The study compared the perception of ordinary citizens from Curitiba, Brazil (OB) and Clermont-Ferrand, France (OF), as well as OB, Brazilian veterinarians (VB), biologists (BB) and animal scientists (AB), concerning animal welfare and sentience. An online survey containing 18 open-ended, multiple choices and Likert scale questions was conducted from November 2014 to May 2016. The survey covered questions on demographics, perception of animal welfare, sheep welfare, sentience and animals’ emotional capacities. In total, 1103 respondents participated in the survey (388 OB, 350 OF, 248 VB, 92 BB and 25 AB); data were compared using non-parametric tests. Brazilian citizens (46.9%) believed more than OF (3.7%) that welfare is not considered for farm animals and OB attributed higher scores of suffering to sheep during management procedures (median 4, severe suffering) than OF (3, moderate suffering). Additionally, OB gave higher scores of emotions to animals (5) than OF (4). In general, OB and BB had similar perceptions; OB and BB differed from VB and AB who were similar to each other. Citizens (46.9%) and BB (29.3%) believed more than VB (18.5%) and AB (12.0%) that welfare is not considered for farm animals; OB and BB also attributed higher scores of suffering to sheep during management procedures than VB and AB. Women and older respondents showed higher perception of animal welfare issues. There was no clear correlation between perception of animal welfare or sentience and education. Overall, ordinary citizens differed on their perceptions of welfare and sentience in livestock and specifically in sheep, and sheep suffering during management procedures. Ordinary citizens from Curitiba showed higher perception of animal welfare issues as compared to respondents from Clermont-Ferrand and to veterinarians and animal scientists. Ensuring a better consideration of welfare at farm level and in educational programs seems warranted according to the results of this study.

Funding: The authors acknowledge the Coordination for the Improvement of Higher Education (Capes) Programa Ciências Forenses nº 25/2014– Pró-forenses to CFMM and Science Without Borders (CSF-CNPq) processo 206931/2014-0 to CFMM and PRT, for funding and supporting the project. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Copyright: © 2018 Tamioso et al. This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

By contrast to cattle, pigs and poultry, that are intensively managed, sheep are not commonly given significant societal attention for animal welfare, since they are frequently associated with extensive production systems. Such systems convey the idea that the animals are raised in a more natural situation and that, therefore, experience adequate levels of welfare [ 5 ]. However, due to certain potentially harmful management procedures employed in the sheep industry, as well as other practices that have raised attention of the general public, such as transport and slaughter, there seems to be a growing awareness and concern about sheep welfare [ 6 ]. So far there have been few studies about the society perception in relation to sheep welfare and sentience [ 7 – 10 ]. Therefore, the study aimed to describe and compare the perception of animal welfare and sentience, more particularly in sheep, between ordinary citizens from Curitiba, Brazil and Clermont-Ferrand, France, as well as ordinary citizens and different professionals from Curitiba who interact with animals.

Citizens participate in political processes that may influence or define the conditions domestic animals face throughout their lives, therefore it is important to understand citizens’ perception of animal welfare and sentience. Studies on the perception of professionals who interact with animals also seem essential, as they are directly involved in issues associated with animal welfare and contribute to spread information on animal welfare to several sectors of society, as citizens, consumers, farmers and stock people. The more people attribute emotional capacities to animals, the more the animals will be respected and their welfare status preserved. In addition, the recognition that animals experience emotions will have relevant consequences by contributing to the appreciation of their moral status [ 4 ].

Scientific studies showing evidence of rich emotional capacities in farm animals contributed to a growing interest in ethical and welfare issues. Such concern influences more and more consumer choices for animal products associated with higher levels of animal welfare and lower levels of suffering. According to Te Velde et al. [ 1 ], perceptions of animal welfare may be related to culture, traditions, beliefs, values and interests. Perceptions and attitudes are also related to the degree of proximity and information about the maintenance conditions of the species with which people interact. Furthermore, the attribution of emotional experiences to animals is directly associated with a positive treatment towards them [ 2 , 3 ]. Combined with scientific studies on affective states and cognition in farm animals, the recognition that they are sentient beings may increase the value given to the need for prioritizing their welfare.

Data were analyzed by comparing responses of OB and OF, as well as OB, VB, BB and AB. Gender, age and education were considered in comparisons within groups. For comparisons within VB, BB and AB, only gender and age were considered, since all veterinarians, biologists and animal scientists were, at least, graduated. Comparisons between cities (Curitiba and Clermont-Ferrand) and gender (men and women) were performed using the Mann-Whitney test; the Kruskal-Wallis test, followed by Dunn's post hoc test, was used for comparisons among Brazilian participants (OB, VB, BB and AB), age (18–29 years-old, 30–39 years-old, 40–49 years-old and 50 or more years-old) and education (secondary or less, higher (in progress or interrupted), higher (complete) and higher (post-graduation)). Such tests were applied for Q01, Q03, Q05, Q06, Q07, Q08 and Q09. The Wilcoxon test for pair-wise comparisons was used between Q07 and Q08. All tests were applied using the Minitab software package, version 17.

Responses to Q02 and Q04 were analyzed descriptively and classified according to the Five Freedoms [ 15 ]. Responses that could not be classified into the Five Freedoms were considered as “other”. Responses to Q10, Q11 and Q12 were also analyzed descriptively and categorized by the valence of the adjectives cited in each video, as 1) Positive, 2) Negative and 3) Others (e.g. “I do not know”, “I could not open the video”, “I do not want to watch the video” and adjectives that could not be categorized as positive or negative, such as “adapted”).

The questionnaire contained 18 open-ended, multiple choices or 5-point Likert-type scale format questions on demographic data, animal welfare in general and sheep welfare and sentience, divided into six sections. Demographic questions, as gender, age and education constituted the first section. The second section comprised four questions about animal welfare in general (Q01-Q04) ( Table 1 ). The third section was composed of two questions about proximity to sheep and sheep welfare and sentience (Q05-Q06) ( Table 1 ). The fourth section introduced two questions about sheep suffering, through different management procedures that are commonly performed in the sheep production chain. Such questions were presented twice, so that the answers were evaluated according to the respondents’ perception when the management procedures were presented without descriptions (identification1, castration1, tail docking1, shearing1, reproductive techniques1 and weaning1) (Q07) and with descriptions of how they are commonly performed (identification2, castration2, tail docking2, shearing2, reproductive techniques2 and weaning2) (Q08) ( Table 1 ). The fifth section was related to sentience in different animal species (Q09) ( Table 1 ). The last section covered the perception toward three videos up to 50 seconds showing sheep in situations that elicited different emotional states. The first video showed a female lamb exploring pasture and expressing play behaviour (V1); the second, an isolated female lamb in an unfamiliar pen (V2); and the third video exhibited a male sheep being brushed by a familiar person (V3). Each video was introduced twice: first, the respondents described the emotional state of the animal using three adjectives of their choice (Q10-Q12) and second, they chose three from 10 descriptors with different emotional valences, adapted from the Qualitative Behavior Assessment—QBA ® (Q13-Q15) ( Table 1 ). Before the beginning of the survey, three experts on animal emotions evaluated the valence of the videos, and they agreed that V1 represented a potentially positive event, V2, a potentially negative event and V3, another potentially positive event. Furthermore, the valence of the event exhibited in each video was supported by scientific findings: play behaviour by Holloway and Suter [ 12 ]; social isolation by Boissy et al. [ 13 ]; and brushing by Tamioso et al. [ 14 ].

Respondents from Curitiba, South of Brazil and Clermont-Ferrand, Center of France were invited to participate in an online survey on Survio ® platform from November 2014 to May 2016, available in their respective languages. The link to the survey was distributed by e-mail and social networks. In Curitiba, the target respondents were expanded to include four groups: ordinary citizens (OB), veterinarians (VB), biologists (BB) and animal scientists (AB). From a total of 985 respondents in Brazil, 753 were selected, as they lived in Curitiba, Brazil, being 388 OB, 248 VB, 92 BB and 25 AB. In Clermont-Ferrand, only ordinary citizens (OF), i.e. without distinction of socio-professional category, were assessed. A total of 376 respondents participated in the survey in France, and 350 were selected, as they lived in the city of Clermont-Ferrand. In total, responses from 1103 participants were evaluated (data in S1 Dataset ). The minimum sample in each group of respondents was obtained through a formula for unrestricted random sampling by Schaeffer et al. [ 11 ], according to the population of Curitiba, in the 2010 Census and Clermont-Ferrand, in the 2014 Census. For VB, BB and AB, both the Regional Council of Veterinary Medicine and the Regional Council of Biology of the State of Parana provided the number of veterinarians, animal scientists and biologists registered in Curitiba. The survey comprised a sample with a margin of error equal to 5% and a confidence level of 95% for each respondent group. The level of significance was set at p<0.05. The study was approved by the Human Research Ethics Committee of the Federal University of Paraná (Comética—SCS/UFPR), under protocol number 814 835/2014. An electronic consent form was displayed prior to starting the survey.

Results and discussion

Demographic data The demographic data presented on Table 2 show that, in general, most respondents were women, aged 18–29 years-old and having higher education (complete or post-graduation) (Table 2). The considerably higher percentage of women, as compared to the overall population in Curitiba, Brazil (47.7% men and 53.3% women) [16] and Clermont-Ferrand, France (48.0% men and 52.0% women) [17], may be related to the fact that women have greater concern and empathy toward animal welfare and sentience [2, 18]; consequently, they are probably more motivated to participate in this type of study. A higher number of younger participants and respondents with higher education was also expected, as they seem to show higher interest by animal welfare issues [19, 20]; however, this may be also related to their potential closer stance regarding internet use. High participation of younger respondents is in accordance with age distribution in Curitiba, Brazil (26.4% aged 15–19 years-old) [16], but not in Clermont-Ferrand, France (38.1% aged 50 years-old or more) [17]. PPT PowerPoint slide

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larger image TIFF original image Download: Table 2. Demographic data of 1103 respondents to a survey on animal welfare and sentience, November 2014 to May 2016. https://doi.org/10.1371/journal.pone.0200425.t002

General animal welfare issues No significant differences were found between OB and OF on their knowledge about animal welfare (p>0.05), as 43.5% OB and 60.3% OF have heard of the subject superficially, and 42.3% OB and 35.1% OF have heard of the subject more deeply. The results indicate that animal welfare might be an important theme for the studied citizens. A total of 15.2% OB responded that they have never heard of animal welfare, as compared to 0.0% VB, 1.1% BB and 0.0% AB (p<0.01). Schnettler et al. [21] also found that 17% of the consumers in Chile stated that they did not have knowledge about animal welfare. Age differences were noted only among BB. All BB aged 50 years old or more claimed to know about animal welfare, when compared to younger respondents, aged 18–29 years-old (71.2%) (p<0.05). Such result may be related to animal welfare teaching in Brazil. In veterinary and animal science areas, animal welfare teaching is still considered limited [22]. There is no animal welfare teaching in the curriculum of Brazilian biologists, suggesting that the issue may be even more incipient; consequently, younger biologists might show little knowledge about the subject due to lack of exposure to animal welfare issues during their graduate degree studies. Younger biologists also have less professional experience compared to older biologists, who may have had more opportunity to face animal welfare issues. Significant differences concerning education were observed for OB. Most OB with secondary or less education (29.7%) reported that they have never heard of animal welfare, differing from other respondents (p<0.01). Such result indicates a positive correlation between education and knowledge about animal welfare, in agreement with other studies showing positive association between education and animal welfare perception and behaviour [20]. Terms related to the freedom from fear and distress were the most used to define animal welfare, cited 27.0% of the times by OB, 33.4% by OF, 24.8% by VB, 25.9% by BB and 21.9% by AB (Fig 1). Te Velde et al. [1] also found that consumers and farmers defined animal welfare mostly in terms of physical and mental well-being. The results point to an association between animal welfare definition and emotional states by the respondents. PPT PowerPoint slide

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larger image TIFF original image Download: Fig 1. Definition of animal welfare (Q02), according 1103 respondents, being 388 ordinary citizens from Curitiba, Parana, Brazil (OB), 350 ordinary citizens from Clermont-Ferrand, Theix, France (OF), 248 veterinarians (VB), 92 biologists (BB) and 25 animal scientists (AB) from Curitiba, Parana, Brazil; November 2014 to May 2016. 1 Freedom from hunger, thirst and malnutrition 2 Freedom from pain, injury and disease, 3 Freedom to express normal behaviour, 4 Freedom from discomfort, 5 Freedom from fear and distress and 6 Other. https://doi.org/10.1371/journal.pone.0200425.g001 A total of 46.9% OB and 3.7% OF believed that welfare is not taken into consideration for farm animals (p<0.01) (Fig 2). Such difference is likely multifactorial, potentially due to different animal welfare scenarios and to different perceptions in both cities. European countries dispose of a great availability of labelled welfare-friendly products [23], higher than in Brazil [24]; consequently, French consumers may have the idea that farm animals experience several levels of welfare, in addition to the fact that the consumers have more options and more information on the products they buy. In studies by Evans and Miele [25] and Miele and Evans [26], French participants tended to associate quality products (as “Label Rouge”) and local, regional products with higher animal welfare. However, a recent research revealed that specific welfare aspects assessed in industrial broiler farms were superior in South Brazilian flocks than in Belgian flocks [27]. In addition, Souza et al. [28] compared broiler chicken welfare in certified and non-certified intensive farms in South of Brazil and found no differences for some broiler chicken critical welfare issues, such as lameness, panting and contact dermatitis. Such results indicate the need for the development of more rigorous standards in certification schemes. PPT PowerPoint slide

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larger image TIFF original image Download: Fig 2. Consideration of welfare in the animal farming scenario (Q03), according to 1103 respondents, being 388 ordinary citizens from Curitiba, Parana, Brazil (OB), 350 ordinary citizens from Clermont-Ferrand, Theix, France (OF), 248 veterinarians (VB), 92 biologists (BB) and 25 animal scientists (AB) from Curitiba, Parana, Brazil; November 2014 to May 2016. The asterisk indicates significant differences between OB and OF (p<0.05, Mann-Whitney test); letters indicate significant differences between respondents in Curitiba, Parana, Brazil (p<0.05, Kruskal-Wallis test). https://doi.org/10.1371/journal.pone.0200425.g002 Significant differences were also found among Brazilian respondents; OB (46.9%) and BB (29.3%) believed that welfare is not taken into consideration for farm animals, in comparison with VB (18.5%) and AB (12.0%) (p<0.01) (Fig 2). Te Velde et al. [1] observed that consumers showed a negative perception of the life of farm animals, citing environmental aspects, as lack of space, fresh air and light, and emphasized values related to the freedom to move and freedom to fulfill natural desires. Higher perception of consideration of animal welfare by VB and AB is an important result which requires further attention. We hypothesize that it may be related to the desensitization of these professionals regarding animal welfare issues throughout academic years [29]. However, it may also be related to a more detailed knowledge of animal production scenarios by VB and AB. It is a complex discussion since it involves knowledge regarding the actual level of consideration of farm animal welfare issues. It is also very relevant for animal welfare, due to the impact these professionals have in many different decisions related to animal farming. Gender differences were noted among VB: 22.4% female VB believed that farm animal welfare is not considered, in comparison with 7.7% male VB (p<0.05), which suggests higher perception of welfare issues by women, in agreement with other studies [30]. These results are also in agreement with those reported by Paul and Podberscek [29]. The authors observed that female students showed similar levels of empathy to animals throughout graduate studies, as opposed to male students, who presented less empathy each successive year. Aspects related to freedom from discomfort were cited 31.3%, 36.8%, 27.7% and 34.0% of the times by OB, OF, VB and BB, respectively, as the most important issues of animal farming that contribute to good animal welfare. For AB, aspects related to freedom from hunger, thirst and malnutrition contribute the most to good animal welfare, mentioned 25.7% of the times. Aspects related to animal nutrition (feed and water), animal health, in addition to environmental aspects were also acknowledged by Belgian citizens and farmers in a study by Vanhonacker et al. [31]. Our results are in agreement with these findings, suggesting higher societal concern about comfort and nutritional aspects of animal welfare.

Sheep suffering The perception of suffering differed significantly from the first and second questions for the following management procedures among OB: identification, castration, tail docking, reproductive techniques and weaning (p<0.05) (Fig 7); among OF: identification, tail docking, reproductive techniques and weaning (p<0.05) (Fig 7); among VB: castration, tail docking and reproductive techniques (p<0.05) (Fig 7); among BB: castration, tail docking and reproductive techniques (p<0.01) (Fig 7) and among AB: reproductive techniques (p<0.01) (Fig 7). Significant differences between the two questions were expected; OB and OF may not have been used to such procedures and, consequently, may not have knowledge about them. In addition, when the questions were introduced for the second time, the explanations might have elicited higher concern from the participants. All invasive management procedures that are routinely performed in the sheep industry have the potential to cause stress and suffering to sheep, which may last a few to several days. Management procedures that potentially cause mental or physical injury may be related to animal mistreatment and abuse. Due to differences in both questions, including for VB, it seems necessary to discuss more about suffering caused by invasive management procedures and also improve veterinary teaching content on these issues in order to increase recognition that sheep are sentience beings. Increase in knowledge about animal suffering might also contribute for the identification of animal abuse by professionals that interact with animals. PPT PowerPoint slide

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larger image TIFF original image Download: Fig 7. Levels of suffering attributed to different management procedures (Q07 and Q08) by 1103 respondents, being 388 ordinary citizens from Curitiba, Parana, Brazil (OB), 350 ordinary citizens from Clermont-Ferrand, Theix, France (OF), 248 veterinarians (VB), 92 biologists (BB) and 25 animal scientists (AB) from Curitiba, Parana, Brazil; November 2014 to May 2016. 1 = no suffering; 2 = mild suffering; 3 = moderate suffering; 4 = severe suffering; 5 = very severe suffering; I1 = identification1; I2 = identification2; C1 = castration1; C2 = castration2; T1 = tail docking1; T2 = tail docking2; S1 = shearing1; S2 = shearing2; R1 = reproductive techniques1; R2 = reproductive techniques2; W1 = weaning1; W2 = weaning2; the asterisk indicates significant differences between the first and second questions concerning sheep suffering due to management procedures (p<0.05, Wilcoxon test). https://doi.org/10.1371/journal.pone.0200425.g007 Citizens differed on their perception toward all the management procedures (Table 3). Citizens from Curitiba showed higher perception of sheep suffering during identification1 and 2, castration2, tail docking1 and 2, shearing1 and 2, reproductive techniques1 and 2 and weaning 1 and 2 than OF (p<0.01) (Table 3). These results might be related to the fact that French participants believed, more than Brazilian respondents, that animal welfare is taken into consideration in the livestock scenario. Consequently, French citizens might have the perception that the management procedures frequently performed in the sheep industry cause low levels of suffering to the animals. PPT PowerPoint slide

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larger image TIFF original image Download: Table 3. Levels of suffering attributed to different management procedures (Q07 and Q08) by 1103 respondents, being 388 ordinary citizens from Curitiba, Parana, Brazil (OB), 248 veterinarians (VB), 92 biologists (BB) and 25 animal scientists (AB) from Curitiba, Parana, Brazil; November 2014 to May 2016. Values in percentage (%). https://doi.org/10.1371/journal.pone.0200425.t003 Significant differences were also found among Brazilian groups for identification1, castration2, taildocking1 and 2, shearing1 and 2, reproductive techniques1 and 2 and weaning1 and 2 (p<0.01) (Table 3). The results show that, in general, OB and BB had similar perceptions of sheep suffering, and differed from VB and AB, who were similar to each other (Table 3). Higher perception of pain in sheep by OB and BB suggests a potential demand for higher level of animal welfare during management procedures, and the need for new strategies to increase sensibility and empathy of VB and AB toward pain. Lower perception of suffering by VB and AB might be due to decreased sensitivity in the end of graduation, which might persist during professional life. Paul and Podberscek [29] found a negative association between year of study and belief in animal sentience, as veterinary students in their later years of study rated some animals as having lower levels of sentience. An alternative interpretation of our results, that professionals in the field may have a more knowledgeable and correct interpretation of suffering signs in animals, seems controversial and warrants further studies. Scientific knowledge about stress and suffering during common farming practices is abundant, as for identification through metal and plastic tags [37], tail docking and castration [38], shearing [39], reproductive techniques [40] and weaning [41]. Significant differences found in our study may be also related to the limited teaching of animal welfare and pain in Brazilian veterinary programs [42]. Therefore, there is a need to protect and promote sensibility during undergraduate courses, as a way to improve perception of pain by VB and AB, since such professionals are involved in decisions regarding animal management.

Effect of gender on the perception of sheep suffering Female VB and BB attributed higher scores of suffering to sheep during tail docking1 and 2 (VB), reproductive techniques1 (VB and BB) and 2 (BB) and weaning1 (VB and BB) and 2 (VB) than male VB and BB (p<0.05) (Fig 8). Higher concern from women toward management procedures was expected, as women tend to react more emotionally and empathetically to animal suffering [43, 44]. PPT PowerPoint slide

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larger image TIFF original image Download: Fig 8. Gender differences on levels of suffering attributed to different management procedures (Q07 and Q08) by 248 veterinarians (VB) and 92 biologists (BB) from Curitiba, Parana, Brazil; November 2014 to May 2016. 1 = no suffering; 2 = mild suffering; 3 = moderate suffering; 4 = severe suffering; 5 = very severe suffering; I1 = identification1; I2 = identification2; C1 = castration1; C2 = castration2; T1 = tail docking1; T2 = tail docking2; S1 = shearing1; S2 = shearing2; R1 = reproductive techniques1; R2 = reproductive techniques2; W1 = weaning1; W2 = weaning2. The asterisk indicates significant differences between male (M) and female (F) respondents (p<0.05, Mann-Whitney test). https://doi.org/10.1371/journal.pone.0200425.g008

Effect of age on the perception of sheep suffering A general high perception of sheep pain was noted among older OF, VB and OB (p<0.05). A total of 44.0% OF aged 30–39 years-old attributed moderate suffering to sheep during identification1 (p<0.01). A total of 53.9% OF aged 18–29 years-old attributed no suffering to sheep during shearing1 (p<0.01). A total of 13.3% VB aged 40–49 and 13.3% aged 50 years-old or more attributed severe level of suffering to sheep during shearing2 (p<0.05). All AB aged 40–49 years-old attributed moderate suffering to sheep during castration2, higher perception of suffering than by other age groups (p<0.05). These results contradict literature reports, in which older participants generally show less concern about animal welfare and suffering [19]. More studies are necessary to understand the effect of age on the perception of suffering by the studied groups, mainly veterinarians and animal scientists, as both professionals are directly involved in animal husbandry.

Effect of education on the perception of sheep suffering French citizens with higher educational levels attributed severe suffering to sheep during identification1, when compared with other groups (p<0.05). In addition, OF having secondary or less education and incomplete graduation attributed moderate suffering to sheep during shearing2, lower perception of suffering than by other groups (p<0.05). Such findings indicate that higher levels of education might be associated with more positive perception of animal welfare [20, 45]. Further research focusing on French respondents would be helpful to better understand the effect of education on animal suffering.