Behavioral Ecology Vol. 14 No. 6: 793-801
© 2003 International Society for Behavioral Ecology
Food limitation in asynchronous bluethroat broods: effects on food distribution, nestling begging, and parental provisioning rules
Department of Zoology, Norwegian University of Science and Technology, N-7491 Trondheim, Norway
Address correspondence to P.T. Smiseth who is now at the School of Biological Sciences, 3.614 Stopford Building, University of Manchester, Oxford Road, Manchester M13 9PT, UK. E-mail: per.t.smiseth{at}man.ac.uk.
Received 18 April 2002; revised 18 November 2002; accepted 13 December 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Scramble competition models of begging predict that junior nestlings will be more affected by food limitation than seniors. These models assume that food allocation is under offspring control and, hence, predict that this change in food distribution is caused by a differential behavioral response by seniors and juniors. By using the bluethroat (Luscinia svecica svecica) as our model species, we induced food limitation by removing the male parent temporarily. We found that, as predicted, food distribution became more biased in disfavor of juniors when food was limited. However, there was no significant difference in the behavioral responses of seniors and juniors (i.e., positioning in the nest or begging postures) to food limitation that could explain the change in food distribution. Hence, there was no evidence that seniors controlled food distribution. As predicted if parents preferentially fed seniors, nestling rank affected food distribution when controlling for variation in nestling behaviors. Furthermore, as expected if the increased skew in food distribution under food limitation was caused by active food allocation by parents, nestling rank had a greater effect on food distribution under food limitation than under normal conditions. The present study suggests that food distribution in passerine birds is determined not only by nestling behaviors (begging posture and positioning) alone but also by parental preferences for seniors based on nonsignaling cues, such as body size.
Key words: hatching asynchrony, Luscinia s. svecica, mate removal, sibling competition, signaling of need, size asymmetry.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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For birds that provision their offspring repeatedly with food obtained from the surrounding environment, food abundance is likely to be unpredictable at fertilization. Lack (1947
, 1954) suggested that parents maximize reproductive output by producing an optimistic clutch size that can be adjusted downward through selective brood reduction if conditions later turn out to be unfavorable. Lack argued that hatching asynchrony provides parents with a low-cost means of adjusting brood size by establishing within-brood competitive asymmetries. Hence, senior nestlings exert behavioral control over food allocation and brood reduction through their competitive superiority, but the ultimate control lies with the parents, which establish competitive asymmetries through asynchronous hatching (Mock and Parker, 1997). This scenario fits well for some nonpasserine birds, such as ardeids, in which aggressive sibling interactions establish a competitive hierarchy and a nestling's dominance rank is determined by hatching order (Mock, 1987; Mock and Parker, 1997). However, for passerine birds, in which interactions are nonaggressive, it is unclear whether behavioral control over food allocation is exerted by senior nestlings or by parents (Mock and Parker, 1997; Royle et al., 2002).
In passerine birds, nestlings display conspicuous begging signals to which the parents respond by adjusting feeding rates and patterns of food distribution (Budden and Wright, 2001; Kilner and Johnstone, 1997; Wright and Leonard, 2002). Nestlings increase their begging intensity as they get hungrier, suggesting that begging acts as a signal of need to the parents (for review, see Budden and Wright, 2001; Kilner and Johnstone, 1997). The finding that begging reflects need has been interpreted as support for honest-signaling models, which assume that food allocation is under parental control (Godfray, 1991, 1995). However, scramble competition models, assuming that food allocation is under offspring control, make the same prediction (Parker et al., 2002; Rodríguez-Gironés et al., 2001). Thus, although the two types of models differ fundamentally in the assumptions they make about who controls food allocation, they are indistinguishable in light of current evidence (Parker et al., 2002; Royle et al., 2002).
Although Lack's (1947, 1954) brood reduction hypothesis has been contested (Amundsen and Slagsvold, 1991; Magrath, 1990; Stoleson and Beissinger, 1995), it is well established that size asymmetries resulting from hatching asynchrony bias food distribution and mortality in disfavor of juniors (see Magrath, 1990; Stoleson and Beissinger, 1995; Amundsen and Slagsvold, 1998). Empirical evidence suggests that size asymmetries also affect nestling begging, as juniors often receive less food than do seniors, even though the former beg more intensively (see Cotton et al., 1999; Kilner, 1995; Lotem, 1998; Price and Ydenberg, 1995). Theoretical considerations suggest that only scramble competition models can be extended to situations in which food is limited and nestlings differ in competitive ability (Parker et al., 2002; Royle et al., 2002). Honest-signaling models assume that food is not limited, and may be evolutionarily unstable under food limitation because parents are predicted to feed the neediest nestling, resulting in undernourishment of the whole brood (Royle et al., 2002). In contrast, scramble competition models predict that when nestlings differ in competitive ability, senior nestlings would receive more food and be more likely to survive under food limitation than would juniors (Parker et al., 2002).
The aim of the present study was to test for short-term effects of food limitation on food distribution and begging behavior in asynchronous broods as predicted by scramble competition models. Small insectivorous passerines, which typically feed the nestlings with small food items at a very high rate, are ideal as model species because limitations in food supply are likely to have an immediate effect on nestling hunger. We used the bluethroat (Luscinia svecica svecica) as our model species. The bluethroat is a small passerine with moderate asynchronous hatching (mean hatching span = 1.1 days, range = 0.5–2 days; Hansen, 1997), typical of many passerine birds. Experimentally induced size asymmetries affect food distribution, with seniors being fed more often than juniors, but not prefeeding begging behavior, suggesting that seniors are more effective at begging (i.e., have higher returns for a given level of begging; Smiseth and Amundsen, 2002). In the present study, we removed one parent (the male) temporarily to induce food limitation. We used a paired experimental design in which the same brood was studied under normal (both parents) and limited (female alone) food conditions. From the nestlings' point of view, this treatment mimics deterioration of environmental conditions. In many passerine species, including bluethroats, male removal results in an overall reduction in food supply (see Bart and Tornes, 1989; Smiseth and Amundsen, 2000). Male and female bluethroats do not differ in how they distribute food among different-sized nestlings (Smiseth et al., 1998). Thus, male removal by itself should not affect food distribution except through the effect of food limitation.
The present study is the first to test for short-term effects of food limitation on food distribution and begging in passerine birds. If the treatment (male removal) had the intended effect (food limitation), we expected a reduction in per capita feeding rates and an increase in begging levels, reflecting higher hunger levels. If size asymmetries affected competitive ability, we expected seniors to receive more food than did juniors under both normal and food-limited conditions because of the seniors' competitive superiority. Scramble competition models predict that food limitation will affect juniors more than seniors; that is, skew the distribution of food in disfavor of juniors (Parker et al., 1989, 2002). Scramble competition models assume that food allocation is under offspring control and, hence, predict that changes in food distribution result from a differential behavioral response by seniors and juniors. Seniors could control food allocation through physical competition by excluding juniors from favorable positions near the parent, as reported for some passerine species (Cotton et al., 1999; Kilner, 1995). If so, we predicted seniors to respond to food limitation by moving closer to the parent than do juniors. An alternative mechanism is that seniors control food allocation through begging. This could be because seniors have lower costs of begging than do juniors (Parker et al., 2002; Rodríguez-Gironés et al., 2001), which could enable seniors to escalate their begging levels further than do juniors. If so, we predicted seniors to increase their begging levels more strongly in response to food limitation than did juniors. We focused on the largest (senior) and smallest (junior) nestlings in each brood because effects of food limitation are predicted to be most profound for the smallest nestling in the brood (Parker et al., 1989).
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Fieldwork was performed during the nestling period in June–July 1997 in Øvre Heimdalen (61°25' N, 8°52' E; 1100 m above sea level), southern Norway. Bluethroats nest on the ground, typically under cover of small bushes, with the entrance facing an opening in the vegetation (Arheimer, 1982
). Males and females feed the nestlings at similar rates (Smiseth and Amundsen, 2000; Smiseth et al., 1998). One or two nestlings are normally fed during each feeding visit. When two nestlings are fed, the second feeding tends to be very small compared with the first one (Smiseth et al., 1998).
Experimental procedure
Nests found before hatching (n = 21) were visited daily to record the exact hatching date. Broods found shortly after hatching (n = 5) were aged on the basis of nestling body mass assuming normal growth (Rangbru, 1994). Parent birds may adjust their provisioning to brood size (see Wright and Cuthill, 1990). Therefore, we standardized brood size to six nestlings, identical to the mean clutch size (mean ± SE, 6.0 ± 0.1 eggs, range = 5–7, n = 23) but slightly above the mean brood size (mean ± SE, 5.3 ± 0.2 nestlings, range = 3–7, n = 23), in the year of study. We adjusted brood size on days 4–6 after hatching by removing or adding intermediate-sized nestlings as far as this was possible. We added one nestling to eight broods, two nestlings to three broods, and three nestlings to two broods, and we removed one nestling in two broods. In four broods, an added nestling assumed the senior rank on the day of recording, whereas in one brood an added nestling assumed the junior rank. The range for the difference in mass between seniors and juniors within these broods (1.9–5.6 g) was well within the range for the broods in which both seniors and juniors were native to their brood (1.0–6.4 g). The broods in which the added nestling assumed the junior rank, and one of the broods in which an added nestling assumed senior rank, were not included in the analyses of nestling behavior owing to technical problems (see below).
We video-recorded parental and nestling behavior on day 7 (n = 22) or 8 (n = 4) after hatching. Although sound was recorded, we did not analyze for effects on vocal begging because it was impossible to distinguish each nestling's vocalizations. On the previous day, we placed a tripod about 1 m from the nest to habituate the parents to the equipment. We painted each nestling with a dot of nontoxic acrylic paint on the top of its head to allow individual recognition during video analyses. Each nestling was assigned a unique color chosen randomly in relation to size rank. We removed minor twigs and grass obstructing the view into the nest from the camera position. Under natural conditions, parents enter nests almost solely from one direction, typically from where the nest faces an opening in the vegetation (Smiseth PT and Amundsen T, unpublished data). Clearance of vegetation might have enabled the parents to access the nest from more variable directions than under natural conditions. To avoid such effects, we placed minor juniper branches in a semicircle around the nest, away from the camera and the natural opening.
On the experimental day (7 or 8 days after hatching), we obtained two 3-h video recordings of each brood: one with both parents present (i.e., normal conditions), and one in which the male had been removed (i.e., food limitation). Nestling rank was determined by weighing the nestlings immediately before recording. Thus, the senior was defined as the heaviest nestling in the brood on the day of recording, and the junior was defined as the lightest one. The first recording (both parents present) was started as early in the day (mean ± SE removal time = 0800 ± 0019 h, range = 0647–1318 h) as permitted by the weather conditions (no nests were recorded during rain). Shortly after this recording, males were caught by mist netting. They were brought to the field station, placed in individual and visually isolated cages, and fed ad libitum with mealworms. We allowed ample time (median = 5 h 6 min, range = 1 h 55 min–8 h 18 min) after male removal before starting the second recording of the unassisted female (median starting time = 1740 h, range =1544–1908 h) to ensure that females were aware of the males' absence. After completion of this recording, males were released near the nest site (median removal time = 10 h 4 min, range = 5 h 56 min–11 h 20 min). All males resumed feeding after being released.
We chose the design described above because this was best suited for the conditions under which our study population breeds. In Scandinavia, bluethroats breed at high altitudes in the subalpine vegetation zone where severe weather conditions, such as low temperatures, strong winds, and precipitation, occur at irregular intervals and impose limitation in food supply. To minimize noise owing to day-to-day variation in weather conditions, we sampled information for both treatments on the same day. We did not randomize treatment order, because this procedure would generate heterogeneity in the normal conditions treatment caused by potential long-term effects of food limitation if male removal had been the first treatment of the day. Because nests are hard to find and broods often are lost to predators, we could not expect to get a large enough sample size to deal with such heterogeneity. Although our design by definition cannot test for possible order effects, it should be noted that for the purpose of this study, it is irrelevant whether food limitation is also influenced by order (i.e., time-of-day) effects, as long as male removal limits the food supply. To date, no study has found any evidence of systematic time-of-day effects on feeding rates in bluethroats at our (Hansen, 1997; Reinsborg, 1995; Smiseth and Amundsen, 2000) or other study sites (Arheimer, 1982).
Data analyses
We obtained video recordings from 26 nests. Because of technical problems, seven nests could not be analyzed with respect to begging activity. For the remaining nests (n = 19), we analyzed nestling behavior during the last 40 visits of each recording. The last 40 visits were chosen to produce data for a representative sample of visits and to allow as much time as possible since male removal. For each visit, we noted parental sex (both-parents recordings only), the time of parental arrival, the time the first nestling in the brood started to beg, the time of feeding, the identity of nestlings being fed, and the time of parental departure. For each nestling (the two focal nestlings, plus the second largest and second smallest), we noted whether they begged during the parent's presence, the time they started and stopped begging, and the duration of all interruptions in begging during the parent's presence. Data on the two additional nestlings were included to produce mean values for each brood (see below). From these data, we produced five begging parameters for each nestling: (1) begging frequency, the proportion of feeding visits during which a nestling begged; (2) begging intensity, the maximum degree of body stretching from parental arrival until feeding (1 = no stretching, 2 = stretching neck, 3 = stretching body, 4 = stretching body and tarsi); (3) begging start, the time a nestling started to beg in relation to the time of parental arrival; (4) begging latency, the time a nestling started to beg in relation to when the first nestling out of the six in the brood started; and (5) begging duration, the summed duration of time spent begging during parental attendance. For begging duration, we excluded all visits in which the actual nestling was fed. All time measures were to the accuracy of 1/25 s (identical to one video frame). At the time of parental arrival, we also noted nestling position: the position of a nestling's beak in relation to three sections of the nest cup. The sections were of equal width and perpendicular to the parental feeding position (1 = frontal, 2 = middle, 3 = distal). For all parameters, we used average values for each nestling over the 40 visits in statistical analyses.
We tested for effects of male removal on food distribution and the behavior of seniors and juniors using a repeated-measure ANOVA with food limitation (two versus one parent feeding) as within-subject (repeated) factor and nestling rank (senior versus junior) as between-subjects factor. To remove any variance associated with an individual brood, thereby increasing the statistical power, we calculated the absolute difference for seniors and juniors from the mean value for each brood. Such mean values were calculated for each parameter on the basis of 80 visits (40 from each recording) for each of four nestlings (the two largest and two smallest) in a brood. Variables that were not normally distributed were subject to either arcsine or square-root transformations to achieve normal distribution. All analyses were performed by using SPSS 10, except for the posthoc univariate general linear models presented under the final subheading of the Results section, which were performed by using Systat 10. Descriptive data are given as mean ± SE. All tests are two-tailed.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Within-brood size asymmetries
On day 7 or 8 after hatching, the average difference in body mass between the senior and junior nestling within broods was 3.1 ± 0.3 g (range = 1.0–6.4 g) (Figure 1). The body mass of juniors averaged 78.4 ± 1.9% of that of seniors (range = 52.9–93.1%). The difference in body mass was significantly larger between the two lowest-ranking nestlings of the brood (body mass of the junior relative to the nearest ranking nestling = 91.0 ± 1.6%) than between the two highest-ranking ones (body mass of the second largest relative to the senior = 95.6 ± 0.8%; Wilcoxon signed-rank test: Z = -2.69, n = 26, p =.007). Thus, the size hierarchy was more pronounced between the two lowest-ranking nestlings (Figure 1). We had information on nestling body mass both at hatching and on day 7 after hatching for 12 broods. Nestlings ranked as senior on day 7 ranked as senior at hatching in five broods (i.e., 42% of the broods) and as intermediate in the remaining seven broods. In contrast, nestlings ranked as junior on day 7 also ranked as junior at hatching in 10 broods (i.e., 83% of the broods) and as intermediate in the remaining two broods. Nestlings ranked as senior on day 7 never ranked as junior at hatching, and nestlings ranked as junior on day 7 never ranked as senior at hatching. Thus, although seniors often changed rank, juniors tended to retain their rank throughout the nestling period.
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Feeding rate and distribution of food
With both parents feeding, there was no significant difference between the sexes in the proportion of food delivered to seniors or juniors (paired t test; senior nestlings: t25 = 0.12, p =.91, junior nestlings: t25 = -0.86, p =.40). Thus, there was no evidence that males and females differed in how they distributed food among different-sized nestlings, supporting our initial assumption that male removal by itself would not affect food distribution except through the effect of food limitation.
When both parents were present, the combined feeding rate to the brood was 25.7 ± 1.0 visits/h. With the male removed, the feeding rate was reduced to 19.8 ± 1.0 visits/h, which comprises 77.9 ± 0.4% of the combined feeding rate with both parents present. As intended, the removal of the male led to a significant reduction in per capita feeding visits (Figure 2a and Table 1). When both parents were present, the female feeding rate was 13.4 ± 0.8 visits/h, and that for the male was 12.3 ± 0.8 visits/h. Females contributed 51.0 ± 2.5% of the total number of visits. There was no significant difference in the feeding rate of males and females (paired t test: t25 = 0.91, p =.37).
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Nestling rank significantly affected both number of feeds and proportion of feeds measured over all six nestlings in the brood, with seniors being fed more often than juniors (Figure 2 and Table 1). As predicted, there was a significant interaction between food limitation and nestling rank on the proportion of feeds received, reflecting an increased skew in the distribution of food in disfavor of juniors when food was short (Figure 2b and Table 1). For the number of feeds received by nestlings, there was a close-to-significant effect of the interaction between food limitation and nestling rank (Figure 2a and Table 1). Although not statistically significant, the direction of this trend was in the predicted direction, with food limitation seemingly having a greater impact on juniors than on seniors.
Behavior of senior and junior nestlings
There was a strong and significant effect of food limitation on nestling position and on all measures of begging behavior except begging latency: nestlings begged more often, more intensively, sooner in relation to the time of parental arrival, and longer, and they moved to more frontal positions when food was short (Table 2 and Figure 3). Thus, nestling hunger levels increased in response to the removal of the male. Nestling rank had a significant overall effect on nestling position, but contrary to what would be expected if seniors controlled food allocation through physical competition, juniors were positioned closer to the site of parental arrival than were seniors (Table 2 and Figure 3a). Nestling rank had significant effects on begging start and begging latency, with seniors starting to beg earlier than juniors (Table 2 and Figure 3d,e). Thus, seniors may have exerted behavioral control over food allocation through begging start and latency. However, there was no evidence for an interaction between food limitation and nestling rank on nestling position or begging behavior (Table 2 and Figure 3). Thus, there was no support for the prediction that the changes in food allocation were associated with a differential behavioral response by seniors and juniors. Instead, seniors and juniors seemed to respond similarly to food limitation.
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Parental provisioning rules
To test whether food limitation affected parental food allocation rules, we generated posthoc statistical models by using the proportion of feedings as dependent variable. Nestling behaviors were entered as covariates to control for variation in nestling behavior. For those behaviors in which there was a difference between seniors and juniors (i.e., nestling position, begging start and begging latency) (Table 2), we also included the interaction term between nestling rank and behavior. If parents had a feeding preference for seniors, nestling rank would be a significant predictor of food distribution.
We first tested for a sex difference in the provisioning rules of males and females under normal food conditions (Table 3). Parent sex was not a significant predictor of food distribution (Table 3), confirming that males and females used similar provisioning rules. Consistent with the idea that parents play an active role in controlling food allocation, nestling rank was a significant predictor of food distribution. The only nestling behavior that came out as a significant predictor in this model was nestling position. Nestlings positioned closed to the parents were more likely to be fed than those positioned further away (Figure 4a).
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The repeated-measures design of our experiment is not suited for a direct test of the effects of food limitation on the parents' provisioning rules, because nestling behaviors are not constant in the two treatments. Therefore, we generated separate statistical models for normal and food-limited conditions. In both models, nestling rank was a significant predictor of food distribution, which is consistent with parents playing an active role in allocating food (Table 4). If food allocation was under parental control, parents would be expected to show a stronger preference for seniors under food limitation than under normal conditions. Consistent with this suggestion, nestling rank appeared to be better predictor of food distribution under food limitation than under normal conditions (Table 4). Under normal conditions, the only nestling behavior that came out as a significant predictor was nestling position. Under food-limited conditions, only the interaction term between nestling rank and begging latency was a significant predictor (Table 4). The feeding success of seniors improved with a decrease in begging latency (i.e., as they started to beg earlier relative to the first nestling), whereas that of juniors was unrelated to begging latency (Figure 4b).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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We found that, as predicted from scramble competition models of begging (see Parker et al., 2002
), food limitation led to an increased skew in food distribution in disfavor of juniors. However, in contrast to what we predicted, there was no evidence that this change was associated with a differential behavioral response by seniors and juniors. Instead, seniors and juniors responded similarly to food limitation. As predicted if parents preferentially fed seniors, nestling rank had a significant effect on food distribution when we controlled for variation in nestling behavior. Furthermore, as expected if the increased skew in food distribution under food limitation resulted from active parental food allocation, nestling rank had a greater effect on food distribution under food limitation than under normal conditions. Below we provide a more detailed discussion of the implications of our findings for the understanding of food allocation and nestling begging in asynchronous broods.
Male removal and food limitation
We induced food limitation experimentally by removing the male parent temporarily. As predicted if our treatment had the intended effect, male removal led to a reduction in per capita feeding rates and an increase in begging levels, reflecting higher hunger levels. Females increased their care in response to male removal, but not enough to compensate completely for the loss of male care (Smiseth and Amundsen, 2000). Thus, females behaved in accordance with previous theoretical (see Houston and Davies, 1985) and empirical (see Bart and Tornes, 1989) studies of biparental care in passerine birds. This suggests that food limitation was caused by male removal and not by disturbances from the experimental procedure or other aspects of our design (see also Methods). Nestlings responded to food limitation by moving closer to the parents' feeding position (i.e., nestling position) and by begging more frequently, more intensively, sooner in relation to the parents' arrival (i.e., begging start) and by begging longer. These findings are consistent with the prediction that begging reflects need common to honest-signaling (see Godfray, 1995) and scramble competition models (see Parker et al., 2002), and are in agreement with previous experimental studies showing that food deprivation increases nestling begging activity (Budden and Wright, 2001; Kilner and Johnstone, 1997). There was no effect of food limitation for one begging parameter, begging latency. Begging latency is a measure of when each nestling started to beg relative to the first nestling. Thus, food limitation would only affect begging latency by increasing the variation within the broods in when nestlings start to beg. There was no evidence that food limitation had such an effect in our study.
Size asymmetries and competitive ability
In passerine birds, hatching asynchrony contributes to the establishment of size hierarchies, which, in turn, bias nestling mortality in disfavor of juniors (Amundsen and Slagsvold, 1991; Magrath, 1990; Stoleson and Beissinger, 1995). Parents control hatching asynchrony through the onset of incubation, which usually starts on the day the penultimate egg is laid (Stoleson and Beissinger, 1995). The start of incubation before the last egg is laid generates a size hierarchy that will be more pronounced between the two lowest-ranking nestlings than for the rest of the brood. Our findings that the relative difference in size was larger between the two lowest-ranking nestlings than between the two highest-ranking ones, and that juniors usually retained their rank over time whereas seniors often changed rank, are therefore consistent with the establishment of size asymmetries through hatching asynchrony.
Size asymmetries are expected to cause variation in the nestlings' ability to compete for food, with seniors being competitively superior to juniors (Parker et al., 2002; Rodríguez-Gironés et al., 2001). In support of this prediction, we found that seniors received significantly more food than did juniors. We also found evidence that size asymmetries affected the nestlings' competitive behavior. Seniors started to beg significantly earlier than did juniors, both relative to the parents' arrival (begging start) and relative to the first nestling in the brood (begging latency). The statistical models on parental provisioning suggest that begging latency was used in competition for food, as shorter begging latency improved the feeding success of seniors, but not of juniors, under food limitation. There was no evidence that seniors controlled food distribution by physical competition. In fact, juniors were positioned closer than were seniors to the site of parental arrival. This finding contrasts with previous findings for passerine species, in which seniors have been reported to be positioned in the most favorable positions (Cotton et al., 1999; Kilner, 1995). The statistical models on parental provisioning suggest that nestlings positioned closer to the parents had higher feeding success under normal, but not food-limited, conditions. Thus, under normal food conditions, juniors may have competed for frontal positions to improve their feeding success.
Food limitation and distribution of food
A central prediction of scramble competition models is that juniors will be more strongly affected by food limitation than will seniors (Parker et al., 1989, 2002). In support of this prediction, we found that the interaction between food limitation and nestling rank had a significant effect on the proportion of feeds received by nestlings, with a greater contrast between seniors and juniors when food was short. Thus, as predicted, food limitation induced by male removal led to a more uneven distribution of feeds within the brood in disfavor of juniors. In addition to effects owing to food limitation, male removal may change patterns of food distribution if males and females distribute food differently among seniors and juniors, as has been reported for some, but not all, passerine birds (see Amundsen, 1999; Lessells, 2002; Slagsvold, 1997). This suggestion can be ruled out from our study because males and females distributed food similarly among different-sized nestlings. This agrees with a previous experimental study reporting no difference in how male and female bluethroats distribute food among different-sized nestlings (Smiseth et al., 1998).
Food limitation and competition between seniors and juniors
Scramble competition models of begging assume that food allocation is under offspring control (Parker et al., 2002; Rodríguez-Gironés et al., 2001), and predict that changes in food distribution induced by food limitation result from a differential behavioral response by seniors and juniors. We found no significant interaction effect between food limitation and nestling rank for any of the nestling behaviors measured in the present study. Instead, the behavioral responses of seniors and juniors to food limitation were similar. Thus, there was no evidence for the assumption that food allocation was under sole offspring control, raising the theoretically important suggestion that parents play a more active role in controlling food allocation than is assumed by scramble competition models. Before returning to a discussion of parental feeding preferences, we first address the possibility that the change in food distribution was caused by nestling traits other than those we focused on.
Seniors might have received more food by reaching over the juniors. Begging height influences food distribution in some passerine birds, most notably in hole-nesters (see Leonard and Horn, 1996). Begging height is a composite trait that is determined in part by begging intensity (i.e., the amount of body stretching), which is a signaling trait, and body size, which is not. There was no evidence that seniors and juniors responded differently with respect to begging intensity (i.e., the signaling component of begging height). However, begging intensity increased from normal to limited-food conditions, and if the difference in height reached by seniors and juniors increased with begging intensity, seniors might have reached higher relative to juniors under food limitation. It is questionable if begging height is equally important in ground-nesters as in hole-nesters. Although begging height will bring a nestling closer to the beak of the incoming hole-nesting parent, this will not necessarily be so for ground-nesters, in whom food is offered from the side. Accordingly, horizontal position (measured in the present study) and begging eagerness (reflected in several measured parameters) are likely to be of greater importance. None of these parameters showed any interaction response that could explain the increased feeding skew.
Seniors and juniors may also have responded differently to food limitation by use of vocal, rather than visual, components of begging. In tree swallows (Tachycineta tricolor), begging vocalizations differ between seniors and juniors (Leonard and Horn, 2001). We did not analyze vocal begging because it is impossible to distinguish each nestling's vocalizations from our recordings. In bluethroats, the intensity of vocal begging tends to increase after the parent has delivered the food item (personal observation), suggesting that vocalizations affects the parents' feeding rates rather than how food is distributed during the current visit.
Food limitation and parental provisioning rules
The lack of a differential behavioral response by seniors and juniors suggests that parents play a role in controlling food allocation. As expected if parents preferentially feed seniors, our statistical models found a significant effect of nestling rank on food distribution when controlling for variation in nestling behavior. Nestling rank appeared to be a better predictor of food distribution under food limitation than under normal conditions, suggesting that parents showed a stronger preference for seniors under food limitation. However, this trend should be interpreted with caution because food limitation also affected nestling behaviors. Our analyses cannot distinguish between the following two suggestions: (1) that females changed their provisioning rule in response to food limitation, or (2) that they used a fixed provisioning rule, which caused the change in food distribution by interacting with the changes in nestling behavior caused by food limitation. An example of the latter would be if parents preferentially fed the larger nestling when two or more nestlings begged at similar levels, so that juniors would be fed only when they were the nestlings begging at the highest intensity. Food limitation might then reduce the success of juniors because they would be competing more often with a larger nestling.
In summary, the present study suggests that food distribution in passerines is not determined by nestling behavior (begging posture and positioning) alone but also by parental preferences for nonbegging cues such as nestling size (Godfray, 1995; Redondo and Castro, 1992), gape size, or color (Kilner, 1997; Saino et al., 2000). Theoretically, active parental preferences for seniors can be expected when parents have higher marginal benefits from feeding seniors than juniors, and seniors do not have behavioral control over food distribution. Royle et al. (2002) suggested that honest-signaling models may be evolutionarily unstable under food limitation because parents would be predicted to feed the neediest nestling, resulting in the undernourishment of the whole brood. However, honest-signaling models may be evolutionarily stable under food limitation if parents integrate information on nestling size with information on nestling begging to preferentially feed the nestlings with the highest value (see also Parker et al., 2002). We encourage the design of future experiments specifically aimed to test for active parental preferences. Future studies should focus on the effects of environmental variability on parental provisioning patterns, and on how parents integrate signaling (begging) and nonsignaling traits (nestling size, relative or absolute) in their provisioning rules.
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ACKNOWLEDGEMENTS |
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We thank Per-Anders Elvertrø, Asle Moen, Sonja Mork, and Roar Sandodden for valuable field assistance and Arild Johnsen, Jan T. Lifjeld, and Jonas Örnborg for much-appreciated cooperation during fieldwork. We thank Allen Moore and Richard Preziosi for statistical advice and Andrew Bourke, Douglas Mock, Jon Wright, and two anonymous reviewers for valuable suggestions. Financial support was provided by the Research Council of Norway and the Nansen Endowment. We adhered to the legal requirements of performing experiments on animals in Norway.
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