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Sows show stronger responses to isolation calls of piglets associated with greater levels of piglet need
Anim. Behav., 1996, 52, 1247–1253
Sows show stronger responses to isolation calls of piglets associated with greater levels of piglet need DANIEL M. WEARY, GARETH L. LAWSON & BRIAN K. THOMPSON Centre for Food and Animal Research, Agriculture and Agri-Food Canada, Central Experimental Farm, Ottawa (Received 31 October 1995; initial acceptance 26 February 1996; final acceptance 15 May 1996; MS. number: 7437)
Abstract. Natural sequences of calls produced by isolated domestic piglets were played to lactating sows (N=24) separated from their litters. Two piglets from each of eight litters were recorded under conditions designed to influence their need for a rapid response from the sow. The ‘needy’ piglet was the smallest and slowest growing in the litter, had just missed a nursing and was isolated in a relatively cool enclosure. The ‘un-needy’ litter-mate was the largest and fastest growing, had just nursed and was isolated in a relatively warm enclosure. Calls from the needy piglets were of a higher rate, higher in frequency, and longer than those from the un-needy piglets. Sows responded to playback by orientating towards the loudspeaker and approaching it, by moving about the area near the speaker, by vocalizing and by reducing the duration of their own calls. Sows showed stronger responses to playback from needy piglets than from un-needy piglets by vocalizing more, moving more and spending more time near the playback speaker. Sows responded to the calls of their own piglets and to those from other litters, but showed a stronger response to calls of their own piglets. ?
Young animals often direct vocal signals towards parents, and these calls can provide information about varying aspects of the young’s condition. The best known examples of this type are the begging calls of nestling birds. Nestlings of different species call more when they have been longer without food, and these higher call rates evoke a stronger feeding response by parents (e.g. Redondo & Castro 1992). Young birds and mammals will also signal aspects of their condition in other situations, such as during periods of isolation. For example, rodent pups isolated from the dam and nest will produce ultrasonic distress calls and produce more of these calls if they are kept in a cold enclosure (Blumberg & Alberts 1990; 1991). If these sorts of calls provide reliable information about offspring need (Maynard Smith 1991, 1994; Johnstone & Grafen 1992; Godfray 1995), then parents should show stronger Correspondence: D. M. Weary, Centre for Food and Animal Research, Building 94, Central Experimental Farm, Ottawa, K1A 0C6, Canada (email: [email protected]). 0003–3472/96/121247+07 $25.00/0
?
1996 The Association for the Study of Animal Behaviour
responses to calls indicating higher degrees of need. In fact, parents may still respond in this way when some variation in calling is independent of or even inversely related to need (Johnstone & Grafen 1993), as might be the case if larger young incurred a lower cost to calling and could thus call more than siblings with the same level of need. In birds, there is evidence from a number of studies that the parental response varies in relation to calling by the chick. For example, young American white pelicans, Pelecanus erythrorhynchos, produce a characteristic ‘squawk’ when they are exposed to low ambient temperatures, and the likelihood of parents responding by brooding their chicks depends on the number of squawks produced in a calling bout (Evans 1992, 1994). Similarly, magpie nestlings, Pica pica, that have been kept longer without food beg by calling more and displaying in a more intense manner, and parents are more likely to feed young that beg in this way (Redondo & Castro 1992). Playback studies have shown that female rodents will respond to the ultrasonic calls of isolated young by orientating towards them and searching (e.g. Sewell 1970; Allin & Banks 1996 The Association for the Study of Animal Behaviour
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1972), but we are not aware of experimental evidence in mammals for a stronger parental response to calls associated with greater levels of offspring need. Piglets produce distinctive distress calls when isolated from the sow (e.g. Fraser 1975). Variation in these calls relates to the piglet’s state: hungry or slow-growing individuals call more, and use longer, louder and higher pitched calls (Weary & Fraser 1995a), as do piglets that are cold (D. Weary, unpublished data). Our observations of natural interactions indicate that sows respond to these calls by approaching the piglet and by vocalizing. A simple playback experiment demonstrated that sows show a stronger response to these calls than to a white-noise control (Weary & Fraser 1995a). The aim of the present experiment was to determine whether the sows also show a stronger or faster response to the more extreme calls of piglets.
METHODS Subjects were 24 lactating sows from a Yorkshire and Landrace research herd. Sows were housed with their litters in farrowing pens (1.9#2.1 m), with food and water available ad libitum. We tested subjects between 0930 and 1600 hours. We made playback stimulus tapes from recordings of vocalizations of piglets subjected to two different conditions. For each litter, we weighed piglets when the litter was aged 3–6 days and calculated the linear regression of these weights versus birth weight. The ‘relative weight gain’ was the residual from the regression line. The piglet with both the highest body weight and largest positive residual (‘un-needy’ piglet) and the piglet with both the lowest body weight and largest negative residual (‘needy’ piglet) were selected for audio recording. In the two instances where the two highest or two lowest measures (i.e. body weight and residual weight) did not correspond, the piglets were ranked by each measure within litter, and the sum of the two ranks was used to determine which piglet was the most or least needy. The needy piglet was removed from the sow’s udder during a nursing just before milk ejection (i.e. before receiving any milk) and then placed in an enclosure kept in a cool room (13–15)C). The un-needy piglet was removed from the udder after
milk ejection, and placed in an enclosure kept in a warmer room (21–24)C). The aim of these manipulations was to create two classes of piglets that could reasonably be expected to differ in their need to be reunited rapidly with the sow. There was, of course, no way to determine how these different manipulations independently affected the piglets’ vocal behaviour, although in other experiments we have found that each of these manipulations can increase the rate of calling by isolated piglets (Weary & Fraser 1995a, unpublished data). Piglets were audio-recorded for a 10-min period. The enclosures (56#56#70 cm) were in separate, acoustically isolated rooms. Vocalizations were recorded on a Sony DAT TCD-D3 via a Symetrix SX202 preamplifier and a Beyer Dynamic MCE86 N(C) microphone suspended 40 cm above the floor. We assigned the 24 litters to eight blocks each of three litters. Calls were measured from each litter, but playback stimuli were taken only from the litter in each block of three that had the greatest difference in call rate between the needy and un-needy litter-mates. Thus in each block, one sow was played recordings of her own piglets and the other two were played calls from piglets of another sow. Call rate was measured during each minute of the 10-min recording period, and playback tapes were made from the 1-min period where the difference in call rate between the needy and un-needy piglets was the greatest. We analysed the calls in each of the 16 (the needy and un-needy piglet from litters from each of the 8 blocks) 1-min playback tapes using Signal software (Engineering Design 1991). The needy playback tapes had more calls (mean& 70&6.1 versus 29&2.8), and these calls were longer (330&42 versus 202&14 ms) and at a higher frequency (1036&115 versus 353&57 Hz) than those from the less needy litter-mates. Typical differences between calls of needy and un-needy piglets tend to be less than these extreme differences presented in our playback tapes (D. Weary, unpublished data). Thus our experiment tested only whether sows respond differently to the extremes from the two classes of piglets. We performed trials when litters had reached 7–11 days of age. The test room (4.6#3.6 m) was visually and acoustically isolated from the farrowing pens, and the floor was divided into nine equal sections. On the side of the room opposite to the
Weary et al.: Sow response to piglet calls entrance was a plywood barrier that ran the width of the room at a height of 90 cm. A playback speaker (Fostex 6301B) was positioned behind the barrier at a height of 70 cm. We played stimulus tapes on a Sony DAT TCD-D3. Sows were recorded using a Sony video-recorder SLV494HF, with video input from two Burle TC651EA black and white video-cameras in opposite corners of the room and audio input from a Beyer Dynamic MCE86 N(C) microphone suspended from the centre of the ceiling. Once in the test room, the sow was acclimatized for 30 min before the first playback. We played two 1-min sequences, one consisting of the calls of a needy piglet and the other the calls of an un-needy litter-mate. The two playbacks were separated by 15 min of silence, and 10 min of silence followed the second playback. Once the 57-min trial was complete, we returned the sow to her home pen. The order in which sows received the playback stimuli was varied systematically within each block of three sows. All three sows were played the calls from the same two piglets from one of the three litters. For the two sows played the calls of piglets that were not their own, one heard the needy piglet first and the other the un-needy piglet first, as determined at random. For sows played calls from their own piglets, the playback order was assigned such that half the sows heard the needy piglet first and the others the un-needy first, with allocation randomly determined. We scored sow responses from the videotape during each of the 1-min playback and 5-min post-playback periods. For both playback and post-playback periods we recorded the number of sow vocalizations/min, the duration (ms) of these vocalizations, the number of movements/min, and the time (s/min) spent at the barrier, as well as latency to vocalize, move and approach the barrier. A sow was defined as being at the barrier if her front legs were in any of the three sections adjacent to the barrier. Sow movements were defined as the number of boundary lines between sections that the sow crossed. To improve the normality of the distributions, the variables were log transformed. These dependent variables were subjected to an ANOVA model that included block (7 df ), order (needy versus un-needy played first, 1 df ), and relatedness (playback from own versus other piglets, 1 df ) as between-subject effects tested
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against an error term with 14 df. Piglet condition (needy versus un-needy, 1 df ) and the interactions of order by piglet condition and relatedness by piglet condition were tested as within-subject effects against an error term with 21 df. Period (during versus after playback, 1 df ), order by period, relatedness by period and period by piglet condition were tested as within-stimulus effects against an error term with 44 df. To determine how response varied across the 16 playback sequences (the needy and un-needy piglet from each of the eight blocks), we calculated the Pearson correlation coefficient for the relationship between features of the playback sequence (the number, frequency and duration of the piglet calls played) and the response. Each playback sequence was played to three different sows, so the mean response across the three subjects was used in these correlations.
RESULTS During the 30-min pre-playback period, sows spent most of their time lying near the door, but they also occasionally vocalized (2.19&1.05 calls/min), spent some time near the barrier (8.13&1.14 s/min) and made some movements (1.19&1.05 movements/min). During playback, however, sows vocalized more (5.96&1.07 calls/min), spent more time at the barrier (14.80&0.06 s/min), and moved more (2.80&0.05 movements/min). Sows also responded by raising the head, orientating the head and body towards the speaker and approaching the barrier. Movements during response normally involved pacing back and forth along the barrier, or circling next to the barrier. All sows responded to at least one, and usually both of the playback sequences. They also gave stronger responses to the playback of the needy piglet’s calls than to those of the un-needy piglet (Fig. 1). Sows called more (P<0.0001), moved more (P<0.0001) and spent more time at the barrier (P<0.01) when played the isolation calls of a needy piglet. Also, the latencies until first incidence of each of the three variables were smaller in response to playback from the needy piglets (P<0.001). In terms of all measures, responses were slightly stronger during than after playback (0.3>P>0.06). There was also an interaction between piglet condition and playback period
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Figure 1. The mean+2 (a) number of sow movements/min, (b) latency to first movement, (c) s/min spent within a quadrant adjacent to the barrier obscuring the loudspeaker, (d) latency to approach the barrier, (e) number of calls/min, and (f) latency to produce first call (N=24 sows). Responses are shown separately for playback of calls from needy (/) and un-needy piglets (.). Parts a, c, and e show responses separately during the 1 min of playback and during a 5-min period after playback.
for the vocalization (P<0.04) and movement responses (P<0.01), resulting from a larger effect of piglet condition during playback than after.
Sows responded both to the calls of their own piglets and to those from other litters. Sows responded to playback from their own piglets by
Weary et al.: Sow response to piglet calls vocalizing more quickly (own 14.8&1.1 s versus other 29.4&0.8 s; P<0.01), but there was no significant difference for any of the other response variables (P>0.1). There were also no interactions between this effect and piglet condition or period for any of the response measures (P>0.06). We also found no effect of order (i.e. needy stimulus first or last; P>0.1) and no interaction between order and period (P>0.1). We did find an interaction between order and piglet condition for latency to vocalize (P<0.002), and number of vocalizations (P<0.05), resulting from a larger effect of piglet condition when the un-needy calls were played first. This interaction was not significant for any of the other response measures (P>0.1). We also found no relationship between the response measures and sow parity, litter size, or piglet age. Calls produced by sows when separated from their litters are often very long. Sows responded to playback not only by calling more, but also by reducing the duration of these vocalizations. Sows produced shorter calls during playback (556&22 ms) than after playback (836&21 ms; P<0.0001), and also produced shorter calls in response to playback from needy piglets (640&34 ms) than from the un-needy ones (774&40 ms; P<0.002). There was no interaction between piglet need and playback period for this variable (P>0.1). Across the 16 playback sequences there was a continuous range of variation in the number, frequency and duration of the piglet calls played, and this variation appeared to affect the sow’s response. All measures of sow response were significantly correlated with the number of piglet calls played (0.50
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sequences of isolated piglets in greater need of the sow’s response. They responded to playback by approaching the speaker, by moving about the area near the speaker, by vocalizing more and by shortening the duration of their calls. The subjects responded to calls from their own piglets and those from other litters, but showed a slightly faster response to the former. In a much simpler experiment, Weary & Fraser (1995a) found that sows responded more to playback of piglet isolation calls than to white-noise. Other experiments on pigs have shown that sows respond to the calls of trapped piglets (such as when they are crushed underneath a sow: Hutson et al. 1991, 1992, 1993). In these experiments, only about 50% of sows responded (compared with 100% of subjects in the current experiment), despite the fact that the signal was related to an extremely urgent situation. It has been argued that the isolation calls of rat pups and perhaps other neonates may be a by-product of laryngeal braking, a respiratory mechanism for increasing the uptake of oxygen by the lungs (Blumberg & Alberts 1990, 1991). According to this view, calling increases as an isolated pup chills because of the higher oxygen requirements of thermoregulation. Our results for piglets indicate that at least one function of the isolation calls is to attract a response from the sow, and that variation in calling functions to vary the likelihood or strength of this response. Other work has shown that piglets increase their call rate in response to playback of sow calls (Walser 1986; D. Weary, unpublished data), a social stimulus that should not directly affect the piglets’ oxygen requirements. In the current study we detected only a minor effect of the piglet’s identity on the sow’s response. Horrell & Hodgson (1985) also tested whether sows discriminated between the calls of their own piglets and piglets from other litters, but did not find a significant difference. Piglets, however, are able to distinguish the calls of their own sow from those of another (Horrell & Hodgson 1985; Walser 1986). There are, of course, good reasons for animals to be able to distinguish between individuals or classes of individuals on the basis of their vocalizations (Falls 1982). In the wild, sows remain isolated from their group for about 10 days after parturition, but then return to the multi-sow herd where they are in contact with piglets from other litters (Jensen 1986). Sows
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clearly have more to gain by retrieving one of their own lost piglets than one from another litter. This benefit will be reduced when litters are closely related, however, as might be expected given the social structure of these groups (Mauget 1981), and there is some evidence that sows will provide care to the piglets from litters other than their own (Graves 1984; Newberry & Wood-Gush 1985). The reduced duration of sow calls during playback might reflect an attempt by the sow to avoid interfering with her piglet’s calls. Reducing call duration might be adaptive if sows are unable to properly hear or localize the calls of the piglet when vocalizing themselves. At other times, long calls may be more effective, because these may be easier for piglets to detect and localize. It has been hypothesized that birds should use short songs when they must listen for a response (as in during interactions with another male) but should use longer songs when listening for a response is less important (as when attempting to attract a mate; Catchpole 1980). Birds will sometimes switch to singing shorter songs, or to producing calls (which are normally shorter than songs) in response to playback of male song (e.g. Adhikerana & Slater 1993). Also, frogs will respond to another male’s calls by adjusting their inter-call interval in a way that avoids overlap (Klump & Gerhardt 1992). An applied aim of this work on piglet isolation calls is to determine whether these can be used in the assessment of certain aspects of the piglet’s welfare (Weary & Fraser 1995b). If these calls can provide reliable information about the caller’s needs, they should be useful in assessing how well the animal is adjusting to changes in housing or management conditions at key periods in its life such as after weaning. The results of this experiment, showing that sows respond to these calls and respond more to more extreme sequences, help explain why piglets call and why needy piglets call more, and hence help validate the application of these calls as a tool in welfare assessment.
ACKNOWLEDGMENTS We thank David Fraser, Don Kramer and Ed Pajor for their many contributions, Del Buckley and Marcel Lalonde for help with Signal, and Sue Leffler and the staff of our research barn for their help in running experiments. We are also grateful
to Leah Braithwaite, Roger Evans, Bennett Galef, Andy Horn, Gudrun Illman, Barry Milligan, Marek Spinka and two anonymous referees for commenting on earlier drafts of this manuscript. G.L.L. thanks the Natural Sciences and Engineering Research Council of Canada for support from a summer studentship and from an operating grant to Don Kramer.
REFERENCES Adhikerana, A. S. & Slater, P. J. B. 1993. Singing interactions in coal tits, Parus ater: an experimental approach. Anim. Behav., 46, 1205–1211. Allin, J. T. & Banks, E. M. 1972. Functional aspects of ultrasound production by infant albino rats, Rattus norvegicus. Anim. Behav., 20, 175–185. Blumberg, M. S. & Alberts, J. R. 1990. Ultrasonic vocalizations by rat pups in the cold: an acoustic by-product of laryngeal braking? Behav. Neurosci., 104, 808–817. Blumberg, M. S. & Alberts, J. R. 1991. Both hypoxia and milk deprivation diminish metabolic heat production and ultrasound emission by rat pups during cold exposure. Behav. Neurosci., 105, 1030–1037. Catchpole, C. K. 1980. Sexual selection and the evolution of complex songs among European warblers of the genus Acrocephalus. Behaviour, 74, 149–166. Falls, J. B. 1982. Individual recognition by sounds in birds. In: Acoustic Communication in Birds, Vol. 2 (Ed. by D. E. Kroodsma & E. H. Miller), pp. 237–278. New York: Academic Press. Engineering Design. 1991. Signal: User’s Manual. Belmont, Massachusetts: Engineering Design. Evans, R. M. 1992. Embryonic and neonatal vocal elicitation of parental brooding and feeding responses in American white pelicans. Anim. Behav., 44, 667–675. Evans, R. M. 1994. Cold-induced calling and shivering in young American white pelicans: honest signalling of offspring need for warmth in a functionally integrated thermoregulatory system. Behaviour, 129, 13–34. Fraser, D. 1975. Vocalizations of isolated piglets. I. Sources of variation and relationships among measures. Appl. Anim. Ethol., 1, 387–394. Godfray, H. C. J. 1995. Signaling of need between parents and young: parent–offspring conflict and sibling rivalry. Am. Nat., 146, 1–24. Graves, H. R. 1984. Behavior and ecology of wild and feral swine (Sus scrofa). J. Anim. Sci., 58, 482–492. Horrell, I. & Hodgson, J. 1985. Mutual recognition between sows and their litters. In: Proceedings of the International Congress on Applied Ethology of Farm Animals, Kiel, 1984 (Ed. by J. Unshelm, G. van Putten & K. Zeeb), pp. 108–112. Darmstadt: KTBL. Hutson, G. D., Wilkinson, J. L. & Luxford, B. G. 1991. The response of lactating sows to tactile, visual and auditory stimuli associated with a model piglet. Appl. Anim. Behav. Sci., 32, 129–137.
Weary et al.: Sow response to piglet calls Hutson, G. D., Argent, M. F., Dickenson, L. G. & Luxford, B. G. 1992. Influence of parity and time since parturition on responsiveness of sows to a piglet distress call. Appl. Anim. Behav. Sci., 34, 303–313. Hutson, G. D., Price, E. O. & Dickenson, L. G. 1993. The effect of playback volume and duration on responsiveness of sows to piglet distress calls. Appl. Anim. Behav. Sci., 37, 31–37. Jensen, P. 1986. Observations on the maternal behaviour of free-ranging domestic pigs. Appl. Anim. Behav. Sci., 16, 131–142. Johnstone, R. A. & Grafen, A. 1992. The continuous Sir Philip Sidney game: a simple model of biological signalling. J. theor. Biol., 156, 215–234. Johnstone, R. A. & Grafen, A. 1993. Dishonesty and the handicap principle. Anim. Behav., 46, 759–764. Klump, G. M. & Gerhardt, H. C. 1992. Mechanisms and functions of call-timing in male–male interactions in frogs. In: Playback and Studies of Animal Communication (Ed. by P. K. McGregor), pp. 153–174. New York: Plenum Press. Mauget, R. 1981. Behavioural and reproductive strategies in wild forms of Sus scrofa (European wild
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boar and feral pigs). In: The Welfare of Pigs (Ed. by W. Sybesma), pp. 3–13. The Hague: Martinus Nijhoff. Maynard Smith, J. 1991. Honest signalling: the Philip Sidney game. Anim. Behav., 42, 1034–1035. Maynard Smith, J. 1994. Must reliable signals always be costly? Anim. Behav., 47, 1115–1120. Newberry, R. C. & Wood-Gush, D. G. M. 1985. The suckling behaviour of domestic pigs in a semi-natural environment. Behaviour, 95, 11–25. Redondo, T. & Castro, F. 1992. Signalling of nutritional need by magpie nestlings. Ethology, 92, 193–204. Sewell, G. D. 1970. Ultrasonic communication in rodents. Nature, 227, 410. Walser, E. E. S. 1986. Recognition of the sow’s voice by neonatal piglets. Behaviour, 99, 177–188. Weary, D. M. & Fraser, D. 1995a. Calling by domestic piglets: reliable signals of need? Anim. Behav., 50, 1047–1055. Weary, D. M. & Fraser, D. 1995b. Signalling need: costly signals and animal welfare assessment. Appl. Anim. Behav. Sci., 44, 139–157.
Sows show stronger responses to isolation calls of piglets associated with greater levels of piglet need DANIEL M. WEARY, GARETH L. LAWSON & BRIAN K. THOMPSON Centre for Food and Animal Research, Agriculture and Agri-Food Canada, Central Experimental Farm, Ottawa (Received 31 October 1995; initial acceptance 26 February 1996; final acceptance 15 May 1996; MS. number: 7437)
Abstract. Natural sequences of calls produced by isolated domestic piglets were played to lactating sows (N=24) separated from their litters. Two piglets from each of eight litters were recorded under conditions designed to influence their need for a rapid response from the sow. The ‘needy’ piglet was the smallest and slowest growing in the litter, had just missed a nursing and was isolated in a relatively cool enclosure. The ‘un-needy’ litter-mate was the largest and fastest growing, had just nursed and was isolated in a relatively warm enclosure. Calls from the needy piglets were of a higher rate, higher in frequency, and longer than those from the un-needy piglets. Sows responded to playback by orientating towards the loudspeaker and approaching it, by moving about the area near the speaker, by vocalizing and by reducing the duration of their own calls. Sows showed stronger responses to playback from needy piglets than from un-needy piglets by vocalizing more, moving more and spending more time near the playback speaker. Sows responded to the calls of their own piglets and to those from other litters, but showed a stronger response to calls of their own piglets. ?
Young animals often direct vocal signals towards parents, and these calls can provide information about varying aspects of the young’s condition. The best known examples of this type are the begging calls of nestling birds. Nestlings of different species call more when they have been longer without food, and these higher call rates evoke a stronger feeding response by parents (e.g. Redondo & Castro 1992). Young birds and mammals will also signal aspects of their condition in other situations, such as during periods of isolation. For example, rodent pups isolated from the dam and nest will produce ultrasonic distress calls and produce more of these calls if they are kept in a cold enclosure (Blumberg & Alberts 1990; 1991). If these sorts of calls provide reliable information about offspring need (Maynard Smith 1991, 1994; Johnstone & Grafen 1992; Godfray 1995), then parents should show stronger Correspondence: D. M. Weary, Centre for Food and Animal Research, Building 94, Central Experimental Farm, Ottawa, K1A 0C6, Canada (email: [email protected]). 0003–3472/96/121247+07 $25.00/0
?
1996 The Association for the Study of Animal Behaviour
responses to calls indicating higher degrees of need. In fact, parents may still respond in this way when some variation in calling is independent of or even inversely related to need (Johnstone & Grafen 1993), as might be the case if larger young incurred a lower cost to calling and could thus call more than siblings with the same level of need. In birds, there is evidence from a number of studies that the parental response varies in relation to calling by the chick. For example, young American white pelicans, Pelecanus erythrorhynchos, produce a characteristic ‘squawk’ when they are exposed to low ambient temperatures, and the likelihood of parents responding by brooding their chicks depends on the number of squawks produced in a calling bout (Evans 1992, 1994). Similarly, magpie nestlings, Pica pica, that have been kept longer without food beg by calling more and displaying in a more intense manner, and parents are more likely to feed young that beg in this way (Redondo & Castro 1992). Playback studies have shown that female rodents will respond to the ultrasonic calls of isolated young by orientating towards them and searching (e.g. Sewell 1970; Allin & Banks 1996 The Association for the Study of Animal Behaviour
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1972), but we are not aware of experimental evidence in mammals for a stronger parental response to calls associated with greater levels of offspring need. Piglets produce distinctive distress calls when isolated from the sow (e.g. Fraser 1975). Variation in these calls relates to the piglet’s state: hungry or slow-growing individuals call more, and use longer, louder and higher pitched calls (Weary & Fraser 1995a), as do piglets that are cold (D. Weary, unpublished data). Our observations of natural interactions indicate that sows respond to these calls by approaching the piglet and by vocalizing. A simple playback experiment demonstrated that sows show a stronger response to these calls than to a white-noise control (Weary & Fraser 1995a). The aim of the present experiment was to determine whether the sows also show a stronger or faster response to the more extreme calls of piglets.
METHODS Subjects were 24 lactating sows from a Yorkshire and Landrace research herd. Sows were housed with their litters in farrowing pens (1.9#2.1 m), with food and water available ad libitum. We tested subjects between 0930 and 1600 hours. We made playback stimulus tapes from recordings of vocalizations of piglets subjected to two different conditions. For each litter, we weighed piglets when the litter was aged 3–6 days and calculated the linear regression of these weights versus birth weight. The ‘relative weight gain’ was the residual from the regression line. The piglet with both the highest body weight and largest positive residual (‘un-needy’ piglet) and the piglet with both the lowest body weight and largest negative residual (‘needy’ piglet) were selected for audio recording. In the two instances where the two highest or two lowest measures (i.e. body weight and residual weight) did not correspond, the piglets were ranked by each measure within litter, and the sum of the two ranks was used to determine which piglet was the most or least needy. The needy piglet was removed from the sow’s udder during a nursing just before milk ejection (i.e. before receiving any milk) and then placed in an enclosure kept in a cool room (13–15)C). The un-needy piglet was removed from the udder after
milk ejection, and placed in an enclosure kept in a warmer room (21–24)C). The aim of these manipulations was to create two classes of piglets that could reasonably be expected to differ in their need to be reunited rapidly with the sow. There was, of course, no way to determine how these different manipulations independently affected the piglets’ vocal behaviour, although in other experiments we have found that each of these manipulations can increase the rate of calling by isolated piglets (Weary & Fraser 1995a, unpublished data). Piglets were audio-recorded for a 10-min period. The enclosures (56#56#70 cm) were in separate, acoustically isolated rooms. Vocalizations were recorded on a Sony DAT TCD-D3 via a Symetrix SX202 preamplifier and a Beyer Dynamic MCE86 N(C) microphone suspended 40 cm above the floor. We assigned the 24 litters to eight blocks each of three litters. Calls were measured from each litter, but playback stimuli were taken only from the litter in each block of three that had the greatest difference in call rate between the needy and un-needy litter-mates. Thus in each block, one sow was played recordings of her own piglets and the other two were played calls from piglets of another sow. Call rate was measured during each minute of the 10-min recording period, and playback tapes were made from the 1-min period where the difference in call rate between the needy and un-needy piglets was the greatest. We analysed the calls in each of the 16 (the needy and un-needy piglet from litters from each of the 8 blocks) 1-min playback tapes using Signal software (Engineering Design 1991). The needy playback tapes had more calls (mean& 70&6.1 versus 29&2.8), and these calls were longer (330&42 versus 202&14 ms) and at a higher frequency (1036&115 versus 353&57 Hz) than those from the less needy litter-mates. Typical differences between calls of needy and un-needy piglets tend to be less than these extreme differences presented in our playback tapes (D. Weary, unpublished data). Thus our experiment tested only whether sows respond differently to the extremes from the two classes of piglets. We performed trials when litters had reached 7–11 days of age. The test room (4.6#3.6 m) was visually and acoustically isolated from the farrowing pens, and the floor was divided into nine equal sections. On the side of the room opposite to the
Weary et al.: Sow response to piglet calls entrance was a plywood barrier that ran the width of the room at a height of 90 cm. A playback speaker (Fostex 6301B) was positioned behind the barrier at a height of 70 cm. We played stimulus tapes on a Sony DAT TCD-D3. Sows were recorded using a Sony video-recorder SLV494HF, with video input from two Burle TC651EA black and white video-cameras in opposite corners of the room and audio input from a Beyer Dynamic MCE86 N(C) microphone suspended from the centre of the ceiling. Once in the test room, the sow was acclimatized for 30 min before the first playback. We played two 1-min sequences, one consisting of the calls of a needy piglet and the other the calls of an un-needy litter-mate. The two playbacks were separated by 15 min of silence, and 10 min of silence followed the second playback. Once the 57-min trial was complete, we returned the sow to her home pen. The order in which sows received the playback stimuli was varied systematically within each block of three sows. All three sows were played the calls from the same two piglets from one of the three litters. For the two sows played the calls of piglets that were not their own, one heard the needy piglet first and the other the un-needy piglet first, as determined at random. For sows played calls from their own piglets, the playback order was assigned such that half the sows heard the needy piglet first and the others the un-needy first, with allocation randomly determined. We scored sow responses from the videotape during each of the 1-min playback and 5-min post-playback periods. For both playback and post-playback periods we recorded the number of sow vocalizations/min, the duration (ms) of these vocalizations, the number of movements/min, and the time (s/min) spent at the barrier, as well as latency to vocalize, move and approach the barrier. A sow was defined as being at the barrier if her front legs were in any of the three sections adjacent to the barrier. Sow movements were defined as the number of boundary lines between sections that the sow crossed. To improve the normality of the distributions, the variables were log transformed. These dependent variables were subjected to an ANOVA model that included block (7 df ), order (needy versus un-needy played first, 1 df ), and relatedness (playback from own versus other piglets, 1 df ) as between-subject effects tested
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against an error term with 14 df. Piglet condition (needy versus un-needy, 1 df ) and the interactions of order by piglet condition and relatedness by piglet condition were tested as within-subject effects against an error term with 21 df. Period (during versus after playback, 1 df ), order by period, relatedness by period and period by piglet condition were tested as within-stimulus effects against an error term with 44 df. To determine how response varied across the 16 playback sequences (the needy and un-needy piglet from each of the eight blocks), we calculated the Pearson correlation coefficient for the relationship between features of the playback sequence (the number, frequency and duration of the piglet calls played) and the response. Each playback sequence was played to three different sows, so the mean response across the three subjects was used in these correlations.
RESULTS During the 30-min pre-playback period, sows spent most of their time lying near the door, but they also occasionally vocalized (2.19&1.05 calls/min), spent some time near the barrier (8.13&1.14 s/min) and made some movements (1.19&1.05 movements/min). During playback, however, sows vocalized more (5.96&1.07 calls/min), spent more time at the barrier (14.80&0.06 s/min), and moved more (2.80&0.05 movements/min). Sows also responded by raising the head, orientating the head and body towards the speaker and approaching the barrier. Movements during response normally involved pacing back and forth along the barrier, or circling next to the barrier. All sows responded to at least one, and usually both of the playback sequences. They also gave stronger responses to the playback of the needy piglet’s calls than to those of the un-needy piglet (Fig. 1). Sows called more (P<0.0001), moved more (P<0.0001) and spent more time at the barrier (P<0.01) when played the isolation calls of a needy piglet. Also, the latencies until first incidence of each of the three variables were smaller in response to playback from the needy piglets (P<0.001). In terms of all measures, responses were slightly stronger during than after playback (0.3>P>0.06). There was also an interaction between piglet condition and playback period
Animal Behaviour, 52, 6
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Figure 1. The mean+2 (a) number of sow movements/min, (b) latency to first movement, (c) s/min spent within a quadrant adjacent to the barrier obscuring the loudspeaker, (d) latency to approach the barrier, (e) number of calls/min, and (f) latency to produce first call (N=24 sows). Responses are shown separately for playback of calls from needy (/) and un-needy piglets (.). Parts a, c, and e show responses separately during the 1 min of playback and during a 5-min period after playback.
for the vocalization (P<0.04) and movement responses (P<0.01), resulting from a larger effect of piglet condition during playback than after.
Sows responded both to the calls of their own piglets and to those from other litters. Sows responded to playback from their own piglets by
Weary et al.: Sow response to piglet calls vocalizing more quickly (own 14.8&1.1 s versus other 29.4&0.8 s; P<0.01), but there was no significant difference for any of the other response variables (P>0.1). There were also no interactions between this effect and piglet condition or period for any of the response measures (P>0.06). We also found no effect of order (i.e. needy stimulus first or last; P>0.1) and no interaction between order and period (P>0.1). We did find an interaction between order and piglet condition for latency to vocalize (P<0.002), and number of vocalizations (P<0.05), resulting from a larger effect of piglet condition when the un-needy calls were played first. This interaction was not significant for any of the other response measures (P>0.1). We also found no relationship between the response measures and sow parity, litter size, or piglet age. Calls produced by sows when separated from their litters are often very long. Sows responded to playback not only by calling more, but also by reducing the duration of these vocalizations. Sows produced shorter calls during playback (556&22 ms) than after playback (836&21 ms; P<0.0001), and also produced shorter calls in response to playback from needy piglets (640&34 ms) than from the un-needy ones (774&40 ms; P<0.002). There was no interaction between piglet need and playback period for this variable (P>0.1). Across the 16 playback sequences there was a continuous range of variation in the number, frequency and duration of the piglet calls played, and this variation appeared to affect the sow’s response. All measures of sow response were significantly correlated with the number of piglet calls played (0.50
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sequences of isolated piglets in greater need of the sow’s response. They responded to playback by approaching the speaker, by moving about the area near the speaker, by vocalizing more and by shortening the duration of their calls. The subjects responded to calls from their own piglets and those from other litters, but showed a slightly faster response to the former. In a much simpler experiment, Weary & Fraser (1995a) found that sows responded more to playback of piglet isolation calls than to white-noise. Other experiments on pigs have shown that sows respond to the calls of trapped piglets (such as when they are crushed underneath a sow: Hutson et al. 1991, 1992, 1993). In these experiments, only about 50% of sows responded (compared with 100% of subjects in the current experiment), despite the fact that the signal was related to an extremely urgent situation. It has been argued that the isolation calls of rat pups and perhaps other neonates may be a by-product of laryngeal braking, a respiratory mechanism for increasing the uptake of oxygen by the lungs (Blumberg & Alberts 1990, 1991). According to this view, calling increases as an isolated pup chills because of the higher oxygen requirements of thermoregulation. Our results for piglets indicate that at least one function of the isolation calls is to attract a response from the sow, and that variation in calling functions to vary the likelihood or strength of this response. Other work has shown that piglets increase their call rate in response to playback of sow calls (Walser 1986; D. Weary, unpublished data), a social stimulus that should not directly affect the piglets’ oxygen requirements. In the current study we detected only a minor effect of the piglet’s identity on the sow’s response. Horrell & Hodgson (1985) also tested whether sows discriminated between the calls of their own piglets and piglets from other litters, but did not find a significant difference. Piglets, however, are able to distinguish the calls of their own sow from those of another (Horrell & Hodgson 1985; Walser 1986). There are, of course, good reasons for animals to be able to distinguish between individuals or classes of individuals on the basis of their vocalizations (Falls 1982). In the wild, sows remain isolated from their group for about 10 days after parturition, but then return to the multi-sow herd where they are in contact with piglets from other litters (Jensen 1986). Sows
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clearly have more to gain by retrieving one of their own lost piglets than one from another litter. This benefit will be reduced when litters are closely related, however, as might be expected given the social structure of these groups (Mauget 1981), and there is some evidence that sows will provide care to the piglets from litters other than their own (Graves 1984; Newberry & Wood-Gush 1985). The reduced duration of sow calls during playback might reflect an attempt by the sow to avoid interfering with her piglet’s calls. Reducing call duration might be adaptive if sows are unable to properly hear or localize the calls of the piglet when vocalizing themselves. At other times, long calls may be more effective, because these may be easier for piglets to detect and localize. It has been hypothesized that birds should use short songs when they must listen for a response (as in during interactions with another male) but should use longer songs when listening for a response is less important (as when attempting to attract a mate; Catchpole 1980). Birds will sometimes switch to singing shorter songs, or to producing calls (which are normally shorter than songs) in response to playback of male song (e.g. Adhikerana & Slater 1993). Also, frogs will respond to another male’s calls by adjusting their inter-call interval in a way that avoids overlap (Klump & Gerhardt 1992). An applied aim of this work on piglet isolation calls is to determine whether these can be used in the assessment of certain aspects of the piglet’s welfare (Weary & Fraser 1995b). If these calls can provide reliable information about the caller’s needs, they should be useful in assessing how well the animal is adjusting to changes in housing or management conditions at key periods in its life such as after weaning. The results of this experiment, showing that sows respond to these calls and respond more to more extreme sequences, help explain why piglets call and why needy piglets call more, and hence help validate the application of these calls as a tool in welfare assessment.
ACKNOWLEDGMENTS We thank David Fraser, Don Kramer and Ed Pajor for their many contributions, Del Buckley and Marcel Lalonde for help with Signal, and Sue Leffler and the staff of our research barn for their help in running experiments. We are also grateful
to Leah Braithwaite, Roger Evans, Bennett Galef, Andy Horn, Gudrun Illman, Barry Milligan, Marek Spinka and two anonymous referees for commenting on earlier drafts of this manuscript. G.L.L. thanks the Natural Sciences and Engineering Research Council of Canada for support from a summer studentship and from an operating grant to Don Kramer.
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