Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72(S1): e58228, marzo 2024 (Publicado Mar. 01, 2024)

Ethics and Welfare in invertebrates:

a stepping-stone to research and animal production

Augusto C. Crespi-Abril1,3*; https://orcid.org/0000-0002-6278-2787

Tamara Rubilar2,3; https://orcid.org/0000-0003-1728-3273

1. Instituto Patagónico del Mar (IPaM), Universidad Nacional del a Patagonia San Juan Bosco (UNPSJB), Boulevard

Brown 2915, Puerto Madryn 9120, Argentina; crespi@cenpat-conicet.gob.ar (*Correspondence)

2. Laboratorio de Química de Organismos Marinos (LabQuiOM), Instituto Patagónico del Mar (IPAM), Facultad de

Ciencias Naturales y Ciencias de la Salud, Universidad Nacional de la Patagonia San Juan Bosco. Bv. Brown 2930,

Puerto Madryn 9120, Chubut, Argentina; rubilar@cenpat-conicet.gob.ar

3. Laboratorio de Oceanografía Biológica (LOBio), Centro para el Estudio de Sistemas Marinos (CESIMAR–CONICET).

Boulevard Brown 2915, Puerto Madryn 9120, Argentina.

Received 23-I-2023. Corrected 14-IX-2023. Accepted 27-IX-2023.

ABSTRACT

Introduction: Even though only a few species are considered to be dangerous, pests or vectors, the majority

of invertebrates produce a feeling of aversion in humans. This has contributed to the delay in the development

of ethical considerations as regards this group in contrast with vertebrates, with the exception of cephalopods.

Objective: In the present study, we provide an overview of the current situation on animal ethics and welfare in

order to contribute to the development of a framework for ensuring invertebrate welfare.

Methods: Today, animal welfare is multidisciplinary in nature to a very high degree as it includes ethology,

physiology, pathology, biochemistry, genetics, immunology, nutrition, cognitive-neural, veterinary medicine, and

ethics. Animal welfare is a complex concept, difficult to achieve successfully from one perspective.

Results: As a consequence, we propose to include the five domains (nutrition, environment, health, behaviour

and mental state) along with the three conceptions (basic health and functioning, affective state and natural

living), as well as the 5R Principle (Replace, Reduction, Refinement, Respect and Responsibility) in seeking to

achieve a comprehensive welfare state.

Conclusions: We consider that in both research and animal production, the individual and collective ethical

concerns coexist and, in fact, the main moral concern to account for is the collective one and that, within that

collective view, the individual moral concern should be applied with responsibility and respect for the individual.

Finally, we propose a practical example of invertebrate welfare production in sea urchin aquaculture with the aim

of including animal production of invertebrates in this important discussion.

Key words: animal production; animal welfare, ethical concerns, invertebrate welfare, sea urchin, 5R principle.

RESUMEN

Ética y bienestar en invertebrados: una piedra fundamental en investigación y producción animal

Introducción: Aunque sólo unas pocas especies son consideradas peligrosas, plagas o vectores, la mayoría de

los invertebrados producen un sentimiento de aversión en el ser humano. Esto ha contribuido al retraso en el

desarrollo de consideraciones éticas respecto a este grupo en comparación con los vertebrados, a excepción de

los cefalópodos.

https://doi.org/10.15517/rev.biol.trop..v72iS1.58228

SUPPLEMENT

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72(S1): e58228, marzo 2024 (Publicado Mar. 01, 2024)

INTRODUCTION

Humans have been using and working

with animals for their own purposes through-

out their entire history. The most notable uses

have been, and are, for food, for transport,

for research (primarily medical research), for

clothes and as companions. Invertebrates are

not the exception in this long history of inter-

action; they are fully inherent in many aspects

of human lives and existence. Some aspects of

these relationships are clearly positive (use-

ful) to humans as invertebrates provide food,

research models or companionship, while other

aspects are negative (without purpose or, actu-

ally, harmful). This may be due to the fact

that certain invertebrates are considered to be

pests or vectors of human diseases. In general,

they are called bugs in a pejorative way. Such

negative interactions with humans produce

general feelings of aversion or fear towards a

large number of invertebrates (Kellert, 1993).

As a result, there are minimal ethical concerns

which need to be addressed as regards these

animals in order to ensure that they can be

treated as a good alternative in terms of serving

as models for experiments, instead of verte-

brates. Currently, the most worldwide-accepted

policy tool guiding practices in animal research

is the Three R’s principle postulated by Russell

& Burch (1959). One dimension of this prin-

ciple is Replacement, which states that research

should seek “any scientific method employing

non-sentient material [to] replace methods

which use conscious living vertebrates” (Russell

& Burch, 1959). Ideally, replacement should

promote the use of lower levels of organization,

such as cell culture and even artificial models

such as computational simulations. However, in

practice, the replacement dimension achieved,

generally speaking, “lowers” invertebrate taxa as

common models for experimental research as

such taxa are considered non-sentient animals.

In recent years, the ethical concerns regard-

ing invertebrates have started to change and

several studies have established the philosophi-

cal background for incorporating invertebrates

into the framework of ethics (Carere & Mather,

2019; Crespi-Abril & Rubilar, 2021; Horvath

et al., 2013; Mather, 2016). This change was

mainly driven by the complex behavior of cer-

tain invertebrates, such as octopus (Cephalo-

pods). The close interaction with octopus in an

aquarium environment allowed for empathiz-

ing with individuals and from this relationship

individuals’ behaviors (personalities) could be

observed (Mather, 2012; Mather & Carere,

2019) and it was seen that octopus have the

ability to individualize persons (Anderson et

Objetivo: En el presente trabajo, proporcionamos una visión general de la situación actual en materia de

ética y bienestar animal con el fin de contribuir al desarrollo de un marco para garantizar el bienestar de los

invertebrados.

Métodos: Hoy en día, el bienestar animal es de naturaleza multidisciplinaria en un grado muy alto, ya que incluye

etología, fisiología, patología, bioquímica, genética, inmunología, nutrición, cognitivo-neural, medicina veteri-

naria y ética. El bienestar animal es un concepto complejo, difícil de lograr con éxito desde una sola perspectiva.

Resultados: Como consecuencia, proponemos incluir los cinco dominios (nutrición, ambiente, salud, compor-

tamiento y estado mental) junto con las tres concepciones (Salud básica y funcionamiento, estado afectivo y vida

natural), así como el Principio 5R (Reemplazar, Reducir, Refinar, Respetar y Responsabilidad) en la búsqueda de

alcanzar un estado de bienestar integral.

Conclusiones: Consideramos que tanto en la investigación como en la producción animal coexisten las preocu-

paciones éticas individuales y colectivas y, de hecho, la principal preocupación moral a dar cuenta es la colectiva

y que, dentro de esa visión colectiva, se debe aplicar la preocupación moral individual. con responsabilidad y

respeto por la persona. Finalmente, proponemos un ejemplo práctico de producción de bienestar de invertebra-

dos en la acuicultura de erizos de mar con el objetivo de incluir la producción animal de invertebrados en esta

importante discusión.

Palabras clave: producción animal; bienestar animal, consideraciones éticas, bienestar de los invertebrados, erizo

de mar, principio 5R.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72(S1): e58228, marzo 2024 (Publicado Mar. 01, 2024)

al., 2010). All of this evidence has proven that

octopuses are extremely intelligent animals and

are also sentient individuals even though they

do not have the same nervous system structure

as vertebrates (Schmidt-Rhaesa et al., 2015).

Moreover, cephalopods were included in 2013

in the EU legislation on the protection of ani-

mals used for scientific purposes at the same

level of vertebrates (European Union, Directive

2010/63/EU, 2010). This new insight comprised

a stepping-stone in increasing the ethical con-

cern for invertebrates as a whole (Crespi-Abril

& Rubilar, 2021; Mikhalevich & Powell, 2020;

Pollo & Vitale, 2019). A main point to empha-

size is that we do not understand invertebrate

behaviors, it does not mean that they are not

sentient or capable of reacting to negative expe-

riences in a non-anthropocentric manner that

may cause pain and suffering (Elwood, 2019).

Simultaneous with this growing ethical con-

cern, a significant effort has been focused on

invertebrate welfare in experimental research

(Carere & Mather, 2019; Horvath et al., 2013).

However, information regarding the implica-

tions for invertebrate welfare is scattered, scant

and even contradictory. Consequently, in the

present study we provide a review of the current

situation on animal ethics and welfare in order

to contribute to the development of a frame-

work for invertebrate welfare.

Human perception of invertebrates

Invertebrates represent more than 90 %

of the total biodiversity of the planet (Kellert,

1993). This vast biological sphere includes 36

invertebrates phyla of which eight can be con-

sidered as most commonly having relationships

with humans: Porifera, Cnidaria, Platyhelmin-

thes, Nematoda, Annelida, Arthropoda (the

largest phylum in animal kingdom), Mollusca

(the second largest phylum in the animal king-

dom), and Echinodermata (Kellert, 1993). Even

though all of these phyla are considered to be

invertebrates comprising a sole group, they

could not be more diverse in nature. Their

morphology, nervous systems and behavior are

characteristic for each phyla and can also vary

within a given phyla (Crespi-Abril & Rubilar,

2018; Pollo & Vitale, 2019; Schmidt-Rhaesa et

al., 2015). The human perception of inverte-

brates varies among phyla and cultures. Some

are considered to comprise food (Crustacea,

Mollusca Cnidaria, Echinodermata, etc), others

are used in cosmetics and pharma (Porifera,

Echinodermata, Cnidaria, etc), also are impor-

tant depending on culture (traditions, offerings

to gods, literature, etc) or considered to be pests

or dangerous (Arthropoda, Cnidaria, Echino-

dermata, etc). This emphases the point that

invertebrates can not be considered to comprise

one sole group of organisms.

The human moral value of invertebrates

depends on the benefit or damage a single spe-

cies generates. In this manner, a species can

be considered to be “good” or “bad”. However,

there are many cases where one single species

can be both good and bad according to human

perception. For example, bees are considered a

good species since they are necessary for pol-

lination and honey production; however, bees

can also be bad for allergic people and can even

cause several deaths a year. Caterpillars are

considered to be pests in agriculture; however,

butterflies are considered to be beautiful by the

majority of people. Sea urchins are considered

a source of an exquisite food and are heav-

ily fished in some regions of the world, and in

other regions they are considered to be pests

due to the production of barrens where kelp

forests were previously growing. As a result,

individual human perception may not be the

only aspect to consider in invertebrate ethics. In

addition, given that each species has a particu-

lar niche necessary to preserve the ecosystem,

all invertebrates species should be included in a

broad ethic perspective.

Echinoderms

Echinoderms includes over 7 000 species

that are divided into five distinct taxonomic

groups: the Crinoidea, Asteroidea, Ophiuroi-

dea, Holothuroidea, and Echinoidea. They are

distributed From the intertidal region to the

deepest parts of the oceans (Brusca et al., 2016).

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The nervous system of this group is char-

acterized by a circumoral ring connecting the

nerve cords, which innervates the digestive

tube and appendages (tentacles, oral podia,

and oral spines), as well as nerve cords with

ganglion structures in each arm. According to

Mashanov et al. (2006), the nervous system is

in charge of starting and directing responses.

The ganglia are thought to be the processing

centers for the messages that the nerve cords

send to the muscles and organs and the sen-

sory organs receive from the outside world

(Mashanov et al., 2015).

Echinoderms react chemical, mechanical,

thermal, gravitational, stimuli (Mashanov et

al., 2015). The method of transducing the

experience of painful feeling, or nociception,

has not yet been exhaustively examined in

this group, but that does not imply that it does

not exist. However, it is known that they have

the ability to create memories in response

to harmful or detrimental stimuli. They can

also recognize and remember the place where

they live and avoid locations with unfavorable

conditions (Martín-García & Luque-Escalona,

2008; Pan et al., 2015; Yoshimura & Motokawa,

2008; Yoshimura & Motokawa, 2010). These

abilities suggest that they have some form of

learning capacity.

Welfare: Where science and ethics meet.

Public concerns regarding the use of ani-

mals in experiments have been present for

a long time (Singer, 1990). These concerns

focus on an ethical question: Do humans have

the right to use animals in experiments? The

answer to this question depends on the ethics

framework. According to Fraser (1999) type 1

ethics (based on Regan, 1983 and Singer, 1990

views) would limit and create barriers for using

animals. In contrast, type 2 ethics (based on

a broader range of authors like Donovan &

Adams, 1996; Lehman, 1988; Midgley, 1983;

Midgley, 1986; Preece & Chamberlain, 1993;

Rollin, 1990; Rollin, 1992; Rollin, 1993; Rollin,

1994, Rollin 1995; Thompson 1993) allows the

use of animals based on concepts of welfare

(see below). Public concern and pressure and

the type 2 ethics framework have helped to cre-

ate normative, guidelines and laws to improve

animal welfare during experimental research.

In scientific research, the 3R Principle by Rus-

sell & Burch (1959) helped to provide guide-

lines and normative practices, and the recently

proposed 5R Principle (Crespi-Abril & Rubilar,

2021) can help to improve this normative. In

animal production, similar concerns have come

to the fore and in 1965 the Brambell Report

on the welfare of farm animals was issued by

the British government to address these con-

cerns and since then, such demands continue

to be made.

Today, animal welfare is considered to

comprise a scientific discipline. Animal welfare

is multidisciplinary as it includes ethology,

physiology, pathology, biochemistry, genetics,

immunology, nutrition, cognitive-neural, veter-

inary, and ethics (Fraser, 2008a, Fraser, 2008b;

Fraser et al., 1997; Lassen et al., 2006; Mason

& Mendl, 1993; Mellor et al., 2009; Sandøe &

Simonsen, 1992). However, there are many dif-

ferent definitions of animal welfare and in lit-

erature three types of definitions can be found

(Stafleu et al., 1996; Veissier & Forkman, 2008).

Lexical definition: definitions provided

in dictionaries and generally known in society.

With this definition, welfare is a wide term

embracing both the physical and mental well-

being of the animal (Brambell, 1965).

Explanatory definitions: definitions pro-

viding the theoretical framework for lexical

definitions. Here, welfare is achieved when the

animal can fulfil its needs and wants (Stafleu et

al., 1996) with an emphasis on when the animal

cannot adapt to its environment (Jensen &

Toates, 1997).

Operational definitions: these are the

parameters by which welfare can be measured,

such as longevity, cortisol levels, normal behav-

ior, etc.

Since the publication of the Bram-

bell Report (1965), animal welfare has been

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72(S1): e58228, marzo 2024 (Publicado Mar. 01, 2024)

established as a scientific discipline evolving

through different approaches (Fraser, 2008a,

Fraser, 2008b; Green & Mellor, 2011; Mellor

et al., 2009). There has been an evolution of

concepts, from the “Five Freedoms” principle

that maintains that animal welfare has to ensure

compliance with the five freedoms (Farm Ani-

mal Welfare Committee [FAWC], 1992, FAWC,

2009); through the improvement of conditions

of animals in order to promote positive states

such us satiety, vitality, reward, contentment,

curiosity and playfulness (Green & Mellor,

2011), to the purpose of a multifactorial and

comprehensive understanding of animal wel-

fare, by improving the “Five Freedoms” into the

“Five Domains” concept in order to evaluate

the impacts on animal welfare (Mellor & Reid,

1994; Mellor & Stafford, 2011), and finally, to

the “Three Conceptions” that summarize the

components of animal welfare that cannot be

assessed independently but, rather, need to

overlap to assure welfare (Fraser, 2008a; Fraser,

2008b). To recently incorporate the human per-

spective (animal taker, researcher, veterinary,

etc.) with the 5R Principle based on empathy.

The “Five Freedoms’’ has been used as the

basis in the European Union and other parts

of the world to create animal protection laws.

The “Five Freedoms” are: 1. Freedom from

thirst, hunger, and malnutrition 2. Freedom

from discomfort 3. Freedom from pain, injury,

and disease 4. Freedom to express normal

behavior 5. Freedom from fear and distress

(FAWC, 1992, FAWC, 1993). This approach

has several shortcomings. For instance, only

the last freedom considers the animal mental

state, as the other four are based on biological

needs and on preventing negative states rather

than promoting positive ones. To enhance this

approach, the promotion of the positive welfare

states came to the fore in the improvement of

animal welfare. Here, there is an active seek-

ing to generate positive animal welfare both in

research and in production (Edgar et al., 2013;

FAWC, 2009; Fraser, 2008a, Fraser, 2008b; Mel-

lor & Beausoleil, 2015; Webster, 2011). With

this new approach the “Five Freedoms” became

“Five Domains”: 1. Nutrition, 2. Environment,

3. Health, 4. Behaviour and 5. Mental state.

These domains integrate the biological function

into the affective state (Fraser, 2008a; Fraser,

2008b). The “Three Conceptions” improved the

domains, as they refer to the main important

components involved in animal welfare: 1. Basic

health and functioning, 2. Affective state and 3.

Natural living. Each conception, by itself, can-

not provide animal welfare; instead, a combina-

tion and overlapping of the three conceptions

may ensure a higher level of animal welfare

(Fraser, 2008a; Fraser, 2008b). Furthermore,

and developed more recently, the 5R Principle

(Crespi-Abril & Rubilar, 2021) comprises a

more comprehensive approach including the

3R Principle (Russell & Burch, 1959) but also

incorporating Respect and Responsibility from

the human perspective based on empathy with

the aim of generating a good human-animal

relationship (Crespi-Abril & Rubilar, 2021).

Animal welfare is a complex concept, dif-

ficult to achieve successfully from only one

perspective. We propose to include the 3R Prin-

ciple, along with the “Five Domains”, the “Three

Conceptions” within a larger framework of

Respect and Responsibility (5R Principle) for

animal life (Fig. 1).

Assessment of invertebrate welfare

The assessment of animal welfare has tra-

ditionally been focused on vertebrates (Hem-

sworth et al., 2015). When the assessment is

to apply to invertebrates, the task is complex

due to the diversity levels. On the first hand,

the basic indicators (cortisol, longevity, feeding

rate, behaviour, etc) for a welfare assessment

fall into the operational definition of welfare

state stated above. Secondly, the assessment

only covers two of the “Three Conceptions”

(Basic health and function and Natural living)

and four of the “Five Domains” (Nutrition,

Environment, Health and Behaviour) (Fig. 1).

By definition, the basic assessment is incom-

plete. In addition, in invertebrates, excluding

cephalopods, the Mental State Domain and the

Conception of Affective State are, currently,

very difficult to evaluate. Even though we do

6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72(S1): e58228, marzo 2024 (Publicado Mar. 01, 2024)

not have the tools to assess the mental states of

invertebrates, there is undoubtable evidence of

social behaviour in many species and it is prob-

able that the lack of interactions with the inver-

tebrates is a detriment in terms of their mental

state (Bovenkerk & Verweij, 2016). Even if it is

currently not possible to undertake a compre-

hensive invertebrate welfare assessment, it is,

still, our responsibility to ensure that the high-

est welfare conditions possible are achieved.

According to Botreau et al. (2007), it is

necessary to have a set of criteria for animal

welfare in order to execute an overall assess-

ment. Criteria must incorporate the following

requirements: 1. Each and every important

aspect must be addressed in order for the

assessment to be exhaustive, 2. The criteria

must not be redundant or irrelevant, 3. Each

criterion must be independent of the other

criteria, 4. The criteria must be agreed upon by

all stakeholders and have a practical basis, 5.

The criteria, as well as their application should

be transparent and easy to understand, and 6.

The number of criteria should be limited (12 as

a maximum).

Taking these recommendations into

account and considering the diversity of inver-

tebrates, it is important to acknowledge that a

specific set of criteria assessing the invertebrate

welfare of each phylum, or even each Order,

would need to be constructed.

Ethics in research and in animal production

Individual animal ethics is based on the

premise that the moral concern should be

focused on the state of the individual. In other

words, the moral concern should consist of

thinking about the manner in which we treat

the animal in terms of it experiencing its own

interest (Palmer, 2010). This premise is based

on the principle that collectives or groups of

animals do not have conscious experiences

(Bovenkerk & Verweij, 2016). Collective animal

ethics considers the moral concern as regards

the group, even if the interest of the collective

is against, or in conflict, with the individual’s

interests (Johnson, 1992).

Whilst these perspectives on ethics would

appear to oppose each other, they are, actu-

ally, fully simultaneously applicable in terms of

the varying situations involving human-animal

relationships and, in fact, they co-exist. We

consider that, first of all the main moral con-

cern is a collective one and within the collective

view the individual moral concern should be

applied with responsibility and respect for the

individual. For example, in research, the moral

concern seems to be at individual level, since

the individual response is the main goal, the

Fig. 1. Animal welfare is a complex concept. It is fundamental to include multiple approaches to successfully achieve animal

welfare. The overlapping of the Domains with the Conceptions including the 3R Principle within a larger framework of the

5R Principle, may help to achieve a more comprehensive animal welfare.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72(S1): e58228, marzo 2024 (Publicado Mar. 01, 2024)

requirements of statistics, such as pseudo repli-

cas, are to be avoided and therefore individuals

are kept alone in their cages or aquariums. How-

ever, under the animal welfare 5R Principle, the

researcher must first apply a collective moral

concern in implementing the Reduce concept

(minimizing the numbers of individual harm)

(Bovenkerk & Verweij, 2016; Crespi-Abril &

Rubilar, 2021; Russell & Burch, 1959). In animal

production (e.g. farms and aquaculture), the

most appropriate moral concern is a collective

one without losing the individual perspective.

For example, in a group with herd immunity

the benefit is incurred by every individual, even

those without immunization, or who are weak

or ill (Bovenkerk & Verweij, 2016). In a similar

manner, a healthy environment in farms or in

aquaculture facilities benefits the collective and

the individuals, considering animal welfare at

both levels. Sick animals in production facilities

have to be managed (see Varner, 1995 for con-

cept), and are often removed from the group

to a quarantine area or even apply euthanasia

plans (FAWC, 2012; Turner & Doonan, 2010).

This requires both the collective and individual

ethical perspectives. On one hand, the farmer

takes care of the group to prevent an epidemic

and in order to diminish the scope of animal

harm and, on the other hand, takes care of the

sick animal to recover from the disease or to

minimize suffering from a slow death of that

animal. We propose that with both research

and animal production, the 5R Principle, in

particular, the Respect and Responsibility con-

cepts (Crespi-Abril & Rubilar, 2021), are to

be applied as they involve both collective and

individual ethics (Fig. 2).

Practical Application of welfare

assessment in invertebrates: Sea urchin

aquaculture as a model

Sea urchins have been consumed by

humans since ancient times (Lawrence, 2007).

Market demand is higher than the offer in

the market and natural stocks are in decline

(Stefansson et al., 2017). As a result, sea urchin

aquaculture is in demand (Rubilar & Cardozo,

2021). In addition, global warming is compro-

mising the fishing supply of sea urchins (Lucey

et al., 2022), making sea urchin aquaculture a

priority worldwide to meet the market demand.

This is a novel industry where a practical appli-

cation of invertebrate welfare assessment can be

undertaken from the very beginning.

There is no secret that animal production

is focused on the outcome, an improved out-

come and quality, and on a better profit. In ani-

mal production, as we have seen, there are laws

and principles to regulate animal welfare (eg.

European Union, Directive 2010/63/EU, 2010;

3R Principle; 5R Principle) and, often, bet-

ter welfare will produce a better outcome and

profit. However, these regulations are primarily

focused on vertebrates and cephalopods. When

it comes to considering low trophic species,

such as sea urchins, crabs, mussels, shrimps,

among others, there are, largely, no guidelines

to follow. Still, the incorporation of moral

concerns and invertebrate welfare will most

likely improve the production and practices of

aquaculture facilities. Healthy individuals are

more productive and their welfare can often

contribute to the overall health of the group.

As shown in Fig. 1, a sea urchin aquaculture

facility could be seen to require consideration

Fig. 2. The main moral concern in research and

production is a collective one and within the collective

view the individual moral concern should be applied with

Responsibility and Respect for the individual.

8Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72(S1): e58228, marzo 2024 (Publicado Mar. 01, 2024)

of the “Five Domains” (with specific crite-

ria), the “Three Conceptions” and the 5 R

Principle, in order to secure a comprehensive

welfare approach. The Domain of Nutrition

refers to fulfilling the nutritional requirements

of the species by offering, in this case, a spe-

cific type of sea urchin feed. This Domain can

be assessed by measuring the rates of non-

consumed food and feces. The Health Domain

refers to the absence of disease. This Domain

can be assessed on the basis of the record of the

number of lost spines, the color of epidermis

and immunological profiles (number and type

of coelomocytes). The Environment Domain

refers to the habitat. In low trophic aquaculture,

the best way to achieve a good environment

is through Integrated Multi Trophic Aquacul-

ture (IMTA). This ensures good water quality,

as well as a heterogeneous environment and

also ensures natural refugees. This domain

can be assessed on the basis of physicochemi-

cal values (temperature, salinity, ammonium,

nitrite, nitrate, phosphates) in the water, as well

as in terms of the microbiome present in the

water. The Behavior Domain refers to the natu-

ral behavior of the individuals. This Domain

can be assessed on the basis of the “righting

behavior” (a specific behavior of sea urchins),

adherence to the surface, food seeking, tube

feet and spine movements, and on the aggrega-

tion of individuals. The Mental State domain

in invertebrates, especially in marine ones,

such as sea urchin, is a challenging Domain in

terms of determining and assessing its nature

and parameters. However, knowledge regarding

the behavior of the species in nature is crucial.

For example, sea urchins are often found in an

aggregative distribution, i.e. patches of indi-

viduals. In animal production, the presence

of this type of aggregation of individuals may

most likely contribute to the mental state of the

individuals. Patchy aggregations benefit their

constituent organisms, including maintaining a

desirable internal environment despite variable

ambient conditions, enhancing locomotion,

and avoiding predation (Camazine et al., 2001;

Moussaid et al., 2009; Parrish & Edelstein-

Keshet, 1999; Sumpter, 2006) which may relieve

individual stress. Furthermore, even if there

is, at the moment, no means of assessing the

impact of this distribution on the mental health

of the animals, it is important to respect the

natural distribution of the species. However,

future evidence may provide insights into this

Domain and by using the 10th criteria, it would

appear to be possible to assess the welfare of sea

urchins in aquaculture facilities.

Conclusion

The majority of ethical and welfare animal

approaches are based on vertebrates. The work

with invertebrate welfare is challenging and it

will take time for both researchers and produc-

ers to embrace these concepts. However, there

are major advances in this context (Carere &

Mather, 2019) and if there is public awareness

and concern, this may help to accelerate the use

of these concepts and, hopefully, one will see,

quite soon, guidelines, normatives and laws in

this area.

Animal welfare implications: We have

been working on invertebrate ethics and wel-

fare for several years and we hope that animal

production will also be included in this discus-

sion regarding invertebrates.

ACKNOWLEDGMENTS

We would like to thank Kathleen Anderson

for the English revision and to Florencia Santi

for a critical review of the manuscript. We also

thanks, anonymous reviewers who helped to

improve the manuscripts with their sugges-

tions. This work was supported by the Nation-

al Scientific and Technical Research Council

(R&D Transfer Agreement PR5287, FWL-194).

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