Behavioral Ecology Advance Access originally published online on April 15, 2008
Behavioral Ecology 2008 19(4):847-853; doi:10.1093/beheco/arn035
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Sex, melanic coloration, and sibling competition during the postfledging dependence period
Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales-CSIC, José Gutiérrez Abascal 2, 28006 Madrid, Spain
Address correspondence to P. Vergara. E-mail: vergara{at}mncn.csic.es.
Received 2 May 2007; revised 3 February 2008; accepted 4 March 2008.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONSUPPLEMENTARY MATERIALFUNDINGREFERENCES |
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Success in sibling competition is one of the main factors determining individual body condition in the early stages of life and consequently offspring survival and fitness. In birds, most studies on this topic have been focused on the nesting period, but sibling competition still continues during the postfledging period. We studied sibling competition over 3 years during the postfledgling dependence period in the Eurasian kestrel Falco tinnunculus, a reversed sexually size dimorphic species. Contrary to that in the nesting stage, male fledglings showed a higher competitive capacity than females resulting from their greater success in capturing larger prey items delivered by parents. Furthermore, male fledglings showing grayer coloration in the rump captured greater number of larger prey than browner males. Our results suggest that patterns of sibling competition in nestlings can differ from those found during postfledging, revealing the importance of studying this period in order to achieve a more complete view of sibling competition. In addition, kestrel fledglings with grayer rumps were more likely to have larger prey items, suggesting that this character can be interpreted as a phenotypic indicator of quality.
Key words: brood hierarchies, Falco tinnunculus, hatching order, prey delivery, sex differences, status signaling.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONSUPPLEMENTARY MATERIALFUNDINGREFERENCES |
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Sibling competition is one of the main factors that may influence body condition in the early stages of life and consequently survival and individual fitness (Mock and Parker 1998
). Usually, smaller and/or younger individuals show a competitive disadvantage in sibling rivalry. In birds, hatching asynchrony, sexual size dimorphism, brood sex ratio (in sexually size dimorphic species), and within-brood ranking position are factors modulating sibling competition for limited resources in the nest (Clutton-Brock et al. 1985; Arroyo 2002; Fargallo et al. 2003, 2006; Carranza 2004; Kalmbach and Becker 2005; Müller et al. 2005). However, sibling competition does not stop at the nestling stage but continues during the fledging and postfledging periods if siblings continue competing with each other for limited resources (Mock and Parker 1997). Most studies on sibling competition in birds have been carried out at the nestling stage, for which our knowledge on processes shaping sibling rivalry is partial and limited to nest environmental conditions and to physical determinants that nestlings experience during growth, such as a limited mobility or within-brood size hierarchies. Few studies have been carried out to investigate this topic at the fledging or postfledging periods or at the dependence period in other taxonomic groups (see Yoerg 1998), possibly due to the arduousness of monitoring interactions among siblings outside the nest. During the postfledging dependence period (PFDP), defined as the period from the first flight until young birds gain independence from their parents, dominant siblings try to monopolize prey (Arroyo et al. 2002; Kitowski 2005), as occurs during the nestling period (Mock and Parker 1997). This would mean that the chick hierarchy, established during the nestling stage, could continue into the PFDP (Kitowski 2005). However, capacities other than those expressed at the nest, such as flight ability or status signaling, can define sibling competition during these stages.
Bird colors are produced by pigment deposition in feathers (mainly carotenoids and melanins) or by varying the feather structure reflecting wavelengths in the visible spectrum (Hill and McGraw 2006a, 2006b). Nutrition has rarely been shown to affect melanic coloration (Veiga and Puerta 1996; Fargallo, Laaksonen, et al. 2007; McGraw 2007), whereas carotenoid- and structural-based coloration have been found to be positively correlated and experimentally affected by nutritional condition (reviewed by Hill 2006). This difference has led to the general idea that carotenoid color expression is linked to sexual signaling while melanic coloration can function in social status signaling (Hill 2006; Senar 2006). Plumage and bare parts are used to signal the fighting ability of individuals (Senar 2006). These signals may decrease the risk of accidental injury or waste energy between individuals of unequal fighting abilities by assessing the relative fighting ability of each opponent (Rohwer 1982). In connection with this, colorful offspring displays have been reported to develop in situations of increased levels of sibling competition for parental care. Lyon et al. (1994) demonstrated that parents are sensitive to offspring color expression and that they differentially provide food to offspring depending on its coloration (but see Tschirren et al. 2005), suggesting that nestling coloration can mediate sibling competition.
The Eurasian kestrel Falco tinnunculus is a reversed sexually size dimorphic raptor (females 20% heavier than males, Village 1990) in which male chicks are more negatively affected by food restrictions (Dijkstra et al. 1990; Wiehn and Korpimäki 1997; Fargallo et al. 2002) and have lower competitive capacity in the nest than female nest mates (Fargallo et al. 2003). Sibling competition is especially high in kestrel nestlings close to fledging because at that age, parents leave the prey in the nest while nestlings fight among themselves for the prey (Village 1990; Fargallo et al. 2003). In this species, a high proportion of nestling males and a very low proportion of nestling females express gray instead of brown coloration on the rump and upper tail coverts, a character that increases in better environmental conditions during nestling growth, decreases with higher concentrations of testosterone in plasma, and is positively correlated with body mass in stressful nest situations (increased levels of testosterone) (Fargallo, Laaksonen, et al. 2007; Fargallo, Martínez-Padilla, et al. 2007). Gray rump coloration is composed of melanin pigments in a eumelanin/pheomelanin ratio of 7.1 (Fargallo, Laaksonen, et al. 2007). Previous works showed that gray rump coloration may act as an indicator of condition and parasite resistance, suggesting a function of status signaling by assessing the individual fighting ability in a social context (Fargallo, Laaksonen, et al. 2007; Fargallo, Martínez-Padilla, et al. 2007; Vergara 2007). The aim of the present work is to study sibling competition during the PFDP in the Eurasian kestrel. By monitoring nests during the PFDP, we analyze parental feeding behavior (rate and type of prey delivered) and sibling competition for food. In addition, we study whether nestling sex, hatching order, body size, and body condition, variables indicating condition during the nestling period (Fargallo et al. 2002, 2003; Blanco et al. 2003, 2006), can also explain patterns of sibling competition during the PFDP. We expect that siblings that compete better in the nestling period (females, first-hatched, and healthy siblings) continue their dominance over the PFDP (Arroyo et al. 2002; Kitowski 2005) and consequently obtain more prey. In this sense, we tried to decrease sexual and rank differences in body condition during the nestling period by experimentally supplementing with food the nestlings from hatching to fledging and comparing with a control group in order to study whether patterns of sibling competition observed during the nestling phase can alter those at PFDP. If so, we predict a higher competitive capacity of females in control than in food-supplemented broods as females compete better for food than males during the nestling stage (Arroyo et al. 2002; Fargallo et al. 2003). Finally, we study for the first time whether coloration expression (rump coloration) of fledglings is related to their competitive capacity during the PFDP. If gray rump coloration is an index of individual quality, we expect that grayer siblings compete better for prey than browner fledglings.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONSUPPLEMENTARY MATERIALFUNDINGREFERENCES |
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Study species
Eurasian kestrels (hereafter kestrels) lay 5.0 eggs (range = 3–7) and produce 4.1 (range = 1–7) fledglings on average in the study population (Fargallo et al. 2001
). Also in our population, nestling kestrels fledge at 31.3 ± 0.4 (mean ± standard error [SE]) days (data from 2005, 2006, and 2007) in the same range as in other populations (27–32 days old; Cramp and Simmons 1980). The duration of the PFDP is highly variable among populations (16–41 days, reviewed by Bustamante 1994a). Fledglings of the same brood do not become independent on the same day, and the maximum difference in independence dates within a brood averaged 11.6 days (Bustamante 1994a). During the PFDP, fledglings stay in the nest (nest-box in our case) or nest surroundings and parents transfer the prey to groups of fledglings and apparently they do not show a selection for the fledgling to which they transferred the prey (Bustamante 1994a). Prey transfers take place on perches or on the ground rather than on air (aerial transfers) (Bustamante 1994a). In 59% of cases, parents give the prey directly to a given fledgling, in 31% of cases they leave the prey at the group of fledglings, and in 10% of cases they leave the prey on the ground or on a perch several meters distant from fledglings (this study). All these parental behaviors promote sibling competition to capture the prey from parents or to arrive sooner at the prey site (this study).
Study area and general procedures
The study was conducted during the breeding seasons of 2005, 2006, and 2007 in the Campo Azálvaro region (central Spain) where most kestrels breed in nest-boxes (Fargallo et al. 2001). The study area contains 64 nest-boxes in which about 30–40 kestrel pairs breed each year. Only nests placed in nest-boxes were included in this study (20, 25, and 7 nests during 2005, 2006, and 2007, respectively). The study area is an open, flat, and treeless grassland that makes kestrels easily detectable in nest surroundings from long distances (see Vergara and Fargallo 2007). Nests were monitored every 1–2 days to detect laying date (day of the first egg laid in the nest) and hatching date. Hatchlings were marked with indelible ink and again monitored every 5 days until banding (25 days after hatching). We used 3 categories for hatching order: first-hatched chick, last-hatched chick, and middle-hatched chicks (the remaining chicks between first and last hatched). At the age of 25 days, we measured the number of fledglings (2–6), took body measurements (tarsus length and body mass), and extracted 1 mL of blood from the brachial vein with a syringe for sexing chicks using molecular methods as described by Fridolfsson and Ellegren (1999) applied on kestrels (Fargallo et al. 2002). Moreover, the common assay of intradermal injection in the wing web of the T-cell mitogen phytohemagglutinin (PHA)-P (0.3 mg of PHA dissolved in 0·1 mL of phosphate-buffered saline; for procedures, see Fargallo et al. 2002) was measured as an index of health and condition (Tella et al. 2000; Alonso-Álvarez and Tella 2001). Chicks were injected at 25 days old and the reaction measured with a digital caliper the day after. At day 26, we measured the percentage of gray with respect to brown covering the whole rump by digitally photographing the rump and placing the bird under a sunshade and against a brown material (camera: Nikon D70, objective: 18–70 mm AF-S Nikkor DX). We then imported the images into the ImageJ 1.33u program developed at the US National Institutes of Health (Bethesda, MD) (http://rsb.info.nih.gov/ij/download.html.) to determine the gray area (number of pixels) in the rump. Repeatability of measurements was estimated from separate photos of 20 birds that were taken 20 s apart. Measurements of gray coloration areas were highly repeatable (r = 0.98, F19,20 = 92.2, P < 0.001; for details, see Fargallo, Laaksonen, et al. 2007; Fargallo, Martínez-Padilla, et al. 2007). We found that 11 out of 104 nestling females (10.5%) and 87 out of 118 nestling males (73.7%) showed gray in the rump (n = 212 nestlings from 52 nests). In nestlings showing gray in the rump, the ranges of gray percentage covering the rump were 2.2–12.2% and 2.24–34.3% for females and males, respectively. Rump coloration was grouped into 3 categories (Fargallo, Laaksonen, et al. 2007). In the category 1, we included all individuals with 0% of gray (brown individuals) and used the median (14.5%) to separate the other 2 categories, that is, category 2 <14.5% of gray and category 3 >14.5% of gray. We banded nestlings with a combination of 3 color rings. Adults were captured at the nest when nestlings were 10–13 days old, and body size measurements (tarsus length and body mass) were taken. Age of breeders (1 year old or adult) was determined by ring codes of individuals marked as nestlings or by plumage (Village 1990; Vergara and Fargallo 2007).
Fledging observations
We began observations at the fledgling age of 32 days. By that date, all individuals had fledged. We monitored nests and their surroundings during the PFDP for 20- to 120-min periods to record the number of fledglings (fledglings from the same brood become independent at different ages), the proportion of fledglings remaining in the nest or their surroundings (number of fledglings observed during the observation/number of fledglings counted at 26 days), and to identify the individuals present at nest surroundings. In the analyses, we controlled for the duration of the observation. In total, we carried out 372 different observations on 52 nests (108 observations from 20 nests during 2005, 242 observations from 25 nests during 2006, and 22 observations from 7 nests during 2007). For each observation, we noted the presence (1) or absence (0) of prey deliveries by adults. We observed 78 cases of prey delivery by parents. In only 8 cases out of 78, parents delivered more than one prey per observation (range 2–3). These cases were considered as "1" in the analyses of prey delivery by adults but were considered as different observations in the rest of the analyses, including the nest as random factor to avoid pseudoreplication (see below). We identified the prey species delivered, the size of the prey, the sex of the delivering adult, the place where parents left or transferred the prey (nest, wall, air, etc.), and the fledgling that obtained the prey (success of prey capture, see later). In addition, we recorded whether adults transferred directly the prey to a given fledgling (direct transfers) or they delivered the prey to the group of fledglings or far from fledglings (indirect transfers). In a total of 51 observations, we were able to identify the delivered prey species, the size of the prey, the sex of the delivering adult, and the place where the prey was left. We classified prey size into 2 groups: "small prey" including insects and small reptiles and "large prey" including voles, birds, and large lizards (see Supplementary material). Weights were estimated according to the mean value of each prey type in the study zone (Supplementary material). We also calculated the total biomass in grams consumed by each fledgling during the observations. In all cases, the prey were consumed by only one fledging, and we identified which fledging consumed the prey and whether it was involved in sibling fighting or not. In only 53 out the 78 observations, we were able to identify all the fledglings involved in the sibling fight, the fledgling that consumed the prey, and the prey size. These 53 observations (including 2 more observations in which we could not identify parent sex) were used to analyze sibling competition. We categorized the success of prey capture in sibling fights by each fledgling as a binary variable (1 = prey capture and 0 = no prey capture). Observations were performed with binoculars (8 x 30) and a telescope (20 x 60–80) and were carried out between 5:00 AM and 11:00 AM and between 3:00 PM and 7:30 PM by a single observer in a car situated more than 100 m from the nest to avoid disturbance. We randomly modified the order in which nests were monitored each day to avoid daytime bias.
Experimental treatments
In 2005, we carried out an experimental supplementation of carotenoids to adult females. Briefly, we administered 5 mg of carotenoids in 15 g of Japanese quail C. coturnix. japonica that was added every 2 days in occupied nest-boxes prior to laying (De Neve L et al. 2008). This experiment was done to study whether carotenoids (a prominent compound of egg yolk) can affect embryo development or nestling health and whether this potential effect can be modulated by mothers during laying. Mothers, but not nestlings, increased plasma carotenoid levels in response to carotenoid supplementation and had an effect on parasite infestation, lymphocyte concentration, and immune response of chicks. However, no significant differences were found between experimental and control groups in prey delivery rate of parents (generalized linear mixed model [GLIMMIX], male: F1,87 = 1.05, P = 0.31; female: F1,87 = 0.62, P = 0.43), prey size (GLIMMIX, F1,11 = 0.01, P = 0.92), nestling sex ratio (GLM, F1,18 = 0.25, P = 0.61), male–female success of prey capture (GLIMMIX, F1,35 = 0.32, P = 0.72), gray rump coloration of male nestlings (general linear mixed model [GLMM], F1,40 = 0.93, P = 0.34), and prey capture in relation to rump coloration in males (GLIMMIX, F1,11 = 0.33, P = 0.57). None of the nestling variables studied in the present work were affected by carotenoid supplementation to parents (GLMM, all P > 0.1). For this reason, we used observations obtained in 11 nests from the carotenoid group, but we included PHA assay as a covariate in the analyses of sibling fights, as it did affect PHA assay of chicks.
In order to test whether nestling body condition affects postfledging sibling competition, we performed a food supplementation experiment during 2006. We randomly selected 12 nests (52 fledglings) for feeding every 2 days from hatching to the age of 26 days of the chicks with commercial 1-day-old chickens. Thirteen nests (52 fledglings) were left as control nests, which were visited with the same frequency. Supplemented food was proportional to the number of nestlings and their age (half a chicken until the nestlings were 5 days old and 1 chicken per nestling afterward). As in the previous experimental treatment, we did not find significant differences between experimental and control groups in prey delivery rate of parents (GLIMMIX, male: F1,216 = 0.03, P = 0.85; female: F1,216 = 0.41, P = 0.52), prey size (GLIMMIX, F1,18 = 2.50, P = 0.13), nestling sex ratio (GLM, F1,23 = 0.01, P = 0.92), male–female success of prey capture (GLIMMIX, F1,50 = 0.01, P = 0.91), gray rump coloration of male nestlings (GLMM, F1,35 = 0.11, P = 0.73), and prey capture in relation to rump coloration in males (GLIMMIX, F1,22 = 0.92, P = 0.34). None of the nestling variables studied in the present work were affected by the food supply (GLMM, all P > 0.1), not even nestling body mass (GLMM, P = 0.32). No sex x treatment interactions were observed in any of the nestling variables (GLMM, all P = 0.19). For this reason, we included food-supplemented group in the analyses.
Fieldwork and animal manipulation were carried out according to ethical procedures of the Guidelines for the Use of Animals in Research. The permission to carry out the study was given by the Consejería de Medio Ambiente de la Junta de Castilla y León.
Statistical procedures
We used GLIMMIXs in SAS statistical software (SAS 1989–1996 Institute Inc., Cary, NC) with binomial error and logit link function to analyze 1) prey delivery by parents (0 = no prey delivery and 1 = prey delivery) in relation to the following explanatory variables, such as observation duration, number of fledglings, proportion of fledglings remaining at the nest, fledgling age (time elapsed between hatching of the first chick and the day of observation), parent sex, parent age (1 year old vs. adult), prey delivery of the partner, parent body size, hatching date, and also their interactions with parent sex. Note that in this model we have 2 values per observation (prey delivery by male and prey delivery by female). 2) Prey size (large vs. small) delivered by parents in relation to the same explanatory variables and the type of prey transfer (direct vs. indirect). 3) Success of prey capture by fledglings (0 = no capture and 1 = capture) in relation to fledgling sex, body size, hatching order, PHA test, and rump coloration. Rump coloration gradation differed between sexes. Females showed only 2 categories, whereas males showed 3 categories of coloration (see below). This prevented us to analyze the interaction sex x rump coloration when analyzing success of prey capture in relation to rump coloration. For this reason, we analyzed the relationship between prey capture and rump coloration in each sex separately. We used GLMMs to analyze whether biomass consumed by fledglings was correlated with rump coloration and sex. In all models, nest was included as a random factor to avoid pseudoreplication, continuous variables as covariates, and categorical variables as fixed factors. In the case of fledglings, fledgling identity was also included as a random factor in the models. All tests are 2 tailed. Means ± SEs are given.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONSUPPLEMENTARY MATERIALFUNDINGREFERENCES |
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Adult prey delivery
Controlling for observation duration (GLIMMIX, F1,688 = 50.55, estimate = 0.04, P < 0.01), prey delivery by parents was positively correlated with the proportion of fledglings remaining at the nest, negatively correlated with fledgling age, and also parent sex significantly explained variation in prey delivery, that is, male parents fed fledglings more frequently than females (GLIMMIX, proportion of remaining fledglings, F1,688 = 6.40, estimate = 0.02, P = 0.01; fledgling age, F1,688 = 3.94, estimate = –0.06, P = 0.04; parent sex, F1,688 = 25.31, estimate = –1.62 (females), P < 0.01; n = 744, corresponding with 372 observations from 52 nests). The rest of variables (see above) were not significantly correlated with parent prey delivery (GLIMMIX, all P > 0.1). In relation to prey size, both male and female parents captured prey of similar size (GLIMMIX, F1,21 = 1.49, P = 0.23, n = 51), and direct transfers to nestlings were more frequently observed in small prey deliveries, whereas indirect transfers were more frequently observed in large prey deliveries (GLIMMIX, F1,21 = 38.46, P < 0.01). The rest of the studied variables (see above) were not significantly correlated with prey size (GLIMMIX, all P > 0.1). Controlling for prey size (GLIMMIX, F1,21 = 39.06, P < 0.01), male and female parents did not differ in the frequency of direct or indirect transfers (GLIMMIX, F1,21 = 0.05, P = 0.81). Nineteen out of 30 (63.3%) direct transfers were carried out on the top of the nest-box, 10 (33.3%) on the ground, and 1 on a pole close to the nest (3.3%). In the case of indirect transfers, 3 out of 21 (14.3%) were on the nest-box, 14 (66.6%) on the ground, and 4 (19.1%) on a pole close to the nest.
Sex and sibling competition
Food supplementation during the nestling phase did not vary sexual dimorphism in body mass compared with control nests. This may have been because 2006 was a year of high food abundance for our kestrel population. This prevented us from examining the effect of nestling conditions on postfledging sibling competition. None of the nestling variables (sex, hatching order, body size, and PHA test) were correlated with the success of prey capture in sibling fights (GLIMMIX, all P > 0.11, 211 observations, 113 fledglings, 53 prey deliveries, and 29 nests). However, there was a significant interaction between sex and prey size (GLIMMIX, sex x prey size: F1,96 = 4.11, P = 0.04; sex: F1,96 = 1.24, P = 0.26; prey size: F1,96 = 0.04, P = 0.84). When we included only the observations in which both sexes were present during the sibling fights (184 observations, 100 fledglings, 43 prey deliveries, and 24 nests), the interaction sex x prey remained significant (Table 1, Figure 1.), and similarly, the remaining variables did not explain significantly the success of prey capture (GLIMMIX, all P > 0.17). Males captured more large prey than females and females more small prey than males (Figure 1). Due to the difficulty in obtaining observations of fledglings fighting and because the experimental manipulations did not appear to have a significant effect on the variables in which we were interested, so as to increase sample size, we included all the observations made of experimental nests. Nevertheless, using only control nests in which both sexes were present during the observation (81 observations, 51 fledglings, 21 prey deliveries, and 14 nests), the interaction sex x prey size was similarly significant (GLIMMIX, sex x prey size: F1,28 = 4.51, P = 0.04; sex: F1,28 = 2.06, P = 0.16; prey size: F1,28 = 0.12, P = 0.73), and as in the previous model, males captured more large prey than females and females more small prey than males. In relation to the total biomass received, the model showed differences between sexes, that is males receiving more biomass than females, although not significantly so (GLMM, P = 0.07). Hatching order, body size, and PHA test were not significantly correlated with the total biomass received (GLMM, all P > 0.15).
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Rump coloration and sibling competition
We found that 18 of 59 (30.5%) male fledglings had rump coloration categorized as "3," 29 (49.2%) categorized as "2," and 12 (20.3%) as 1, that is, with brown rumps. We did not find females with rump coloration categorized as 3, and only 10 of 54 (18.5%) categorized as 2. In the case of males (99 observations, 59 males, 50 prey deliveries, and 28 nests), we observed that the grayest males (category 3) captured more large prey than males from categories 1 and 2 (Figure 2). The within-brood success of prey capture was significantly explained by the interaction between prey size and rump coloration (Table 1). This was due to that no differences among fledglings of different rump categories were observed in the capture success of small prey (GLIMMIX, F2,18 = 0.66, P = 0.52, n = 48), but we observed significant differences in large prey (GLIMMIX, F2,8 = 4.48, P = 0.04, n = 51). Analyzing the biomass consumed by fledglings during the observations, we found significant differences between categories (GLMM, F2,44 = 3.86, P = 0.03, n = 99). The grayest males (category 3) consumed more biomass than male fledglings of categories 1 and 2 (mean ± SE category 1 = 13.5 ± 5.1, n = 12 males; category 2 = 2.3 ± 3.2, n = 29 males; category 3 = 15.6 ± 4.1, n = 18 males). Using only males from control nests (53 observations, 34 males, 27 prey deliveries, and 17 nests), we did not observed a significant interaction between prey size and rump coloration (GLIMMIX, F2,16 = 1.99, P = 0.16). However, when grouping individuals of categories 1 and 2 and comparing that with category 3, the interaction between prey size and rump coloration was marginally significant (GLIMMIX, F1,17 = 3.14, P = 0.09). Also, analyzing only control males, we found significant differences between gray rump categories (GLMM, F2,19 = 4.99, P = 0.02). The grayest males (category 3) received more biomass than browner fledglings in control nests (mean ± SE category 1 = 8.5 ± 6.9, n = 7 males; category 2 = 2.1 ± 4.6, n = 16 males; category 3 = 24.3 ± 5.5, n = 11 males). There were no differences in prey capture success or biomass consumed by females in relation to their rump coloration (all P > 0.25), but this is likely to be due to the small sample sizes (44/54 females had completely brown rumps).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONSUPPLEMENTARY MATERIALFUNDINGREFERENCES |
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Sex and sibling competition during the PFDP
Our study shows that sibling competition patterns at the nesting stage differ from those found at fledgling and postfledging stages. In American Falco sparverius and Eurasian kestrels, male nestlings have lower competitive capacity to obtain the food provided by parents (Anderson et al. 1993
; Fargallo et al. 2003). This results in a reduction of condition or body mass with respect to sisters when food becomes scarce (Dijkstra et al. 1990; Anderson et al. 1993; Korpimäki and Wiehn 1998; Fargallo et al. 2002). However, we found that male fledglings were more successful in obtaining prey that contribute higher biomass (large prey) during the PFDP, indicating a higher competitive capacity of males during this period with respect to their female brood mates. It is noteworthy that parents mainly leave large prey on the ground or on a perch several meters distant from fledglings, which could favor males due to their better-developed flight capacities. One of the ideas proposed to explain reversed sexual size dimorphism in raptors is that a lighter body and smaller size confers the males advantages in food competition with respect to females because smallness increases the hunting efficiency and success of birds of prey (Andersson and Norberg 1981; Massemin et al. 2000). In the case of the Eurasian kestrel, this has been specifically addressed. Hakkarainen et al. (1996) found that adult males were more efficient in prey capture than adult females, and also within males, lighter individuals showed the highest hunting success. In the Eurasian kestrel, males are 20% lighter than females but only 10% smaller in wing length (Hakkarainen et al. 1996; Massemin et al. 2000), which diminishes the loading index (body mass/flying area) with respect to females, increasing thus the flying capacity, which is positively correlated with feeding rate (Hakkarainen and Korpimäki 1995). This potential capacity of males can explain the pattern found during the PFDP, in which males outcompeted females in gaining access to larger prey items. Optimal foraging theory predicts that a predator should select the prey for which it gains the most energy per unit of time and thereby maximizing its fitness (Stephens and Krebs 1986). Although no sex differences were observed in the total biomass consumed, by obtaining large prey, males can save energy during a critical period (the PFDP) by diminishing the number of flights and reducing the number of injuries produced by the hard fights among siblings when competing for food. Although this has yet to be tested directly, it is expected that this higher competitive capacity could give the males the opportunity to recover or to gain body and health condition with respect to females during this period. The ecological importance of this result lies in the fact that male disadvantages observed in nesting stages could be compensated for later in the fledging period.
We did not find that parents had preference for feeding a chick of one sex over another, as previously reported during the nesting phase in correlative (Fargallo et al. 2003) and experimental (Laaksonen et al. 2004) studies. In addition, large prey (those preferentially consumed by male fledglings) are mainly given to the fledglings through indirect transfers, suggesting a behavior of parents focused on promoting sibling competition.
Rump coloration and competitive capacity
Previous works found parent preference in food provisioning related to offspring coloration (Lyon et al. 1994), although others have not found such a relationship (Tschirren et al. 2005) suggesting that nestling coloration can mediate sibling competition, although this mechanism do not always occur in bird species. Here, we showed that the grayest males obtain larger prey. This is consistent with the interpretation that gray rump coloration in male nestlings reflects quality (a positive correlation with body mass: Fargallo, Martínez-Padilla, et al. 2007; a negative correlation with parasite species richness: Vergara 2007). Rump coloration in male kestrel nestlings could act as an intra-age class indicator of dominance (Senar 2006). A higher expression of gray coloration could provide benefits in competition for food or other resources such as winter territories and thus in breeding performance in the following reproductive season (Fargallo, Laaksonen, et al. 2007; Fargallo, Martínez-Padilla, et al. 2007; Vergara and Fargallo 2007). There is no clear association between rump coloration and success in prey capture in females, which may be because we have seen so few females with any significant gray in their rumps (2, 5, and 4 in 2005, 2006, and 2007, respectively), although none was categorized as 3, that is the category showing clear advantages in male competitiveness. A specific experiment should be carried out to test the role of parents in the food obtained by fledglings in relation to rump coloration. However, as in the case of sex, the differences in sibling competition were much more obvious when the prey was made available by the parents via indirect transfers, suggesting the importance of the individual capacity to compete for food against brood mates.
Parental behavior during the PFDP
In kestrels, males are the main food provider to females and chicks during the breeding period, from laying to fledgling dependence (Village 1990; Tolonen and Korpimäki 1994; this study). Males progressively increase their hunting effort and prey delivery rate over the breeding season from courtship to chick rearing, peaking when chicks reach the age of 12 days, at which time females begin to feed chicks (Tinbergen 1940; Village 1990). We found that during the PFDP, males feed fledglings at a higher frequency than females, thus providing the greatest part of fledgling food requirements. In addition, we found that the rate of prey delivery by parents positively correlated with the number of fledglings remaining in the surroundings of the nest and with the fledgling age. These results are in agreement with previous results in raptors (Bustamante 1993; Bustamante and Negro 1994; Arroyo et al. 2002, but see Bustamante and Hiraldo 1990; Bustamante 1995) and suggest that the duration of PFDP is in part an adult decision and that it is dependent on the adult prey delivery rate (Davies 1978; Ferrer 1992; Kenward et al. 1993; Bustamante 1994b; Eldegard et al. 2003).
In sum, our study reveals the necessity to explore fledging and postfledging periods to have a more realistic understanding on the mechanisms underlying sibling competition in birds. The study of the fledging and postfledging periods informed us that other traits, such as flight ability, can contribute to the competitive capacity of individual birds. The sex considered to be more handicapped in sibling competition during the nesting stage may not be so during the postfledging period. In addition, our study represents the first case to our knowledge showing a positive correlation between offspring coloration and competitive capacity during the postfledging period. In this sense, more ornamented male fledglings seem to have a higher competitive capacity than less ornamented ones as resulted by the higher rate of large prey items got by the former.
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Supplementary material can be found at http://www.beheco.oxfordjournals.org/
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Spanish Ministry of Education and Science (Project: CGL2004-04479/BOS).
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ACKNOWLEDGEMENTS |
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The Finat family and J. San Teodoro collaborated in our field studies. L. de Neve, J. Martínez-Padilla, H. Dexon, J. Fernández, I. López, M. Gil, E. Banda, and M. C. López Agúndez helped in the field. Sarah Young revised the English. Sue Healy and 2 anonymous referees substantially improved the manuscript.
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