Effects of reduced kinematic and social play experience on affective appraisal of human-rat play in rats.

BACKGROUND: Play is a common and developmentally important behaviour in young mammals. Specifically in Norway rats (Rattus norvegicus), reduced opportunity to engage in rough-and-tumble (RT) play has been associated with impaired development in social competence. However, RT play is a complex behaviour having both a kinematic aspect (i.e., performing complex 3D manoeuvres during play fights) and a social aspect (interacting with a playful partner). There has been little research so far on disentangling the two aspects in RT play, especially on how these two aspects affect the affective appraisal of the intense physical contact during play. RESULTS: To examine the developmental effects of kinematic and social play reduction on affective appraisal in rats, we subjected male Long-Evans rats from 21 days old to RT play experience that was reduced either kinematically (through playing in a low ceiling environment) or socially (through playing with a less playful Fischer-344 rat). Starting at 35 days, we measured their production of positively (50-kHz) and negatively (22-kHz) valenced ultrasonic vocalisations (USVs) in a 2-min standardised human-rat play procedure that mimicked the playful sequences of nape contact, pinning, and belly stimulation ('tickling') for ten days. We hypothesised that the rats with kinematically or socially reduced play would perceive the 'tickling' less positively and thus emit positive ultrasonic vocalisations at lower rates compared to control rats with non-reduced play experience. Our results confirmed that each of the treatments reduced play differently: while the kinematic reduction abolished playful pinnings entirely, the social reduction decreased the pinnings and made play highly asymmetric. During the tickling procedure, rats mostly produced 50 kHz USV, indicating that they appraised the procedure as positive. There was a wide inter individual variance and high individual consistency in rats' USV responses to 'tickling'. Crucially, neither the kinematically nor the socially reduced play experience affected either type of USV production when rats were 'tickled'. CONCLUSIONS: This finding indicates that the ability to appraise play-like interactions as positive remains unaffected even when the kinematic or the social aspect of play experience was substantially curtailed.

The practicality of practice: A model of the function of play behaviour.

The function of play has been a long-debated topic in animal behaviour. One popular class of accounts is that play offers practice for serious adult behaviour, but little has been done to model the circumstances where this could be true. In this paper, we model an individual who, over the juvenile and subadult ontogenetic periods, has a choice between three behaviours: foraging, playing and rest, where playing improves an individual's ability in some component of a serious adult behaviour. Using stochastic dynamic programming, we show that even when play is more energetically costly and an inferior form of practice than foraging itself, it still may be optimal to play under a variety of circumstances. We offer several instantiations of the play as practice concept to show the possibility of play improving a variety of different adult abilities: antipredatory, foraging and reproductive behaviour. These models show the environmental conditions where play might be expected, as well as the predicted occurrences of play throughout ontogeny. This is a first step in showing the ecological feasibility of the practice hypothesis of play and raises further questions about why playful activity is more beneficial than more deliberate directed practice.

Indication of social buffering in disbudded calves.

Most dairy calves are housed individually in early ontogeny but social housing has positive effects on calf welfare including an advantage of social buffering, i.e., when negative effects of stress are mitigated through social support of conspecific. The effects of social buffering has not yet been examined in relation to disbudding; a painful husbandry procedure commonly performed on young dairy calves. The objective of this study was to investigate the effect of pair versus individual housing on calves' behavioral reaction to disbudding. In total 52 female calves were randomly allocated either to individual (n = 16) or pair housing (n = 36, 18 focal). Calves were hot-iron disbudded with a local anesthetic and their spontaneous behavior in home pens was recorded for 24 h pre- and post-disbudding. Eating forage, ruminating, resting, exploration, play, self-grooming, and pain-related behaviors were quantified during eight 20 min intervals during the 24 h periods pre- as well as post-disbudding. In pair-housed (PAIR) calves social resting, active and passive allo-grooming were additionally recorded. The differences between individually housed (INDI, n = 10) and PAIR calves (n = 12) were tested by general linear models. The changes in pre- and post-disbudding behaviors in all calves as well as in social behaviors of PAIR calves were tested by paired t-test. We found that head shaking (t = - 3.46, P = 0.0024), head rubbing (t = 4.96, P < 0.0001) and self-grooming (t = 2.11, P = 0.04) increased in all calves after disbudding. Eating forage increased only in PAIR calves (t = 2.50, P = 0.030) which also resulted in a difference between treatments with PAIR calves fed more often than INDI calves (F1,18 = 12.96, P = 0.002). Differences in eating forage may be an indication of improved ability of PAIR calves to recover from disbudding. No other significant differences were detected between treatment groups which might have been caused by our limited sample. Our results provide the first evidence that housing treatment affects calves' reactions to disbudding, with possible indication of social buffering.

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.

The Joint Log-Lift Task: A Social Foraging Paradigm.

Behavioural cooperation is under intense research. Yet, popular experimental paradigms often employ artificial tasks, require training, or do not permit partner choice, possibly limiting their biological relevance. We developed the joint log-lift task, a social foraging paradigm in which animals have to jointly lift a log to each obtain a food reward. The task relies on an obligate strategy, meaning that the only way to benefit is to work jointly. We hypothesised that (1) animals learn to spontaneously solve the task, and that (2) kin and (3) more sociable individuals would engage more often together in the task and achieve greater success than non-kin and less sociable individuals, respectively. We presented the task to 8 groups of juvenile domestic pigs (Sus scrofa domesticus) in their home pen for 30 min daily. Over the course of 9 days, the pigs showed evidence of learning by progressively switching from individual to joint behaviours, leading to 68% (62 out of 91 pigs) spontaneously solving the task. Success was influenced by sociability, but not kinship. There were large differences in success among dyads, hinting at the possible role of social dynamics and inter-individual differences in the ability and/or motivation to solve the task. The joint log-lift task allows researchers to investigate spontaneous cooperative tendencies of individuals, dyads and groups in the home environment through ad libitum engagement with the apparatus. This ecologically relevant paradigm opens the way to investigate social foraging experimentally at large scale, by giving animals free choice about when and with whom to work jointly.

The effect of pair housing on dairy calf health, performance, and behavior.

Individual housing of dairy calves prevails in Europe and North America despite its negative effects on calf development. One of the main reasons is that farmers find individual housing of calves more practical than group housing. A compromise between practice and welfare could be housing calves in pairs. Therefore, we aimed to compare health, feed intake, growth, and behavior in a novel arena of 22 individually (INDI) and 44 pair-housed calves that were randomly assigned a treatment. Diarrhea and respiratory problems were recorded every day for the period of 49 d. Intake of calf starter and milk were measured every day for the period 48 and 49 d, respectively. Calf body weight gains were calculated as average daily gain. Calves were individually tested in a novel arena at 11 to 18 d, and their behavior was recorded according to an ethogram including 8 behavioral categories. Behavioral categories were first diminished by principal component (PC) analysis. We found that 2 PC explained 66% of the total variation in calf behavior. Movement-related behaviors (activity, play, and crossing the stair) loaded positively on PC1, and PC2 had positive loading on self-grooming and negative loading on exploration. There were no effects of housing on calf health, feed intake, or average daily gain. The INDI calves had higher PC1 scores than pair-housed calves, indicating a rebound effect of movement. Our results are consistent with other studies that found no negative effect of pair housing of calves on their health, feed intake, or growth compared with individually-housed calves. The rebound effect of movement-related behaviors of INDI calves in a novel arena implies that individual housing of calves causes activity deprivation by the second week of age.

Negative play contagion in calves.

Play is a strong outwardly directed, emotional behaviour and can contagiously spread between individuals. It has been suggested that high-playing animals could 'seed' play in others, spreading positive affective states. Despite the current interest in play contagion there has been no previous attempt to measure the strength of the play contagion effect. The calf (Bos taurus) is ideal for testing the strength of play contagion as play in calves is strongly related to energy intake from milk. We manipulated play in calves through their milk allowances and housed the calves in uniform groups all on the same milk allowance (high = UHigh or low = ULow) or in mixed groups with calves in the same group receiving either a high (= MHigh) or low (= MLow) milk allowance. We measured locomotor play using accelerometers on two consecutive days when calves were four and eight weeks old, in order to study play contagion over a protracted developmental window. We anticipated that differences in the level of play contagion between treatment groups would result in difference in the play levels observed in the MLow and ULow individuals. Contrary to our expectations we found that spontaneous play was suppressed in the high-milk calves housed in mixed groups (MHigh), in comparison to calves housed with group mates all receiving high-milk (UHigh). These results are the first to quantify a negative play contagion effect, particularly in a situation of long-term contact, and may suggest that negative contagion has a stronger effect on play behaviour than positive contagion.

Pair housing makes calves more optimistic.

Individual housing of dairy calves is common farm practice, but has negative effects on calf welfare. A compromise between practice and welfare may be housing calves in pairs. We compared learning performances and affective states as assessed in a judgement bias task of individually housed and pair-housed calves. Twenty-two calves from each housing treatment were trained on a spatial Go/No-go task with active trial initiation to discriminate between the location of a teat-bucket signalling either reward (positive location) or non-reward (negative location). We compared the number of trials to learn the operant task (OT) for the trial initiation and to finish the subsequent discrimination task (DT). Ten pair-housed and ten individually housed calves were then tested for their responses to ambiguous stimuli positioned in-between the positive and negative locations. Housing did not affect learning speed (OT: F1,35 = 0.39, P = 0.54; DT: F1,19 = 0.15, P = 0.70), but pair-housed calves responded more positively to ambiguous cues than individually housed calves (χ21 = 6.79, P = 0.009), indicating more positive affective states. This is the first study to demonstrate that pair housing improves the affective aspect of calf welfare when compared to individual housing.

Ontogeny of individual and litter identity signaling in grunts of piglets.

Many studies have shown that animal vocalizations can signal individual identity and group/family membership. However, much less is known about the ontogeny of identity information-when and how this individual/group distinctiveness in vocalizations arises and how it changes during the animal's life. Recent findings suggest that even species that were thought to have limited vocal plasticity could adjust their calls to sound more similar to each other within a group. It has already been shown that sows can acoustically distinguish their own offspring from alien piglets and that litters differ in their calls. Surprisingly, individual identity in piglet calls has not been reported yet. In this paper, this gap is filled, and it is shown that there is information about piglet identity. Information about litter identity is confirmed as well. Individual identity increased with age, but litter vocal identity did not increase with age. The results were robust as a similar pattern was apparent in two situations differing in arousal: isolation and back-test. This paper argues that, in piglets, increased individual discrimination results from the rapid growth of piglets, which is likely to be associated with growth and diversification of the vocal tract rather than from social effects and vocal plasticity.

Emotional contagion of distress in young pigs is potentiated by previous exposure to the same stressor.

This study tested whether emotional contagion occurs when piglets directly observe a penmate in distress (restraint) and whether there is an effect of previous experience on the response to subsequent restraint or exposure to conspecific distress. Piglets (49.7 ± 0.7 days) were exposed in pairs to two stress phases (SP1 and SP2) in an arena divided into two pens by a wire mesh wall. During SP1, one of the pigs of a pair was either restrained (Stress treatment) or sham-restrained (Control treatment), while the other pig was considered observer. During SP2, the previous observer was restrained, while its penmate took the observer role. Heart rate variability, locomotion, vocalizations, body/head/ear and tail postures were monitored. During SP1, observer pigs responded to conspecific distress with increased indicators of attention (looking at, proximity to and snout contacts with the distressed pigs) and increased indicators of fear (reduced locomotion, increased freezing). During SP2, the observer pigs that had been restrained previously reacted more strongly (through higher proximity, decreased locomotion, increased freezing) to observing the penmate in restraint than pigs without the previous negative experience. This study suggests that young pigs are susceptible to emotional contagion and that this contagion is potentiated by previous exposure to the same stressor. These findings have implications for pig welfare in practical animal husbandry systems.

Expression of Emotional Arousal in Two Different Piglet Call Types.

Humans as well as many animal species reveal their emotional state in their voice. Vocal features show strikingly similar correlation patterns with emotional states across mammalian species, suggesting that the vocal expression of emotion follows highly conserved signalling rules. To fully understand the principles of emotional signalling in mammals it is, however, necessary to also account for any inconsistencies in the way that they are acoustically encoded. Here we investigate whether the expression of emotions differs between call types produced by the same species. We compare the acoustic structure of two common piglet calls-the scream (a distress call) and the grunt (a contact call)-across three levels of arousal in a negative situation. We find that while the central frequency of calls increases with arousal in both call types, the amplitude and tonal quality (harmonic-to-noise ratio) show contrasting patterns: as arousal increased, the intensity also increased in screams, but not in grunts, while the harmonicity increased in screams but decreased in grunts. Our results suggest that the expression of arousal depends on the function and acoustic specificity of the call type. The fact that more vocal features varied with arousal in scream calls than in grunts is consistent with the idea that distress calls have evolved to convey information about emotional arousal.

Decoding of Baby Calls: Can Adult Humans Identify the Eliciting Situation from Emotional Vocalizations of Preverbal Infants?

Preverbal infants often vocalize in emotionally loaded situations, yet the communicative potential of these vocalizations is not well understood. The aim of our study was to assess how accurately adult listeners extract information about the eliciting situation from infant preverbal vocalizations. Vocalizations of 19 infants aged 5-10 months were recorded in 3 negative (Pain, Isolation, Demand for Food) and 3 positive (Play, Reunion, After Feeding) situations. The recordings were later rated by 333 adult listeners on the scales of emotional valence and intensity. Subsequently, the listeners assigned the eliciting situations in a forced choice task. Listeners were almost perfectly able to discriminate whether a recording came from a negative or a positive situation. Their discrimination may have been based on perceived valence as they consistently assigned higher valence when listening to positive, and lower valence when listening to negative, recordings. Ability to identify the particular situation within the negative or positive realm was substantially weaker, with only three of the six situations being discriminated above chance. The best discriminated situation, Play, was associated with high perceived intensity. The weak qualitative discrimination of negative situations seemed to be based on graded perception of negative recordings, from the most intense and unpleasant (assigned to Pain) to the least intense and least unpleasant (assigned to Demand for Food). Parenthood and younger age, but not gender of listeners, had weak positive effects on the accuracy of judgments. Our results indicate that adults almost flawlessly distinguish positive and negative infant sounds, but are rather inaccurate regarding identification of the specific needs of the infant and may normally employ other sensory channels to gain this information.

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.

General Principles for the welfare of animals in production systems: the underlying science and its application.

In 2012, the World Organisation for Animal Health adopted 10 'General Principles for the Welfare of Animals in Livestock Production Systems' to guide the development of animal welfare standards. The General Principles draw on half a century of scientific research relevant to animal welfare: (1) how genetic selection affects animal health, behaviour and temperament; (2) how the environment influences injuries and the transmission of diseases and parasites; (3) how the environment affects resting, movement and the performance of natural behaviour; (4) the management of groups to minimize conflict and allow positive social contact; (5) the effects of air quality, temperature and humidity on animal health and comfort; (6) ensuring access to feed and water suited to the animals' needs and adaptations; (7) prevention and control of diseases and parasites, with humane euthanasia if treatment is not feasible or recovery is unlikely; (8) prevention and management of pain; (9) creation of positive human-animal relationships; and (10) ensuring adequate skill and knowledge among animal handlers. Research directed at animal welfare, drawing on animal behaviour, stress physiology, veterinary epidemiology and other fields, complements more established fields of animal and veterinary science and helps to create a more comprehensive scientific basis for animal care and management.

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.

When to go with the crowd: modelling synchronization of all-or-nothing activity transitions in grouped animals.

For groups of animals to keep together, the group members have to perform switches between staying in one place and moving to another place in synchrony. However, synchronization imposes a cost on individual animals, because they have to switch from one to the other behaviour at a communal time rather than at their ideal times. Here we model this situation analytically for groups in which the ideal times vary quasinormally and grouping benefit increases linearly with group size. Across the parameter space consisting of variation in the grouping benefit/cost ratio and variation in how costly it is to act too early and too late, the most common optimal solutions are full synchronization with the group staying together and zero synchronization with immediate dissolution of the group, if the group is too small for the given benefit/cost ratio. Partial synchronization, with animals at the tails of the distribution switching individually and the central core of the group in synchrony, occurs only at a narrow stripe of the space. Synchronization cost never causes splitting of the group into two as either zero, partial or full synchronization is always more advantageous. Stable solutions dictate lower degree of synchrony and lower net benefits than optimal solutions for a large range of the parameter values. If groups undergo repeated synchronization challenges, they stay together or quickly dissolve, unless the animals assort themselves into a smaller group with less variation in the ideal times. We conclude with arguing that synchronization cost is different from other types of grouping costs since it does not increase much with increasing group size. As a result, larger groups may be more stable than smaller groups. This results in the paradoxical prediction that when the grouping benefit/grouping cost ratio increases, the average group sizes might decrease, since smaller groups will be able to withstand synchronization challenges.

Revisiting play elements and self-handicapping in play: a comparative ethogram of five Old World monkey species.

Play behavior has been viewed as a mixture of elements drawn from "serious" behavior, interspersed by ritualized play signals. Two other types of play behaviors have been overlooked: patterns that are dissimilar from any serious behavior and patterns with self-handicapping character, that is, those that put the animal into unnecessary disadvantageous positions or situations. Here the authors show that these 2 types of patterns can constitute a major part of play repertoire. From our own videorecordings and observations, we constructed play ethograms of 5 monkey species (Semnopithecus entellus, Erythrocebus patas, Chlorocebus pygerythrus, Cercopithecus neglectus, and Cercopithecus diana). The authors evaluated the self-handicapping character of each pattern and in Hanuman langurs also the (dis)similarity to serious behavior. Of the 74 patterns in the 5 species, 33 (45%) were judged to have a self-handicapping character. Of 48 patterns observed in langurs, 16 (33%) were totally dissimilar to any serious langur behavior known to us. The authors discuss the possibility that the different types of play elements may have different functions in play.