Behavioral Ecology Advance Access originally published online on October 26, 2005
Behavioral Ecology 2006 17(1):132-137; doi:10.1093/beheco/arj008
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Sex differences in provisioning rules: responses of Manx shearwaters to supplementary chick feeding
a Ecology and Evolution Group, School of Biology and Earth Biosphere Institute, University of Leeds, Leeds LS2 9JT, UK, b Institute of Biomedical and Life Sciences, University of Glasgow, Glasgow, UK, c Max Planck Institute for Ornithology, Vogelwarte Radolfzell, Germany, and d Game Conservancy Trust, Barnard Castle, County Durham, UK
Address correspondence to K.C. Hamer. E-mail: k.c.hamer{at}leeds.ac.uk.
Received 24 March 2005; revised 5 October 2005; accepted 5 October 2005.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Sex differences in food provisioning have been found in a number of socially monogamous birds with biparental care, but the reasons remain unclear. In Manx shearwaters, males provide 40–50% more food for chicks than do females, and previous empirical data have suggested that this difference could arise because females are able to regulate food delivery by reducing the provisioning of well-nourished chicks, whereas males are not (hypothesis 1). Alternatively, however, males may be as capable as females of assessing and responding to the variation in the nutritional requirements of their chick but have a higher threshold for reducing food delivery to well-nourished chicks (hypothesis 2). To test these two hypotheses, we used supplementary feeding to manipulate the nutritional status of chicks and then examined the responses of male and female parents and their offspring. Supplementary feeding significantly reduced both the begging behavior of chicks and the frequency and sizes of meals delivered by parents. Males and females reduced their overall provisioning rates to a similar extent (males by 38%, females by 42%), so maintaining the same difference in contributions to provisioning in the control group (males 58%, females 42%) and the experimental treatment (males 59%, females 41%). These data strongly support hypothesis 2. Supplementary feeding of chicks resulted in fewer visits by parents and a higher proportion of long trips in both sexes (4 days for males, 5–7 days for females). However, maximum trip durations were unchanged, suggesting that supplementary feeding of chicks had no effect on the foraging ranges or overall food-provisioning strategies of parents.
Key words: begging, mating systems, parental care, parent-parent conflict.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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About 90% of bird species have biparental care, with both sexes contributing to the provision of food for offspring (Bennett and Owens, 2002
; Lack, 1968). Male and female parents need not, however, contribute equally to food provisioning, and sexual conflict over how much each individual contributes is inescapable except under true monogamy (Parker, 1985). Sexual differences in foraging behavior and provisioning rates of offspring have been recorded in a number of socially monogamous but sexually size-dimorphic species, including passerines (Aho et al., 1997; Morse, 1968), raptors (Marquiss and Newton, 1982; Newton, 1979), and seabirds (Table 1 in Lewis et al., 2002), and these differences are usually ascribed to the influence of body size on foraging efficiency and competitive ability (Gonzáles-Solís et al., 2000; Weimerskirch and Lys, 2000). Recent evidence, however, has indicated that differences between males and females in foraging and food-provisioning behavior can occur in the absence of sexual size dimorphism (Bradley et al., 2002; Fraser et al., 2002; Wiggins and Morris, 1987). For instance, in Manx shearwaters, Puffinus puffinus, body measurements of males and females differ by <3% (Hamer, 2003), yet the mean trip duration was significantly longer in females (2.1 days) than in males (1.5 days). Males thus fed their chick on a greater proportion of nights and made a 40–50% greater contribution to overall food provisioning (28.9 g per night for males, 20.1 g per night for females on average; Gray and Hamer, 2001a). Sex-specific differences in food provisioning may therefore arise not through differences in body size but through other factors, such as differences in the responsiveness of males and females to the food requirements of chicks.
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Manx shearwaters are widely distributed in the North Atlantic Ocean and show the typical procellariiform pattern of a single-egg clutch and slow chick development, with an average fledging period of 72 days (breeding biology summarized by Brooke, 1990
, and Hamer, 2003). They have stable pair bonds with an annual divorce rate of about 10%, usually after breeding failure. They exhibit biparental care during incubation and chick feeding, with adults returning to feed their chicks only during hours of darkness. Chicks are fed exclusively in the nest burrows. They attain maximum body masses of 130–150% of adult mass at around 55–60 days posthatching and then lose the mass in response to a reduction in the size and frequency of parental feeds (Gray and Hamer, 2001b; Hamer and Hill, 1997).
Indirect evidence from chick weights (Hamer and Hill, 1997), supplementary feeding (Hamer et al., 1998), and chick switching (Hamer et al., 1999) all indicated that food provisioning in Manx shearwaters was influenced by characteristics of both chicks and parents. Moreover, chicks conveyed information about their body condition through begging, but male and female parents responded differently to that information (Quillfeldt et al., 2004): females varied meal sizes and subsequent trip durations according to the nutritional status of the chick, as indicated by begging behavior, whereas males did not alter meal size or trip duration. This raises the possibility that the greater contribution of males to food provisioning arises as a consequence of their inability to regulate food delivery by reducing the provisioning of well-nourished chicks. Alternatively, however, males may be as capable as females of assessing and responding to the variation in the nutritional requirements of a chick but have a higher threshold for reducing food delivery to well-nourished chicks. To test between these two hypotheses, we used supplementary feeding to manipulate the nutritional status of chicks. We then examined the responses of male and female parents and their offspring to test whether or not male parents regulated food delivery to the same extent as females under such conditions.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Fieldwork was carried out at Skomer Island, Southwest Wales, U.K. (51° 44' N, 5° 17' W) from 12 July to 10 August 2002. All work was approved by the Countryside Council for Wales, the Wildlife Trust West Wales, and the Skomer and Skokholm Islands Management Committee. Manx shearwaters are burrow nesters, and we reached chicks in their nest chambers via short access tunnels in the roof of each burrow, capped with removable earth lids. This system facilitated rapid access to chicks, reducing overall disturbance, and had no adverse effects on burrow occupancy, food-provisioning rates, or breeding success (Brooke, 1990
; Hamer and Hill, 1997).
We determined hatching dates of chicks (to the nearest day) at 60 nests by calibrating wing length (maximum flattened chord measured to the nearest 1 mm with a stopped wing rule) against wing growth in chicks of known age (Brooke, 1990). Chicks at 20 of these nests with hatching dates ±10 days of the sample mean were then weighed to the nearest 5 g using a Pesola spring balance, at 0430 and 2030 h each day from 19 July to 5 August (range of ages = 15–51 days; mean = 33.5 days, SD = ±8.2). Meal sizes and feeding frequencies were calculated from changes in chick body mass recorded overnight, using equations in Hamer and Hill (1997) to correct for the mass lost through digestion, respiration, and excretion between weighings. Both meal size and feeding frequency are independent of chick age over this age range (Hamer and Hill, 1997).
Supplementary feeding
Chicks were assigned at random to a treatment group shortly after hatching. Each chick in the experimental group (n = 10) received 20–30 g of fresh whitebait Sprattus sprattus (mean = 25.1 g, n = 120, SD = ±2.0, determined by weighing the chick immediately before and after feeding) daily from 21 July until 1 August (12 days, chick ages 18–45 days). This was equivalent to about half the normal daily food delivery for chicks in this age range (53 g per night; Hamer and Hill, 1997). Whitebait were stored frozen until required and warmed to about 25°C before delivery. Supplements were always given around 2100 h; this ensured that chicks in the supplemented group were relatively satiated when their parents returned overnight. However, chicks were still capable of accepting a normal-sized meal from their parents; the average quantity of food delivered overnight is about 50 g, but chicks of this age range can consume >120 g of food in a single night (Hamer and Hill, 1997). Chicks in the control group (n = 10) were subjected to the same degree of handling but received no supplementary food.
Vocal behavior of chicks
The vocal behavior of nestlings at each of the 20 study nests was recorded overnight on 15 consecutive nights (21 July–4 August, including 3 nights after the cessation of supplementary feeding), by placing a portable tape recorder outside the nest entrance and an external microphone with a 2-m connection in the nest entrance close to the nest chamber. Chicks beg only in the presence of a parent, and for all recorded begging sessions, the following parameters were measured by counting the calls for each minute of the session (starting with the first begging call): the duration of the session (in minutes), the total number of begging calls in the session, the call rate (begging calls per minute) over the complete session, the call rate (begging calls per minute) over the first 5 min, and the maximum call rate sustained for 1 min. The recorders were switched on at 2300 h each night (before the first adults returned) and recorded at low speed until the end of the tape (approximately 95 min). On those occasions, when no adult had returned to the nest prior to 0030 h (as determined by radio tracking, see below; 82 occasions in total), the tape was turned on at 0040 h to start a second recording period. Up to five begging sessions were registered in a chick-night (n = 55, 22, 8, 3, and 1 chick-nights with one, two, three, four, and five recorded sessions, respectively). Because our recordings terminated before the adults left the burrows at the end of the night, we may have missed some late feedings. In order to compare all chick-nights, we therefore included only first begging sessions in the analyses of begging behavior, following Quillfeldt et al. (2004). This way, daily variation in begging behavior reflected the chick's need at the time of the arrival of the adult.
Food delivery by males and females
We caught both adults at each of the 20 study nests (40 adults in total) by hand, over a period of 7 nights from 13 July. We weighed each adult to the nearest 5 g with a Salter spring balance and fitted it with a VHF radio transmitter (Biotrack, Dorset, U.K.). The transmitters weighed 2 g (<1% of body mass) and measured 19 x 10 x 8 mm, with an external aerial measuring 135 x 0.6 mm. They were attached to two central tail feathers with a self-amalgamating tape (RS Components, Newcastle, U.K.), which formed a seal over the feathers and transmitter, and were covered by the surrounding feathers. The aerial was thin and flexible and extended approximately 60 mm beyond the tail. The process from capture to returning a bird to its burrow took no longer than 10 min.
We monitored visits of tagged birds to the colony for 16 consecutive nights (21 July–5 August), using a scanning receiver (MVT-7100, Yupiteru Industries, Tokyo, Japan) with a three-element Yagi antenna located on a hillside at a distance of 100 m and elevation of 20 m from the study nests. Trials at the colony indicated that the range of this system was <1 km, so we were confident that signals received were from birds in the colony and not at sea. Signals were detected for 2–3 min before birds entered their nest. We monitored attendance overnight from 2230 h (before the first adults returned) to 0430 h (after the last adults had left the colony). Adults were sexed from cloacal inspection shortly after egg laying in May (Gray and Hamer, 2001a), and sexes were confirmed from vocalizations recorded at the nest (Quillfeldt et al., 2004). We recaptured tagged birds over 6 nights after the tracking period to remove tags. Two radio tags lost their aerial after attachment, and a further three emitted weak or intermittent signals toward the end of the tracking period. These birds were excluded from further analysis after the tags were known to be unreliable, giving attendance and feeding data for 615 parent-nights at 20 nests (298 nest-nights for female parents and 317 nest-nights for males). Chicks were caught by hand, weighed, and given supplementary food when nests were not attended by an adult. No chicks regurgitated stomach oil or food during handling, no adults deserted, and all study chicks fledged normally.
Statistical analysis
Data obtained during the study were used to examine nest attendance and sizes of meals delivered by males and females up to and including the first occasion that a bird returned after 1 August (the last day of supplementary feeding). Data were collected repeatedly at each nest, and so to avoid pseudoreplication, the vocal behavior of chicks and the sizes of meals delivered by parents were analyzed using a single mean value for each individual, while feeding frequency was analyzed in terms of the proportion of nights (arcsine transformed) that each parent returned to feed its chick. Parental response data were nonetheless not fully independent because males and females were paired at each nest, and so these data were analyzed using general linear models, including nest identity as a random factor and sex and treatment as fixed factors. Data on vocal behavior were nonnormal and so were analyzed using nonparametric tests.
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RESULTS |
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Vocal behavior of chicks
During the period of supplementary feeding, supplemented chicks begged significantly less than unsupplemented controls (Figure 1; Mann-Whitney U tests using mean values for each chick; total number of calls, U18 = 2.84, p = .003; duration of begging, U18 = 2.40, p = .016; maximum begging rate, U18 = 2.93, p = .002; overall begging rate, U18 = 3.29, p < .001). For chicks in the experimental treatment, three of these four parameters of begging intensity increased significantly after the cessation of supplementary feeding (Figure 2; Wilcoxon signed-ranks tests comparing last night with adult present during supplementary feeding and first night with adult present after the end of supplementary feeding; total number of calls, Z6 = 2.37, p = .018; maximum begging rate, Z6 = 2.21, p = .027; overall begging rate, Z6 = 2.37, p = .018; there were 6 df for these tests because we did not obtain good recordings of vocal behavior from three chicks in this treatment after the end of supplementary feeding). Only the duration of begging did not increase after the end of supplementary feeding (Z6 = 1.58, p = .115). Chicks responded very rapidly, with begging call rate and total number of calls increasing to a similar level to controls within a day of the end of supplementary feeding (Figure 3).
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Food delivery by parents
Food provisioning can be viewed from the chick's or the parents' perspectives. From the chick's perspective, supplemented chicks were fed on significantly fewer nights than unsupplemented controls (Table 1; t test using combined variance estimate for arcsine-transformed data; t18 = 2,3, p = .03). When they were fed, supplemented chicks also received smaller meals (Table 1; t test using mean meal size at each nest; t18 = 3.4, p < .01), and so the overall provisioning rate of supplemented chicks (40 g per night) was much smaller than that of control chicks (64 g per night; Table 1; t18 = 6.6, p < .001). This reduction in parental food delivery (24 g per night) closely matched the rate at which chicks in the experimental group were supplemented (25 g per day; see Methods).
From the parents' perspective, males in both treatments returned to their chick significantly more often than did females (Table 2; general linear model using arcsine-transformed data; F1,36 = 30.7, p < .001; there was no significant variation among nests in either treatment). Supplementary feeding resulted in reduced attendance by both sexes (Table 2; F1,36 = 4.5, p < .05), and males and females reduced their attendance to the same extent (interaction F1,36 = 0.02, p = .9). Despite these significant differences in nest attendance and corresponding differences in the mean trip duration (males: control nests = 1.47 nights, n = 79, SD = ±0.75; supplemented nests = 1.65 nights, n = 71, SD = ±0.91; females: control nests = 2.04 nights, n = 57, SD = ±1.36; supplemented nests = 2.40 nights, n = 48, SD = ±1.71), there was no difference between treatments in the maximum trip duration of either males or females (4 nights and 7 nights, respectively, in both treatments; Figure 4).
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Males and females delivered meals of similar sizes (Table 2; general linear model using a single mean value for each bird, aggregated over each of the nights when it was the only parent to return to the nest; F1,32 = 0.1, p = .8), and both sexes delivered smaller meals to supplemented chicks (Table 2; F1,32 = 7.0, p = .01) with no interaction between the effects of treatment and sex (F1,32 = 0.01, p = .9).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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For nests in the control group, foraging trip durations, proportions of chicks fed overnight, and sizes of meals delivered to chicks were all similar to those recorded in previous years (Gray and Hamer, 2001a
; Hamer and Hill, 1997), indicating that collection of data had no adverse effects on food-provisioning rates. The present study demonstrated that Manx shearwater chicks conveyed information about their nutritional status through begging and that parents were responsive to the level of solicitation, as was also found in a study of natural variation in the begging behavior of unmanipulated chicks (Quillfeldt et al., 2004) and in other species with single-chick broods and hence no within-brood competition (Quillfeldt, 2002; Quillfeldt and Masello, 2004).
Previous empirical evidence indicated that female Manx shearwaters adjusted meal size and feeding frequency in response to the variation in the nutritional status of their chick, whereas males did not (Quillfeldt et al., 2004). In contrast, the two sexes responded similarly to supplementary feeding of chicks, in terms of reducing both meal sizes and feeding frequency. Smaller meals could have been due to supplemented chicks not accepting some of the food delivered by their parents, although any such effect should have been small because the supplements given to chicks (25 g on average) were much smaller than the maximum quantity of food that chicks can consume overnight (>120 g; Hamer and Hill, 1997). Moreover, male and female parents also responded similarly to each other in terms of adjusting their rate of return to the nest.
These data indicate that the greater contribution of males to food provisioning in Manx shearwaters does not arise from an inability of males to adjust their level of provisioning in response to information obtained from the chick. Rather, males appear to have a higher threshold for reducing their level of provisioning and so do so only when the chick is consistently well nourished. Ottosson et al. (1997) suggested that parents may independently adjust their effort to the begging level of nestlings and may have different optima of expenditure of effort on the current brood. In Manx shearwaters, if the costs of care are greater for females than for males, for instance, as a result of sex-specific differences in feeding locations or foraging behavior (Lewis et al., 2002), then females may be selected to allocate care more precisely than males. It is also possible that males respond to different cues than the measures we took, such as elements of call structure or tactile cues such as bill touching, that may be reduced only when the chick is consistently well nourished. In support of this notion, sex differences in responses to different elements of the begging display have been found in several species of passeriform birds (reviewed by Kilner, 2002) and in budgerigars Melopsittacus undulatus (Stamps et al., 1985, 1987).
Males and females reduced their provisioning rates to a similar extent (males by 38%, from 41.1 to 25.7 g per night; females by 42%, from 30.3 to 17.6 g per night; calculated from data in Table 2), so maintaining their relative contributions to food delivery (males provided 58% and 59% of food delivered to chicks in control and supplemented treatments, respectively; Table 2). As a result, the reduction in food delivery to supplemented chicks (24 g per night; see Results) almost exactly matched the supplementation rate (25 g per day), which suggests that parents compensated completely for the effects of experimental manipulation. However, this does not mean that parents necessarily compensate completely for changes in the provisioning effort by their partners. For instance, the pattern of response by males (complete compensation when the chick is consistently well nourished [this study] but no response to short-term variation in the nutritional status of the chick [Quillfeldt et al., 2004]) may be a mechanism allowing males to compensate only partially for changes in provisioning by females, as predicted in some circumstances by mathematical models of negotiations between parents over parental effort (McNamara et al., 1999, 2003; Royle et al., 2004; Schwagmeyer et al., 2002).
Adults responded to supplementary feeding of chicks by reducing both feeding frequency and meal size. A more efficient response in terms of central place foraging may have been to reduce feeding frequency further without reducing the meal size (Ydenberg et al., 1994). However, there were probably other benefits to nest attendance, such as territorial defense and accurate monitoring of chick condition, that outweighed any costs in terms of reduced efficiency of prey delivery to the nest.
Like other procellariiforms (Chaurand and Weimerskirch, 1994; Weimerskirch et al., 1997), adult Manx shearwaters may use a dual foraging strategy in which individual parents intersperse short foraging trips to obtain food for the chick with long trips to feed themselves, although in Manx shearwaters, long trips (5–7 days) are used only by females (Gray and Hamer, 2001a). In this study, supplementary feeding of chicks resulted in fewer visits by parents and a higher proportion of trips of 4 days by males and 5–7 days by females (Figure 4). However, the maximum trip durations of males and females were unchanged, suggesting that supplementary feeding of chicks had no effect on the foraging ranges or overall food-provisioning strategies of parents.
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ACKNOWLEDGEMENTS |
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We thank the Countryside Council for Wales, the Wildlife Trust West Wales, and the Skomer and Skokholm Islands Management Committee for permission to work on Skomer and Juan Brown and Chris Perrins for logistical support and advice. This study was part funded by a grant provided to P.Q. by the German Academic Exchange Service (DAAD).
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