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Abstract and Figures

Despite increasing numbers of publications showing that many animals possess the neural substrates involved in emotions and consciousness, and exhibit agency in their behavior, many animals are still restrained and forced to take part in applied or fundamental research. However, these restraints and procedures, because they stress animals and because they limit the expression of adaptive behavior, may result in compromised findings. Researchers should alter their research paradigms to understand mechanisms and functions of the brain and behavior so that the paradigms incorporate animals’ agency. This paper discusses how animal agency can not only be the key to more wide-ranging and improved research in existing domains, but can also lead to new research questions about behavior and brain evolution.
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Incorporating animal agency into research design could improve behavioral and 1
neuroscience research 2
Cédric Sueur1,2,3, Sarah Zanaz1,4, and Marie Pelé5. 3
1 Université de Strasbourg, CNRS, IPHC UMR 7178, Strasbourg, France. 4
2 Institut Universitaire de France, Paris, France. 5
3 CEERE Centre Européen d’Enseignement et de Recherche en Ethique, Strasbourg, France. 6
4 Benemérita Universidad Autónoma de Puebla, Facultad de Filosofía y Letras, Puebla 7
5 Anthropo-Lab, ETHICS EA7446, Université Catholique de Lille, F-59000 Lille, France. 8
The authors declare no competing interests. 10
Correspondence to Cédric Sueur: 12
Abstract 15
Despite increasing numbers of publications showing that many animals possess the neural 16
substrates involved in emotions and consciousness, and exhibit agency in their behavior, 17
many animals are still restrained and forced to take part in applied or fundamental research. 18
However, these restraints and procedures, because they stress animals and because they 19
limit the expression of adaptive behavior, may result in compromised findings. Researchers 20
should alter their research paradigms to understand mechanisms and functions of the brain 21
and behavior so that the paradigms incorporate animals’ agency. This paper discusses how 22
animal agency can not only be the key to more wide-ranging and improved research in 23
existing domains, but can also lead to new research questions about behavior and brain 24
evolution. 25
Keywords: 3Rs, animal research, ethology, ethics, animal welfare, scientific advance 27
Introduction 30
By definition, animal research requires the involvement of animals. Although researchers 31
have made great progress and improved experimental conditions for animals through the 32
application of the 3R (Replace, Reduce, Refine) rules, some behavioral experiments showed 33
that animals are still restrained through different methods, such as the use of throw nets, 34
primate restraint chairs (specifically-designed chairs that require non-human primates to ‘sit’ 35
in place for sustained periods of time (NC3Rs,
restraint-training-non-human-primates)), rat restrainer, cages, or by food deprivation (Ben-Ami 37
Bartal et al., 2011; Chang et al., 2017; He et al., 2020; McMillan et al., 2017; Prescott & 38
Buchanan-Smith, 2003; Slater et al., 2016). According to McMillan et al. (2017), too many 39
researchers continue to use methods that entail negative reinforcement (when the 40
individual has to perform an action to remove a stressor), whilst procedures using restraint 41
chairs in primates or similar restrainers in other species could comprise positive 42
reinforcement methods (when the individual receives a reward after entering in the chair 43
and then getting its head out from the chair) (McMillan et al., 2017). These protocols are 44
used to obtain results in behavioral or neuroscience research but are problematic for several 45
reasons. Beyond the ethical issues of such restraints for animals, these examples of 46
experimental setups lead us to consider which possibilities and results have yet to be 47
investigated and more importantly, whether such compulsory protocols could lead to false 48
negatives or false positives (Chang et al., 2017; Huttunen et al., 2017; Liu et al., 2017). False 49
negatives or false positives mean that studies show respectively negative (not expected, H0) 50
or positive results (expected, H1) but these results are not due to the tested condition (e.g. a 51
drug, a gene, an environmental condition) but to uncontrolled factors (e.g. stress, 52
personality). Indeed, stress and coercion (i.e., the animal is immobilized and restrained in an 53
apparatus, such as a chair for primate or a box or a system of collars for rats or dogs) can not 54
only modify some behaviors but also entirely prevent others from being displayed (Lecorps 55
et al., 2021; Mason et al., 2019; Prescott, 2016). Some authors, such as Van Patter, Blattner, 56
Matsuzawa, King and McMillan consider that the current 3R framework is not sufficient to 57
ensure that animals are meaningful participants in experiments, which is crucial to 58
guarantee that scientific results are not altered by stress or personality of animals (King, 59
2021; Matsuzawa, 2016a; McMillan et al., 2014; Van Patter & Blattner, 2020). Studies carried 60
out on animals under restraints offer few meaningful opportunities for them to show their 61
full behavioral and cognitive capacities, and in this way to exercise agency with their 62
environment and in their relationships, both with each other and with humans (Homo 63
sapiens) (Blattner et al., 2020). Gillespie (2019) wrote that ‘there is a long tradition of 64
studying nonhuman animals in spaces of animal use and exploitation, where researchers and 65
teachers in effect become complicit through passive participation in violence against 66
nonhuman animals…’ (p. 19). According to Blattner et al. (2020), who worked on animal 67
agency in rehomed farm animals and from which this paper is inspired, ‘longstanding 68
ideological blinders and anthropocentric bias frame animals as limited beings whose lives 69
unfold according to fixed genetic or species-specific scripts, rather than as complex subjects 70
who act with intention and purpose, both individually and collectively’ (p. 1). 71
Culture, ontology, political leaning, as well as university courses influence how a person 72
considers animals as objects (Bègue & Vezirian, 2021; Furnham & Heyes, 1993; Miele et al., 73
1993). It would be interesting to look at the textbooks of comparative cognition to find 74
evidence that students are being taught to think of animals as objects; that is the method 75
(Andrews, 2020b) used to defend the claim that comparative cognition eschews the study of 76
consciousness. This view of animals as objects is not limited to research but is also found in 77
different aspects of everyday life (food, work, clothing, etc.). In this way, the consideration of 78
animals as agents could be extended from research to other domains: a new ontology 79
considering non-human animals as agents can have political, ethical, and legal 80
consequences. 81
We argue that restraint-based experiments are severely limited in terms of what researchers 82
can learn from animals, in individual and group contexts. In contrast, letting animals express 83
their will or intentions in behavior could bring new advances in research and human-animal 84
cooperation. Incorporating animal agency should be considered a central feature of research 85
and husbandry protocols, particularly when applying for funding. In this article we seek to 86
provide researchers with arguments in favor of this practice. 87
Animal agency 88
Agency is the capacity of an individual to act in a given environment. In the broadest sense, 89
agency is the ability to have an influence or an effect on something. However, agency is 90
considered here as the expression or manifestation of a subjective existence; agency implies 91
affecting the world in ways that reflect a subject’s desires or will (Krause, 2013). It refers to 92
an individual pursuing its own good in its own way (Taylor, 2011). Gergely & Jacob (2012) 93
described that from birth on, human infants are exposed to two basic kinds of agency: 94
instrumental action and communicative action. When researchers allow too little room for 95
the animals’ own forms of agency, the true abilities of these individuals are obscured 96
(McFarland & Hediger, 2009). 97
Blattner et al. (2020) investigate animal agency in a sanctuary for rehomed farm animals, 98
considering how a careful exploration of dimensions of agency in this setting might inform 99
ideas of interspecies interactions (work, research, politics, etc.) and ethics. Their study 100
focused on animals of many species living in this sanctuary. For the owners of the sanctuary 101
and the researchers, the sanctuary is an ‘integrated multispecies community or society 102
whose members shape spaces and practices together, take on recognized social roles, and 103
create and transmit social norms across species lines’. Blattner et al. (2020), De Waal (2016), 104
Le Neindre et al. (2017, 2018), and Meijer (2019) affirm that researchers need to spend time 105
in community with animals, learn from them, and be prepared to respond and adjust 106
scientific learning process through relationships with them. This means that animals should 107
no longer be considered as the subjects of scientific experiments, but rather as participants108
that is, as agents (Haraway, 1989). For example, when it comes to assessing cognitive 109
abilities, the researchers’ focus should encompass goals that are meaningful, useful, and of 110
interest to animals instead of focusing on goals that are only relevant to the human scientist 111
(Pepperberg, 2006). 112
It is also important to recognize animals as agents by forming relationship with them. As 113
Andrews (2020) notes, it is important to treat animals as sentient research participants who 114
exist within their own context and with whom researchers will be in a relationship. She 115
defends a range of scientific benefits that come from forming relationships with animal 116
research subjects and that we develop below. Interaction and communication have to go in 117
both directions. Researchers need to make themselves understandable to animals as many 118
species are able to understand our facial expressions and emotions (Bhattacharjee et al., 119
2019; Good et al., 2018; Hoffman et al., 2018; Patterson & Cohn, 1990; Pedersen, 2020; 120
Savage-Rumbaugh & Lewin, 1994). For instance, applying the same agency and research 121
protocols in horses (Equus caballus) as were applied in primates led to advances in our 122
understanding of equine cognition (Matsuzawa, 2017). The first study with horses using 123
computer touch panels was realized recently (Tomonaga et al., 2015). The primary 124
motivation to study horses comes from the idea of understanding humans not just from a 125
primate perspective, but from a broader mammalian (Mammalia) perspective. Tomonaga et 126
al. (2015) used a computer-controlled touchscreen system to show differences in 127
discrimination abilities between horses, chimpanzees (Pan troglodytes) and humans. 128
Animals may act in different dimensions as space and time and different situations as 129
socializing, foraging, parenting, etc. Blattner et al. (2020) analyzed in their paper what 130
freedoms of actions may result in the expression of agency in animals as well as how humans 131
take up these freedoms, meaning how they use these dimensions to enhance animals’ 132
agency or the behavioral repertoire. Their observational analysis, using multispecies 133
ethnography (i.e., the study of the interconnectedness and inseparability of humans and 134
other life forms; Kirksey & Helmreich, 2010; Ogden et al., 2013) and directed toward a 135
number of methodological and ethical questions on animal-human and animal-animal 136
relationships, led them to divide animal agency into four domains (Figure 1): 137
1. Agency through space and time: 138
Animals are mobile and explore/exploit their environments. Their exploration and 139
exploitation can be used to better understand animals’ preferences in terms of habitats, 140
sleeping areas, and social relationships. Studies on these issues contribute to the emergence 141
of new disciplines such as animal geographies (Buller, 2014) or animal mobilities (Hodgetts & 142
Lorimer, 2020). Whilst this form of agency seems obvious to many researchers and the 143
criteria are often applied to livestock and farmed animals (Bouissou et al., 2001; Scanes, 144
2018; Sosa et al., 2019), it is less often applied in comparative psychology or neuroscience, 145
despite well-known works on exploration and curiosity in animals published more than half a 146
century ago (Berlyne, 1966; Glickman & Sroges, 1966). In neurophysiological studies of 147
nonhuman primates, restraint chairs are widely used (McMillan et al., 2017) as boxes or 148
other systems in rats (Bartal et al., 2011; Galichanin et al., 2011). 149
Modifications of the environment can be used to shape animalsdecisions and can remove 150
some of the negative reinforcement that is still applied to animals. For example, animals 151
could experience less stress in some parts of their environment than others, and carrying out 152
experiments in these places could increase their motivation to participate and increase the 153
power of the study to detect experimental effects (Coe & Hoy, 2020; Matsuzawa, 2020). Of 154
course, this statement implies that the housing of animals should be designed to take 155
advantage of animals’ preferences and adjustments to features of their environment. For 156
example, boundaries and fences cannot be only considered as barriers and limitations of 157
freedoms but also as security and communication touchstones as suggested by Blattner et 158
al. (2020) or Grandin (1987, 1989). Humans should create barriers and fence placements 159
according to the behavior of animals. Similarly, for behavioral experimental apparatus, 160
animals should not be forcibly brought to where researchers want to test them but 161
researchers should observe animals to determine the best position to place the devices. 162
Good urban design is adapted to human behavior in order to increase health, decrease 163
stress, and the costs of urban refurbishment (Park & Evans, 2016; Pereira et al., 2019). A 164
similar way of thinking could be applied to designing housing and testing spaces for 165
nonhuman animals. For example, in “modern” zoos animals of different species are housed 166
together in larger enclosures, while retaining the possibility for each species to be isolated 167
from the others if needed. This is a way to apply the concept of nudge (i.e. any aspect of the 168
choice architecture that alters behavior in a predictable way without forbidding any options, 169
Thaler, 2008) to some captive animals studies, as has already been done for species 170
conservation (Czap et al., 2015; Eberle, 2021; Reddy et al., 2017). Kyoto University applied 171
this concept with the WISH cages, a set of enclosures connecting habitats and equipped with 172
a computer-controlled touch panel system for cognitive tests. This framework increases the 173
fission-fusion dynamics of chimpanzees, i.e. their social agency, and their cognitive agency 174
(Matsuzawa, 2020). Other labs provide similar voluntary participation testing stations 175
associated with group-living such as the Goffin laboratory in Vienna with cockatoos (Cacatua 176
goffini) (O’Hara et al., 2021) or the Living Links station with nonhuman primates at 177
Edinburgh zoo (Jordan et al., 2022). This principle is not restricted to vertebrates as ants for 178
instance showed their abilities to escape their captive nest when it was not well designed, 179
thanks to behaviors as raft, bridge, jump or even tool use (Dussutour & Wystrach, 2022). 180
2. Agency through practice and routine: 181
Animals have habits. Social animals collectively organize their day in order to meet their 182
requirements and maintain the advantages of living in groups (Sueur, 2011). Allowing 183
animals to accept or refuse to participate in a research activity according to their routine 184
would increase the robustness and reliability of the results. For example, some studies allow 185
an animal to use a digital tablet or workstation or to open boxes to obtain food inside (Aplin 186
et al., 2015, Whiten et al., 1996). In domains such as visual cognition testing could be 187
conducted in a naturalistic environment with an integrated touchscreen workstation, 188
favoring animal exploration (Jacob et al., 2021). Specific protocols for individuals in a group 189
can be based on technologies like RFID (Radio Frequency IDentification) (Claidière et al. 190
2017; Matsuzawa, 2013); these tools allow individuals to participate in the testing at the 191
time and for the duration of their choosing. Health checks or medical procedures that 192
require restraints, should also be based on these routines in order to decrease animal stress 193
and injuries, as already shown in their use by zoos (e.g., the Great Ape Heart Project, 194
Murphy et al., 2018). Knowing routines of animals or observing why the routine of an animal 195
is different from others or for a day allows us to better understand their behavior without 196
the need to disturb them by subjecting them to experiments or health checks. Moreover, 197
modifying the routines of animals is a way to measure their behavioral flexibility, 198
personality, and group cohesiveness. 199
Whilst many researchers working with captive nonhuman primates already invoke a form of 200
consent to work with animals (Fenton, 2014), this protocol could be applied to many other 201
orders and classes, such as rodents. To our knowledge, there are no testing devices that can 202
be used in the cages of rats with which they can play when they want and for the duration 203
they want (although some housing includes different kinds of objects and surfaces for 204
voluntary activity; Bailoo et al., 2018; Crawford et al., 2020). This kind of system should be 205
extended to all species involved in research. 206
3. Agency in the social environment: 207
A social role is the behavior expected of an individual who occupies a given social position or 208
status. Individuals understand the place that conspecifics hold in their society (Borgeaud et 209
al., 2016; Bret et al., 2013; Levé et al., 2016). The adoption of roles that are recognized and 210
acknowledged by others, and indeed mutually constructed with conspecifics, is an important 211
dimension of relational agency and a means by which researchers can effectively affirm their 212
subjective existence within a community. This role can be intraspecific or interspecific. Roles 213
of individuals inside their group have been amply described in terms of dominance (policing 214
behaviors, protecting groups), kinship, and maternal relationships (Krause & Ruxton, 2002). 215
Individuals also develop strong relationships when they share similar attributes, such as sex 216
or age (Abeyesinghe et al., 2013; Massen & Koski, 2014; Rault, 2012; Silk, 2002; Tsuji et al., 217
2007). These affiliative but interspecific relationships are used in the case of animal 218
mediation and zootherapy where dogs, cats, and horses respond to the pain of patients, not 219
only passively but also proactively by initiating for instance play sessions (Chouinard, 2021; 220
Muschel, 1984). With time, these mediation animals developed strong relationships with 221
certain patients. When doing tests, researchers also know which pairs of individuals can 222
easily be tested together or not. Group members influence each other (Duboscq et al., 2016) 223
and can transmit important information to others (Grampp et al., 2019). Social learning can 224
aid animals learning to use experimental apparatus or spaces (Biro et al., 2006; Whiten, 225
2011). This works in many vertebrate species and even in invertebrates: fruitflies (Drosophila 226
sp.) are able to learn from their conspecifics where to lay eggs and bumblebees (Bombus 227
terrestris) learn to pull a string to obtain food when interacting with another bumblebee that 228
does so (Alem et al., 2016; Battesti et al., 2015; Pasquaretta et al., 2016). Biased attention of 229
group members towards dominant or older individuals in some species (Grampp et al., 2019) 230
might be used by researchers to make animals more rapidly or more efficiently learn a new 231
behavior. By influencing the leaders, researchers can manage the movements of an entire 232
group (Ramos et al., 2018, 2021). 233
4. Agency through social norms: 234
Social norms are the customary rules that govern behavior in groups and societies (Bicchieri 235
& Muldoon, 2011). Behavioral rules and social systems are partly genetic in animals but are 236
also transmitted through learning (Brent et al., 2013; Krause & Ruxton, 2002; Sinha, 2005; 237
Sueur, 2015; Ward & Webster, 2016). There is a debate as to whether animals have social 238
norms, but all theorists agree that social norms require a social maintenance constraint, 239
such that other group members care whether an individual follows the pattern or not 240
(Andrews, 2020a; Fitzpatrick, 2020). This might be the case in animal collective decisions 241
(Sueur et al., 2021). Although collective decision processes are species-specific, variations 242
are observed between groups and individuals of the same species. The roles played by 243
individuals can lead to a strong leadership or the development of a more democratic 244
process, such as voting (King & Sueur, 2011). Voting systems (Pennisi & Giallongo, 2018) are 245
described in many species, reinforcing the idea of agency. A sense of community (Blattner et 246
al., 2020) seems to exist in chimpanzees and cetaceans (Cetacea), and indeed animals of 247
many species know exactly who belongs or does not belong to their group. 248
Figure 1: The four schemes of animal agency (squares) and the environmental factors 250
affecting them (circles). 251
These different instances show that animals have agency over their spatial, temporal, and 253
social environment. Animals can therefore be viewed as agents; their choice to act has direct 254
consequences on their environment, or they can also resist conditions that do not please 255
them and act accordingly to change them (Carter & Charles, 2013). The behavior that 256
animals show, the facial expressions they display, and the places they occupy are cues to 257
indicate their intentions as well as their stress. By observing these intentions and/or stress, 258
researchers could use animals’ agency to improve their welfare and to obtain more robust 259
experimental results whilst extending the scope of behavioral and neuroscience research to 260
more natural conditions. Indeed, a major challenge facing behavioral neuroscientists today is 261
to measure the behaviors and the neuronal activities of sentient animals in natural 262
conditions. We have to keep in mind that in the research process, some of the limitations 263
shown by the animals are actually the limitations of the scientific methods, rather than the 264
animals themselves (Savage-Rumbaugh et al., 2006). This is particularly the case with visual 265
cognition (Hopper et al., 2021; Jacob et al., 2021) and auditory cognition (Calapai et al., 266
2022) with new systems allowing significant advances in testing animals. Similarly, De Waal 267
(2006) argues, about studies with apes (Hominidae) aiming to examine their theory of mind: 268
‘All that most experiments have done thus far is test the ape’s theory of the human mind. 269
We would do better to focus on the ape’s theory of the ape mind’, (p. 70). Following the 270
concept of animal agency, this paper proposes a future research framework to work with 271
animals and progress in research. 272
Evidence that animals have agency 274
Many animals (mammals, birds, and other classes) possess the neural substrates involved in 275
emotions and consciousness (Ben-Haim et al., 2021; Low et al., 2012). Authors have argued 276
that nonhuman animals may evidence several aspects of cognition that until recently were 277
attributed to humans but not other animals. For example, rats, apes, macaques (Macaca 278
sp.), and pigeons (Columba livia) may be capable of metacognition, i.e., knowing if they are 279
wrong or right in a test (Le Neindre et al., 2017, 2018). Cetaceans and apes may be conscious 280
of their own existence, and that of others (Gallup et al., 2002). Cleaner fish may have some 281
elements of self-awareness (Kohda et al., 2019). Apes may know what their conspecifics 282
know (Kaminski, Call, & Tomasello, 2008) and believe (Krupenye et al., 2016). Apes (De Waal, 283
2012) and rats (Ben-Ami Bartal et al., 2011) may experience empathy. Finally, some apes 284
may have a sense of morality (De Waal, 2006; Jensen et al., 2007; Tomasello & Vaish, 2013). 285
Of course, there remains debate on how to interpret behavioral studies when it comes to 286
the cognitive capacities we listed above (Bekoff & Allen, 1997; Buckner, 2011; Sober, 2009), 287
and we need to be careful about how to interpret these results (Janson & Byrne, 2007; 288
Péron, 2012). Whilst some individuals show the particular capacities in some experiments, 289
other members of the same species fail in other studies or replications (Boyle, 2021; Voelkl 290
et al., 2020, 2021), thus proving the importance of comparative methods to investigate 291
these phenomena (Krasheninnikova et al., 2019; Schmitt et al., 2012). Moreover, there is no 292
need to have these specific cognitive capacities to be an agent according to some views of 293
agency (Carter & Charles, 2013). Methods used by ants to find resources are used as an 294
algorithm for the traveling salesman problem (Dorigo & Gambardella, 1997a, 1997b). In both 295
illustrations, the organisms are not only an inspiration for researchers to resolve a problem, 296
they resolved it with their own capacities in their own world. In that sense, both can be 297
considered as co-creators of the new knowledge, even if they are not aware of it. Accepting 298
this paradigm of co-creation of knowledge can create new research questions that are 299
different from those made under an anthropocentric view. 300
More and more, researchers showed that animals may have previously unrecognized 301
cognitive capacities by changing their way of thinking from an anthropocentric approach, 302
looking for human-like cognition to hypothesizing that animals can think in a way different 303
from how humans do (Andrews, 2020b; Birch et al., 2020; De Waal, 2016). For instance, 304
some species do not respond to mark on themselves when looking in a mirror (Gallup et al., 305
2002) but do respond in a self-directed manner, suggesting a sense of self, when researchers 306
presented stimuli in a sensory modality relied upon by the particular animal, such as the 307
sense of smell for dogs (Cazzolla Gatti, 2016) or hearing in gibbons (Nomascus leucogenys) 308
(D’Agostino et al., 2017). As the same way for mirror and face recognition, researchers 309
presented to gibbons and dogs respectively vocalizations and odors of themselves and 310
observed how they reacted compared to vocalizations and odors of conspecifics. Merleau-311
Ponty had already noted this problem in his Causeries back in 1948: researchers usually do 312
not try to understand animals in their singularity, as they are, but rather in comparison with 313
human beings, projecting what are essentially human characteristics onto animals (Merleau-314
Ponty, 2017). However, this is a means to measure the distance between human beings and 315
other animals rather than a tool allowing a real understanding of how animals live and 316
express a subjective existence (Sueur et al., 2020; Sueur & Pelé, 2017; Tokuyama et al., 317
2012). Studied in the light of human normative references, animals always lack something 318
(Merleau-Ponty, 2017). For as long as animals are studied from a human perspective and are 319
tested in terms of human problems (capacity to count, to draw, to speak a human language) 320
instead of their own questions and problems, they will always respond ‘as they can’ 321
(Canguilhem, 1992), without ever being able to fully express their agency. However, there 322
have been philosophical and anthropological attempts to blur the boundaries between 323
humans and other animals (Andrews, 2020b; Böhnert & Hilbert, 2018; Daly Bezerra de Melo, 324
2012, 2018; De Waal, 2016; Langlitz, 2020; Wendler, 2020). As Jacques Derrida wrote in The 325
Animal That Therefore I Am (2008), the traditional scientific and philosophical discourse on 326
animals observes and speaks of non-human animals but never really engages with, 327
experiments with, or gains experience with the latter (Derrida, 2008): this type of discourse 328
can therefore only position animals as mere passive objects of the theoretical knowledge 329
these disciplines build. Such methods are completely blind to the animals’ own processes of 330
interacting with their world (Derrida, 2008), and are completely blind to their agency. 331
Animals interact with the world in their own ways and these ways, i.e. their agency, are 332
precisely the view that researchers need to adopt to perform better research and develop a 333
better understanding of how the brain and behavior evolve. 334
Future research framework 336
1. Testing agency from the laboratory 338
Some studies, especially in the biomedical or physiological/cellular domains, cannot be 339
performed outside the laboratory. It is important for these experiments to respect the 3Rs 340
(Replace, Reduce, Refine) but also to think about the Bateson cube (Bout et al., 2014), 341
meaning that scientists need to evaluate the ethical acceptability of their research for 342
society as a whole, including animals. Bateson's cube is a model of the costbenefit analysis 343
for animal research in which research protocols are evaluated through three criteria: the 344
degree of animal suffering, the quality of the research and the potential applied or 345
fundamental benefit. The principles can be extended by testing animals in correct 346
conditions, meaning in conditions not leading to strong false negatives or strong false 347
positives. Overly standardized laboratory conditions, for instance, decrease the replicability 348
of studies by decreasing behavioral variability; this is commonly known as the 349
standardization fallacy (Voelkl et al., 2021; Würbel, 2000). 350
Indeed, laboratory conditions for nonhuman primates and rodents were standardized for 351
many years in terms of husbandry and diet, in order to support comparisons across 352
experiments and laboratories. However, this way of conducting research is criticized today 353
because the conditions in which animals live have a strong effect on them, and thus on the 354
scientific results, so studies of animals in narrow conditions provide results relevant only to 355
those narrow conditions. Moreover, it is difficult to replicate conditions across laboratories, 356
specifically in studies about comparative cognition because of a large variance of 357
physiological, behavioral or cognitive traits between individuals (Boyle, 2021). Indeed, it is 358
first difficult to replicate same group living conditions in terms of animal density, group 359
composition, conditions which have an impact on cognitive capabilities (Meguerditchian et 360
al., 2021), but even when it is possible, animals that are genetically similar and live in similar 361
environments develop different personalities (Bierbach et al., 2017). Lastly, poor husbandry 362
conditions stress individuals (Cait et al., 2022; Pomerantz et al., 2022) and do not allow them 363
to express their full agency. Indeed, sociality has an important impact on the health of 364
animals, and a large number of publications highlight the link between sociality and health 365
aging (Boyer et al., 2019; Lacreuse et al., 2020; Rosati et al., 2020). Enabling animals’ social 366
agency can even reverse cognitive decline and extend longevity (Baker et al., 2012; 367
Richardson et al., 2020; Wild et al., 2021). Sociality is an important part of animal agency and 368
social life of animals has to be respected even in laboratory conditions, for their welfare as 369
well as for the robustness of scientific results. 370
2. … To the wild or at least in more natural conditions 371
Traditional approaches to studying for instance visual cognition or decision-making involve 372
bringing animals into a laboratory and restraining them while they perform tasks in order to 373
ensure accurate measurements, for example, of gaze-tracking and neural activity (see for 374
instance D’Souza et al., 2021; Honda et al., 2021). However, this unnatural setting does not 375
permit the study of brain activity during natural, social, and complex behaviors (Testard et 376
al., 2021). Many discoveries about ants’ behavior could not be made if not in natural 377
conditions (Dussutour & Wystrach, 2022) as the one showing that the termite-hunting ant 378
(Megaponera analis) is capable of saving injured individuals by taking them back to the nest 379
(Frank et al., 2017). Ideally, experimental settings will permit animals to move normally and 380
to engage in natural activities, such as foraging and in social interactions, but this requires 381
that animals accept to wear some devices, not tear off some cables or even just come at the 382
right place at the right time. Culture of animals also have to be considered and for instance, 383
study of percussive tools by nonhuman primates, known from field observations, has been 384
difficult to achieve in the laboratory. Laboratory studies of this phenomenon (e.g., Bril et al., 385
2009) have been less numerous than field experiments, that have been very productive (e.g., 386
Biro et al., 2006; Leca et al., 2007; Visalberghi et al., 2009). In the same way, field 387
experiments or experiments close to natural conditions led to important results in 388
understanding foraging strategies in bees (Apidae) (Pasquaretta et al., 2017) and 389
hummingbirds (Trochilidae) (Bateson et al., 2002). Several authors highlight that studying 390
animals in nature instead of in the laboratory provides more easily interpretable findings 391
(Cauchoix et al., 2017; Kumpan et al., 2020; Verhaeghen et al., 2012). Specific ethical 392
guidelines exist now for behavioral or psychological research in the wild (Costello et al., 393
2016; Soulsbury et al., 2020). The likely benefits and possible negative effects of researchers’ 394
presence and field methods on study subjects, their environment, and the local human 395
community should, of course, be considered (MacKinnon & Riley, 2010). 396
Progress has to be made first to avoid restraining animals in a captive environment and 397
second, to conduct tests on animals in more natural conditions. Such processes are applied 398
today to not only different primate species (Huebner et al., 2018; Schofield et al., 2019; Van 399
de Waal et al., 2013) but also to horses (Maeda et al., 2021; Matsuzawa, 2017), birds (Aplin 400
et al., 2015; Shaw, 2017), and even bees (Muth et al., 2018). These studies, conducted on 401
different species all showed that testing in the wild is more productive than testing in the 402
labs in terms of ecological and social cognition (Pritchard et al., 2016). An intermediate 403
method would be research in zoos. Zoos provide more adequate living conditions than many 404
laboratories. This seems to allow animals to express their agency (McEwen et al., 2022). 405
Testing these same species in more natural and more complex captive habitats or even in 406
natural settings could enhance the possibility of them expressing their agency. 407
3. Agency promotes the use of new technologies and vice-versa 408
Researchers need to change their way of thinking to a perspective of working with animals 409
rather than on animals. Researchers need to trust their capabilities (Nielsen, 2018; Nielsen, 410
2020) in order to increase research possibilities. Experimental setups, such as restraint chairs 411
or food privation, cause stress to animals and prevent them (both physically and mentally) 412
from fully expressing their agency. This challenge of giving animals more freedoms may 413
certainly takes time but would be hugely beneficial. Van Patter and Blattner (2020) suggest 414
core principles to follow with animals: non-maleficence, beneficence, and voluntary 415
participation (Webb et al., 2019). Positive methods exist and have proved to be efficient 416
(Laule et al., 2003; Prescott et al., 2010; Prescott, 2016; Prescott & Buchanan-Smith, 2003; 417
Prescott & Buchanan-Smith, 2007; Schapiro et al., 2003). Use of cooperation handling in 418
macaques instead of chair restraint leads to a diminution of stress, decreases the use of 419
sedation and increases behavioral acquisition (Graham et al., 2012). The readiness of 420
chimpanzees (which are no longer used for invasive experiments Matsuzawa, 2016b) to 421
voluntarily participate in interactions or allow humans to observe them can facilitate the 422
measurement of embryo development and brain activities in unanesthetized and 423
unrestrained individuals (Figure 2 - Matsuzawa,2013; Sakai et al., 2011, 2012; Ueno et al., 424
2010). Unrestrained or minimally restrained and voluntary animals can be trained to put 425
their head in a mask voluntarily (Slater et al., 2016) and be tested whilst receiving fruit juice. 426
This allows the measurement of different metrics with eye tracking (apes: Kano & 427
Tomonaga, 2009; Krupenye et al., 2016; monkeys: Machado & Nelson, 2011; Ryan et al., 428
2019) and non-invasive neuroimaging (Basso et al., 2021) (Figure 3.A). Magnetic resonance 429
imaging (MRI) requires the subject to remain still during the scan. Dogs can be trained to 430
remain still during fMRIs without any restriction (Berns & Cook, 2016). Surely, this 431
cooperation can be achieved with other species, allowing testing emotions and cognitive 432
capacities as done with humans (Cheng et al., 2010; Eisenberger et al., 2003; Yang et al., 433
2022; Yates et al., 2021). 434
Figure 2: (A) Developmental neuroscience. Fetal brain development in chimpanzees was 437
measured by a non-invasive ultrasound technique. (B) EEG recordings in a chimpanzee. The 438
chimpanzee quietly sat on the chair and allowed the experimenter to put electrode patches 439
on the skin of her forehead and the top of her head. Photos provided courtesy of Satoshi 440
Hirata. 441
Touchscreens are useful tools that demonstrate agency in nonhuman animals. Individuals 443
have to learn by themselves how to solve visual problems. Software running the displays and 444
data collection systems are easy to adapt to individuals’ cognitive capacities and perception. 445
Researchers can measure different parameters (time of answering the test, success, type of 446
answers) for each individual and species. The possibility of more freedoms of action can 447
produce individual and group specificity. For instance, Claidière et al. (2014) gave a task to 448
baboons (Papio papio) where they have to click on red squares on a 4*4 squares matrix. 449
Instead of forcing animals to answer specific patterns, the authors took into account how 450
baboons succeed to click on some patterns to transmit these patterns to other baboons and 451
showed evidence of cultural transmission in baboons as in humans. Some years ago, 452
applying the use of touchscreens with nonhuman animals, or studying mouse personality 453
was almost unimaginable in neuroscience. Yet today, these projects have become reality. For 454
instance, the use of a touchscreen was initially difficult but eventually, use of this testing 455
method led to tests of new concepts more quickly than tests without touchscreens in 456
chimpanzees (Gao et al., 2018; Inoue & Matsuzawa, 2007; Martinet et al., 2021) and 457
macaques (Ballesta et al., 2021; Ferrucci et al., 2019; Huskisson et al., 2021). In the same 458
vein, it took time for naïve capuchins (Sapajus sp.), macaques (Macaca sp.), and apes (Pan 459
troglodytes, Pongo pygmaeus abelii) to understand a food for - food exchange task (Dufour 460
et al., 2007; Pelé et al., 2009; Pelé et al., 2010; Ramseyer et al., 2006), but once the behavior 461
was acquired, it was easily transmitted from adults to their young (Pelé, personal 462
observation). Touchscreens or joysticks are now used to understand cognition (Kaneko & 463
Tomonaga, 2011) in a wide range of species (pigs Sus scrofa, macaques, baboonsPapio 464
papio, marmosets - Callithrix jacchus, goats, horses, rats, micemus musculus, etc.) (Belsey 465
et al., 2020; Calapai et al., 2022; Claidière et al., 2017; Croney & Boysen (2021); Jacobson et 466
al., 2019; Tomonaga et al., 2015; Washburn et al., 2004; Yang et al. 2022; Zeagler et al., 467
2014). Researchers trained archerfish (Toxotes chatareus) to spit on a touchscreen and 468
showed that they are able to differentiate human faces (Newport et al., 2016). However, 469
touchscreen technology is still limited despite its potential and even if more and more 470
neuroscience studies have been using it in mice or rats (Bussey et al., 1997, 2008; Delotterie 471
et al., 2015; Slutzky et al., 2010). So, touchscreens and joystick apparatuses promote animal 472
agency, even though it is in a limited artificial environment. However, these devices can be 473
extended to the wild and the principle of touchscreen (touching for a visual choice) should 474
be extended to other senses as it was done for testing auditory capabilities in common 475
marmosets (Calapai et al., 2022). 476
Other new technologies allow us to bring devices into natural settings to test unrestrained 477
animals in their natural (including social) environment, thus removing experimental sources 478
of stress and allowing them agency and expression of their entire behavioral repertoire. 479
Field experiments of this type are possible in many species including rodents (Evans et al. 480
2020; Lopes & König, 2020; Raulo et al., 2021). The animals can be identified individually by 481
observation or by using RFID techniques (Fehlmann & King, 2016) or via artificial intelligence 482
with the recognition of individuals by video tracking (Charpentier et al., 2020; Ferreira et al., 483
2020; Schofield et al., 2019). The latter removes the need to capture animals. RFID 484
techniques allowed demonstration, for example, that bats (Myotis bechsteinii) form long-485
term social relationships (Kerth et al., 2011) and that tits (Parus major) learned according to 486
their social networks (Aplin et al., 2015). Face and behavioral recognition using artificial 487
intelligence gave some indices about social networks in chimpanzees (Schofield et al., 2019) 488
and signaling kinship in mandrills (Mandrillus sphinx) (Charpentier et al., 2020). It could also 489
be extended to theory of mind and intentionality as gaze-following (Horschler et al., 2020) or 490
false belief attribution (Krupenye et al., 2016). 491
A general idea of how a laboratory- bound experimental method could be adapted for use 492
in a field experiment is given in Figure 3.B. A location is defined where different operable 493
devices can be installed, such as touchscreens, to deliver food or another valuable 494
commodity, with activation only for certain species and individuals. Researchers can imagine 495
implementing eye tracking and other apparatus in the wild when technology permits. This 496
could open up new research avenues in species that cannot be maintained in captivity. 497
Some automatic devices already exist to make some playback experiments as BoomBox: An 498
Automated Behavioral Response (ABR) camera trap module for wildlife experiments (Palmer 499
et al., 2022). Food containers of various kinds, have been used in field experiments (De la 500
Fuente et al., 2022; Van de Waal et al., 2013) and robots are increasingly used with wild 501
animals (Grémillet et al., 2012; Le Maho et al., 2014). Research possibilities in this domain 502
are huge. 503
Although there are logistical challenges attendant on any new methodology, we should 504
consider how to take advantage of technological advances to bring our science to animals in 505
natural settings, while ensuring the health and security of the animal participants. As 506
Schaefer and Claridge-Chang (2012) wrote, ‘the new automation is not just faster: it is also 507
allowing new kinds of experiments, many of which erase the boundaries of the traditional 508
neuroscience disciplines (psychology, ethology, and physiology) while producing insight into 509
problems that were otherwise opaque’ (p. 170). Figure 3 illustrates a hypothetical system for 510
conducting eye tracking while an individual voluntarily operates a touchscreen apparatus, in 511
the laboratory and in field settings. 512
Figure 3: (A) Hypothetical non-invasive neuroimaging and eye-tracking system with 515
touchscreen interactive component and voluntary participation in the laboratory. (B) 516
Hypothetical touchscreen system with voluntary engagement and individual identification in 517
the field. In setup A, the subject would show better agency than if it was restrained in a 518
chair. However, the same subject in setup B would show greater agency than in setup A, as it 519
is free to express its entire behavioral repertoire in natural conditions. The box is needed to 520
assure the isolation of the tested individual and the resistance of the materials to outside 521
conditions. This figure was realized using and Biorender. 522
Conclusion 524
Great efforts have been made toward enabling the agency of animals in behavioral research 525
but there is still much progress to be made to obtain a more compassionate, less stressful, 526
and more robust animal research model. This requires training and teaching researchers to 527
adopt new methods including animal agency and to change their view of the role animals 528
play in research (see for instance the book “Handbook of Primate Behavioral Management” 529
Schapiro, 2017, for methods to achieve voluntary participation of primates in various health-530
related and husbandry procedures). Animals are agents in scientific research. They are active 531
in the research process and agency may promote the use of new technologies. This 532
recognition of animals as agents rather than objects is not approved by some researchers, 533
who consider that this position is tantamount to committing over-anthropomorphism, and 534
overstepping the will of animals to cooperate. However, acknowledging animal agency could 535
facilitate broader social acceptance of research with nonhuman animals (Webb et al., 2019) 536
and be of benefit to the animals concerned (supporting well-being through learning, 537
creating, and participating Franks et al., 2020). 538
Considering the agency of the animals we work with is clearly a time investment that 539
ultimately pays off for more time-efficient data collection in the long term. This time 540
investment in animal agency should be highlighted and recognized as promoting animal 541
welfare (in the same way as plans for adoption research animals, for instance) when 542
readying a proposal for financial support. This new way of viewing animal agency can 543
therefore raise critical ethical questions in regard to the treatment of animals in research 544
and to the place humans grant them in the human social world. 545
Author Contributions Statement 547
Conceptualization: CS and MP; Project administration: CS and MP; Writing original draft: CS; 548
Review and editions: all authors. 549
Acknowledgments 551
We thank the three anonymous reviewers who accepted to revise our manuscript and the 552
editor Dorothy Fragaszy for their helpful comments. 553
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