Behav Ecol Sociobiol (2002) 51:336Ð344 DOI 10.1007/s00265-001-0441-3

ORIGINAL ARTICLE

Memuna Z. Khan á Jeffrey R. Walters Effects of helpers on breeder survival in the red-cockaded (Picoides borealis)

Received: 14 March 2001 / Revised: 9 November 2001 / Accepted: 15 November 2001 / Published online: 16 January 2002 © Springer-Verlag 2002

Abstract Helpers can gain future indirect fitness bene- Introduction fits by increasing the survival of breeders that produce offspring related to the helper. Helping augments group Historically, helping behavior has posed an evolutionary size through the helper’s presence and, in some cases, by paradox, because helpers seem to enhance the fitness of increasing fledging success. Breeders may then experi- other individuals at their own expense. This paradox is ence enhanced survivorship because of the benefits of addressed by considering how helping behavior might living in large groups. Helping may also reduce the enhance a helper’s own fitness. Helpers may gain indi- workload of the breeder, which in turn may increase the rect fitness benefits if they increase the production of likelihood that the breeder will survive to breed again. non-descendent kin (Hamilton 1964). Indirect fitness We used Cox’s proportional hazards model to examine benefits may be gained during the current breeding sea- whether breeders’ survival in two populations of the red- son if a helper increases the production of offspring by cockaded woodpecker (Picoides borealis) was enhanced related breeders, or in future breeding seasons, if a help- when group size was increased in the presence of (1) the er increases the probability that related breeders will sur- helper itself, or (2) “extra” fledglings (fledglings pro- vive to reproduce again (Mumme et al. 1989). duced by the breeder because of helping behavior). We Two general mechanisms have been proposed to ex- found that in the presence of helpers, the risk of a breed- plain enhanced breeder survival in the presence of help- er dying declined by 21Ð42% for males and 0Ð14% for ers: decreased breeder workload (Brown 1974, 1978; females. Our results suggest reduced breeder workload Ricklefs 1975; Brown et al. 1978; Ligon and Ligon as one mechanism to explain reduced breeder mortality 1978), and benefits of group living (Hamilton 1971; in the presence of helpers: breeders spent less time incu- Pulliam 1973). Breeders may profit in several ways if bating and provisioning nestlings when assisted by help- they expend less effort on current reproduction when as- ers. The risk of a breeder dying declined by 16Ð42% in sisted by a helper. Helpers will receive fitness benefits if males and 26–43% in females in the presence of “extra” breeders are more likely to survive to breed again or pro- fledglings. We speculate on possible mechanisms by duce more offspring in subsequent years when the breed- which fledglings might affect breeder survival. Our re- er’s workload is reduced. Breeders may experience en- sults support the hypothesis that helpers gain future indi- hanced survivorship because of the benefits of group liv- rect benefits by reducing breeder mortality. ing, such as decreased predation and increased foraging efficiency (Pulliam and Caraco 1984). The helper in- Keywords Red-cockaded woodpecker á Picoides creases the group’s size, both by their own presence and borealis á Co-operative breeding á Breeder survival by augmenting the number of fledglings produced by the breeding pair. Red-cockaded (Picoides borealis) occur Communicated by J. Dickinson in groups that consist of a pair of breeders and 0Ð4 non- breeding adult helpers (Ligon 1970; Lennartz et al. 1987; M.Z. Khan (✉) á J.R. Walters Walters et al. 1988; Walters 1990; Haig et al. 1994). Not Department of Biology, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061-0406, USA all breeding groups have helpers and most groups that do have only a single helper (Walters et al. 1992). Helpers Present address: are usually previous male offspring of either the breed- M.Z. Khan, Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ 08544, USA, ing male or both breeders, but helpers sometimes assist e-mail: [email protected], older siblings or other male relatives that have inherited Tel.: +1-609-2586788, Fax: +1-609-2582712 the natal territory,and occasionally aid unrelated breed- 337 ers. Helpers participate in territory defense, constructing USFWS band and a unique color band combination. Adults were and maintaining nest and roost cavities, incubating eggs, identified during repeated visits to each occupied territory. If a ’s identity was uncertain, the group was followed or the bird feeding and brooding nestlings, removing fecal sacs was captured to verify its identification. Walters et al. (1988) esti- from the nest cavity, and feeding fledglings. Helpers ac- mated that 94% of the were censused each year. The status quire breeding status either through inheritance of the (e.g., helper, breeder, floater) of each individual was determined natal territory or by filling neighboring breeding vacan- based on several criteria described in detail in Walters et al. (1988). The breeding system is monogamous, even in groups with cies (Walters et al. 1988). unrelated male helpers (Haig et al. 1994). Some males and a few Previous work has shown that red-cockaded wood- females remain on the natal territory as helpers at age 1. They may pecker helpers gain current indirect fitness benefits by remain as helpers for 1Ð7 years, until they disperse or inherit improving the reproductive success of the breeding pair breeding status on the natal territory (Walters et al. 1992). (Heppell et al. 1994), to which they usually are related Reproduction was monitored by visiting the cavity trees of each group every 9Ð14 days during the breeding season. Nestlings (Haig et al. 1993, 1994). Here, we test the hypothesis are altricial and were banded between 6 and 10 days after hatch. that helpers gain future indirect fitness benefits by en- Fledging occurs 26Ð29 days after hatch and fledglings were identi- hancing the survival of related breeders. We examined fied by following groups after the projected fledging date. Fledg- the survival of breeders as a function of group size in lings were sexed by the presence (male) or absence (female) of a red crown patch. Pairs normally produce only one brood a year, two populations of red-cockaded woodpeckers. Territory but will re-nest if nest failure occurs early in the breeding season quality may confound analyses of mortality as a function (Jackson 1994). of group size, if group size correlates with the quality of the site. Therefore, we analyzed the data using two mod- els: one excluding and one including effects of territory Breeder workload quality on survival. To determine if breeders reduced We conducted 1-h nest watches in the morning (0600Ð1200 hours) their workload when assisted by a helper, we sampled in- and afternoon (1201Ð1800 hours) to determine incubation effort of cubation and nestling provisioning of pairs with and eight unassisted pairs and five pairs with one male helper in the without a helper. Sandhills during the 1996 breeding season. We measured incuba- tion effort as the proportion of the observation period during which the nest was incubated. We pooled observations taken throughout the day because time of day had no effect on incuba- Methods tion effort (n=14, t=Ð1.69, P=0.11). In 1994, we observed each nest for 1.5 h to measure the nes- Study areas tling provisioning behavior of six pairs assisted by a helper. In 1996, we conducted 2-h observations on 11 assisted and 14 unas- Red-cockaded woodpeckers are endemic to pine forests of the sisted pairs. We analyzed data from morning and afternoon obser- southeastern United States. One study population of red-cockaded vations separately because the hourly feeding rate (all feedings of woodpeckers is located in longleaf pine (Pinus palustris) forest in nestlings by all group members) varied significantly according to the Sandhills region of south-central North Carolina, occupying the time of day (Wilcoxon signed ranks test: D=419.5, P<0.001). the Fort Bragg Military Reservation, the Sandhills Game Lands, We combined data across years because the feeding rate at a given and the resort towns of Southern Pines and Pinehurst. Detailed de- time of day did not differ between years (n=28, df=26; morning scriptions of the Sandhills study area are provided in Carter et al. samples: t=0.65, P=0.52; afternoon samples: t=1.82, P=0.08). We (1983) and Walters et al. (1988). measured feeding effort as the number of feedings per nestling per The Coastal Plain study area, located along the southeastern hour (f/n/h) because feeding rates increase linearly with brood size coast of North Carolina, includes Camp LeJeune Marine Base and both in the morning (F1,29=20.54, P<0.0001) and afternoon (F1, Croatan National Forest. Red-cockaded woodpeckers are concen- 29=25.99, P<0.0001). Mean brood size of unassisted pairs trated in pine flatwoods and pine/scrub oak communities in both (mean±SE; 2.64±0.17) was equal to that of assisted pairs longleaf and loblolly pine (Pinus taeda) (Walters et al. 1995). De- (2.71±0.21, df=29, t=Ð0.23, P=0.82). We conducted observations scriptions of the Coastal Plain study areas are provided in Zwicker when nestlings were 10Ð16 days old. Over this span of ages, the and Walters (1999) and Walters et al. (1995). total feeding rate (f/n/h) was unaffected by nestling age (n=63, morning: F1, 61=0.07, P=0.80; afternoon: F1,61=1.35, P=0.25). We used Kolmogorov-Smirnov tests of normality to determine Demographic data whether to use parametric or non-parametric statistical tests. We conducted two-tailed tests for differences between incubation and Demographic data were collected for 17 years (1980Ð1997) from feeding rates of breeders in groups with a helper and those without the Sandhills population, and 10 years from Camp LeJeune and a helper, using a two-sample t-test or Mann-Whitney test. Croatan National Forest, respectively. The western half of the Sandhills population (approximately 220 groups on 110,000 ha) and the entire Coastal Plain population (approximately 100 Risk analyses without controlling for territory quality groups) were completely marked and monitored. A complete de- scription of monitoring methods can be found in Walters et al. We analyzed breeder survival, measured as the life-span of an in- (1988). Briefly, censuses were conducted annually during the dividual, using PROC PHREG (SAS 6.12). The PHREG proce- breeding season, from early April to mid-July, to identify all mem- dure is a semi-parametric method that uses Cox’s proportional bers of each group of red-cockaded woodpeckers. Annual mortali- odds model to estimate how particular variables influence the sur- ty was estimated by the proportion of birds identified in the annual vival time of a subject. Although these methods are called survival census that were not seen in subsequent censuses (Walters et al. analyses, the model actually estimates rates of death or hazards. 1988). Censuses were conducted once a year, so detailed analyses The model is expressed as follows: of the timing of death (during the breeding season, after the breed- (1) ing season) were not possible. During each breeding-season census, all unbanded immigrants where the log hazard function (h) for individual i at time t (mea- and nestlings were marked with a uniquely numbered aluminum sured as an individual’s age at death, or life-span) is a function of 338 has a χ2 distribution, to determine if estimated regression coeffi- cients are significantly different from zero. Details for calculating the Wald statistic are presented in Allison (1995). PHREG calcu- lates a hazard ratio, which is the ratio of the rate of death when a single variable is increased by a single unit (x+1), to the rate of death when the variable is equal to x, holding all other variables constant. The hazard ratio is more easily interpreted by calculating the percent change in the rate of death [%∆=(hazard ra- tioÐ1)*100]. When %∆ is negative, a one-unit increase in a single variable, holding all other variables constant, results in a %∆ de- crease in the rate of death. We assessed model fit by using the likelihood ratio to deter- mine if the alternative model containing k regression coefficients β β ( 1..... k, likelihood=lk) explains the observed data more accurate- ly than the null model, in which no variable influences survivor- β β ship ( 1..... k=0; likelihood=l0). Under the hypothesis of no differ- χ2 ence between the two models, the likelihood ratio (l0/lk) has a distribution with degrees of freedom df=k (Allison 1995).

Risk analyses controlling for territory quality

To control for territory quality, we included an extra term in our survival analysis model: (2) where the life-span of an individual was a function of the baseline hazard function, (α(t)) the number of adults on the territory rela- tive to the territory average (Dadults), the number of fledglings rela- tive to the territory average (Dfledge) and an index of territory qual- ity (Tavg), the average group size on a territory over the time peri- od that the territory has been in the monitoring study, including Fig. 1 The probability of breeder survival is a function of age for the year the breeder died. Dadults was calculated as the difference both female (A) and male (B) breeders. The probability of survival between the number of adults (i.e., breeding pair and helpers) re- is measured as the probability that the bird will be resighted in the siding on the territory in the year a breeder died and the mean next year. Data from the Sandhills population are shown number of adults on the territory over the entire study period. Dfledge was calculated as the difference between the number of fledglings residing on the territory in the year a breeder died and the baseline hazard function, α(t), and the independent variables the mean number of fledglings produced per year on the territory Adults (number of adults in the group) and Fledglings (number of for the entire study period. fledglings in the group). The baseline hazard function [α(t)] is left Our index of territory quality, and representation of group size unspecified in PHREG, allowing it to control for age effects on as deviations from the territory average, was justified because β β group size, habitat quality measures (J.R. Walters and S.J. Daniels, mortality (Fig. 1). The regression coefficients, 1 and 2, reflect the degree to which each variable in the model increases the prob- unpublished data) and fledgling production are highly correlated ability of mortality before a given time. We used two measures of (Walters 1990). group size the year the breeder died to discriminate between the effect of the presence of the helper(s) itself and the helper’s aug- mentation of group size through the production of fledglings. We included only birds of known age in the analysis. The last Results year of observation was 1997, so all breeders observed in 1997 were labeled as censored (not dead by the end of the study period). Breeder workload Breeders not observed in 1997 were presumed dead. Male breed- ers rarely disperse (Walters et al. 1988; Daniels 1997), so presum- ing they had died rather than dispersed is reasonable. About 10% The cumulative time eggs were incubated by all group of breeding females disperse per year, but most move only short members in groups of three adults (pairs with a helper; distances (Daniels and Walters 2000), and thus would not leave 94% of observation time), although higher, was not sta- the study area (Walters et al. 1988). We assumed that the few in- tistically different than that of groups of two (pairs with- stances of undetected dispersal of breeding females out of the out a helper; 90%; df=11, t=Ð1.44, P=0.18). Male and fe- study area were independent of group size. We modeled ties in the data using the Discrete option, which male breeders significantly reduced their individual in- assumes that when two or more events appear to happen simulta- cubation effort in the presence of helpers (Fig. 2: male neously, there is no underlying . This assumption is reason- breeder: t=3.7, P=0.01; female breeder: Mann-Whitney able because our census methods are discrete; the age of death for W=72, P=0.02). an individual can only be an integer value expressed in years. The Comparing total feedings among groups, the mean odds that individual i dies at time t is Oit=Pit/(1ÐPit), where Pit is the conditional probability that individual i dies at time t, given hourly feeding rate of pairs with a helper (a.m., that individual i has not died already. The model assumes that the 7.79±2.12; p.m., 6.02±1.71) was not statistically differ- ratio of the odds for any two individuals Oit/Ojt does not depend ent from that of pairs without a helper (a.m., 6.36±2.17, on time,which is reasonable for this because yearly varia- tion in mortality is low (Walters et al. 1988). The Discrete option t=Ð1.39, P=0.18; p.m., 5.62±1.32, t=Ð1.41, P=0.17), al- for ties in PHREG estimates regression coefficients using methods though the trend was for pairs with a helper to feed of partial likelihood. PROC PHREG uses the Wald statistic, which more. During the morning hours, individual feeding rates 339

Fig. 2 Incubation effort (+1SE) measured as proportion of obser- vation time spent incubating by female breeders, male breeders, and male helpers. Unassisted pairs (n=8) and pairs assisted by a single helper (n=5) were observed during the 1996 breeding sea- son of breeding males and females were no different in groups with or without helpers. During the afternoon hours, however, the feeding rate of male breeders was significantly lower in the presence of a helper, and feed- ing rates of female breeders exhibited a similar, margin- Fig. 3 Feeding effort (+1SE), measured as mean number of feed- ally significant, trend (male: t=3.58, P=0.002; female: ing trips per nestling per hour, by female breeders, male breeders, t=Ð1.76, P=0.10; Fig. 3). and male helpers during morning and afternoon observation peri- ods. Unassisted pairs (n=13) and pairs assisted by a single helper (n=18) were observed during the 1996 breeding season Risk analyses excluding territory quality

In these populations, mortality rates of male breeders are (Table 1). In the Sandhills, female breeder mortality also lower than those of female breeders (mean annual mor- declined with increasing numbers of both adults and tality of Sandhills males 23.6%; Coastal Plain fledglings (pseudo-r2=0.15,χ2=62.75, df=2, P=0.0001) males=17.4%; Sandhills females=30.0%; Coastal Plain (Table 1). In the Coastal Plain population, female breed- females=21.9%), and mortality rates of both sexes in- er mortality decreased as the number of fledglings on the crease at older ages (Fig. 1). The risk of male breeder territory increased (pseudo-r2 0.28, χ2=21.39, df=2, mortality decreased with increasing numbers of adults P=0.001), but the number of adults on the territory had and fledglings on the territory, in the Sandhills (pseudo- no significant effect (Table 1). r2=0.14, χ2=35.68, df=2, P=0.001) and the Coastal Plain (pseudo-r2=0.25, χ2=19.74, df=2, P=0.0001) populations

Table 1 Mortality of breeding males and females analyzed as a increased by one unit and all other variables are held constant. For function of the number of Adults and Fledglings on their territory example, a one-unit increase in the relative number of adults on a in the Sandhills and Coastal Plain populations (Eq. 1 in text). The territory results in a 27.3% decrease in the mortality rate for a Wald chi-square test statistic is used to determine if the parameter male breeder in the Sandhills population. Sample size is the num- estimate is significantly different from zero. %∆ is the percent ber of breeders in each population over the study period change in the rate of death when a single independent variable is

Breeder Population n Parameter Estimate Wald χ2 P %∆

Male Sandhills 554 Adults Ð0.32 16.71 0.0001 Ð27.3 Fledglings Ð0.16 10.72 0.0011 Ð15.1 Male Coastal Plain 137 Adults Ð0.57 5.31 0.0212 Ð43.5 Fledglings Ð0.37 6.92 0.0085 Ð31.1 Female Sandhills 747 Adults Ð0.15 4.22 0.0399 Ð13.8 Fledglings Ð0.28 42.10 0.0001 Ð24.4 Female Coastal Plain 173 Adults Ð0.24 2.42 0.1202 Fledglings Ð0.45 16.10 0.0001 Ð36.1 340 Table 2 Breeder mortality as a function of average number of rameter estimate is significantly different from zero. %∆ is the adults on a territory (Tavg), and the number of adults (Dadults) and percent change in the rate of death when a single independent the number of fledglings (Dfledge) relative to their respective terri- variable is increased by one unit and all other variables are held tory averages (Eq. 2 in text). Examining numbers of adults and constant. For example, a one-unit increase in the relative number fledglings in terms of deviations from territory averages instead of of adults on a territory results in a 20.8% decrease in the mortality absolute numbers (Table 1) controls for effects of territory quality. rate for a male breeder in the Sandhills population. Sample size is The Wald chi-square test statistic is used to determine if the pa- the number of breeders in each population over the study period

Breeder Population n Parameter Estimate Wald χ2 P %∆

Male Sandhills 554 Tavg Ð0.77 24.17 0.0001 Ð56.4 Dadults Ð0.23 7.42 0.0064 Ð20.8 Dfledge Ð0.17 9.72 0.0018 Ð15.6 Male Coastal Plain 137 Tavg Ð0.89 7.29 0.0069 Ð59.7 Dadults Ð0.55 3.99 0.0458 Ð42.3 Dfledge Ð0.54 9.60 0.0019 Ð41.8 Female Sandhills 747 Tavg Ð0.32 6.04 0.0142 Ð27.3 Dadults Ð0.17 3.96 0.0473 Ð15.3 Dfledge Ð0.30 39.58 0.0001 Ð26.0 Female Coastal Plain 173 Tavg Ð1.33 20.88 0.0001 Ð73.5 Dadults 0.09 0.23 0.6291 Dfledge Ð0.55 17.78 0.0001 Ð42.5

Risk analyses including territory quality Our results indicate that red-cockaded woodpecker helpers gain indirect fitness benefits through enhanced Male and female breeder mortality significantly de- survival of related breeders. The associations between creased as the index of territory quality (Tavg) increased, breeder survival and numbers of helpers and fledglings in both the Sandhills and Coastal Plain populations (Ta- could be due to effects of the helpers and fledglings ble 2). The major findings from the previous model still themselves, or to other factors correlated with the num- held when we accounted for this effect of territory quali- ber of helpers and fledglings. However, the effects held ty, however. Male breeder mortality in the Sandhills and when we controlled for the most likely such factor, terri- Coastal Plain populations decreased significantly with tory quality (Koenig 1981; Cockburn 1998). We can also increasing number of adults and fledglings, relative to partially account for another likely factor, breeder quali- the territory average (Table 2). In the Sandhills, female ty, because it is confounded with territory quality in our breeder mortality decreased with increasing number of analyses. There may be other factors we have not consid- adults and fledglings, relative to the territory average ered, but here we focus only on the effects of helpers and (Table 2). However, only the number of fledglings rela- fledglings. tive to the territory average resulted in a significant de- Helpers may passively or actively reduce breeder crease in female breeder mortality in the Coastal Plain mortality through “risk dilution” (Hamilton 1971), en- population (Table 2). Among females in the Sandhills hanced predator detection (Pulliam 1973), enhanced for- and Coastal Plain, controlling for territory quality in- aging efficiency (Pulliam and Caraco 1984), and load- creased the magnitude of the negative effect of the num- lightening. These mechanisms are not mutually exclu- ber of adults and fledglings on mortality. Among male sive, and all may operate to reduce breeder mortality. breeders in the Sandhills and Coastal Plain, controlling Here we provide evidence that red-cockaded woodpeck- for territory quality decreased the negative effect of the er breeders reduce incubation and nestling feeding in the number of adults on mortality, and increased the nega- presence of helpers. Load-lightening could translate into tive effect of the number of fledglings. reduced mortality if breeders save energy or reduce pre- dation risk by reducing parental behavior, or devote more time to activities that enhance survival, such as Discussion feeding, preening, or resting (Crick 1992). The effects of helpers on breeder workloads in other species are mixed The fact that we obtained nearly identical results from (Table 3). In some species in which helpers are known to the Sandhills and Coastal Plain populations suggests that assist with provisioning the nest, breeder provisioning is the relationships between breeder survival and numbers compensatory, such that the total provisioning rate of of helpers and fledglings we documented represent gen- groups with helpers is statistically equivalent to that of eral patterns among red-cockaded woodpeckers. The on- groups without helpers. In others, the helper provision- ly difference between the populations we observed, the ing is additive, such that total provisioning increases be- lack of a helper effect in the Coastal Plain population, cause one or both breeders do not fully adjust provision- may be an artifact of the smaller sample available for the ing effort in the presence of a helper. Breeders reduce Coastal Plain. their workload in 15 of the 24 species studied, including 341 Table 3 Results of studies that have analyzed helper effects on to- If no information is available, N/A is noted. If only one sex of the tal feeding rates, individual feeding contributions and/or breeder breeding pair reduces their workload in the presence of a helper, survival. The absence of an effect of helpers is denoted by 0, while then that sex is noted positive and negative effects are denoted by + and Ð, respectively.

Total Breeder Breeder survivorship Source provisioning workload Males Females

Arabian babblers + Ð N/A N/A Wright (1997) Long-tailed tit + Ð N/A N/A Hatchwell and Russell (1996) Purple gallinule + Ð N/A N/A Hunter (1987) Western bluebird + Ð 0 0 Dickinson et al. (1996) Green woodhoopoe 0 Ð N/A N/A Du Plessis (1991) Grey-crowned babbler 0 Ð N/A N/A Brown et al. (1978) Bushtit N/A Ð N/A N/A Sloane (1996) Greater rheas N/A Ð N/A N/A Condenotti and Alvarez (1997) White-throated magpie jay N/A Ð N/A N/A Langen and Vehrencamp (1999) Bicolored wren 0 Esp. femaled + + Austad and Rabenold (1985); Rabenold (1990) Stripe-backed wren 0 Esp. male 0 0 Rabenold (1984) White-browed sparrow weaver + Females 0 + Lewis (1982) Pied kingfisher +b Females 0 + Reyer (1984) Splendid fairy-wren 0 Females 0 + Russell and Rowley (1988) Galapagos mockingbird + Males 0 0c Kinnaird and Grant (1982); Curry and Grant (1990) Rifleman 0 Males 0 + Sherley (1990) Acorn woodpecker + 0 + 0 Mumme and de Querioz (1985); Koenig and Mumme (1987) Florida scrub Jaya +0 00a McGowan and Woolfenden (1990); Mumme (1992) Grey-capped social weaver + 0 N/A N/A Bennun (1994) Small green bee-eater + 0 N/A N/A Sridhar and Karanth (1993) White-browed scrub wren + 0 0 0 Magrath and Yezerinac (1997) White-fronted bee-eater + 0 0 0 Emlen and Wrege (1989, 1991) Bell miner + N/A N/A N/A Clarke (1984) Chestnut-bellied starling + N/A N/A N/A Wilkinson and Brown (1984) White-winged chough + N/A N/A N/A Heinsohn (1995) Pygmy nuthatch 0 N/A N/A N/A Sydeman (1991) barbet 0 N/A N/A N/A Restrepo and Mondragon (1998) a Experimental removal of non-breeders survival (59% unaided vs 63% aided) was not significant over the b Helpers have an effect on feeding rates at Lake Victoria but not 5-year study at Lake Naivasha, indicating that breeders adjust their effort ac- d Both sexes reduce their workload, but the reduction by females is cording to need greater c Curry and Grant (1990) demonstrated that female survival in- creased from 59% to 83% in 1 year, but the average increase in the red-cockaded woodpecker, suggesting that this is a because one must account for the numerous other factors common effect of helpers. Variation in parental response that affect survival. If breeders spend time gained from to the presence of helpers may be explained by costs of reduced parental effort on other energetically demanding reducing parental effort. Comparative analyses of pub- activities, no effect on survival is expected, but other lished data suggest that compensatory responses are as- benefits may be derived from these activities. For exam- sociated with low levels of brood reduction from starva- ple, red-cockaded woodpecker breeders, in addition to tion, while additive responses are associated with high tending eggs and young, forage, excavate cavities, de- rates of nestling starvation (Hatchwell 1999). Partial fend their territories, and rest. Excavation of cavities is brood loss is common in red-cockaded woodpeckers most frequent during the summer months, so pairs with (LaBranche and Walters 1994), but whether starvation is helpers may spend their “extra” time and energy exca- an important mechanism is unknown. vating cavities. Because the birds tend to use their new- Only six studies, including this one, have documented est cavity for nesting (Conner et al. 1998), and years of an increase in breeder survival with a concomitant de- work are required to complete a cavity (Conner and crease in the breeder’s workload: white-browed sparrow Rudolph 1995; Harding 1997), having time to excavate a weaver (Plocepasser mahali; Lewis 1982), splendid cavity could enhance future reproduction by the breeder. fairy-wren (Malurus splendens; Rowley and Russell We can only speculate on the mechanism by which 1997), bicolored wren (Campylorhynchus griseus; fledglings might enhance breeder survival. It is unlikely Austad and Rabenold 1985), pied kingfisher (Ceryle ru- that breeders have increased foraging efficiency in large dis; Reyer 1984), and riflemen (Ancanthisitta chloris; groups with many fledglings (Pulliam and Caraco 1984) Sherley 1990). Determining effects of reduced breeder because fledglings are not efficient foragers and continue workload on breeder survivorship is not straightforward to be fed by adults for many weeks (Jackson 1994). That 342 breeders benefit from enhanced predator detection when al Forests of North Carolina, Croatan National Forest, and the Na- more fledglings are present (Pulliam 1973; for a review tional Science Foundation (BSR-8307090 and BSR-8717683) for funding that supported data collection. We also thank all of the of evidence see Roberts 1996) is unlikely because fledg- graduate students, undergraduates, and field technicians who have lings are inexperienced with respect to predators. One contributed to collection of data from the Sandhills and Coastal possible mechanism for a survival benefit from fledglings Plain populations, and P.D. Doerr and J.H. Carter III for their ef- is “risk dilution” (Hamilton 1971), in which the probabil- forts directing and managing the woodpecker project. R. Andrews, S. Schoech, and several anonymous reviewers provided helpful ity of a given individual being attacked declines with in- comments. The Virginia Tech Statistical Consulting Center pro- creasing group size (Dehn 1990; Sadedin and Elgar vided assistance with the survival analyses. M.Z. Khan thanks her 1998). A similar mechanism is that young birds may be 1996 field assistant, Ian Nelson, for enduring incubation watches. preferred targets of predators, and hence vulnerability of She also thanks J. Allen, S. Daniels, S. Harding, and J. Lyons for adults is reduced if young birds are present. Finally, the creating a graduate laboratory with healthy doses of constructive criticism, and especially K. Loewenstein who often pretends to be correlation between breeder survival and the number of a field biologist. fledglings might be the result of a third variable, pheno- typic quality of the breeder. In other words, breeders that produce many fledglings might be high-quality individu- References als that are naturally long-lived. However, it is unlikely that correlation with breeder quality is a sufficient expla- Allison PD (1995) Survival analysis using the SAS system: a practical guide. SAS Institute, Cary, N.C. nation, as one would expect this factor to be captured by Austad SN, Rabenold KN (1985) Reproductive enhancement by our territory-quality variable to some extent. helpers and an experimental inquiry into its mechanisms in the The effects of group size on breeder survival have bicolored wren. Behav Ecol Sociobiol 17:19Ð27 been examined in several other co-operatively breeding Bennun L (1994) The contribution of helpers to feeding nestlings species (Table 3). These data clearly demonstrate that the in grey-capped social weavers, Pseudonigrita arnaudi. Anim Behav 47:1047Ð1056 benefits of group living are not unilateral and survivor- Brown JL (1974) Alternate routes to sociality in jays Ð with a the- ship must be examined for each group member. For ex- ory for the evolution of altruism and communal breeding. Am ample, future indirect benefits due to positive effects of Zool 14:63Ð80 helpers on survival of the male breeder, but not the fe- Brown JL (1978) Avian communal breeding systems. Annu Rev Ecol Syst 9:123Ð135 male breeder, are estimated to contribute one-third of the Brown JL, Douglas DD, Brown ES, Brown SD (1978) Effects of fitness benefits of helping among acorn woodpeckers helpers on feeding nestlings in the grey-crowned babbler (Koenig and Stacey 1990). (Pomatostomus temporalis). Behav Ecol Sociobiol 4:43Ð59 We conclude that future indirect fitness benefits re- Carter JH III, Stamps RT, Doerr PD (1983) Status of the red-cock- aded woodpecker in the North Carolina Sandhills. In: Wood sulting from reduced breeder mortality contribute to the DA (ed) Proceedings of red-cockaded woodpecker symposia. maintenance of helping behavior in the red-cockaded II. Florida Game and Fresh Water Fish Commission and U.S. woodpecker. Reduced breeder mortality appears to be a Fish and Wildlife Service, Atlanta, pp 24Ð29 function of both the presence of a helper and the pres- Clarke MF (1984) Co-operative breeding by the Australian bell ence of fledglings. Our results implicitly support the hy- miner Manorina melanophrys. Behav Ecol Sociobiol 14:137Ð 146 pothesis that helpers reduce breeder mortality by reduc- Cockburn A (1998) Evolution of helping behavior in cooperative- ing breeder workload because breeders reduce their incu- ly breeding birds. Annu Rev Ecol Syst 29:141Ð177 bation and provisioning effort in the presence of a helper. Condenotti TL, Alvarez F (1997) Cooperative breeding between However, a causal link between reduced breeder work- males in the greater rhea, Rhea americana. Ibis 139:568Ð571 Conner RN, Rudolph DC (1995) Dynamics and time requirements load and reduced breeder mortality has yet to be demon- of red-cockaded woodpeckers cavity excavation. In: Kulhavy strated. The only hypothesis to explain helping behavior DL, Hooper RG, Costa R (eds) Red-cockaded woodpecker: re- by red-cockaded woodpeckers not yet examined is the covery, ecology and management. Center for Applied Studies, benefit through production of young that assist non- College of Forestry, Stephen F. Austin State University, Nacogdoches, Tex, pp 343Ð352 descendent kin of the helper in a subsequent season Conner RN, Saenz D, Rudolph DC, Ross WG, Kulhavy DL (Reyer 1984; Rabenold 1985). That helpers benefit di- (1998) Red-cockaded woodpecker nest cavity selection: rela- rectly through improved reproductive ability due to help- tionships with cavity age and resin production. Auk 115:447Ð ing experience has been ruled out for this species (Khan 454 and Walters 1997). Khan and Walters (2000) also Connor RC (1986) Pseudoreciprocity: investing in mutualism. Anim Behav 34:1562Ð1584 showed that helpers do not benefit from aid provided by Crick HQP (1992) Load-lightening in cooperatively breeding former recipients of help, once the helper inherits the na- birds and the cost of reproduction. Ibis 134:56Ð61 tal territory and becomes a breeder (Connor 1986; Emlen Curry RL, Grant PR (1990) Galapagos mockingbirds: territorial and Wrege 1989). The only demonstrated benefit of cooperative breeding in a climactically variable environment. 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