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Pigs learn what a mirror image represents and use it to obtain information

Authors:
  • BioInnova Laboratory

Abstract

Mirror usage has been taken to indicate some degree of awareness in animals. Can pigs, Sus scrofa, obtain information from a mirror? When put in a pen with a mirror in it, young pigs made movements while apparently looking at their image. After 5 h spent with a mirror, the pigs were shown a familiar food bowl, visible in the mirror but hidden behind a solid barrier. Seven out of eight pigs found the food bowl in a mean of 23 s by going away from the mirror and around the barrier. Naïve pigs shown the same looked behind the mirror. The pigs were not locating the food bowl by odour, did not have a preference for the area where the food bowl was and did not go to that area when the food bowl was visible elsewhere. To use information from a mirror and find a food bowl, each pig must have observed features of its surroundings, remembered these and its own actions, deduced relationships among observed and remembered features and acted accordingly. This ability indicates assessment awareness in pigs. The results may have some effects on the design of housing conditions for pigs and may lead to better pig welfare.
1"
Broom, D.M., Sena, H. and Moynihan, K.L. 2009. Pigs learn what a mirror image 1"
represents and use it to obtain information. Anim. Behav., 78, 1037-1041. 2"
DOI: 10.1016/j.anbehav.2009.07.027 3"
4"
5"
Pre-publication copy 6"
Pigs learn what a mirror image represents and use it to obtain information 7"
8"
Donald M. Broom, Hilana Sena and Kiera L. Moynihan 9"
Centre for Animal Welfare and Anthrozoology 10"
Department of Veterinary Medicine 11"
University of Cambridge 12"
Madingley Road, Cambridge CB3 0ES, U.K. 13"
14"
Correspondence: D. M. Broom, Centre for Animal Welfare and Anthrozoology, 15"
Department of Veterinary Medicine, University of Cambridge, Madingley Road, 16"
Cambridge CB3 0ES, U.K. dmb16@cam.ac.uk. 17"
18"
ABSTRACT 19"
Mirror usage has been taken to indicate some degree of awareness in animals. Can pigs 20"
obtain information from a mirror? When put in a pen with a mirror in it, young pigs 21"
made movements while apparently looking at their image. After 5 hours spent with a 22"
mirror, the pigs were shown a familiar food bowl, visible in the mirror but hidden 23"
behind a solid barrier. Seven out of eight pigs found the food bowl in a mean of 23s by 24"
going away from the mirror and around the barrier. Naïve pigs shown the same, looked 25"
behind the mirror. The pigs were not locating the food bowl by odour, did not have a 26"
preference for the area where the food bowl was and did not go to that area when the 27"
food bowl was visible elsewhere. To use information from a mirror and find a food 28"
bowl, each pig must have observed features of its surroundings, remembered these and 29"
its own actions, deduced relationships among observed and remembered features and 30"
acted accordingly. This ability indicates assessment awareness in pigs. The results may 31"
2"
have some effects on the design of housing conditions for pigs and may lead to better 32"
pig welfare. 33"
34"
Keywords: awareness, cognition, learning, mirror, pigs, 35"
36"
INTRODUCTION 37"
38"
The E.U. Treaty of Amsterdam refers to domestic animals as sentient and a sentient 39"
being has been defined as “one that has some ability: to evaluate the actions of others in 40"
relation to itself and third parties, to remember some of its own actions and their 41"
consequences, to assess risk, to have some feelings and to have some degree of 42"
awareness” (Broom 2007). Hence the extent to which an animal can learn about 43"
complex aspects of its world and the level of awareness which it has can influence 44"
human attitudes to the moral status of such animals and hence the ways in which they 45"
are treated (Mendl et al 2001, Broom 2003). 46"
Griffin (1981) said that awareness involves the experiencing of inter-related mental 47"
images and awareness has been defined as “a state in which complex brain analysis is 48"
used to process sensory stimuli or constructs based on memory” (Broom 1998). The 49"
term “complex brain analysis” implies that there is some degree of interpretive thought 50"
over and above perceptual processing and a gradation has been proposed with four 51"
categories of awareness: unaware but responsive, perceptual awareness, cognitive 52"
awareness, assessment awareness and executive awareness (Sommerville and Broom 53"
1998). For example, in assessment awareness the individual is able to assess and deduce 54"
the significance of a situation in relation to itself over a short time span. The individual 55"
would not only be sensible to stimuli but would have memory of events and mental 56"
images of non-current events that could be used when taking appropriate action, both to 57"
avoid the negative and to increase positive consequences. This use of the concept of 58"
awareness is similar to that of Snyder et al (2004) who refer to awareness of concepts 59"
and equate consciousness with executive awareness. Mendl and Paul (2004, 2008) 60"
discuss “basic awareness” of sensations, feelings, emotions and memories. One level of 61"
self-cognition is to be self-referent and to discriminate labels of self from labels of non-62"
self (Hauber and Sherman 2001) and this has been described as different from being 63"
self-aware “the cognitive process that enables an individual to discriminate between its 64"
3"
own body or possessions from those of others” Bekoff and Sherman 2004). However, 65"
this is a description of a consequence rather than a definition of self-aware as an 66"
individual could be self-aware in the absence of any cue from others. Most discussions 67"
of awareness refer to the social context and to whether animals are able to infer the 68"
mental states of others (Gallup 1998). 69"
A prediction if an individual can have assessment awareness is that if it has a novel 70"
visual experience, like viewing images in a mirror, this could be followed by learning 71"
about what it sees in the mirror in relation to itself and then using such information at a 72"
later time. Human infants can use mirrors in the course of shape discrimination (Itakura 73"
and Imamizu 1994) and, if given sufficient exposure to mirrors at appropriate age, will 74"
discover the contingency between visual and proprioceptive feedback from their own 75"
body movements (Lewis and Brooks-Guy 1979). At five months of age they look more 76"
at their own image in a mirror than at the image of another infant or a puppet (Bahnick 77"
et al 1996) and at nine months they are able to discriminate self from other in a mirror 78"
(Rochat and Striano 2002). At 14-18 months, when looking in a mirror infants are 79"
described as showing self-referencing activities, self-labeling and embarrassment at 80"
rouge on the face (Bertenthal and Fisher 1987). These children would have been told 81"
that the image in the mirror is of themselves. Povinelli et al (1996) allowed children to 82"
see a television image of themselves, very similar to a mirror image, and found that 83"
when a sticker was put on their head, no 2-year-olds reached for the sticker, 25% of 84"
three-year-olds reached for it and 75% of 4-year-olds reached for it. Also using live 85"
television images, Menzel et al (1985) reported that chimpanzees could use these 86"
images to find targets visible only on the television screen. Iriki et al (2001) observed 87"
that Japanese monkeys could use televised images of their hands to pick up food while 88"
Anderson et al (2009), showed live television images of themselves to capuchin 89"
monkeys and concluded that their behaviour strongly suggested recognition of the 90"
correspondence between kinaesthetic information and external visual effects. Dolphins 91"
have been reported to use a television image, apparently to explore themselves visually 92"
(Marten and Psakoros 1995). Tests with chimpanzees, an elephant, dolphins and 93"
magpies that had had previous experience of mirrors, using marks on the body visible 94"
in a mirror, led to the individuals touching or apparently looking at the marks (Gallup 95"
1982, Reiss and Marino 2001, Plotnik et al 2006, Prior et al 2008). 96"
4"
The abilities indicated by these mirror and television image studies range from 97"
discrimination of images, through learning that what is seen in a mirror is on the same 98"
side as the observer, learning that own movements can be monitored by looking at the 99"
mirror, to appreciating that the image is the self. As Rochat (2002) puts it, in this last 100"
case the specular image is standing for the identified or conceptual self, not somebody 101"
else, and the self is as seen by others. 102"
Pigs have complex social behaviour (Jensen 1982, Broom and Fraser 2007) and a 103"
series of experimental studies have also provided evidence of their substantial cognitive 104"
ability (Mendl et al 1997, 2001, Croney et al 2003, Laughlin and Mendl 2004, Held et al 105"
2005). For example, pigs can recall where food was encountered, integrate this 106"
information with information about type of food and replenishment rate and avoid 107"
unproductive visits to potential food sites (Mendl and Paul 2008). The present study 108"
was designed to find out whether or not pigs could use information from a mirror to 109"
locate an object that could only be seen in the mirror. Pigs which had not had 110"
experience of a mirror were compared with pigs which had. 111"
The vision of pigs is adequate for mirror images to be perceived and eyeball size, 112"
retina, pupil and lens are similar to those of humans (Piggins 1992, Zonderland et al 113"
2007). Pigs have fewer cone cells than humans so their spatial discrimination is poorer 114"
(Zonderland et al 2007). However they show preferences for food bowls of certain 115"
colours (Deligeorgis et al 2006). Olfactory signals are used for social recognition and 116"
regulation of sexual behaviour but pigs can successfully find food sources using visual 117"
or olfactory cues (Kristenson et al 2001, Croney et al 2003, Zonderland et al 2007). 118"
In a preliminary study the behaviour of pigs was recorded when they first encountered 119"
a mirror and after 24 hours with it. The response of pigs naïve to a mirror was then 120"
compared with pigs with five hours experience of a mirror when they saw a food bowl 121"
reflected in the mirror. The distribution of time in different parts of the test pen prior to 122"
seeing the food bowl in the pen was also observed in separate trials. In a subsequent 123"
test, the mirror was replaced by wire-mesh with the food in the position visually the 124"
same as when the mirror was present. 125"
METHODS 126"
The subjects were 4-8 week Large White x Landrace pigs housed in strawed pens 127"
with natural light and food and water ad libitum. All were familiarised with a red food 128"
5"
bowl as a food container. None had seen a mirror, or other reflecting surface, before the 129"
studies described here. 130"
The trials took place in a 4.6 x 2.8 m. strawed pen located approximately 30 m away 131"
from the home pen. All behaviour was video-recorded. The 0.6 x 0.7 m. mirror was in a 132"
1.2 x 1.4 m. frame. A 1.7 m. long 1.4 m. high barrier could be attached to the mirror 133"
frame, 0.09 m. from the mirror, so the pig couldn’t pull it and pass between it and the 134"
frame (Fig. 1). In the preliminary study, seven pigs were put individually into the pen 135"
for 24 hours with the mirror and food present. Their behaviour was recorded for the first 136"
two hours and from 23 to 24 hours. 137"
During the trials with the mirror and food bowl (Mirror Test), the pig was put in a small 138"
pen (area 7) with solid wooden walls. A curtain covered the exit from the small pen so 139"
that the pig could not see outside it. The curtain was opened and the pig left inside this 140"
small pen for 1 minute before the front gate of the small pen was opened with a pulley 141"
to allow the pig to leave. During the minute before the gate was opened in the Mirror 142"
Test the pig could see the barrier and the right hand side of the mirror with the image of 143"
the food bowl through the front section. When in Area 4 or Area 7 the pig could see the 144"
food bowl but could not see whether or not there was food in it. 145"
146"
147"
148"
6"
Fig. 1 Plan of the pen where the experiments were carried out, showing the small pen with solid walls 149"
(area 7), mirror (or wire mesh) in a frame, solid wood barrier, fan position (above pig head level in the 150"
pen) and the numbers of floor sections used to describe the position of the pig. Area 3 is where the red 151"
food bowl, whose reflection was visible in the mirror when the pig was in areas 4 or 7, was placed during 152"
the mirror test. The food bowl would appear to be in area 1 to a naïve pig that had not had experience 153"
with a mirror. 154"
155"
156"
The mirror tests were carried out during nine non-consecutive weeks between 09.00 157"
and 18.00 hours. Firstly, pigs with no previous experience of a mirror were tested, then 158"
pigs that had experience with a mirror. 159"
160"
Eleven “mirror naïve” pigs, six males and five females, which had never seen a mirror 161"
were released, singly, into the pen (Fig. 1) with the red food bowl, containing food, 162"
present on the left side of the barrier and visible only in the mirror. A fan was 163"
positioned slightly behind and above the food. This was intended to ensure that the 164"
smell of the food could not be localised by the pig. Observation of the movement of 165"
particles in the air indicated that air flowed initially from the front towards the back of 166"
the pen but then became mixed throughout the pen. The behaviour of the pigs was 167"
recorded during the Mirror Test with the intention of continuing for one minute or, if it 168"
occurred earlier, until the pig moved behind the barrier or mirror. Each of the 11 pigs 169"
was observed in the Mirror Test once and not used in any subsequent test. 170"
171"
In order that the “mirror experienced” would have the opportunity to learn about a 172"
mirror, eight pigs, four females and four males, were put into the pen with a mirror in it 173"
for 5h. They were in pairs, so that they would not associate the visits to the pen with 174"
social isolation. This provided company but also allowed them to observe the other 175"
animal as a moving reference point in the mirror. The subsequent tests, described 176"
below, were conducted on the same day. 177"
178"
In order to find out where the “mirror experienced” pigs would go by chance in the test 179"
pen after leaving the small pen, two males and two females were observed. Only four of 180"
the eight pigs used in the Mirror Test were used because the desirability of this control 181"
study was only appreciated after the first four pigs had been tested. They were left in the 182"
small pen for 15 s and then allowed to go out of it for 25 s. The barrier and mirror were 183"
7"
in place but no food or food bowl was present. The amount of time spent in areas 1 to 7, 184"
including area 1 behind the mirror and area 3 where the food was located in the mirror 185"
test, was recorded. 186"
187"
The Mirror Tests were done once with each of eight “mirror experienced” animals using 188"
the pen shown in Fig. 1. The bowl with food was placed on the left side of the barrier in 189"
such a way that it could be seen from the small pen via the mirror. Each pig was in the 190"
Area 7 pen and then released, as explained above. After release it was left in the test pen 191"
for a maximum of one minute and its behaviour video-recorded. 192"
193"
After the “mirror experienced” pigs had completed the Mirror Test, in order to check 194"
whether the pigs had just changed their behaviour to show a preference for Area 3 195"
(behind the barrier) wire mesh of mesh diameter approximately 3 cm was put in the 196"
frame in place of the mirror. The food in the food bowl was put behind the frame so the 197"
pig could see it through the wire mesh in the same position that a mirror image would 198"
appear to have. The same methodology was used in the Wire-Mesh Test as in the 199"
Mirror Test for each of the eight pigs. In an extra, subsequent test, with only the last of 200"
the pigs previously tested, wire-mesh was in place of the mirror, the familiar bowl 201"
behind the wire-mesh was clean and empty and there was food in a bowl on the other 202"
side of the barrier, i.e. in the place where the food was put in the Mirror Test. 203"
204"
205"
206"
RESULTS 207"
208"
Initial observations: qualitative descriptions of first contact with the mirror 209"
When first encountering the mirror, all seven pigs whose behaviour was recorded in 210"
detail walked towards it, sometimes vocalising, stopped with nose pointing towards the 211"
mirror, moved forward again and made contact with the mirror surface with their nose. 212"
Some pigs looked behind the mirror after looking at their reflection in it. One female 213"
pig, observed during preliminary studies, moved rapidly towards the mirror and broke 214"
it, perhaps attacking her mirror image. After initially encountering the mirror the pigs 215"
moved back from the mirror surface, oriented nose and eyes towards it apparently 216"
looking at it and made movements looking again from different angles. Three pigs 217"
8"
showed some weaving movements. In the preliminary studies, the mean time before 218"
there was a break of more than 30s in attending to the mirror was 20 minutes. Some 219"
habituation to the mirror was apparent and from 23 to 24 hours after the mirror was put 220"
in the pen, much less time was spent looking at it than in the first hour. Similar 221"
behaviour was shown during the 5h exposure to the mirror by the pigs that would 222"
experience the Mirror Test. Sometimes pigs lay down in front of the mirror, looking at 223"
it or in parallel with it as if lying beside another pig. 224"
225"
“Mirror naïve” pigs in the Mirror Test. 226"
Of the eleven pigs that had never seen a mirror, in the Mirror Test where they could 227"
see a familiar food bowl reflected in a mirror, but not directly visible because it was 228"
behind the barrier, nine approached the mirror then walked behind it to area 1 (Table 1). 229"
One pig knocked over the barrier and one walked around the whole pen including going 230"
behind the barrier. In each case, the trial was then terminated. The nine pigs that went 231"
behind the mirror did so in 15-50 seconds (mean 25.7, s.d. 11.6). 232"
233"
“Mirror experienced” pigs: activity in Mirror Test pen prior to Mirror Test. 234"
The animals observed were able to go anywhere in the test pen for 25s with no food 235"
present, so the total time, during four repeats for 4 animals, was 400 seconds. In the 16 236"
periods, Area 1 was visited by three pigs on one occasion each whilst Area 3 was 237"
visited by four pigs on one occasion each as the pig walked around the pen. The total 238"
time spent in Area 3 was 66s (mean per individual 16.5s, S.D. 9.8). The 66s spent in 239"
Area 3 out of a total time observed of 400 s gives a probability of one in six of a pig in 240"
this pen being in Area 3 at any one time and a probability of one in four of visiting Area 241"
3. A statistical comparison with Mirror Test data is not accurate because some cell sizes 242"
are too small. 243"
244"
245"
“Mirror experienced” pigs in the Mirror Test. 246"
When the eight pigs with previous experience of the mirror were released from the 247"
small pen during the Mirror Test, they walked out, looked around the test pen and 248"
looked at the mirror where the food dish was visible. Seven of the eight pigs went to 249"
Area 3 on the left side of the barrier and reached the food (Table 1). They all moved 250"
away from the mirror, around the end of the barrier, and then directly to the food. The 251"
9"
times taken to reach it were 11s, 29s, 23s, 10s, 46s, 13s, 32s, mean 23.4 s, S.D. 13.3s. 252"
One pig took 41s to decide and then went to Area 1 behind the mirror. For comparisons 253"
of the numbers of naïve and experienced pigs reaching Area 1: p<0.01 and Area 3: 254"
p<0.01 (Fisher Exact Test). 255"
256"
Table 1. Comparison of “Mirror naïve” and “Mirror experienced” pigs in the Mirror 257"
Test and Wire-Mesh Test. 258"
“Mirror naïve” “Mirror experienced” “Mirror experienced” 259"
Mirror present Wire-Mesh present 260"
n 11 8 8 261"
Number going to: 262"
Area 1 (behind mirror) 9 1 6 263"
Area 3 (with food bowl) 1 7 2 264"
Other action 1 265"
266"
Mean latency if reached Area 1 41s (n=1) 14s SD 3.9s 267"
Mean latency if reached Area 3 23s SD 13.3s 43s (n=2) 268"
269"
270"
“Mirror experienced” pigs in the Wire-Mesh Test. 271"
In this test, conducted after the Mirror Test, six of eight pigs went to Area 1, behind 272"
the wire-mesh frame, and reached the food (Table 1). Of the two pigs that went to Area 273"
3, one took 44s to decide and was the individual that did not reach the food in the 274"
Mirror Test, whilst the other took 42s to decide before going to the wrong place. Both 275"
showed frequent hesitation when moving. Comparing 6 out of 8 pigs going to Area 1 276"
with 1 out of 8 in the Mirror Test, p < 0.01 (Fisher Exact Test). In the test on a single 277"
pig with an empty bowl behind the wire mesh and a full food bowl behind the barrier, 278"
the pig went behind the mirror to the empty bowl in Area 1. 279"
280"
281"
282"
DISCUSSION 283"
284"
10"
The aim of this study was to find out whether or not pigs can obtain information from 285"
a mirror, as has been demonstrated for humans and other primates, dolphins, elephants, 286"
magpies and an African grey parrot (Pepperberg et al 1995). The 4-6-week-old pigs 287"
studied responded to a mirror initially as if to another pig but later by looking at it as 288"
they moved. They moved and then stopped still, apparently looking at their image and 289"
its surroundings, oriented either with nose towards the mirror or with the head parallel 290"
to it. As a consequence of the lateral position of the pig’s eye, it is not possible to record 291"
duration of looks towards the mirror and pigs show little change in facial expression. 292"
They do vocalise and some of these pigs did so when exposed to the mirror. As with the 293"
movements in front of a novel mirror described for chimpanzees, humans, capuchin 294"
monkeys, dolphins and elephants (Gallup 1982, Reiss and Marino 2001, Keenan et al 295"
2003, Plotnik et al 2006, Anderson et al 2009) some of the movements of these young 296"
pigs suggest that they could have been monitoring the movements in the mirror image 297"
when they moved their own head or body. As Anderson et al (2009) put it, the animals 298"
could be comparing the kinaesthetic information and the external visual effects. 299"
300"
Although the naïve pigs exposed to the Mirror Test went behind the mirror to the 301"
apparent position of the food bowl, five hours experience with the mirror in a pen 302"
changed the behaviour of the pigs. When they were subjected to the Mirror Test, all but 303"
one of them went away from the mirror to the actual position of the food bowl within 304"
23s. This movement is first with the air-stream, then against it. The results in total, in 305"
particular the difference between the naïve and mirror-experienced pigs, makes it clear 306"
that the pigs were not locating the food bowl by odour. Pigs often use smell to reach 307"
food (Zonderland et al 2007), but the fan blew air away from the food bowl and 308"
circulated it in the pen. The single pig in the Wire Mesh Test that could see a bowl 309"
through the wire mesh but could not see that the bowl was empty went to the empty 310"
bowl rather than to a bowl containing food behind the barrier. It would seem that 311"
localisation of the food bowl when the fan was on was impossible, or at least more 312"
difficult than using the visual information. The association between visual cues and 313"
food reward is sometimes not an easy task for pigs (Zonderland et al 2007) but it seems 314"
that they learned how to do so in this study. They also learned in five hours to use the 315"
mirror in a way that later allowed them to locate the food. In the Mirror Test, “mirror 316"
experienced” pigs went to the position of the food behind the barrier in Area 3 much 317"
11"
more often than had four of their number, after mirror experience but prior to the Mirror 318"
Test, when their activity was monitored in the Mirror Test pen with no food in it. 319"
320"
The possibility that all pigs had developed a preference for Area 3 at the time of the 321"
Mirror Test was shown not to be the case when the same animals were tested soon 322"
afterwards with the wire-mesh in place of the mirror (Wire-Mesh Test) and six out of 323"
eight went to the food bowl behind the wire mesh in Area 1. One pig went to the wrong 324"
side in both trials, behind the mirror (Area 1) in the Mirror Test and to the left side of 325"
the barrier (Area 3) in the Wire-Mesh Test. This animal either could not learn, or did 326"
not have enough time to learn, about a mirror as it was confused in both trials, taking 41 327"
s and 44 s respectively. Another pig, which reached the food in the Mirror Test but not 328"
in the Wire-Mesh Test, also seemed to be confused in the latter and took 42 s to decide 329"
to go to the left side of the barrier (Area 3) instead of the back of the frame where the 330"
food bowl was located. 331"
332"
A reflecting surface, such as the mirror, was novel to the pigs studied and changes in 333"
their behaviour were apparent when they were exposed to the mirror. Each of the seven 334"
pigs that used information from the mirror and rapidly found the food bowl must have: 335"
observed features of its surroundings, remembered these and its own actions, deduced 336"
relationships among observed and remembered features, and acted accordingly. When a 337"
mirror-experienced pig saw the food in the mirror, it could not smell the food directly, 338"
although it was likely to be able to detect the presence of food throughout the test 339"
period. 340"
341"
The pig has looked at the mirror and appreciated that what it sees is related to its own 342"
movements and that the image reveals objects that are not directly visible and that have 343"
an actual position that has a certain relationship with where they appear to be. When it 344"
looked at the red bowl and then turned away from the mirror to go around the barrier, it 345"
must have remembered that the mirror image gives information about what is positioned 346"
somewhere to the left of perpendicular to the mirror surface. The action of turning away 347"
from the mirror and going behind the barrier to reach the food bowl necessitates 348"
remembering the position of the food while it is navigating around the barrier. The 349"
concept of the food and its position must be remembered while it is carrying out the 350"
12"
actions to get to the food. Some kind of map of its environment and awareness of its 351"
movement ability is needed to do this. The behaviours and ability shown fulfil the 352"
criteria described above for assessment awareness (Sommerville and Broom 1998). 353"
In studies of human infants, and in most studies of other Primates, with mirrors or 354"
television self images, the subjects had prolonged experiences of the images. Human 355"
subjects are generally given much information about mirror images and television 356"
images by their parents and others. The pigs in this study had only five hours of 357"
experience of a mirror before they demonstrated that they could use information from it. 358"
However, no test for self-recognition has been conducted on pigs. Just as in other 359"
studies, e.g. that of Paukner et al (2004) with capuchin monkeys, information from a 360"
mirror or television self-image does not necessarily imply awareness by the subject that 361"
the image is that of itself. 362"
Work with various species of animals indicates that the presence of a mirror or 363"
television image may add complexity to the environment of an individual and improve 364"
its welfare (Plattner and Novak 1997, McAfee et al 2002). These abilities of pigs, and 365"
the awareness indicated by them, may result in some people housing and treating pigs 366"
better than previously, so that poor welfare is minimised. The relationship between the 367"
cognitive ability of animals, sentience and how they should be treated is discussed by 368"
Mendl et al (2001), Broom (2003, 2007), Panksepp (2005), Webster (2006). 369"
ACKNOWLEDGEMENTS 370"
We thank Sophie Prowse for help in caring for pigs, supplying materials and practical 371"
guidance, Francisco Bernal for loan of a camera, Gregorio Pesinato for help during 372"
experimental trials and the editor and reviewers for helpful suggestions.. 373"
374"
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Lay summary (150 words). 471"
How clever are pigs? We tested whether pigs can learn that what they see in a mirror is 472"
in front of it in a certain position and not behind it. Young pigs, shown a mirror for five 473"
hours, moved while apparently looking at their image. Afterwards, the pigs were shown 474"
a familiar food bowl, visible in the mirror but hidden behind a solid barrier. Seven out 475"
of eight pigs rapidly found the food bowl by going away from the mirror and around the 476"
barrier. Naïve pigs shown the same, looked behind the mirror. The pigs were not 477"
locating the food bowl by odour and did not have a preference for the area where the 478"
food bowl was. In order to be aware of the food bowl position, each pig must have 479"
learned how to use a mirror image. Views about pig management and welfare may be 480"
changed by such results. 481"
For version with Figure contact authors. 482"
Figure 1. Plan of the pen where the tests were carried out, showing the small pen with 483"
solid walls (Area 7), mirror (or wire mesh) in a frame, solid wood barrier, fan position 484"
(above pig head level in the pen) and the numbers of floor sections used to describe 485"
the position of the pig. Area 3 is where the red food bowl, whose reflection was visible 486"
in the mirror when the pig was in Areas 4 or 7, was placed during the Mirror Test. The 487"
food bowl would appear 488"
... For example, a study recently demonstrated that a tiny fish, the cleaner wrasse (Labroides dimidiatus) passed the mirror mark test (Kohda et al., 2019), joining an 'elite' handful of other species including chimpanzees (Gallup, 1970), dolphins (Reiss & Marino, 2001), Asian elephants (Plotnik et al., 2006) and Eurasian magpies (Prior et al., 2008). Other animals such as pigs and parrots might be suitable candidates for passing the mirror mark test, as they are able to use a mirror as visual information to find hidden items (Pepperberg et al., 1995;Broom et al., 2009). The mirror mark test involves placing a mark on an animal in a location that can only be seen in a mirror reflection. ...
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The number of animals bred, raised, and slaughtered each year is on the rise, resulting in increasing impacts to welfare. Farmed animals are also becoming more diverse, ranging from pigs to bees. The diversity and number of species farmed invite questions about how best to allocate currently limited resources towards safeguarding and improving welfare. This is of the utmost concern to animal welfare funders and effective altruism advocates, who are responsible for targeting the areas most likely to cause harm. For example, is tail docking worse for pigs than beak trimming is for chickens in terms of their pain, suffering, and general experience? Or are the welfare impacts equal? Answering these questions requires making an interspecies welfare comparison; a judgment about how good or bad different species fare relative to one another. Here, we outline and discuss an empirical methodology that aims to improve our ability to make interspecies welfare comparisons by investigating welfare range, which refers to how good or bad animals can fare. Beginning with a theory of welfare, we operationalize that theory by identifying metrics that are defensible proxies for measuring welfare, including cognitive, affective, behavioral, and neuro-biological measures. Differential weights are assigned to those proxies that reflect their evidential value for the determinants of welfare, such as the Delphi structured deliberation method with a panel of experts. The evidence should then be reviewed and its quality scored to ascertain whether particular taxa may possess the proxies in question to construct a taxon-level welfare range profile. Finally, using a Monte Carlo simulation, an overall estimate of comparative welfare range relative to a hypothetical index species can be generated. Interspecies welfare comparisons will help facilitate empirically informed decision-making to streamline the allocation of resources and ultimately better prioritize and improve animal welfare.
... We focus on pig production because pork accounts for 32% of meat consumption worldwide (FAOSTAT, 2022) and demand is predicted to grow by up to 54% between 2005 and 2050 (Lassaletta et al., 2019). We focus on four externality costs where urgent mitigation is needed and where pig production imposes substantial burdens: land use because pig production already uses 8.5% of arable land (Poore and Nemecek, 2018); GHG emissions (GHGs) because pig production accounts for 9% of GHGs from livestock (Gerber et al., 2013); antimicrobial use (AMU) as pig production uses more antimicrobials than any other livestock sector (Van Boeckel et al., 2015); and welfare because pigs are highly sentient and intelligent (Broom, Sena and Moynihan, 2009). ...
Thesis
Livestock farming generates some striking externalities; whilst it provides 30% of human dietary protein, it occupies 75% of agricultural land, emits 14-17% of anthropogenic greenhouse gas emissions, and uses more antimicrobials than human medicine. Demand for livestock products is high and rising, especially for pork which has quadrupled in the past 50 years. Livestock farming systems vary considerably in the scale of their externalities, but our understanding of how multiple externalities co-vary across contrasting production systems is limited. Research typically focuses on impacts in isolation, and the synergies or tradeoffs among them are assumed. To identify and promote the types of systems that best limit impacts or even carry co-benefits we need to explicitly consider multiple externalities and evaluate them across a wide range of alternative production systems. The main aim of my thesis was to do this for pig production. I recruited, visited, and evaluated over 100 pig farms in the UK and Brazil from those considered to be the most “intensive” through to those certified as Organic. My analyses treat a breed-to-finish system as a datapoint, which may consist of one or several farms (e.g. breeding, rearing and finishing farms). I developed metrics which advanced the quantitative characterisation of farm animal welfare to be compatible with life cycle assessments and to account for both quality of life and the quantity of life years required to produce a unit of product (Chapter 2). I systematically evaluated two externality costs that are commonly perceived to trade off against one another: land use and antimicrobial use (Chapter 3). I found weak evidence of a tradeoff between these externalities but importantly also found several systems characterised by low externality costs in both domains. These systems were spread across different label and husbandry types, and no type was an indicator of systems that performed well in both domains. I built upon these assessments of one or two costs by systematically contrasting the land use, greenhouse gas emissions, antimicrobial use and animal welfare of as many of my UK and Brazilian pig systems as possible (Chapter 4). I found evidence of positive associations between land use and greenhouse gas emissions, and antimicrobial use and poor animal welfare, but tradeoffs between these pairs of externalities - systems with low land use generally had low greenhouse gas emissions, but high antimicrobial use and poor welfare. Again however, I found systems that carried relatively low externality costs in all domains. I 6 conclude that contrary to prevailing wisdom, tradeoffs among these externalities are not inevitable. In parallel with this detailed work on pig production, I explored the viral zoonotic emerging infectious disease risks of contrasting ways of meeting livestock product demand (Chapter 5). Analyses to date typically ignore how land use affects emerging infectious disease risks. I created a framework that considered risk factors associated with livestock management and land use. I identified significant knowledge gaps and argued these shortfalls in understanding mean we cannot currently determine whether lower- or higher-yielding systems would better limit the risk of future pandemics. My findings challenge many commonly held perceptions about the externalities of farming systems and have important implications for mitigation strategies. My work illustrates the importance of using empirical evidence rather than relying on patchily supported assumptions. I believe that this warrants the systematic testing of other assumed relationships among externalities. I addressed some important knowledge gaps for the pork sector, and more broadly for emerging infectious disease risks, but the same must be done on a much larger scale, spanning other externalities and sectors.
... On the first level of self-awareness, the individual understands the difference between the reflection and the environment and observes the contingency between its own movements and the reflection which on the second level is followed by an understanding of the connection between the proprioceptive experience of the movement and the reflected image (as seen in contingency checking behaviors, which have also been observed in nonhuman species Povinelli et al. 1993;Ari and D'Agostino 2016;Vanhooland et al. 2020)). An alternative approach to investigate these levels of mirror understanding seen in the non-human animal literature has been to look at a species' ability to use a mirror to locate, e.g., food (Anderson 1986;Pepperberg et al. 1995;Broom et al. 2009;Medina et al. 2011) or conspecifics (Itakura 1987). On the third level, individuals are able to identify themselves in the reflection and show signs in line with self-recognition (i.e., self-directed behaviors and mark removals in the mark test), as observed in very few non-human animal species passing this task (as discussed above). ...
Article
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Mirror self-recognition (MSR) assessed by the Mark Test has been the staple test for the study of animal self-awareness. When tested in this paradigm, corvid species return discrepant results, with only the Eurasian magpies and the Indian house crow successfully passing the test so far, whereas multiple other corvid species fail. The lack of replicability of these positive results and the large divergence in applied methodologies calls into question whether the observed differences are in fact phylogenetic or methodological, and, if so, which factors facilitate the expression of MSR in some corvids. In this study, we (1) present new results on the self-recognition abilities of common ravens, (2) replicate results of azure-winged magpies, and (3) compare the mirror responses and performances in the mark test of these two corvid species with a third corvid species: carrion crows, previously tested following the same experimental procedure. Our results show interspecies differences in the approach of and the response to the mirror during the mirror exposure phase of the experiment as well as in the subsequent mark test. However, the performances of these species in the Mark Test do not provide any evidence for their ability of self-recognition. Our results add to the ongoing discussion about the convergent evolution of MSR and we advocate for consistent methodologies and procedures in comparing this ability across species to advance this discussion.
... Variations of this test have been applied to many species of vertebrates. Most often, the results are clearly negative, including studies on lesser apes, monkeys, pig, dog, cat, panda, crows, and parrots (e.g., [1][2]5,[8][9][10][11][12][13][14][15][16]). However, a small number of socially intelligent species including a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 ...
Article
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An animal that tries to remove a mark from its body that is only visible when looking into a mirror displays the capacity for mirror self-recognition (MSR), which has been interpreted as evidence for self-awareness. Conservative interpretations of existing data conclude that convincing evidence for MSR is currently restricted to great apes. Here, we address proposed shortcomings of a previous study on MSR in the cleaner wrasse Labroides dimidiatus , by varying preexposure to mirrors and by marking individuals with different colors. We found that (1) 14/14 new individuals scraped their throat when a brown mark had been provisioned, but only in the presence of a mirror; (2) blue and green color marks did not elicit scraping; (3) intentionally injecting the mark deeper beneath the skin reliably elicited spontaneous scraping in the absence of a mirror; (4) mirror-naive individuals injected with a brown mark scraped their throat with lower probability and/or lower frequency compared to mirror-experienced individuals; (5) in contrast to the mirror images, seeing another fish with the same marking did not induce throat scraping; and (6) moving the mirror to another location did not elicit renewed aggression in mirror-experienced individuals. Taken together, these results increase our confidence that cleaner fish indeed pass the mark test, although only if it is presented in ecologically relevant contexts. Therefore, we reiterate the conclusion of the previous study that either self-awareness in animals or the validity of the mirror test needs to be revised.
... Such instrumental mirror use tasks can be categorised into four types (in addition to mirror image stimulation, usually applied prior to the mark test): mirror-triggered search, mirror-mediated object discrimination, mirror-mediated spatial locating, and mirror-guided reaching (Menzel et al. 1985;Povinelli 1989;Pepperberg et al. 1995). In mirror-triggered search, the mirror is a cue to trigger searching behaviour, for either a food item or a positively rewarded stimulus (Anderson 1986;Povinelli 1989;Pepperberg et al. 1995;Broom et al. 2009;Howell and Bennett 2011;Gieling et al. 2014;Wang et al. 2020b); for instance, a location that is only visible with the use of a mirror may be baited with a food reward, and what is observed is whether a subject looks for the food reward in real space after only seeing its reflection. In this task, therefore, the mirror is simply used as a cue to initiate a search, and therefore, it does not require an understanding of the relationship between the object's location in space and its reflection. ...
Article
Full-text available
Mirror tasks can be used to investigate whether animals can instrumentally use a mirror to solve problems and can understand the correspondence between reflections and the real objects they represent. Two bird species, a corvid (New Caledonian crow) and a parrot (African grey parrot), have demonstrated the ability to use mirrors instrumentally in mirror-mediated spatial locating tasks. However, they have not been challenged with a mirror-guided reaching task, which involves a more complex understanding of the mirror’s properties. In the present study, a task approximating the mirror-guided reaching task used in primate studies was adapted for, and given to, a corvid species (Eurasian jay) using a horizontal string-pulling paradigm. Four birds learned to pull the correct string to retrieve a food reward when they could see the food directly, whereas none used the reflected information to accomplish the same objective. Based on these results, it cannot be concluded whether these birds understand the correspondence between the location of the reward and its reflected information, or if the relative lack of visual-perceptual motor feedback given by the setup interfered with their performance. This novel task is posited to be conceptually more difficult compared to mirror-mediated spatial locating tasks, and should be used in avian species that have previously been successful at using the mirror instrumentally. This would establish whether these species can still succeed at it, and thus whether the task does indeed pose additional cognitive demands.
Preprint
Billions of animals across many taxa are extensively farmed, with critical impacts on animal welfare. Societal efforts to reduce animal suffering lack rigorous and systematic approaches that facilitate maximising welfare improvements, such as informed funding allocation decisions. We present a multi-measure, cross-taxa framework for modelling differences in pain, suffering, and related cognition to assess whether certain animals have larger welfare ranges (how well or badly animals can fare). Measures include behavioural flexibility, cognitive sophistication, and general learning. We evaluated 90 empirically detectable proxies for cognition and welfare range (henceforth ‘proxies’) in pigs, chickens, carp, salmon, octopus, shrimp, crabs, crayfish, bees, and silkworms. We grouped a subset of proxies into: A) 10 ideal proxies and B) 10 less ideal proxies but with sufficient data for interspecies comparisons. We graded the strength of evidence per proxy across taxa, and constructed a cognition and welfare range profile, with overall judgement scores (ranging from likely no/low confidence to yes/very high confidence). We discuss the implications of comparisons and highlight key avenues for future research. This work is timely, given recent indications of significant political will towards reducing animal suffering, such as the inclusion of cephalopods and decapods in the Animal Welfare (Sentience) Bill following a UK government-commissioned research review. Given the novelty and robustness of our review, we believe it sets a new standard for investigating interspecies comparisons of cognition and welfare ranges and helps inform future research. This should help streamline funding allocations and improve the welfare of millions of farmed animals. Graphical/ Visual Abstract and Caption Cognition and welfare in farmed animals - from pigs to silkworms (Free stock images: http://www.pixabay.com )
Chapter
Consumers of food and other products now demand sustainability of production methods and, for most people, there is a range of components of sustainability, including welfare of humans and production animals and several environmental factors. Products are not considered to be of good quality unless they are produced with no problems for any components. The growing public knowledge that there are few differences between humans and other animal species leads to the view that each individual life is valued and it is considered morally wrong to cause poor welfare to a farmed animal. All vertebrate animals, including all farmed animals, and some invertebrates are now shown to be sentient, that is they have the capacity to have feelings. This capacity requires levels of cognitive ability and awareness. Every producer needs to change their systems and methods to ensure that production systems are sustainable in all ways.
Chapter
Research in behavioral genetics is important for pig welfare. Consequences of the ongoing selection for high production on pigs’ behavior need to be studied, as well as possibilities to select directly for behavioral traits. The Farm Animal Welfare Council’s definition of welfare is based on five freedoms related to hunger and thirst, discomfort, pain, injury or disease, fear and distress, and normal behavior. All these freedoms are associated with pig behavior. Pig breeding programs could be further developed by including behavioral traits relevant for welfare.
Article
Concept definitions applicable to human and non-human animals should be usable for both. Awareness is a state during which concepts of environment, self, and self in relation to environment result from complex brain analysis of sensory stimuli or constructs based on memory. There are several proposed categories of awareness. The widespread usage of the term conscious is 'not unconscious' so a conscious individual is an individual that has the capability to perceive and respond to sensory stimuli. It is confusing and scientifically undesirable if conscious is also used to mean aware. Hence it is proposed that conscious should be used only as above. Fully functioning and adequately developed humans and members of many other animal species are sentient. Sentience means having the capacity, the level of awareness and cognitive ability, necessary to have feelings. The welfare of an individual is its state as regards its attempts to cope with its environment. This includes feelings, which are important coping mechanisms, and health. Since feelings involve awareness, there is overlap between welfare assessment and awareness assessment. Methods for assessing awareness, consciousness, sentience, and welfare and links to morality are briefly discussed.
Chapter
UK bioethics discourses advocate banning the harvesting of tissues from non-human primates for xenotransplantation (animal-to-human transplantation), for ethical reasons, but make an exception for pigs. This pattern is repeated in most other highly regulated countries. This chapter examines the reasoning and scientific assumptions supporting UK bioethical discourses and justifying this discrimination among species. I argue that bioethics discourses draw on a utilitarian sacrificial logic, validating the redistribution of harm to those figured as less capable of suffering than others. Yet, such redistributions are underwritten by anthropocentric bias in animal science and bioethics, which constructs some animals (primates) as more capable of suffering than others (pigs). Examining utilitarian philosophy, primatology, and scientific research on pigs, I argue that, in the xenotransplantation field, the elevation of non-human primates to the status of (near) persons has a detrimental effect on pigs. Personhood, in this context, operates as a sovereign and biopolitical mechanism that produces a hierarchy of non-human life, making some, but not others, available as transplant sources within a utilitarian calculus of suffering.
Book
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Accepted codes of conduct and established religions are features of human societies throughout the world. Why should this be? In this 2003 book, biologist Donald Broom argues that these aspects of human culture have evolved as a consequence of natural selection; that morally acceptable behaviour benefits the humans and other animals and that a principal function of religion is to underpin and encourage such behaviour. The author provides biological insights drawn especially from work on animal behaviour and presents ideas and information from the fields of philosophy and theology to produce a thought-provoking, interdisciplinary treatment. Scientists who read this book will gain an appreciation of the wider literature on morality and religion, and non-scientists will benefit from the author's extensive knowledge of the biological mechanisms underlying the behaviour of humans and other social animals.
Book
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5th edition published 2015. See separate entry. The Preface of the 5th edition is shown here.
Article
Full-text available
Complex animal societies are most successful if members minimise harms caused to one another and if collaboration occurs. In order to promote this, a moral structure inevitably develops. Hence, morality has evolved in humans and in many other species. The attitudes which people have towards other humans and individuals of other species are greatly affected by this biologically based morality. The central characteristic of religions is a structure which supports a moral code, essentially the same one in all religions. A key obligation to others is to help to promote their good welfare and to avoid causing them to have poor welfare. Human views as to which individuals should be included in the category of those to whom there are moral obligations have broadened as communication and knowledge have progressed. Many people would now include, not only all humans but sentient animals, e.g. vertebrates and cephalopods, as well. Amongst sentient animals, coping with adversity may be more difficult in those with less sophisticated brain processing.
Article
Two Grey parrots (Psittacus erithacus) were tested on various types of mirror use: mirror image stimulation, mirror-mediated object discrimination, and a simple form of mirror-mediated spatial locating. During exposure to a mirror, neither bird clearly demonstrated self-exploratory behavior but responded instead in ways similar to those of marmosets, monkeys, dolphins, extremely young children (< 18 months), and to the initial responses of orangutans and young chimpanzees. The parrots' behavior was not a consequence of an inability to process mirrored information, because in subsequent tasks they used mirrors to discriminate among exemplars and to locate hidden objects; these birds are the first nonmammalian subjects to exhibit all these behavior patterns. Their behavior on all the tasks can be compared to that of humans, great apes, dolphins, monkeys, and Asian elephants.
Article
The assumption that animals are conscious and capable of experiencing negative sensations and emotions is at the core of most people's concerns about animal welfare. Investigation of this central assumption should be one goal of animal welfare science. We argue that theory and techniques from cognitive science offer promising ways forward. Evidence for the existence of conscious and non-conscious cognitive processing in humans has inspired scientists to search for comparable processes in animals. In studies of metacognition and blindsight, some species show behaviour that has functional parallels with human conscious cognitive processing. Although unable to definitively answer the question of whether the animals are conscious, these studies provide fresh insights, and some could be adapted for domestic animals. They mark a departure from the search for cognitive complexity as an indicator of consciousness, which is based on questionable assumptions linking the two. Accurate assessment of animal emotion is crucial in animal welfare research, and cognitive science offers novel approaches that address some limitations of current measures. Knowledge of the relationship between cognition and emotion in humans generates a priori frameworks for interpreting traditional physiological and behavioural indicators of animal emotion, and provides new measures (eg cognitive bias) that gauge positive as well as negative emotions. Conditioning paradigms can be used to enable animals to indicate their emotional state through operant responses. Although evidence for animal consciousness and emotion will necessarily be indirect, insights from cognitive science promise further advances in our understanding of this fundamentally important area in animal welfare science.
Article
The importance of understanding the mental experiences of animals in order to assess their welfare was recognised by the 1965 UK Brambell Committee Report. The report further suggested that the extent to which animals live life in the present moment has a major impact on their capacity for suffering. Limited ability to recall previous events and imagine future ones would protect animals from the worry, ‘rumination’ and associated emotional disorders that contribute so much to human suffering. We investigate these suggestions in the light of new evidence on the capacity of animals to travel mentally through time, and with reference to the subjective experiences of human amnesic patients who are indeed ‘stuck in time’, living their lives in the present. The key human abilities for mental time travel are episodic memory and episodic future thinking, characterised by an ability to place events in time (what, where, when (www)), and to consciously recall or imagine these events. Tests of www memory, recollection vs. familiarity memory, single-trial learning, episodic vs. semantic encoding, and forward planning have been used to investigate whether such cognitive systems also exist in animals. The evidence indicates that some studied species show behaviour consistent with the capacity for mental time travel, while others do not. The extent to which animals consciously experience mental time travel remains unknown. In terms of the implications for welfare, research on human amnesics with damage to brain structures involved in episodic memory suggests that animals lacking mental time travel would miss the beneficial consequences of using previous experience to plan and organise future behaviour, but also the detrimental consequences of being able to ruminate on the recalled past and worry about the imagined future. Emotional responses, including future-directed anxiety would be temporally bound by the presence of relevant stimuli or cues and, therefore, potentially short-lived. However past experiences could, through the actions of non-episodic memory systems attributable to other brain structures, still impact on emotional state via (implicit) learning of associations between cues and emotional events. Cumulative effects of past experience on stress response mechanisms and baseline stress or mood states would also be expected to occur. Mental time travel may thus bring both welfare benefits and problems. Absence of this ability by no means releases animals from many effects of the environment, including the past, on their emotional state.