ET 2018 Nociceptive biology of molluscs and arthropods: Evolutionary clues about functions and mechanisms potentially related to pain. Frontiers in Physiology 9: 1049. https://doi.org/10.3389/fphys.2018.01049CrossRefGoogle ScholarPubMed
Walters, EA, Crowley, CE, Gandy, RL and Behringer, DC 2022 A reflex action mortality predictor (RAMP) for commercially fished blue crab Callinectes sapidus in Florida. Fisheries Research 247: 106188. https://doi.org/10.1016/j.fishres.2021.106188CrossRefGoogle Scholar
Wickens, S 2022 Review of the evidence of sentience in cephalopod molluscs and decapod crustaceans. Animal Welfare 31(1): 155156. https://doi.org/10.1017/S0962728600009866CrossRefGoogle Scholar
Wilson, CH, Wyeth, RC, Spicer, JI and McGaw, IJ 2022 Effect of animal stocking density and habitat enrichment on survival and vitality of wild green shore crabs, Carcinus maenas, maintained in the laboratory. Animals 12(21): 2970. https://doi.org/10.3390/ani12212970CrossRefGoogle ScholarPubMed
Yin, J, Li, JY, Craig, NJ and Su, L 2022 Microplastic pollution in wild populations of decapod crustaceans: A review. Chemosphere 291(2): 132985. https://doi.org/10.1016/j.chemosphere.2021.132985CrossRefGoogle ScholarPubMed
Yue, S 2008 The welfare of crustaceans at slaughter. Agribusiness Reports pp 5.Google Scholar