Factors affecting offspring survival and development in a cooperative ...

Journal of Animal Ecology 2007 76, 750–760

Factors affecting offspring survival and development in a cooperative bird: social, maternal and environmental effects Blackwell Publishing Ltd

A. R. RIDLEY Large Animal Research Group, Department of Zoology, Downing Street, Cambridge CB2 3EJ, UK

Summary 1. In many noncooperative vertebrates, maternal effects commonly influence offspring survival and development. In cooperative vertebrates, where multiple adults help to raise young from a single brood, social effects may reduce or replace maternal effects on offspring. 2. Factors affecting offspring survival and development at different stages (fledging, nutritional independence and adulthood) were tested in the cooperatively breeding Arabian babbler to determine the relative importance of social, maternal and environmental factors at each stage. An influence of maternal effects was found during the nestling stage only. 3. Social factors affected the survival and development of young at all stages. The amount of food received from helpers influenced post-fledging weight gain, development of foraging skills, and survival to reproductive age. Environmental effects were also important, with groups occupying high-quality territories more likely to produce young that survived to maturity. 4. The strong influence of helper contributions on the survival and development of young at all stages from hatching to maturity suggests social factors may have important long-term effects on offspring fitness in cooperative societies. Traditional measures of offspring survival in cooperative birds, which commonly measure survival to fledging age only, may underestimate the significant benefit of helper contributions on the survival and development of young. Key-words: Arabian babbler, cooperative breeding, helpers, maternal effects, offspring survival and development, social effects, Turdoides squamiceps. Journal of Animal Ecology (2007) 76, 750–760 doi: 10.1111/j.1365-2656.2007.01248.x

Introduction Natural selection favours those attributes that increase an individual’s reproductive success (Darwin 1859), and numerous studies have shown that early development can significantly affect reproductive success (Albon, Clutton-Brock & Guiness 1987; Clutton-Brock 1988; Lindström 1999), with maternal investment one of the primary factors affecting variations in early development between individuals (Clutton-Brock 1991; Mousseau & Fox 1998a). However, a mother’s capacity to invest in her young is affected by both environmental © 2007 The Author. Journal compilation © 2007 British Ecological Society

Correspondence and present address: Percy Fitzpatrick Institute, DST/NRF Centre of Excellence, University of Cape Town, Rondebosch 7701, South Africa. Tel.: +27 216503634/ 3291. Fax: +27 216503295. E-mail: [email protected]

and phenotypic characteristics (Clutton-Brock 1991; Lacey 1998; Gorman & Nager 2004), which can have long-term impacts on offspring survival, development and fitness (Lindström 1999; Lummaa & Clutton-Brock 2002; Badyaev 2005; reviewed in Mousseau & Fox 1998b). Maternal effects on offspring can be measured in several different ways, and include both maternal inheritance effects (the resemblance between a mother and her offspring for measured traits) and maternal selection effects (a direct influence on offspring fitness as a result of the mother’s actions) (Kirkpatrick & Lande 1989). In avian species, research has focused on several ways that mothers may influence the survival and development of young. Pre-laying, mothers may manipulate laying date and clutch size (Daan, Dijkstra & Tinbergen 1990), egg size (Cunningham & Russell 2000), or yolk levels of androgens (Groothuis et al.

751 Offspring survival in a cooperative bird

© 2007 The Author. Journal compilation © 2007 British Ecological Society, Journal of Animal Ecology, 76, 750–760

2005), directly affecting the behaviour, growth, survival and immune function of offspring. Post-hatching, the brooding and provisioning rate of both mothers and fathers often directly affects offspring survival and development (reviewed in Price 1998). However, research has focused primarily on species with biparental care, and the importance of maternal effects on young reared cooperatively remain relatively unknown (Russell et al. 2002; MacColl & Hatchwell 2004). Phenotypic traits that may affect the level of maternal investment in young, such as body mass, are often environmentally induced (Lacey 1998; Mousseau & Fox 1998a,b) and it is commonly difficult to disentangle the relative influence of maternal vs. environmental factors on offspring survival and development in non-experimental studies (see Kruuk, Merila & Sheldon 2003; Whittingham, Dunn & Nooker 2005). For example, females with access to high-quality resources are usually in better condition than females that have no such access, and this may result in considerable benefits for offspring born to mothers occupying favourable habitats (reviewed in Lindström 1999). However, resource quality is not necessarily determined primarily by environmental conditions. For example, in cooperatively breeding species where nonbreeding adults assist in rearing the young of a breeding pair, variation in the number of helpers may affect the amount and quality of resources received by young (Emlen 1997; Cockburn 1998). The presence of helpers may allow breeding females to reduce the amount of energy invested in raising each brood (known as ‘load-lightening’, see Crick 1992), without a corresponding reduction in offspring survival or development. In such cases, the influence of maternal effects on offspring survival and development may be reduced or even replaced by social effects. Previous studies on the benefits of helpers in cooperatively breeding birds have found that an increasing number of helpers positively influences offspring survival (e.g. Brown et al. 1982; Mumme 1992; reviewed in Cockburn 1998), although some recent studies have found no relationship (e.g. Magrath & Yezerinac 1997; Eguchi et al. 2002) or even a negative relationship (Legge 2000). This lack of conclusive evidence regarding the benefits of helping behaviour may be due to difficulties in separating social effects from environmental and maternal effects. A recent study on cooperatively breeding meerkats Suricata suricatta (Desmarest) using multivariate analyses revealed that social effects partially, but not wholly, replace maternal effects as important determinants of offspring survival (Russell et al. 2002). The costs of gestation and lactation in mammals (Creel & Creel 1991; Scantlebury et al. 2002) suggests maternal effects will remain an important influence on mammalian young reared cooperatively, and that social effects on offspring survival may vary considerably between cooperative societies of mammals and birds. Traditional measures of offspring survival in avian species focus primarily on the number of fledglings

produced (e.g. Brown 1987; Price 1998). However, this measure may not be appropriate for cooperatively breeding species, which are characterized by a prolonged period of post-fledging care (Langen 2000). During the post-fledging period, offspring are still highly dependent on adult group members for predator detection and food (Heinsohn 1991; Ridley 2003). Consequently, the amount of care received by young post-fledging may be crucial in understanding the relative importance of environmental, maternal and social effects on offspring survival. In addition, few studies have examined social effects on aspects of post-fledgling development, such as weight gain and the acquisition of foraging skills, yet social factors might be expected to affect this as well as survival. For example, Heinsohn (1991) found that the amount of food helpers provided to young post-fledging significantly affected the likelihood of overwinter survival in whitewinged choughs Corcorax melanorhamphos (Vieillot), while Langen (1996) suggested that white-throated magpie-jay Calocitta formosa (Swainson) fledglings may learn foraging skills from watching other group members. Developing good foraging skills may allow young to attain high body mass as adults, which is commonly associated with benefits such as attaining high social rank and the production of many or relatively heavy young (Choudhury, Black & Owen 1996; Wright et al. 2001; Legge 2002). If social factors are an important influence on offspring development, then estimates of the benefits of helpers based on offspring survival alone may underestimate the benefits of cooperative breeding for young. In this paper, I use multivariate analyses to investigate the influence of environmental, maternal and social factors on (1) offspring survival at all stages of development from hatching to maturity; (2) weight gain between fledging and independence; and (3) postindependent foraging success in the cooperatively breeding Arabian babbler Turdoides squamiceps (Cretzschamr). Arabian babblers are obligately cooperative and highly territorial, living in groups ranging from three to 22 individuals (Zahavi 1990). Breeding activity in this species is usually dominated by a single pair in each group (Lundy, Parker & Zahavi 1998), and all adult group members provide help during each breeding attempt (Ridley 2003). Females lay a clutch of three to four eggs, which are incubated for 12–14 days. Incubation starts at clutch completion, and hatching is synchronous. After hatching, young continue to receive care from adult group members for up to 3 months.

Methods      The study was conducted on habituated groups of Arabian babblers located in the Shezaf Nature Reserve, a 30 km2 area of alluvial plain in the Negev desert,

752 A. R. Ridley


southern Israel (30 ° 48 ′ N, 35 ° 13 ′ E). The area is classified as extremely arid, with sparse vegetation concentrated mainly in dry riverbeds. The vegetation is dominated by Acacia tortilis and A. radianna trees and low-lying shrubs, including Lycium shawii, Hammada salicornia and Zilla spinosa. Average annual rainfall during the study was 22 mm, representing drought conditions (Arava Regional Council Weather Station, Hatzeva). Most rain was concentrated around the start and end of the winter period, with no rain during the breeding season. The study population comprised 28 groups, averaging 4·8 (± 1·2) adults per group (range three to nine adults). All groups were habituated to allow observation from a distance of 2 – 3 m without causing any apparent distress. All birds were individually recognizable by a unique combination of one metal and three coloured rings. As it was not possible to determine sex from external characteristics until individuals reached adulthood, small blood samples (50 µL) were collected from nestlings via brachial venepuncture. Nuclear DNA was extracted using a standard phenol/chloroform/ isoamyl alcohol protocol and polymerase chain reaction-based molecular sex determinations were conducted using the method described by Fridolfsson & Ellegren (1999). There are three stages of offspring development in this species. Post-hatching, nestlings remain in the nest for a period of 12 –14 days before fledging. Newly fledged young are unable to fly, have limited mobility, and are entirely dependent on adults for food. Fledglings are defined as independent when they spend more than 90% of the time self-foraging rather than begging, and when more than 95% of their food intake is gained through self-foraging, which occurs approximately 8 weeks post-fledging. The period between independence and maturity, spanning approximately 8 months over winter, is the juvenile period of development. Juveniles were considered adults when they were 12 months old.

only four cases where an individual younger than 12 months old dispersed to a new group in 31 years of research on the study population.

 

  

Behavioural data were collected using both ad libitum and focal methods as described in Martin & Bateson (1986). During each breeding attempt, each group was observed three times a week for 3 – 4 h per observation session (mean ± SE number of observation hours per breeding attempt: 18·54 ± 1·6). Behavioural activities were recorded as they occurred, as well as the identity of the individuals involved and, in the case of provisioning behaviour, the size of the food item. In all cases, individual young could be clearly identified during each provisioning event. For each breeding attempt, the nest was checked daily so that exact hatching and fledging date was known. Nestlings and fledglings were considered to have died when they were no longer present in their natal group. For juveniles, missing individuals were considered dead, as there have been

Group size was measured as the number of adults present in each group at the start of each breeding attempt. For provisioning behaviour, both parent and helper contributions were measured as the total biomass of food provisioned to each nestling or fledgling by each adult per hour and then summed for all ‘parents’ or ‘helpers’ in each group to give a ‘total contribution’ value for each developmental stage. Food items were converted to a biomass value using the same method as described for juveniles above. ‘Helpers’ were defined as all subordinate adult group members, and ‘parents’ were defined as the dominant male and female in each group. Parentage analyses have shown there are very few extra-pair copulations in this species (Lundy et al. 1998), hence the division between parents and helpers was considered valid.

  Brood size was measured as the number of individuals in each brood at the start of each developmental stage. To calculate weight gain between fledging and independence, fledgling body mass was measured by enticing each individual on to a top-pan balance (400 ± 0·1 g) for a small food reward. Weight gain was measured as the difference in body mass of each fledgling at first light (before foraging began) and at the end of each observation session, 3–4 h later. Weight gain per hour was then calculated as the difference in body mass between the start and end of an observation divided by the number of hours in the session. All fledglings were weighed three times per week and weight gain per hour was averaged for the entire post-fledging dependent period for each individual. Body mass at independence was measured as the average weight of each juvenile at first light in the first week following independence. Juvenile foraging efficiency was measured as the amount of biomass captured per hour spent foraging and was measured by conducting 20-min focal observations on each juvenile three times a week for 6 months, or until death. During each focal, the amount of time spent foraging and the size and number of all food items captured by the focal individual was recorded. To calculate biomass, all food items were divided into four size classes and each size class was assigned an average weight derived from weighing 50 prey items representative of that class. Size classes were defined as follows: tiny = barely visible in bill, small = visible in bill, but not hanging out of bill, medium = larger than bill, less than 50% of item hanging out of bill, large = more than 50% of item hanging out of bill. Items larger than this were scored as multiples of the ‘large’ size category.


  Although maternal effects on offspring can encompass a broad range of measures, only the following could be measured in this study: body mass, age and brooding behaviour. Provisioning behaviour was considered a parental effect, and the combined provisioning effort of both the breeding male and female was measured as described above. Maternal body mass was measured in the week prior to egg-laying by enticing females to jump on to a top-pan balance at first light for a small food reward. Maternal age (number of months since hatching) was taken as the age of the breeding female in the week prior to egg-laying. The amount of time breeding females spent brooding per hour was measured during ad libitum observation sessions on each group and averaged over the whole nestling stage. Brooding was considered to have begun if the female visited the nest and settled on top of young rather than standing above them.

 


Environmental factors were measured by habitat surveys of each group territory. For each territory, a belt transect 10 m wide and covering the territory from edge to edge (territory edges are clearly defined by the width of the dry riverbeds crossing the reserve and range in width from 156 to 469 m) was laid every 100 m along the riverbed until the territory borders were reached. Territory borders were identified by the location of regular intergroup interactions. Each time two groups met and displayed aggressively at each other a GPS point was taken. Each GPS point was imported into a mapping document (MapSource version 3·0·2., Garmin, USA) to determine the location of regular intergroup interactions. Most were located in specific areas, and a territory border was defined as an area (20 m wide section of riverbed) where more than 25% of all recorded intergroup interactions occurred. The identity, height and width of all plants within each transect were recorded and the density of plants per hectare was calculated for each territory. Plant diversity was measured using the Simpson’s Diversity Index (Simpson 1949), which measures the probability of picking two plants at random that are of the same species. Habitat type was classified as modified or unmodified according to territory location within the reserve (unmodified) or within agricultural farmland surrounding the reserve (modified). Modified habitats contained roads, areas of open water, and netting, all of which have caused mortalities in the study population in previous years (A. Zahavi, pers. comm.). However, modified habitats also contained irrigated land and agricultural produce as potential additional food resources for foraging babblers.

  For each developmental stage (time to fledging, independence and adulthood), a Generalized Linear Mixed

Model (GLMM) was used to investigate the factors affecting offspring survival. Survival was used as the response variable (where 0 = died and 1 = survived) in GLMMs using a binomial distribution and logit link function in Genstat 8·1 (8th edn, Lawes Agricultural Trust Rothamstead, UK). To determine the overall importance of environmental, social or maternal factors on offspring recruitment to the adult population, an additional GLMM analysis of the factors affecting survival over the entire period from hatching to adulthood was conducted. For each model, group and brood identities were fitted as random terms to control for the effect of repeated measures on the distribution of the data. All two-way interactions were tested, but only those that were significant are presented. The method of fitting data to GLMMs followed Crawley (2002). All terms were added to each GLMM and then sequentially dropped until only those terms whose elimination would have significantly reduced the explanatory power of the model were retained (the minimal model). The significance of each term included in the minimal model was determined by dropping it from the minimal model. The P-value for eliminated terms was determined by adding each individually to the minimal model. The potential explanatory terms fitted were: (1) offspring characteristics [brood size, body mass, sex, foraging success (juvenile period only)]; (2) environmental factors (plant diversity, habitat type); (3) maternal factors [body mass, age of breeding female, time spent brooding young (nestling period only)]; (4) social factors (group size, biomass fed to young per hour by helpers); and (5) parental factors (biomass fed to young per hour by both parents). Only young that survived previous developmental stages were included in analyses of survival for subsequent developmental stages. For the analysis of factors affecting weight gain between fledging and independence, the average weight gain per hour of each fledgling over the entire postfledging dependent period was used as the response variate in a LMM (Linear Mixed Model) with an identity link function. Group and brood identity were included as random terms in the model. The analysis of factors affecting foraging success post-independence used the average foraging success of each juvenile in the 6 weeks following independence as the response variate in a LMM (using an identity link function). Six weeks after independence, several individuals died, and thus the foraging efficiency of all juveniles was averaged for the time period prior to first juvenile death to avoid inflated estimates of foraging success for juveniles that lived longer. The potential explanatory terms used for both development models were similar to those described above for the analyses of factors affecting survival. As the inclusion of terms that are strongly associated with each other together in GLMM analysis can lead to spurious estimates of significance, the association between all potential explanatory terms was checked prior to analysis using linear regression for the association between two variables and one-way  for the

754 A. R. Ridley

association between a variable and a factor. Where necessary, data were transformed to meet the assumptions of normality. There was no relationship between maternal factors and any environmental or social factors, nor was there a relationship between any of the environmental and social factors used, thus all terms were included in GLMM analyses together. Within categories of explanatory terms (e.g. environmental factors), when two terms were highly associated (P < 0·05)

the one that contributed most to model explanatory power was retained. This was determined by adding both terms separately to the full model, the P-values generated from their addition compared, and the one with the least significant value dropped from the model before backward elimination to determine the minimal model occurred. Throughout the text, unless stated otherwise, means are expressed with standard errors, and null hypotheses are rejected at P < 0·05.

Results      There were a total of 65 breeding attempts by 28 groups during the study, 10 of which were abandoned during the nest-building stage. Of 142 eggs laid, 115 (81·0%) hatched and 84 nestlings (73·0%) fledged. Nestling survival to fledging was influenced by social, environmental and maternal factors. The primary determinant of survival was the amount of food received from helpers. Nestlings that received a high biomass of food per hour from helpers were more likely to survive (Fig. 1a). In contrast, there was no effect of parental provisioning rates on nestling survival (Table 1). Environmental factors were also important, with nestlings in territories with high plant diversity more likely to survive (Table 1). Independently of environmental and social effects, males, who are slightly larger than females as adults [average morning weight of adult males: 72·43 ± 3·88 g (n = 62), adult females: 67·60 ± 3·63 g (n = 48)], were more likely to survive if maternal body Table 1. GLMM model (binomial distribution with a logit link function) of the terms associated with nestling survival to fledging. Analysis was conducted on 115 nestlings from 39 broods in 21 different groups. Group and brood identity were included as random terms in the model

Model term

Wald statistic (χ2) d.f. P

Minimal model Constant Biomass received 7·58 from helpers per h Maternal weight × nestling sex male nestlings 5·90 female nestlings Plant diversity 4·97 Maternal weight 0·43 Nestling sex males 0·01 females


Fig. 1. Offspring survival (where 0 = died and 1 = survived) to (a) fledging (b) independence and (c) from hatching to adulthood, in relation to average biomass received from helpers per hour. The biomass received from helpers was summed for all helpers in each group and divided by the number of observation hours over the time period between (a) hatching and fledging, (b) fledging and independence and (c) hatching and independence. Raw data values are displayed. Lines of best fit are generated from the predictions of the binomial GLMMs presented in Tables 1, 2 and 4.

Additional terms tested Maternal brooding 1·23 rate (min h–1) Biomass received 1·18 from parents per h Group size 0·87 Brood size 0·46 Maternal age 0·09 Habitat type 0·08

Average effect SE

–7·22 1·24

3·50 0·48

1·56 0·61 0·52 0·30

0·30 0·39 0·21 0·20

0·74 0·63

0·90 0·75

0·28

1·95

1·85

0·35 0·50 0·77 0·77

0·28 3·39 0·01 0·64

0·35 1·88 0·01 1·65

1

0·01

1

0·02

1 1

0·03 0·53

1

0·93

1

0·27

1 1 1 1 1


Fig. 2. The proportion of all nestlings of each sex laid by each female over the entire study period that survived to fledge in relation to average maternal body mass in the week prior to egg-laying. Raw data values are displayed.

mass was high prior to egg-laying (Fig. 2). Pre-laying maternal body mass averaged 68·5 ± 2·6 g (range 63·2– 73·5 g) for all breeding females in the study population. For females with a pre-laying body mass lower than average (n = 18), 54·8% of males nestlings died, compared with 20·0% of male nestlings for females with above average body mass (n = 10 females).

     Of 84 nestlings that survived to fledge, 55 (65·4%) survived to independence. This period of offspring development was the period of highest mortality. Similar to the nestling stage, the amount of food received from helpers was the most important predictor of survival (Table 2). Fledglings that survived to independence received an average of 0·48 ± 0·07 g of food per hour from helpers, compared with an average of 0·33 ± 0·08 g h–1 for those fledglings that died (Fig. 1b). Environmental factors were also an important determinant of fledgling survival (Table 2). In modified habitat, 68·1% of fledglings survived to independence, compared with only 26·3% of fledglings from groups occupying unmodified habitat. There was no influence of maternal factors or parental provisioning rates on offspring survival at this stage of development (Table 2).

    


Of 55 fledglings that survived to independence, 41 (74·6%) survived to adulthood. Foraging efficiency was the only significant determinant of juvenile survival (Fig. 3). The average foraging efficiency of juveniles that died was 2·07 ± 0·46 g per foraging hour, compared with 5·86 ± 0·79 g per foraging hour for those that survived. None of the maternal or environmental factors measured affected offspring survival during this stage of development (Table 3).

Fig. 3. Juvenile survival to adulthood in relation to average foraging efficiency (grams caught per foraging hour) in the 6-week period following independence. Raw data values are displayed. The line of best fit is generated from the predictions of the binomial GLMM presented in Table 3.

Table 2. GLMM model (binomial distribution with a logit link function) of the terms associated with fledgling survival to independence. Analysis was conducted on 84 fledglings from 23 broods in 15 different groups. Group and brood identity were included as random terms in the model

Model term


Minimal model Constant Biomass received 5·64 from helpers per h Habitat type unmodified 4·50 modified Additional terms tested Plant diversity 0·76 Group size 0·61 Maternal weight 0·22 Brood size 0·20 Fledgling sex 0·17 Biomass received 0·05 from parents per h Maternal age 0·01

Average effect SE

1

0·02

–1·38 4·23

0·75 1·78

1

0·03 –0·96 1·44

0·46 0·52

1 1 1 1 1 1

0·38 –0·24 0·44 0·11 0·64 0·03 0·65 0·50 0·68 0·24 0·83 0·21

0·21 0·22 0·14 0·78 0·90 0·89

1

0·93 –0·01

0·01

       From 115 young hatched during the study period, 41 (35·7%) survived to adulthood. Overall, parents provided less biomass to offspring than helpers (overall average across all groups: parents: 0·31 ± 0·06 g h–1, helpers 0·42 ± 0·05 g h–1). Even in groups containing an equal number of parents and helpers (group size = 4 adults, n = 8 groups), helpers tended to provide more food to young than parents (parents: 0·34 ± 0·09 g h–1, helpers: 0·40 ± 0·10 g h–1). The amount of food received by helpers was a primary determinant of survival from hatching through to adulthood (Fig. 1c, Table 4). Individuals that survived to adulthood received an

756 A. R. Ridley

Table 3. GLMM model (binomial distribution with a logit link function) of the terms associated with the survival of juveniles over the winter period. Analysis was conducted on 55 juveniles from 11 different groups. Group identity was included as a random term in the model

Model term

Wald statistic (χ2)

d.f.

P

Average effect SE

Minimal model Constant Foraging success

5·66

1

0·02

0·04 0·49

0·52 0·21

Additional terms tested Group size 1·05 Habitat type 0·94 Juvenile sex 0·85 Maternal weight 0·50 Plant diversity 0·45 Maternal age 0·13

1 1 1 1 1 1

0·31 0·40 0·33 1·05 0·36 0·69 0·48 –0·11 0·51 –0·22 0·71 0·01

0·37 1·12 0·83 0·16 0·33 0·01

Table 4. GLMM model (binomial distribution with a logit link function) of the terms associated with the survival of offspring from hatching to adulthood. Analysis was conducted on 115 offspring from 39 broods in 21 different groups. Group and brood identity were included as random terms in the model

Model term Minimal model Constant Biomass received from helpers per h Habitat type unmodified modified


7·00

5·70

Additional terms tested Group size 2·09 Maternal weight 1·46 Maternal brooding 1·35 rate (min h–1) Chick sex 1·00 Maternal age 0·77 Brood size 0·30 Plant diversity 0·14 Biomass received 0·08 from parents per h


1

0·01

Average effect SE

2·93 4·56

0·87 1·72

1

0·02 –2·93 0·07

0·67 0·89

1 1 1

0·15 0·47 0·23 –0·25 0·25 –0·01

0·30 0·17 0·01

1 1 1 1 1

0·32 0·73 0·38 0·01 0·58 –0·08 0·71 –0·02 0·77 0·34

0·70 0·01 0·32 0·21 1·36

average of 0·49 ± 0·10 g h–1 from helpers during the nestling and post-fledging dependent stages combined, compared with 0·34 ± 0·06 g h–1 for those that died. Environmental factors were also an important determinant of survival from hatching to adulthood (Table 4). Of 46 nestlings in groups occupying modified habitat, 29 (63·0%) survived to adulthood, compared with 12 of 69 nestlings (17·4%) from groups occupying unmodified habitat. There was no effect of any of the maternal factors measured on overall offspring survival from hatching to adulthood (Table 4).

Fig. 4. Average weight gain per hour for each fledgling in the time period between fledging and independence in relation to average biomass received from helpers per hour. Raw data values are displayed. The line of best fit is generated from the predictions of the LMM presented in Table 5. Table 5. LMM model (with an identity link function) of the terms associated with average fledgling weight gain per hour between fledging and independence. Analysis was conducted on 84 fledglings from 23 broods in 15 different groups. Group and brood identity were included as random terms in the model

Model term


Minimal model Constant Biomass received 6·22 from helpers per h Additional terms tested Biomass received 1·21 from parents per h Maternal age 1·04 Plant diversity 1·04 Habitat type 1·01 Brood size 0·80 Maternal weight 0·44 Group size 0·14 Fledgling sex 0·03

Average effect SE

1

0·01

0·77 0·75

0·09 0·30

1

0·27 –0·43

0·38

1 1 1 1 1 1 1

0·31 0·01 0·31 0·08 0·32 –0·27 0·37 0·13 0·51 0·02 0·71 0·02 0·86 –0·03

0·01 0·06 0·22 0·12 0·03 0·06 0·17

   Fledglings were lighter than adults at the time of fledging (average fledgling weight: 41·76 ± 0·90 g average adult weight: 70·75 ± 0·50 g). The period between fledging and independence was an important growth stage for young, with individuals gaining an average of 44·4 (± 5·6)% of their fledging body mass (average weight gain 18·55 ± 0·81 g). Fledglings regularly provisioned by helpers gained the most weight per hour between fledging and independence (Fig. 4). Neither maternal nor environmental factors had a significant effect on weight gain during this period (Table 5). The heaviest fledglings at independence subsequently developed the best foraging skills as juveniles (Fig. 5, Table 6). The average body mass at independence of juveniles with high foraging success postindependence (where high is equivalent to average adult foraging success ± 1 SD) was 63·2 ± 1·6 g (n = 21),


Fig. 5. Average foraging success for each juvenile in the 6 weeks following independence in relation to body mass at independence. Raw data values are displayed. The line of best fit is generated from the predictions of the LMM presented in Table 6.

Table 6. LMM model (with an identity link function) of the terms associated with juvenile foraging success. Analysis was conducted on 55 juveniles from 11 different groups. Group identity was included as a random term in the model Average effect SE

Wald statistic (χ2)

d.f.

P

4·74

1

0·03

3·62 0·14

0·43 0·06

Additional terms tested Habitat type 3·59 Maternal weight 2·40 Juvenile sex 1·57 Maternal age 0·52 Group size 0·23 Plant diversity 0·01 Constant 3·62

1 1 1 1 1 1

0·06 0·10 0·12 0·13 0·21 –0·40 0·47 0·01 0·63 0·13 0·97 0·33 0·43

0·06 0·08 0·51 0·01 0·15 0·67

Model term Minimal model Constant Body mass at independence

compared with 59·4 ± 1·1 g (n = 34), for juveniles with low foraging success.

Discussion


A comparison of the importance of social vs. maternal and environmental effects on offspring survival and development in the Arabian babbler has revealed that maternal effects are an important influence during the nestling stage only. Similar to findings from several species of mammals and birds (Clutton-Brock 1988; Bradbury & Blakey 1998; Cameron 2004), high maternal body mass prior to reproduction increased the likelihood of survival for the largest sex. As with many other cooperatively breeding species (Langen 2000), there was an extended period of post-fledging care in Arabian babblers. This was the period of highest mortality and thus a crucial development period for young, yet maternal effects had no influence on survival during this critical time. Rather, offspring survival was determined primarily by social and environmental

factors. Thus, in this species, factors affecting offspring survival differ from those in many noncooperative avian species, where maternal effects are commonly an important influence (Mousseau & Fox 1998a). This result also differs from a similar study of the cooperatively breeding long-tailed tit Aegithalos caudatus (Reichenbach), where the provisioning effort of mothers was an important determinant of offspring survival (MacColl & Hatchwell 2004). The likely reason for this difference is that the long-tailed tit is a facultative cooperative breeder, with individuals becoming helpers only when their own breeding attempts fail (MacColl & Hatchwell 2004). When the contribution of helpers is unpredictable, selection may be unlikely to act on females to reduce investment in young. In contrast to maternal effects, environmental factors affected offspring survival from hatching to maturity in the Arabian babbler, supporting the findings of previous studies suggesting strong environmental influences on the survival of young (e.g. Larsson & Forslund 1991; Cohen & Lindell 2004; Adams, Skagen & Savidge 2006). In the Arabian babbler, groups occupying high-quality territories produce significantly more young that survive to maturity than groups occupying low-quality territories, suggesting that individuals may gain more fitness benefits by helping and waiting for a breeding position in high-quality territories than dispersing and attempting to breed in lowquality territories (as predicted by Emlen 1982). This is confirmed by the dispersal patterns prevalent in this species, with individuals in modified territories with access to additional food resources significantly less likely to disperse than individuals in unmodified territories without access to such resources (Ridley 2003). In addition to environmental factors, social factors strongly influenced offspring survival. Previous studies investigating social effects on offspring survival commonly cite group size as an important factor (Emlen 1997; reviewed in Cockburn 1998), particularly in areas of high predator density (Clutton-Brock et al. 1999), yet in the Arabian babbler a group size effect was not evident during any stage of development. This was despite a high predator density in the study area, with many predators attracted by the refuse and open water in human-modified areas surrounding the reserve (A. Ridley, unpublished data). Rather, another social effect, helper contributions to provisioning young, remained a consistent determinant of offspring survival through all stages of development from hatching to maturity. This suggests that studies using correlations between group size and offspring survival may misrepresent the effect of helpers. For example, Woxvold & Magrath (2005) found that although there was a positive relationship between group size and annual fledgling production in the apostlebird Struthidea cinera (Gould), this was a consequence of the number of birds that fed nestlings, and group size was not a significant predictor of fledgling production after controlling for helper contribution. Thus, in species where all group members

758 A. R. Ridley


do not help equally, such as Arabian babblers (Ridley 2003), a negligible relationship between group size and helper contribution may be expected. The strong effect of helpers on offspring survival confirms that helpers in this species contribute substantially to group reproductive success, and are not ‘hinderers’ (Legge 2000; Dickinson 2004) or ‘transients’, simply remaining within a group until breeding or dispersal opportunities become available (e.g. Magrath 2001; Kokko & Ekman 2002). It is unlikely that the positive association between helper provisioning behaviour and offspring survival in Arabian babblers is simply a consequence of high-quality parents retaining more offspring on their territory (Magrath 2001) because (1) helper contributions are a significant predictor of offspring survival independently of group size, and (2) complex group types are relatively common (Zahavi 1990; Ridley 2003), such that helpers may be unrelated to one or more member of the breeding pair. Thus, although helpers enhance the reproductive success of breeders, suggesting some support for kin selection theory (Hamilton 1964), the occurrence of helpers unrelated to the breeding pair suggests kin selection is not a sufficient explanation for the occurrence of all helping behaviour in this species. High rates of provisioning by helpers not only increased offspring survival, but also provided developmental benefits, reflected in high rates of postfledging weight gain and acquisition of foraging skills. High body mass and foraging efficiency could benefit juveniles in several ways. First, they may act as a buffer against weight loss during the winter period when food is scarce (e.g. Heinsohn 1991). Second, juveniles with high body mass may be more likely to become dominant over their broodmates and recruited into the breeding population (Both, Visser & Verboven 1999). Thus, the developmental advantages of high body mass and foraging efficiency in fledglings that received a high level of provisioning from helpers may confer longterm benefits, as observed in other species (e.g. Blums, Clark & Mednis 2002; Hatchwell et al. 2004; Jensen et al. 2004), as individuals that attain dominance in the Arabian babbler are commonly the heaviest adults in their group (Wright et al. 2001). Although helper contributions were found to influence offspring survival and development, several recent studies have suggested that such results could be correlational owing to environmental covariance (e.g. Stinchcombe et al. 2002; reviewed in Kruuk et al. 2003). There are some trends in this study that suggest this may not be the case. For example, if helper provisioning rates are influenced directly by food availability, then we would expect to see that helpers in high-quality territories would feed young at higher rates than helpers in groups not occupying such territories. However, this was not the case, suggesting that either (1) helper provisioning rates are a direct reflection of helper effort rather than territory quality, or (2) the territory quality measures used in this study did not

appropriately account for the difference in food availability between territories. Experimental studies are required to truly determine the relationship between environmental and social effects on offspring survival for this species. The high rate of mortality between fledging and independence, and the importance of helper contributions to fledgling survival and development emphasizes the importance of investigating post-fledging care when considering social effects on offspring in cooperative societies. Traditional measures of social effects on offspring survival have focused primarily on the number of fledglings produced (e.g. Brown 1987; Cockburn 1998), yet the results presented here indicate that such measures would underestimate the effect of helpers because (1) there is significant post-fledging mortality when young are still highly dependent on adults for food, and (2) overwinter survival of young is strongly influenced by juvenile foraging success, which is in turn determined primarily by the amount of food received from helpers post-fledging, suggesting that the benefits of helpers are evident right through to adulthood. Previous studies have found that early development can significantly affect lifetime reproductive success (e.g. Albon et al. 1987; Clutton-Brock 1988; reviewed in Lindström 1999), and the relative absence of maternal effects but the strong effect of helper contributions on offspring survival and development in the Arabian babbler suggests that social effects may have long-term impacts on offspring fitness in this species. However, it is important to note that despite little evidence for maternal effects on offspring survival in Arabian babblers, there are a number of maternal effects (such as hormonal allocation pre-laying, Groothuis et al. 2005) not measured here that could be influencing offspring survival in this species.

Acknowledgements Thanks to Amotz and Avishag Zahavi for introducing me to the babblers and for their continual guidance, encouragement and thoughtful discussions. Thanks also to Tim Clutton-Brock, Phil Hockey, Sarah Hodge, Andy Radford, Andy Russell, Andy Young and three anonymous referees for helpful comments and advice. Kat Munro, Matthew Bell, Kate Smith, Anat Shapira and Sarah Ross-Viles provided valuable help with fieldwork. Paulette Bloomer and Kate Huyvaert helped out with the molecular sexing analyses. This research was supported by grants from The Cambridge Commonwealth Trust, Wingate Scholars Committee, New Zealand Federation of University Women, and the Worts Travelling Scholars Program.

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