Behavioral Ecology Advance Access originally published online on August 16, 2007
Behavioral Ecology 2007 18(6):994-1000; doi:10.1093/beheco/arm074
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Variable postfledging care in a cooperative bird: causes and consequences
a DST/NRF Centre of Excellence, Percy Fitzpatrick Institute, University of Cape Town, Rondebosch 7701, South Africa b Large Animal Research Group, Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, United Kingdom
Address correspondence to A.R. Ridley. E-mail: amanda.ridley{at}uct.ac.za.
Received 12 April 2007; revised 14 June 2007; accepted 25 June 2007.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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Prolonged postfledging care is a commonly observed behavior in many cooperatively breeding species and has been shown to provide young with both survival and developmental benefits. However, the causes of intraspecific variation in postfledging care and the consequences of this variation on the development of young remain unclear. Here we investigate factors affecting the duration of postfledging care in the cooperatively breeding pied babbler (Turdoides bicolor). We show that the duration of care is variable (40–97 days) and is determined primarily by the cost of care. Adults in groups with a low adult:fledgling ratio were unable to maintain body mass during the period of chick provisioning and subsequently ceased care of young earlier. This had a strong influence on offspring development: fledglings that received longer periods of care attained higher foraging efficiency and body mass than their counterparts at 6 months of age. The duration of postfledging care also had long-term effects, with individuals that received longer periods of postfledging care more likely to successfully disperse from their natal group. This had important fitness implications as successful dispersers became reproductively active at an earlier age than their "failed-disperser" counterparts. These findings highlight the importance of considering long-term influences when assessing the benefits of prolonged postfledging care on offspring fitness and development in cooperative societies.
Key words: cooperative breeding, dispersal success, pied babblers, postfledging care, Turdoides bicolor.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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Among biparental avian species, parental care of young is concentrated primarily during the nestling period (reviewed in Price 1998
), with little or no investment after fledging (Langen 2000). In contrast, prolonged postfledging care is a common occurrence among cooperatively breeding bird species (Heinsohn 1991; Langen 2000; Russell 2000; Russell et al. 2004). Such care has been shown to provide young with considerable benefits, including a higher body mass at nutritional independence and an increased likelihood of overwinter survival (Heinsohn 1991, reviewed in Langen 2000). However, owing to the difficulty of monitoring young once they have fledged (Langen 2000; Arroyo et al. 2002), little information is available on intraspecific variation in postfledging care in cooperatively breeding birds. Consequently, the causes of such variation and the consequences on offspring development in the short term and fitness in the long term remain unclear.
In the short term, young are likely to receive direct nutritional benefits from investment in provisioning behavior by both parents and helpers (reviewed in Emlen 1997; Cockburn 1998). However, prolonged parental investment may provide young with other additional benefits, such as increased opportunities to learn foraging techniques (Langen 1996; Thornton and McAuliffe 2006) or reduced vulnerability to parasites (Field and Brace 2004). In addition, young receiving long periods of care may have more time to interact with one another rather than begging or attempting to forage. This may provide young with the opportunity to practise other skills (e.g., fighting) that may affect the likelihood of successful dispersal or attaining a breeding position within a group. Because breeding positions are often more limited in cooperative than biparental breeding systems (owing to the monopolization of breeding activity by a small proportion of the population [Emlen 1995]), the effect of the duration of postfledging care on the ability of young to compete for a breeding position in the future may be an important and yet poorly researched aspect of chick-rearing behavior in cooperative bird species.
Within species, it is possible that the duration of offspring care can vary considerably for several reasons. First, provisioning behavior is assumed to impose a cost to adults (Clutton-Brock et al. 1998; Russell et al. 2003; Varpe et al. 2004; reviewed in Heinsohn and Legge 1999). Adults in groups with a low adult:offspring ratio may therefore incur greater costs of provisioning young and consequently cease care earlier. This may be especially important in cooperatively breeding species, which are characteristically long lived (Ridley et al. 2005) because life-history theory predicts that long-lived species should favor their own survival (and future opportunities for reproduction) over survival of current young (Mauck and Grubb 1995; Ghalambor and Martin 2001). Second, environmental conditions, such as rainfall, may affect food availability and consequent development of foraging skills by young, resulting in variable duration of parental care while young learn to develop foraging skills according to prevailing conditions (Wheelwright and Templeton 2003). Third, it is possible that adults may provide longer periods of care for the most "valuable" sex of offspring (Gowaty and Droge 1991; Lessells 2002; reviewed in Slagsvold 1997). In species with sex-biased philopatry, as is common in many cooperative breeders (Greenwood 1980; Pusey 1987), there is evidence that adults prefer to invest in the sex that will give them the greatest fitness returns. For example, adults may prefer to raise the philopatric sex, which commonly help to raise future young (Clutton-Brock et al. 2002), or the dispersing sex when territory resources are limited (Ridley and Huyvaert 2007). Finally, the duration of adult investment may vary according to brood size. For example, in small broods where several young have died, adults may benefit from terminating investment and investing in a new, larger brood (Ackerman and Eadie 2003; Ackerman et al. 2003) to maximize the potential fitness benefits gained from raising young.
There is increasing evidence that adult investment decisions can have important fitness consequences for young. In noncooperative vertebrates, conditions experienced early in life can significantly affect lifetime reproductive success (Lindström 1999). Comparable influences could help to elucidate the widespread prevalence of extended postfledging care in cooperatively breeding species. Despite this, empirical evidence for long-term effects of postfledging care on offspring fitness in cooperative birds is lacking. In this paper, we investigate the causes and consequences of variation in the duration of postfledging care in the cooperatively breeding pied babbler (Turdoides bicolor). First, we examine the causes for variation in the duration of care between broods. We then investigate the short-term consequences of such variation in care on juvenile body mass and foraging efficiency. Finally, we look at the long-term consequences by investigating how the duration of postfledging care influences dispersal success and concomitant breeding activity.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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Study site and species
We studied patterns of postfledging care in 12 groups of pied babblers at the Kuruman River Reserve in the southern Kalahari Desert, South Africa (26°58'S, 21°49'E), between October 2003 and December 2006. The study area is semiarid grassland and acacia savannah, with an average annual rainfall of 217 mm (a detailed description of climate and vegetation is given in Raihani and Ridley forthcoming).
Pied babblers are medium sized, sexually monomorphic passerines (75–95 g) occupying the semiarid regions of southern Africa. Groups defended year-round territories and foraged closely together throughout the day. The period of peak breeding activity extended from October to early April, and each group raised a maximum of 3 broods to independence per season. All adult group members contributed to feeding the young of each brood (average brood size 2.03 ± 0.14 nestlings per brood, range 1–4). After hatching, young were fed at the nest for 14–18 days (Raihani and Ridley forthcoming). After fledging, young were unable to fly or forage and were entirely dependent on adults for food. Young did not usually attempt to forage for themselves for at least 3 weeks after fledging (range 17–29 days), and first attempts at foraging were very short (averaging 4.8 ± 2.1 s per bout) and always unsuccessful (0 successes from 54 observed first foraging attempts).
Babbler group size during the study period ranged between 2 and 8 adults, averaging 4.2 ± 0.3 adults per group. All individuals older than 12 months or (where exact age was unknown) all individuals with no juvenile plumage were considered adults. All pied babblers at the study site were individually recognizable using a unique combination of colored rings and were habituated to observation from a distance of approximately 2–3 m. For details of the habituation process, see Ridley and Raihani (2007).
Data collection
Behavioral data
During incubation, each nest was checked daily to determine exact hatching date. All nestlings were ringed and weighed on day 11 (posthatching) to gain a measure of nestling condition. We checked each nest daily from day 14 (posthatching) onward to determine the exact date of fledging.
The measurement of the duration of postfledging care followed that of Langen (2000): the number of days after fledging that fledglings were fed directly by adult group members, including the period that fledglings were completely dependent on adults for food and the period in which fledglings could potentially self-feed but still received some food from adults. We considered that significant levels of care had ceased when fledglings received less than one feed per hour. Beyond this period, fledglings were considered nutritionally independent.
Because the duration of care may vary between individuals within broods, duration of care was measured per individual fledgling. We collected data from 84 fledglings that survived up to 6 months of age from 34 broods in 12 groups. Each group was observed 3 times a week for 3–4 h per observation session (n = 2870.5 observation hours). During each observation session, the size and number of all food items delivered by all adults to each dependent fledgling was recorded using a handheld data logger. All food items were divided into 5 size classes (see Raihani and Ridley forthcoming for size classification). Size classes were converted into biomass values by weighing 50 prey items representative of each class. The average biomass that each fledgling received per hour (from all adults combined) during the postfledging dependent period was calculated as the sum of the number of prey items in each size class multiplied by the average weight of that class, divided by the number of observation hours.
We used 20-min time–activity focal watches (Altmann 1974) to determine foraging efficiency of fledglings. During each focal, the amount of time spent foraging (in seconds) and the size and type of each food item found was recorded. At least one focal per week was conducted on each fledgling until individuals reached 6 month of age (posthatching). Foraging efficiency was calculated by converting item size into biomass values as described above. The biomass caught in each focal was then divided by the time spent foraging to give biomass caught per unit foraging time.
Sexing
Because it was not possible to determine sex from external characteristics in this species, small blood samples (50 µL) were collected from nestlings and adults via brachial venipuncture. Nuclear DNA was extracted, and polymerase chain reaction–based molecular sex determinations were conducted using the method described in Radford and Ridley (2006).
Body mass measurements
Body mass was measured by enticing individuals to stand on a top pan balance for a small food reward at first light (before foraging had begun). Juvenile body mass was measured as the average weight of each individual (using a minimum of 3 measurements per individual) at first light in the first 2 weeks after they reached 6 months of age.
Dispersal attempts
An individual was considered to be attempting dispersal when we observed the individual leaving the natal group and subsequently following and physically fighting with other adults at a nonnatal group. Attempted dispersals were differentiated from territory border conflicts because dispersal events involved only one individual (with the rare exception of dispersal cohorts), whereas border conflicts typically involved all group members. Furthermore, dispersal attempts occurred over a protracted period of up to 3 days, whereas border conflicts commonly lasted less than 5 min. An individual was considered to have successfully dispersed into a new group when it foraged and roosted with the new group without receiving aggression from resident group members. This association had to continue for more than 2 weeks for the dispersal to be considered successful.
Rainfall data
Rainfall data were collected daily from the weather station located in the Kuruman River Reserve. Rainfall (millimeters) was summed to give the total amount of rainfall that fell in the 2 months prior to the event of interest. We considered 2 months the appropriate time period to indicate food availability because there is commonly a protracted period of time between rainfall and increased insect abundance (Cumming and Bernard 1997).
Analysis
Data were analyzed using LMMs (linear mixed models) or GLMMs (generalized linear mixed models) in Genstat 8.1 (Genstat 8th edition, Lawes Agricultural Trust, 2005), which allow terms with repeated measures to be fitted as random terms, thus controlling for nonindependence of data. The method of fitting mixed models to data followed Crawley (2002). Model simplification using backward elimination was adopted. Terms were systematically removed from each model and only retained if their removal resulted in a significant loss of model explanatory power (the minimal model). The P value for eliminated terms was determined by adding each individually to the minimal model. All 2-way interactions were tested, but only significant interactions are presented. Throughout the text, means are expressed with standard errors, and null hypotheses are rejected at P < 0.05.
Factors affecting the duration of care
To determine the factors affecting the duration of postfledging care, we specified the duration of care each fledgling received (days after fledging) as the response term in a LMM with an identity link function. Social (adult:fledgling ratio), fledgling (sex, brood size, average foraging efficiency in week prior to cessation of care), and environmental characteristics (total rainfall in 2 months prior to cessation of care) were included as potential explanatory terms in the model, with group and brood identity as random terms.
To determine whether raising young was costly to adults, we investigated factors affecting the change in adult body mass over the course of a breeding event. We calculated the difference between average adult body mass in the 2 weeks prior to hatching of each brood and average body mass after the first 3 weeks postfledging. Data were restricted to this time period only because it was the period when all fledglings were completely reliant on adults for food and made no attempts to self-forage. The change in body mass was set as the response variable, with adult sex, average body mass (at first light in the 2 weeks prior to hatching), and total rainfall in the 2 months prior to fledging included as explanatory terms in a LMM with an identity link function. Adult, group, and brood identity were included as random terms in the model.
To investigate the effect of adult body mass on subsequent breeding attempts, we asked whether the average body mass of each breeding adult after the cessation of care for the first brood influenced the likelihood of investing in a subsequent brood. Data were restricted to those groups who successfully raised their first brood to independence from their first breeding attempt to avoid the potential confounding effects of failed breeding events on body mass and the amount of time left in the breeding season on the likelihood of renesting (e.g., Arroyo et al. 2002; Shutler et al. 2006). Body mass measurements were taken at first light in the first 2 weeks after the cessation of care. Groups were considered to be renesting once incubation was observed. Breeding activity was added as a categorical predictor in the model where "0" = no attempt to breed again and "1" = investment in second clutch. Adult sex, group size (number of adults), and rainfall in the prior 2 months were included as potential explanatory terms, and group identity was included as a random factor.
Factors affecting body mass and foraging efficiency of juveniles
To determine what factors affected body mass and foraging efficiency of juveniles (6 months after hatching), we investigated the influence of social (duration of postfledging care, amount of biomass received per hour), fledgling (sex, prefledging body mass), and environmental characteristics (rainfall). Group and brood identity were included as random terms in each model. Data were analyzed using LMMs with identity link functions.
Factors affecting dispersal success
To determine the factors affecting the success of individuals attempting to join new groups, we gave the value "0" to each failed dispersal attempt and "1" to each successful attempt. This was entered as the response variable in a binomial GLMM with a logit link function. Duration of care, rainfall in the 2 months prior to the dispersal event, age (months since hatching), and sex of the individual were included as potential explanatory terms. Only individuals of known age, where the duration of postfledging care received was known, were included in the analysis. Group and individual identity were included as random terms in the model.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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Factors affecting the duration of care
The duration of postfledging care varied widely between broods, averaging 58.9 ± 1.93 days (range 40–97 days), but varied very little among fledglings within broods (average within-brood difference = 2.16 ± 0. 44 days, range 0–4 days). Adults in groups with a lower adult:fledgling ratio ceased care of young earlier (Figure 1), independently of environmental conditions (Table 1). Adults in groups with a low adult:fledgling ratio also lost more body mass over the duration of a breeding attempt (Figure 2, Table 2). This had an important influence on subsequent breeding attempts: breeding individuals with a lower body mass at the end of the dependent period for the first clutch of the season were less likely to invest in subsequent broods (LMM
2 = 6.58, P = 0.010, n = 41). The body mass of breeding adults that did not reclutch averaged 78.6 ± 0.9 g (78.1 g females [n = 7], 78.8 g males [n = 8]) compared with 81.7 ± 0.7 g (82.0 g females [n = 16], 80.5 g males [n = 10]) for those that did reclutch.
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Factors affecting body mass and foraging efficiency of juveniles
The length of postfledging care that young received had a strong influence on their development. Young that received long periods of postfledging care tended to have higher body mass (Figure 3) and higher foraging efficiency (Figure 4) than their counterparts at 6 months of age, independently of rainfall (Table 3). These effects continued into adulthood, with body mass and foraging efficiency at 6 months significantly associated with adult body mass and foraging efficiency (body mass, linear regression: F1,29 = 10.372, P = 0.003, adjusted R2 = 0.24; foraging efficiency, F1,26 = 7.707, P = 0.010, adjusted R2 = 0.19).
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Factors affecting dispersal success
The duration of postfledging care had long-term consequences for young. From 57 observations of individuals of known age attempting to disperse into a new group (38 female and 19 male dispersal attempts), only 19 (33.3%, 10 females and 9 males) were successful. The length of postfledging care that young received had a strong impact on the outcome of dispersal attempts (Figure 5), with those individuals that received longer periods of postfledging care more likely to successfully gain a position in a new group (Table 4). Of all 19 individuals that successfully dispersed, only one did not have a breeding opportunity in their new group. Eight (42.1%) of the successful dispersers mated and hatched young on their new territory within 6 months of dispersal, compared with none of those that failed in their dispersal attempts and remained on their natal territory.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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The variation in duration of postfledging care in the pied babbler is determined primarily by the ratio of adults to fledglings and the subsequent cost of raising young. Similar to trends reported by Weathers and Sullivan (1989)
and Verhulst and Hut (1996), when the costs of current reproduction are high, adults invest in young for shorter periods of time. Because adult body mass is an important predictor of the likelihood of investing in a second clutch, adults may cease care of young earlier in groups with a low adult:fledgling ratio to increase the chances of successfully breeding again. This relationship between adult condition and care of young is similar to that observed by Mauck and Grubb (1995) in a long-lived petrel species and supports the life-history prediction that long-lived species should cease care of young earlier when the costs of care are high (Williams 1966; Ghalambor and Martin 2001) because they should favor their own survival and future reproductive opportunities over the fitness of current young. It is possible that groups with a high adult:fledgling ratio may be able to invest in young for longer owing to brood division, where particular adults invest in particular subsets of the brood over an extended period of time. However, the ecological causes and adaptive significance of brood division remain unclear (Leedman and Magrath 2003), and the occurrence of this behavior remains to be determined for pied babblers.
Alternative explanations for the duration of postfledging care observed in this species can be ruled out. First, it is unlikely that adults were sensitive to the needs of young by ceasing care when a satisfactory level of foraging efficiency was attained (Wheelwright and Templeton 2003) because 1) there were several cases of fledglings dying of starvation (as determined from daily records of weight loss) after cessation of care and 2) there was no effect of fledgling foraging efficiency on the cessation of care. Second, there was no evidence for adults providing longer periods of care for more "valuable" offspring because 1) there was no difference in the duration of care between males and females and 2) within broods, cessation of care usually occurred simultaneously to all fledglings.
The duration of postfledging care had both short- and long-term consequences for young. In the short term, young that received long periods of care were heavier and better foragers than their counterparts. This may provide them with a buffer against weight loss over winter or drought periods (Heinsohn 1991), greater resistance to disease or parasites (Field and Brace 2004), or more time to practise fighting skills or to become involved in affiliative social behaviors (e.g., allopreening). In the long term, postfledging care had potential fitness implications, with individuals that received longer periods of care more likely to successfully disperse. Almost all the individuals that successfully dispersed had reproductive opportunities in their new group, in contrast to none of the failed dispersers that remained on their natal territories. Thus, successful dispersers were able to gain breeding positions at a younger age and could potentially enjoy greater lifetime reproductive success than their "failed-disperser" counterparts. This could be especially important for females, the dispersing sex, because reproductive opportunities on the natal territory are extremely limited (Raihani NJ, unpublished data).
The critical importance of postfledging care for the development of young is highlighted not only by influences on development and dispersal ability but also by the absence of any effect of nestling body mass on juvenile development. This is in contrast to biparental species (Magrath 1991; reviewed in Price 1998; Lindström 1999), where juvenile condition and fitness are commonly affected by nestling condition. Thus, postfledging care is a crucial stage in the development of pied babbler young, and this effect may be widespread in other cooperatively breeding bird species with extended periods of postfledging care.
These results suggest that studies considering the effect of adult investment on the development of young in the short term (i.e., to independence only) may underestimate the importance of extended parental care on offspring fitness in cooperative societies. Although there is increasing evidence in noncooperative vertebrates that conditions experienced early in life can have long-term effects on adult development and fitness (Lindström 1999; Metcalfe and Monaghan 2001), evidence for such influences on offspring in cooperative societies are rare (but see Russell et al. 2007). The positive influence of prolonged postfledging care on dispersal success in the pied babbler provides one of the few examples of the importance of the duration of care on the fitness of young raised in cooperative societies.
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FUNDING |
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Newnham College, Cambridge (to A.R.R.); Association for the Study of Animal Behaviour (to A.R.R.); Department of Science and Technology/National Research Foundation (to A.R.R.); National Environmental Research Council (to N.J.R.).
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ACKNOWLEDGEMENTS |
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We thank the Northern Cape Conservation Authority for allowing us to work on wild pied babblers and T.H. Clutton-Brock for supporting our establishment of a study population in the Kuruman River Reserve. Thanks to all Meerkat Project members for help and encouragement. We are grateful to Mr and Mrs H. Kotze and Mr and Mrs F. De Bruin for allowing us access to their land and to L. Browning, S. Knowles, M. Nelson, A. Radford, and A. Sommerfield for contribution to habituation and data collection. M. du Plessis, P. Lloyd, and 2 anonymous reviewers provided useful comments and advice that greatly improved the manuscript.
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