If a Baby Girl Guinea Pig Looks Almost Identcal to Its Mother ; {|

Vocal mother-offspring communication in guinea pigs: females adjust maternal responsiveness to litter size

Melanie Kober

ⁱDepartment of Animal Behaviour, University Bielefeld, P.O. Box 100 131, 33501 Bielefeld, Germany

Fritz Trillmich

¹Department of Animal Behaviour, University Bielefeld, P.O. Box 100 131, 33501 Bielefeld, Federal republic of germany

Marc Naguib

^aneDepartment of Animal Behaviour, University Bielefeld, P.O. Box 100 131, 33501 Bielefeld, Federal republic of germany

ⁱⁱNetherlands Institute of Ecology (NIOO-KNAW), Department of Population Biology, P.O. Box 40, 6666 ZG Heteren, The netherlands

Received 2008 Apr 29; Accepted 2008 Sep x.

Abstract

Groundwork

In parent-offspring communication, vocal signals are frequently used to attract attention and offspring might telephone call to induce parental behaviour. In guinea pigs (Cavia aperea f. porcellus) mothers wean larger litters later than pocket-size ones, but it is unknown whether this difference depends on processes induced during pregnancy or is influenced mail-natally by the number of pups present. We hither tested with playback-experiments using pup separation calls whether mothers with cross-fostered large experimental litters (4-pup-litters) were more responsive to offspring calls and maintained responsiveness for longer than mothers with pocket-size experimental litters (2-pup-litters). Mothers were tested when two pups were suckling i.e. when both teats were occupied.

Results

Mothers of four-pup litters responded stronger to circulate pup separation calls than those with two-pup litters. Additionally, we tested the mothers' responsiveness to pup separation calls in the absenteeism of their pups on day 8 and 20 of lactation. Mothers of 4-pup litters responded stronger and showed no decrease in responsiveness from day 8 to 20, whereas mothers of two-pup litters responded less and decreased responsiveness from solar day 8 to xx. Mothers of four-pup litters also weaned their pups 5 days later on than those of two-pup litters.

Conclusion

Measured by their response to pup calls and by fourth dimension to weaning, guinea hog mothers conform maternal responsiveness to litter size. This behaviour is likely to exist an adaptive strategy in resource allocation during reproduction.

Background

Offspring vary in their demand and condition and parents must appraise these parameters to provide optimal care. Therefore, offspring should communicate their needs to the parents and parents should act upon these signals. Studies on altricial animals show that offspring induce and maintain parental intendance by visual, acoustic, olfactory and tactile stimuli [1-6]. Maternal behaviour changes over time either due to a shift in maternal state or to changing stimulus characteristics of the young [3]. In rodents, maternal behaviour is influenced strongly by the age of pups and litter size [7,8]. Absence of sufficient stimuli may issue in females abandoning offspring or even the consummate brood [9,10]. In gild to understand principles of resource allocation, maternal responsiveness to offspring stimuli and its modify over time needs to be determined.

Rodents are an established model in such studies on maternal behaviour and parent-offspring conflict. Nevertheless, most studies take been conducted on altricial species. Reproductive patterns differ for altricial and precocial rodent species particularly due to the fact that young of the latter brainstorm early to contribute to their energy requirements by contained food intake [eleven]. In many species the sucking stimulus affects milk supply and the length of time to weaning [eight,12]. For example in rats, lactation can exist maintained far beyond normal weaning by repeatedly fostering younger pups to a mother [8]. However, in dissimilarity to rats, the milk yield curve in guinea pigs (Cavia aperea f. porcellus) is rather fixed [thirteen]. Mothers terminate lactation and only tend to prolong the lactation period slightly when given much younger foster pups [14]. Thus, these findings raise the question as to whether republic of guinea pig mothers adjust their responses to experimentally manipulated offspring demand [fourteen-xvi].

Previous studies showed that guinea pig females reduce milk output when litter size is reduced. In dissimilarity, they do not increase milk yield proportionally to increases in litter size, at to the lowest degree not in litters consisting of more than than three pups [13]. With an average litter size of more three pups, but but two teats, competition between litter mates virtually admission to milk is likely to occur and models of scramble competition depict pup-interactions better than honest signalling models [fifteen]. Pups testify moderately aggressive behaviour in the form of tussling. However, a previous study showed that pups do not succeed in getting access to a teat through tussling. Instead, hungrier pups reply faster to the presence of the mother and thereby gain preferential admission to a teat [xv].

I strategy by pups to obtain attending past the mother is to activate her past calling [17]. Song communication is important for precocial species where offspring actively moves around. Republic of guinea sus scrofa mothers recognize their pups non only by olfactory cues but also by vocal cues and pup calls tin can induce female vocal responses [18,nineteen]. Equally mothers of larger litters cannot nurse their complete litter simultaneously and as larger litters are weaned subsequently [20], females with larger litters tin be expected to be more often than not more responsive to their offspring for a longer catamenia than females with modest litters.

To test the hypothesis that mothers accommodate responsiveness to calling pups according to litter size, nosotros provided females with small or large litters through cantankerous-fostering and conducted playback experiments with pup separation calls to exam maternal responsiveness. We tested whether lactating mothers of larger (4-pup) experimental litters abandoned their ii suckling pups more often than mothers of smaller (two-pup) experimental litters when another pup's separation calls were broadcast. We likewise tested the mothers' responsiveness to pup separation calls at dissimilar times in the lactation period (day 8 and 20; weaning occurs betwixt 24-hour interval 25 and thirty depending on circumstances) and predicted that mothers with large experimental litters should reply stronger at both stages during lactation than mothers with small and less needy experimental litters.

Methods

We conducted two playback experiments on outbred domestic republic of guinea pigs at the University of Bielefeld, Germany. All subjects were kept indoors on a 14:10 (L:D) photoperiod at 20–23°C. Laboratory guinea grunter chow (Höveler, Langenfeld, Deutschland) and water were provided ad libitum, supplemented with hay and fresh food. Females were allowed to breed in groups of two females and ane male. lx multiparous females were paired. Three days prior to the expected parturition appointment, females were kept singly in holding compartments (0.89 m × 0.89 m × 0.50 g). We created two- and four-pup litters by cross-fostering pups. To treat every litter equally, we cross-fostered pups fifty-fifty if a female's original litter size corresponded to the later experimental litter size, so that each female raised at least one foster pup and most females raised only foster pups and no own pup. We cantankerous-fostered pups from litters born at the aforementioned twenty-four hours or on two subsequent days. Due to low synchrony of birth dates nosotros could utilise only 28 females as experimental animals (13 litters of two and 15 litters of four pups). Original litter sizes did not differ significantly in experimental groups of ii- and four-pup litters (Mann-Whitney U-test; U = 73.5, Due north₁ = 13, Northward₂ = xv, p = 0.27).

Playback Stimuli

As playback stimuli we used pup separation calls [19]. For separation, a pup was removed from its holding compartment and placed in an enclosure (0.30 × 0.25 × 0.twenty m) in an adjacent room. Separation lasted maximally 10 min. As this elapsing is inside the range of natural feeding intervals, nosotros did non provide nutrient and water. We recorded pup separation calls (Fig. ​ 1) using a Sennheiser ME 66/K6 directional microphone and a Sony TCD-D100 DAT-recorder. The microphone was located thirty cm in a higher place of the box. To avoid that potential developmental changes in call structure with age could confound responses [21], we recorded calls from pups of the same age equally the pups of the experimental females at the time of the experiment (see beneath). Recordings were sampled at 44.1 kHz with a resolution of 16 fleck and were transferred to a PC. We used Cool Edit 2000 (Syntrillium Corporation, Phoenix, USA) to generate playback files, and to normalize the recorded call series to the same elevation amplitude to maintain natural variation in sound amplitude among calls. From the recordings nosotros generated files with a 30 s phone call sequence (113 ± 6 calls inside thirty s) that was repeated 15 times interspersed with 30 due south silence so that each playback file had a duration of 15 min. This pattern of calling was within the range of natural calling sequences. In order to avoid pseudoreplication, calls from 72 different pups were used to produce 72 playback files so that each female person received in each experimental part a file with separation calls from a dissimilar unfamiliar unrelated pup (experiment 1: n = 28; experiment 2: two-pup litter mothers: n = 11, iv-pup litter mothers: n = 11, females were tested on day 8 (part 1) and on day xx (office 2)). Unfamiliar pup separation calls were used because females with small-scale litters did non have three pups which would have been required to generate a unique playback file for each of the three playbacks a female received. Since non all mothers with their pups participated in the experiments due to asynchrony in nascency dates, we used preferentially these non-experimental pups for recordings. In a previous study we showed that females respond strongly to unfamiliar pup calls [19]. The employ of calls recorded from pups of unlike litter sizes were counterbalanced across experimental groups. Litter size of pups from which calls were recorded (small (one or two pups) versus larger (iv or five pups)) did non bear upon female responses on neither day 8 nor on 24-hour interval 20 (Isle of man-Whitney U-tests; number of calls; all U > 7, all p > 0.5; approach, all U > 3, all p > 0.06).

Sound spectrogram of a series of pup separation calls. Calls shown were recorded from an eight days erstwhile individual.

Experimental setup and playback experiments

All experiments were conducted indoors using a test-arena (1.48 × 0.98 × 0.47 grand) in an experimental room acoustically separated from the colony room. In club to familiarize subjects to treatment and the examination environment, each subject area was placed together with its pups in the test-arena for fifteen to 30 min two times on the days prior to the experiments.

Experiment 1

Here nosotros examined whether mothers of four-pup litters abandoned their suckling pups in response to playback more oftentimes than mothers of ii-pup litters. We tested lactating females (n = 28) together with two of their pups on day 7 of lactation. On both sides, the test-arena was equipped with huts for shelter and a loudspeaker (Creative Inspire 2.1 2400) placed on each hut (Fig. ​ ii). Since mother and pups could lie downward for suckling anywhere in the box, nosotros equipped both sides of the test-arena with a loudspeaker. Prior to the experiment all pups were separated from their mothers for 90 to 120 min to ensure that pups were hungry at the start of the experiment. Guinea pigs nurse every xx to 60 min [twenty]. Thus the separation time is within natural feeding sequences since oftentimes not all pups accept access to milk during i nursing bout. To maintain possibilities for some social interactions between the pups and their mother, all pups of the litter were jointly separated from their mother past a wire mesh in their belongings compartment permitting visual, olfactory and acoustic contact with the mother, but without the possibility to suckle.

Experimental setup for experiment 1: The exam-arena was equipped with huts for shelter on both sides of the exam-arena and a loudspeaker placed on each hut. The zone closest to the loudspeaker that was used in a given trial was labelled as zone one and the most distant zone as zone 4. Mother and pups could lie downwardly for suckling anywhere in the loonshit. Stimuli were broadcast from the loudspeaker contrary to the animals' position.

For the playback experiment, a mother was transferred together with two of its pups to the test-arena. In iv-pup litters, we randomly selected 2 pups while the other two pups remained in their holding compartment. When both pups were suckling (mother in nursing position and both pups under the female parent for at to the lowest degree 30 s) the playback session started. Playbacks were played direct from a PC and lasted for 15 min. The separation calls were broadcast from the loudspeaker reverse to the animals' position in the box.

Experiment 2

Here we tested whether mothers' responsiveness towards pup separation calls changes with offspring historic period in relation to experimental litter size of two or iv pups. Mothers (without their pups) received a playback of pup calls on twenty-four hour period eight and twenty-four hour period 20 of lactation; both parts followed the same full general experimental process. The exam-arena was equipped with one hut and 1 loudspeaker. Guinea pigs use huts for shelter, so we standardized the starting position of the female by providing a hut on the side of the exam-loonshit reverse to the loudspeaker. We exchanged the position of hut and loudspeaker alternatingly between females, in order to control for possible side preferences. For playback, females were taken from their property compartment and transferred direct to the exam-loonshit. They were accustomed to the environment for 15 min after which the pre-playback period started. Each playback session consisted of a fifteen min pre-playback menstruum, and a 15 min playback menses. Playbacks were played direct from a PC and females were under the hut at the onset of playback in all trials. In full, 22 females (two-pup litter mothers: Northward = eleven, 4-pup litter mothers: N = eleven) received playback on day 8 and solar day 20. Six females had to be excluded because the playback trial either on twenty-four hour period 8 or day 20 was disturbed, precluding a comparison betwixt responses on solar day 8 and twenty in these cases.

In all experiments, calls were broadcast with a peak sound pressure level (SPL) of 75 dB as measured at 1 thou with a audio level meter (Brüel & Kjær precision SPL meter 2233). This corresponds to the amplitude of natural calling as measured on 10 pups (unpublished data). Later on the experiments, subjects were returned immediately to their regular holding compartment.

Weaning

To determine weaning age, pups were placed together with their mother in an elevated observation box (0.72 × 0.54 × 0.25 m) with a plexiglass lesser. Through the bottom it was possible for the observer to distinguish whether pups were suckling or merely sitting under the female parent. The subjects were familiarized to the box repeatedly during lactation. The observations took place once a day for 30 min from lactation day 18 on until a litter was weaned. When no suckling behaviour was recorded on three subsequent days, the first of these three days was defined equally the solar day of weaning.

Response measures and statistical analyses

Responses were recorded by directly observations. The observer [M.K.] sabbatum silently in the same room sidewise to the centre of the test-loonshit and recorded the subject's behaviour (run into below). For experiment ane we counted how often mothers abandoned their two suckling pups. Since mothers and pups could reunite during the experiment, more than one abandoning of the pups per trial was possible. As responses in experiment ii nosotros recorded the subjects' song and spatial behaviour. In order to quantify the approach toward the loudspeaker, we divided the test-arena into four zones (Fig. ​ 2). The observer recorded the subject's vocalizations and position at ten-2d intervals over the 15 min playback menses. Thus, we obtained xc data points for vocalizations and for location within each playback session. For analyses we calculated (a) the number of intervals in which vocalizations occurred, (b) the latency to vocalize (in number of intervals), (c) the number of intervals females spent near the loudspeaker (in zone 4) and (d) the latency to approach zone 4 (in number of intervals). Responses were analyzed with Isle of mann-Whitney-U tests and Wilcoxon matched pairs signed-ranks using SPSS 12.5. Ii-tailed tests were used throughout. Weaning was analyzed using an analysis of variance, with original and experimental litter size every bit stock-still factors.

Results

Mothers of four-pup litters abandoned their pups significantly more often and significantly earlier than mothers of two-pup litters (Figs. 3a, b; Isle of man-Whitney U-tests; abandoned: U = 47; N₁ = 13, N₂ = 15; p = 0.014; latency to abandon: U = 45.5; N_i = 13, Northward_two = 15; p = 0.015). Except for one female, iv-pup-litter mothers abandoned their pups at least once per trial. Moreover, ii-pup-litter mothers decreased the fourth dimension spent about the loudspeaker significantly from day eight to 24-hour interval 20 of the lactation catamenia (Fig. ​ 4a; Wilcoxon exam; T = 3, N = eleven, p = 0.01) whereas mothers of four-pup litters did non (Fig. ​ 4a; Wilcoxon exam; T = 34.5, Due north = eleven, p = 0.91). Similarly, calling activity of ii-pup-litter mothers decreased significantly from twenty-four hour period viii to day 20 (Fig. ​ 4b; Wilcoxon examination; T = 0, N = 11, p = 0.001), whereas that of four-pup litter mothers in contrast remained high (Fig. ​ 4b; Wilcoxon test; T = 28.five, Northward = 11, p = 0.72).

Responses of ii-pup (N = 13) and four-pup (N = fifteen) mothers; (a) frequency to carelessness the suckling pups, and (b) latency to abandon the suckling pups (10 sec intervals) during playback of another pup's calls (experiment 1). Each boxplot depicts median with inter-quartile range; whiskers extend to max. ane.5 times the inter-quartile range, outliers are shown as circles.

Responses of ii-pup (N = eleven) and four-pup litter (N = 11) mothers; (a) intervals spent in zone 4 (closest to the loudspeaker) and (b) intervals with vocalizations during playback of unfamiliar pup calls on mean solar day 8 and mean solar day 20 of lactation (experiment 2). Each box plot depicts median with inter-quartile range; whiskers extend to max. 1.5 times the inter-quartile range, outliers are shown as circles.

In four-pup litters, neither mothers' latency to vocalize (Wilcoxon exam; T = x, Northward = 6, p = 0.13, five females had tied scores) nor latency to arroyo (Wilcoxon test; T = 17, Due north = xi, p = 0.95) differed significantly between mean solar day viii and day xx. Mothers of two-pup litters had a higher latency to vocalize on day 20 than on day 8 (Wilcoxon exam; T = 9, N = 11, p = 0.03) and tended to approach the speaker subsequently day 20 than on day viii (Wilcoxon test; T = 5, N = 11, p = 0.078).

Big experimental litters were weaned on day 30 ± 4.two (mean ± SD, N = fifteen), significantly afterward than small experimental litters, which were weaned on solar day 25 ± 3.i (hateful ± SD, North = xiii). Mothers' original litter size did non influence weaning historic period significantly (ANOVA: experimental litter size, F_1,27 = 10.26, p = 0.004; original litter size, F_1,27 = 2.09, p= 0.12). When cross fostering, we controlled for differences in pup birth weigh among litters, and then that pups of small and large experimental litters did not differ in mean birth weight (pocket-sized litters: 83 ± sixteen (hateful ± SD), Northward = xiii; large litters: 87 ± 20, N = 15; T-test: T = -0.503, p = 0.62). Consistent with before studies [fifteen,22] we plant lower growth rates in larger litters, which were likewise weaned afterward than smaller litters. Because of afterward weaning, pups of large litters did not differ from pups of small litters in trunk mass at time of weaning.

Discussion

Mothers of large experimental litters abased their suckling pups more often than mothers of minor experimental litters when separation calls of another pup were broadcast. Moreover, mothers of pocket-sized litters decreased their responsiveness to pup calls from day 8 to day 20, whereas those of big litters remained strongly responsive. Mothers of small experimental litters as well weaned the pups earlier than did mothers of big experimental litters. Thus, guinea sus scrofa mothers adjusted their level and time menstruum of responsiveness to experimental litter size.

Earlier experiments had shown that guinea sus scrofa females responded, apart from a general decrease of nursing action over time [23], little if at all, to changes in pup need by increasing milk yield [xiii] or by adjusting nursing functioning [14,16]. These experiments suggested that females pay surprisingly niggling attention to pup need or pup country. However, these studies described nursing behaviour and milk yield and did not observe maternal behavioural responsiveness depending on litter size as our playback experiments did. Thus the playback experiments complement previous studies by showing that females indeed adjust behavioural responsiveness to litter size, even if the litter size they are rearing is non the 1 they had produced. These results as well fit with before findings that larger litters are weaned subsequently [fifteen,16] and suggest that maternal motivation is increased through stimuli provided past larger litters. Previous studies on other rodents also had shown that maternal responsiveness depends on litter size. Maternal nest attendance decreased with increasing litter size in golden hamsters (Mesocricetus auratus) [24] and rats (Rattus norvegicus) [25] which may exist due to the increased temperature in the nest or disturbances caused by the activity of many pups. Mongolian gerbil mothers (Meriones unguiculatus) with larger litters spent less time in the nest, but licked and sniffed more than than mothers with small litters [26]. In contrast to these measures of maternal care, our playback experiments provide evidence for changes in maternal responsiveness to pup separation calls in relation to litter size.

The pup separation calls nosotros tested, differ functionally from begging calls tested in other species. They are emitted just when pups are out of contact with their female parent and are not given before and during suckling interactions. Playback experiments on pigs (Hog domestica) demonstrated a stronger response of mothers to needy piglets [27]. In these experiments, the smallest and slowest growing young in the litter which had just missed a nursing and were isolated in a relatively absurd enclosure, chosen nearly intensely. Similarly, in birds a positive relationship betwixt begging intensity and parental feeding rate could exist found [4,28-31]. Not bad tit (Parus major) nestlings showed an increase in hateful begging rates from experimentally reduced to enlarged broods. Their parents adjusted the feeding rates that were similar per nestling over three brood size [32].

Besides, it has been suggested that piglet calls role mainly as a signal to the sow past piglets that are excluded from the current nursing episode [27]. Even though our experiments could be interpreted similarly, this function does not seem to employ to the separation calls as used in guinea pigs. Fey and Trillmich [xv] never observed pups to utter separation calls when they were about their mother but had temporarily no access to the teats in litters of 4. These pups would rather dig in under the mother, presumably to wait for an opportunity to admission a teat. For female republic of guinea pigs, finding lost pups may play a major function in protection of those pups and may also be important in thermoregulation, specially for immature pups that have simply express energy reserves to maintain thermoregulation. Every bit energy input via milk plays but a pocket-size role belatedly in lactation [sixteen], the benefits of lengthening the lactation menses may rather be of social function or to support pups' thermoregulation.

Causally, differences in maternal responsiveness might have been linked to differences in hormonal land, as suggested by correlative studies in humans. In humans, maternal approach behaviour was straight associated with levels of cortisol and multiple regressions revealed that the infants' song behavior significantly predicted maternal level of cortisol [33]. Mothers showing the highest levels of maternal arroyo responses were those with a loftier cortisol concentration and either a positive maternal attitude, or a vocally more than active infant. Based on these data, they speculate that for the new mother to exhibit a high level of responsiveness to her infant, she must attain a sure level of arousal [34], which can be produced by elevated cortisol [35]. Moreover, Fey & Trillmich [15] showed that maternal cortisol levels in republic of guinea pigs decreased as pups grew older, and mothers rearing a litter of four pups maintained, although not significantly and so, college cortisol levels than those with litters of two pups. Thus, auditory stimuli may touch on maternal responsiveness via the general adaptive functions of arousal and evocation of maternal beliefs.

As predicted, guinea grunter mothers with big litters actively interrupted nursing and responded to pup separation calls past budgeted the loudspeaker whereas mothers of small litters most ofttimes did not. This indicates that mothers pay attention to litter size and practice not respond when calling pups cannot exist their own. We previously showed that females can recognize the calls of their own offspring [xix] just nevertheless are responsive to calls of unfamiliar pups. This suggests that the costs of such false alarms are lower than the costs of missed detections [36]. Such a pattern of response is non unusual as too in ungulate hider species a like unspecific response of mothers to separation calls has been reported [37]. In these species, females practice not know the exact hiding location of their offspring and utilise vocalizations to reunite with the fawns [38,39]. Mule deer (Odocoileus hemionus) and white-tailed deer (Odocoileus virginianus) mothers defend their immature vigorously against predators. The fawns' calls activated the mothers and in mule deer, females even responded to separation calls of white tailed deer calves [17,37]. These authors fence that information technology may pay more to mistakenly defend a foreign young than to lose the own fawn. Yet, as females also approached the loudspeaker in an aggressive manner when they were together with their own fawn, factors other than the separation from their fawn must also affect responsiveness to playback by female deer. In dissimilarity to larger mammals, in guinea pigs and their wild ancestors, females accept little possibility to actively defend their offspring, as mammalian and bird predators are able to kill the mother likewise as the offspring. Therefore, the response by guinea grunter mothers is likely to function to reunite with young gone off-target rather than in straight defending them. Mothers with larger offspring numbers then presumably answer stronger than those with fewer offspring as it is more likely to lose young in larger litters. Reuniting with these immature speedily and thereby preventing them from calling is probable to reduce the danger of attracting the attention of predators.

Conclusion

Our findings demonstrate that guinea pig mothers arrange maternal responsiveness to increased litter size through an increased response to pup calls and an increase in time to weaning. This contradicts earlier findings which seemed to indicate that maternal responsiveness was adamant largely during pregnancy and indicates a more complex female parent-pup relation than documented previously.

Authors' contributions

MK, FT and MN designed the experiments and wrote the manuscript. MK conducted the experiments and analyzed the data.

Acknowledgements

We thank the beast care takers and specifically Ursula Rennemann for taking care of the animals during the experimental periods. Nosotros thank Karen Fey for helpful suggestions on designing the experiment. We too thank Sandra Düpjan for helpful discussions and comments on before drafts of this manuscript. The inquiry was funded in part by a research grant provided by the German inquiry foundation to M.N. and F.T. (DFG grant NA 335/seven).

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Source: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2546386/

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