The perception of humans by piglets: recognition of familiar handlers and generalisation to unfamiliar humans.

Humans are part of the environment of domestic animals and interact with them daily, providing a good basis for the study of interspecific relationships. Abilities to discriminate and recognise individuals form the basis of these relationships, and they are crucial skills for domestic animals, since individual humans can differ in their behaviour towards them. At the same time, with experience, animals may develop a general memory of humans and generalise their behaviour towards strangers. This study aimed to determine the extent to which weaned piglets can discriminate familiar humans and generalise their past experience when faced with unfamiliar humans. Forty-eight groups of three piglets were submitted to two consecutive 5-day conditioning periods of the same or opposite valence (positive and/or negative) given by one (A) or two (A then B) handlers. The reactivity of piglets to a motionless human and to an approaching human was measured before and after conditioning periods with unfamiliar and familiar handlers. Thereafter, piglets which received treatments with the two handlers A and B were subjected to a choice test between both handlers. The reactivity to an approaching human appeared to better reflect the past experience with familiar handlers since piglets clearly recognised them and adapted their behaviour accordingly. In contrast, reaction of piglets to a motionless human reflected their natural propensity to seek interaction, even after a negative experience. Although piglets were able to extend their memory of humans to an unfamiliar human through generalisation, many factors seemed to interact in this process, especially the complexity of the previous experience (inconsistent vs consistent) and the context in which piglets met the unfamiliar human (motionless vs approaching). We conclude that discrimination and generalisation processes of reactivity to humans do not simply rely on past interactions, but also depend on the context according to the degree of similitude with their past experience.

Classification of pig calls produced from birth to slaughter according to their emotional valence and context of production.

Vocal expression of emotions has been observed across species and could provide a non-invasive and reliable means to assess animal emotions. We investigated if pig vocal indicators of emotions revealed in previous studies are valid across call types and contexts, and could potentially be used to develop an automated emotion monitoring tool. We performed an analysis of an extensive and unique dataset of low (LF) and high frequency (HF) calls emitted by pigs across numerous commercial contexts from birth to slaughter (7414 calls from 411 pigs). Our results revealed that the valence attributed to the contexts of production (positive versus negative) affected all investigated parameters in both LF and HF. Similarly, the context category affected all parameters. We then tested two different automated methods for call classification; a neural network revealed much higher classification accuracy compared to a permuted discriminant function analysis (pDFA), both for the valence (neural network: 91.5%; pDFA analysis weighted average across LF and HF (cross-classified): 61.7% with a chance level at 50.5%) and context (neural network: 81.5%; pDFA analysis weighted average across LF and HF (cross-classified): 19.4% with a chance level at 14.3%). These results suggest that an automated recognition system can be developed to monitor pig welfare on-farm.

Manipulable Object and Human Contact: Preference and Modulation of Emotional States in Weaned Pigs.

Enriching the life of farm animals is a legal obligation in intensive farming conditions in the European Union, though not worldwide. In pigs, manipulable materials are mandatory when no bedding is available. Like manipulable objects, positive human interactions might also be considered as enrichment, as they provide the animals with opportunities to interact, increase their activity and lead to positive emotional states. In this study, we investigated how weaned pigs perceived an inanimate manipulable object and a familiar human. After a similar (in length, frequency, and procedure) familiarization to both stimuli, 24 weaned pigs were tested for a potential preference for one of the stimuli and submitted to isolation/reunion tests to evaluate the emotional value of the stimuli. We hypothesized that being reunited with a stimulus would attenuate the stress of social isolation and promote a positive state, especially if the stimulus had a positive emotional value for pigs. Although our behavioral data showed no evidence that pigs spent more time close to, or in contact with, one of the stimuli during a choice test, pigs more often approached the human and were observed lying down only near the human. Using behavioral and bioacoustic data from isolation/reunion tests, we showed that a reunion with the human decreased the time spent in an attentive state and mobility of pigs to a greater extent than a reunion with the object, or isolation. Vocalizations differed between reunions with the object and the human, and were different from those during isolation. The human and object presence led to higher frequency range and more noisy grunts, but only the human led to the production of positive shorter grunts, usually associated with positive situations. In conclusion, pigs seemed to be in a more positive emotional state, or be reassured, in the presence of a familiar human compared to the object after a short period of social isolation. This confirms the potential need for positive pseudo-social interactions with a human to enrich the pigs' environment, at least in or after potentially stressful situations.

Evidence of Pain, Stress, and Fear of Humans During Tail Docking and the Next Four Weeks in Piglets (Sus scrofa domesticus).

Tail docking is widely performed in pig farms to prevent tail biting. We investigated the consequences of this practice on behavioral indicators of pain and stress, and on the human-piglet relationship during lactation. Within 19 litters, piglets (1-3 days of age) were submitted on day 0 (D0) to docking with a cautery iron (D), sham-docking (S), or no docking (U). Piglets from the D and S groups were observed during the procedure (body movements and vocalizations) and just after, in isolation, during 20 s for body, tail and ear postures as well as ear movements. Piglets from the three treatments were observed in their home pen after docking on D0 and D3 afternoon for body posture, tail posture and movements. Piglets from the D and U groups were observed on D6, D12, D19, and D26 in their home pen for oral behavior, body, and tail posture. Tail damage and tear staining were scored on D5, D11, D18, and D25. A 5-min motionless human test was performed on D14. During the procedure, D piglets screamed more and with a higher intensity (P < 0.05) than S piglets (n = 48-50). Just after docking, D piglets held their ears in a posture perpendicular to the head-tail axis and changed their ear posture more often (P < 0.05). Between D6 and D26, D piglets kept their tail immobile (P < 0.001) and in a horizontal position (P < 0.01) more often than U piglets (n = 45-47). Between D11 and D25, U piglets had higher scores for tail damage and damage freshness than D piglets (0.09 < P < 0.02) whereas tear-stain score was similar. In the human test, D piglets interacted later with an unfamiliar human than U piglets (P = 0.01, n = 18/group). Present data indicate signs of acute pain and stress in piglets due to docking during the procedure itself and adverse consequences throughout lactation thereafter, including on their relationship with humans. On the other hand, the presence of tail lesions shows that undocked piglets are subject to more tail biting, even before weaning.

Temporal association between food distribution and human caregiver presence and the development of affinity to humans in lambs.

The presence of the caregiver around feeding favors the development of a human-animal relationship. To understand the underlying mechanism, we tested various temporal associations between food distribution and human presence: from an early age, a person was repeatedly present for 2 min just before milk distribution ("Forward"), during milk distribution ("Simultaneous"), and 20 min afterwards ("Delayed"). The "Control" group received no human contacts. During the treatments, "Forward" and "Delayed" lambs had more physical contacts with the person than "Simultaneous" lambs. When tested in unfamiliar environments, they stood longer near the person than did "Control" or "Simultaneous" lambs, which did not differ. Only "Forward" and "Delayed" lambs bleated when separated from the person. Fasting before testing had no effect. "Forward" and "Delayed" seemed to produce the same human-animal relationship, showing that this did not rely only on a conditioning process associating the caregiver with food. The caregiver may acquire properties for social support through other mechanisms (attachment and/or postingestive effects).

Postnatal auditory preferences in piglets differ according to maternal emotional experience with the same sounds during gestation.

Prenatal sensory experience, notably auditory experience, is a source of fetal memories in many species. The contiguity between sensory stimuli and maternal emotional reactions provides opportunity for associative learning in utero but no clear evidence for this associative learning has been presented to date. Understanding this phenomenon would advance our knowledge of fetal sensory learning capacities. In the present study we tested the hypothesis that sounds (human voice) broadcast to pregnant sows while they experienced positive or negative emotional situations influences postnatal reactions of their offspring to these same sounds. The results show that: 1) from the first testing at the age of 2 days, the experimental piglets were less distressed by a social separation than controls if they heard the "familiar" voice, 2) piglets generalized to any human voice although the influence of novel voices was less pronounced, 3) in a challenging situation, piglets were more distressed if they heard the voice that was associated with maternal negative emotional state in utero. These findings open a whole line of new research on the long term effect of in utero associative learning that goes well beyond pigs, providing a framework for reconsidering the importance of sensory and emotional experiences during gestation.

Piglets Learn to Use Combined Human-Given Visual and Auditory Signals to Find a Hidden Reward in an Object Choice Task.

Although animals rarely use only one sense to communicate, few studies have investigated the use of combinations of different signals between animals and humans. This study assessed for the first time the spontaneous reactions of piglets to human pointing gestures and voice in an object-choice task with a reward. Piglets (Sus scrofa domestica) mainly use auditory signals-individually or in combination with other signals-to communicate with their conspecifics. Their wide hearing range (42 Hz to 40.5 kHz) fits the range of human vocalisations (40 Hz to 1.5 kHz), which may induce sensitivity to the human voice. However, only their ability to use visual signals from humans, especially pointing gestures, has been assessed to date. The current study investigated the effects of signal type (visual, auditory and combined visual and auditory) and piglet experience on the piglets' ability to locate a hidden food reward over successive tests. Piglets did not find the hidden reward at first presentation, regardless of the signal type given. However, they subsequently learned to use a combination of auditory and visual signals (human voice and static or dynamic pointing gestures) to successfully locate the reward in later tests. This learning process may result either from repeated presentations of the combination of static gestures and auditory signals over successive tests, or from transitioning from static to dynamic pointing gestures, again over successive tests. Furthermore, piglets increased their chance of locating the reward either if they did not go straight to a bowl after entering the test area or if they stared at the experimenter before visiting it. Piglets were not able to use the voice direction alone, indicating that a combination of signals (pointing and voice direction) is necessary. Improving our communication with animals requires adapting to their individual sensitivity to human-given signals.

Humans (Homo sapiens) judge the emotional content of piglet (Sus scrofa domestica) calls based on simple acoustic parameters, not personality, empathy, nor attitude toward animals.

The vocal expression of emotion is likely driven by shared physiological principles among species. However, which acoustic features promote decoding of emotional state and how the decoding is affected by their listener's psychology remain poorly understood. Here we tested how acoustic features of piglet vocalizations interact with psychological profiles of human listeners to affect judgments of emotional content of heterospecific vocalizations. We played back 48 piglet call sequences recorded in four different contexts (castration, isolation, reunion, nursing) to 60 listeners. Listeners judged the emotional intensity and valence of the recordings and were further asked to attribute a context of emission from four proposed contexts. Furthermore, listeners completed a series of questionnaires assessing their personality (NEO-FFI personality inventory), empathy [Interpersonal Reactivity Index (IRI)] and attitudes to animals (Animal Attitudes Scale). None of the listeners' psychological traits affected the judgments. On the contrary, acoustic properties of recordings had a substantial effect on ratings. Recordings were rated as more intense with increasing pitch (mean fundamental frequency) and increasing proportion of vocalized sound within each stimulus recording and more negative with increasing pitch and increasing duration of the calls within the recording. More complex acoustic properties (jitter, harmonic-to-noise ratio, and presence of subharmonics) did not seem to affect the judgments. The probability of correct context recognition correlated positively with the assessed emotion intensity for castration and reunion calls, and negatively for nursing calls. In conclusion, listeners judged emotions from pig calls using simple acoustic properties and the perceived emotional intensity might guide the identification of the context.

Calling by domestic piglets during simulated crushing and isolation: a signal of need?

This study examined whether piglet distress vocalizations vary with age, body weight and health status, according to the predictions of the honest signalling of need evolutionary model. Vocalizations were recorded during manual squeezing (a simulation of being crushed by mother sow) and during isolation on Days 1 and 7 after birth in piglets from 15 litters. We predicted that during squeezing, younger, lighter and sick piglets would call more intensely because they are in higher risk of dying during crushing and therefore they benefit more from the sow's reaction to intensive vocalization. For isolation, we predicted that lighter and younger piglets would call more because they are more vulnerable to adverse effects of the separation. Calls were analyzed in their time and frequency domain. The rate of calling, call duration, proportion of high-pitched calls and eight acoustic parameters characterizing frequency distribution and tonality were used as indicators of acoustic signalling intensity. Piglets that experienced "squeezing" on Day 1 produced more intense acoustic distress signalling than on Day 7. Lighter piglets called more during squeezing than heavier piglets. Health status did not significantly affect any of the indicators of intensity of vocalization during squeezing. In isolation, none of the parameters of vocalization intensity were affected either by the age or by the weight of the piglets. In summary, the model of honest signalling of need was confirmed in the squeezed situation, but not in the isolation situation.

Encoding of situations in the vocal repertoire of piglets (Sus scrofa): a comparison of discrete and graded classifications.

Two important questions in bioacoustics are whether vocal repertoires of animals are graded or discrete and how the vocal expressions are linked to the context of emission. Here we address these questions in an ungulate species. The vocal repertoire of young domestic pigs, Sus scrofa, was quantitatively described based on 1513 calls recorded in 11 situations. We described the acoustic quality of calls with 8 acoustic parameters. Based on these parameters, the k-means clustering method showed a possibility to distinguish either two or five clusters although the call types are rather blurred than strictly discrete. The division of the vocal repertoire of piglets into two call types has previously been used in many experimental studies into pig acoustic communication and the five call types correspond well to previously published partial repertoires in specific situations. Clear links exist between the type of situation, its putative valence, and the vocal expression in that situation. These links can be described adequately both with a set of quantitative acoustic variables and through categorisation into call types. The information about the situation of emission of the calls is encoded through five call types almost as accurately as through the full quantitative description.

Human perception of vocalizations of domestic piglets and modulation by experience with domestic pigs (Sus scrofa).

Interspecific communication between humans and pets is possible through vocal cues. We studied how humans with differing experience with domestic pigs (Sus scrofa) interpret pig vocalizations. Forty-eight ethologists studying pigs, 31 pig-caretakers and 54 naive students evaluated the emotional intensity and valence (negative/positive) of recordings from two negative (castration, isolation) and two positive (reunion with the sow, postsuckling) contexts. They also identified the context in which the recordings were made. Castration vocalizations were evaluated as highly intense and unpleasant. The positive contexts were evaluated as low in intensity and positive in valence, and isolation fell in the middle for both intensity and valence. Compared with the other two groups, pig-caretakers evaluated the intensity of vocalizations as lower, and ethologists evaluated the valence as more negative. The level of successful classification exceeded that expected by chance for all four contexts but was especially accurate for castration. Ethologists achieved better recognition than students. Classifying (right context) and understanding the emotional content (valence, intensity) of pig vocalizations is thus a general ability of humans, although it varies according to an individual's experience with pigs.

Nonnutritive sucking: one of the major determinants of filial love.

The present study investigated the rewarding effects of nonnutritive sucking on the development of a filial preference. Two experiments were conducted to test whether nonnutritive visceral and oral stimuli have reinforcing properties independent from each other or act in synergy. Lambs could interact freely with their dam but were deprived of suckling by covering the udder for the first 12 hr. In Experiment 1, suckling was prevented and replaced by human giving, in the presence of the mother, either a bottle of water (B5 and B2.5: 5% or 2.5% birth weight, BW, divided into seven portions over 12 hr) or water via tube-feeding (I5 and I2.5: 5% or 2.5% BW, also divided into seven portions over 12 hr). During a two-choice test performed at 12 hr after birth, only B5 and I5 lambs preferred their mother to an alien ewe however, B5 were faster at choosing their mother at the beginning of the test. B2.5 and I2.5 lambs made a random choice. In Experiment 2, suckling was prevented and replaced by human giving, in the presence of the mother, either a bottle of water (B2.5: 2.5% BW, divided into seven portions over 12 hr) or water via tube-feeding (I10 and I2.5: 10% or 2.5% BW, also divided into seven portions over 12 hr). During a two-choice test at 12 hr, tube-fed lambs (I10 and I2.5) preferred their mother to a human. B2.5 lambs were equally attracted to both partners and spent more time near the human than lambs from the other groups. In a test of reactivity to a human performed on neonates isolated from their mother, B2.5 lambs explored the human much more than the other lambs. The presence of the human had soothing properties in B2.5 lambs and once the human left, they were the only lambs displaying enhanced vocal and locomotor activity. In these experiments, nonnutritive gastrointestinal stimuli induced a preference for the mother whereas nonnutritive sucking led to a strong positive relationship with the human. These results suggest that when lambs suckle their dam, the development of filial bonding is facilitated through the combined effects of oral and gastrointestinal stimuli.