| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Behavioral Ecology Vol. 15 No. 2: 233-238
Behavioral Ecology vol. 15 no. 2 © International Society for Behavioral Ecology 2004; all rights reserved
A test of the importance of direct and indirect fitness benefits for helping decisions in western bluebirds
Museum of Vertebrate Zoology, University of California, Berkeley, and Hastings Natural History Reservation, 38601 E. Carmel Valley Road, Carmel Valley, CA 93924, USA
Address correspondence to J. L. Dickinson. E-mail: sialia{at}uclink4.berkeley.edu.
Received 10 October 2002; revised 28 March 2003; accepted 21 April 2003.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
In cooperative breeders, the extent to which helpers at the nest adjust their contributions in accordance with direct and indirect (kin-selected) fitness payoffs remains an open question. In a long-term study of the western bluebird, Sialia mexicana, helpers were exclusively male and helped at nests of both parents, a parent and stepparent, or a brother and unrelated female. This natural variation in the context of helping facilitated comparison of observational data on groups in which one type of fitness benefit (current direct, future direct, or indirect) varied, whereas the other two were constant. Helpers reduced their share of provisioning as they got older, so comparisons were restricted to groups with yearling helpers. When potential direct fitness benefits were identical, but relatedness was reduced by half owing to the presence of a stepparent, yearling helpers failed to reduce their share of feeding trips to the nest. The potential for future direct fitness benefits via possible mate and territory inheritance was low, and did not influence the helper's share of provisioning in a comparison of groups with similar relatedness and opportunities for current direct fitness benefits. Even though cobreeding to gain current direct fitness benefits was infrequent (17% of nests with brother-helpers), it was associated with an increase in the helper's share of provisioning, suggesting that a helper's feeding allocation responds positively to increased opportunity for parentage in the nest. The current study demonstrates a useful framework for separating direct and indirect benefits with respect to helping decisions, and indicates that western bluebird helpers adjust their feeding rates in response to the potential for direct fitness benefits in the current nest, not indirect benefits or future direct fitness payoffs. Although past studies of this population showed that indirect benefits play a role in whether or not helpers help, the current study indicates that they do not play a role in how frequently helpers feed at the nest.
Key words: birds, cooperative breeding, feeding, helping, inclusive fitness, parental care, provisioning, relatedness, share of provisioning.
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
In avian cooperative breeders, helpers often gain indirect fitness benefits by feeding young at nests of close relatives when promising opportunities for independent reproduction are scarce (Stacey and Koenig, 1990
). Although helping usually does not yield benefits that match what helpers would gain by breeding on their own, the relatively small increments of inclusive fitness they gain from helping are better than the projected gains if they remained at home, but did nothing at all. More rarely, helpers gain direct fitness benefits in the form of experience that increases breeding success later in life and increased opportunities for direct reproduction in the future (Clutton-Brock, 2002; Cockburn, 1998; Komdeur, 1996).
Recent evidence suggests that helping may also have significant direct fitness costs (Heinsohn and Cockburn, 1994; Heinsohn and Legge, 1999). In some cases helpers are reported to minimize these costs by consuming food themselves while appearing to feed the nestlings (Boland and Heinsohn, 1997). When the inclusive fitness benefits of helping tend to be small (Dickinson and Akre, 1998) even a rather small cost will render helping nonbeneficial from the helper's point of view, selecting for helpers that are able to fine-tune their allocations in response to the magnitude of potential costs and benefits.
Helpers may fine-tune their helping decisions in several ways to improve their benefit-cost ratio. For example, Seychelles warbler (Acrocephalus sechellensis) females become helpers when the indirect fitness benefits are greater than the direct benefits of breeding on available, but inferior, territories (Komdeur, 1992). They also adjust how much help they give according to their apparent relatedness, which is proportional to the magnitude of the indirect benefits they receive (Komdeur, 1994). Although Seychelles warblers remain the leading test case for assessment in helping decisions, these results are likely to be reevaluated in the light of new evidence that many helpers are actually cobreeders with genetic offspring in the nest (Richardson et al., 2001). The generality of assessment and fine-tuning by nonbreeding helpers has yet to be determined in cooperative breeders.
In western bluebirds (Sialia mexicana), adult helpers are exclusively male and are 10 times as likely to help both parents as to assist pairs in which just one breeder is a first-order relative, suggesting that potential indirect benefits play a role in whether or not sons help (Dickinson et al., 1996). Despite this tendency, western bluebird helpers can be found feeding young of a parent and stepparent or a brother and unrelated female. The result is a two-fold difference in relatedness of helpers to the young in the nests at which they help; this difference can be used to determine whether the magnitude of indirect benefits influences how much assistance helpers give.
Similar to changes in group composition, extrapair paternity influences a helper's mean relatedness to the nestlings (Dickinson and Akre, 1998). Although helpers probably cannot tell whether their social father is their true genetic father, they may be able to use the extrapair behavior of the resident female to assess the potential for extrapair paternity in nests at which they help. Helpers should be even more accurate at assessing their potential for current direct fitness benefits, based on their experience copulating with the female. Because it is not clear what information helpers have available, the question of whether helpers allocate help in accordance with relatedness should be tested by using both actual genetic relatedness, based on molecular fingerprinting, and expected relatedness, based on the helper's prior association with its parents and siblings as a nestling or its likelihood of siring offspring in the nest. If expected relatedness is a good predictor of actual relatedness, it should allow helpers to allocate feeding effort in response to their potential fitness gain.
In the current study, I examine variation in the helper's share of provisioning as a function of its actual and expected relatedness to the nestlings it helps to feed. I also determine whether the helper's share of provisioning is sensitive to the potential for direct and indirect fitness benefits, using a predictive framework that examines differences based on just one type of benefit by using comparison groups in which the other types are held constant.
|
METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Study population
The analyses contained in this article are based on the years 1984–2002 of a long-term study of color-banded western bluebirds at Hastings Reservation in central coastal California. Banding and nest monitoring began in 1983. Provisioning results are based upon watches conducted from 1988–2002. Adults and nestlings have been color-banded throughout the study to determine apparent genealogies. The methods for monitoring the population are provided elsewhere (Dickinson et al., 1996
).
Calculation of relatedness based on DNA fingerprinting
Blood samples taken from nestlings and adults were stored at -20°C to -70°C in lysis buffer (Seutin et al. 1991). Paternity analysis was based on multilocus fingerprints for HaeIII-digested genomic DNA samples by using the Jeffreys probes (Jeffreys et al., 1985). Exclusion was based on the number of unattributable minisatellite bands in the offspring and parent–offspring bandsharing coefficients (for detailed methods, see Dickinson and Akre, 1998).
Actual helper-nestling relatedness was based on use of multilocus DNA fingerprinting to infer parentage for 24 families with helpers (Dickinson and Akre, 1998). Actual helper–nestling relatedness was calculated based on the relationship of the helper to the breeders at the nest. For example, if a nestling was determined via parentage analysis to be a full-sibling of the helper, its relatedness to the helper was calculated at 0.5. Alternatively, if a helper was the genetic offspring of both the breeder male and female, but a chick in the helped nest was assigned only to the breeder female (meaning that the breeder male and helper were excluded from paternity), then the helper's relatedness to that nestling was calculated at 0.25. After calculating relatedness for every helper-nestling dyad, I calculated the helper's mean relatedness to all the nestlings in the nest at which he helped.
Provisioning watches
Feeding data, collected in 1988–2002, were based on up to three 90-min nest watches per nest, conducted in early (age, 4–6 days), middle (age, 9–11 days), and late (age, 14–16 days) stages of nestling growth. Watches began before 1100 h (Pacific standard time) and were timed from the first feed to minimize differences in skittishness among pairs. Nest entrances were watched through a spotting scope from a blind or hiding place approximately 30 m from the next-box. Sex and identity (color bands) of the feeding birds were recorded during each feeding trip.
Each nest was treated as an independent event and given equal weight in the analyses regardless of the total number of feeds. Data were not pseudoreplicated by helper or by parents. When a helper returned to its natal territory to help after its own nest failed, I included only watches occurring after the helper arrived home. In the analysis of expected relatedness, I originally had 54 nests with a mean of 48.3 ± 4.3 feeding trips per nest (range = 5–138). I eliminated from analysis five nests in which the feeding individuals could not be identified for 10% or more of the feeds, as sometimes occurs when the birds enter the box quickly without showing their legs. When analyzing the relationship between share of provisioning and expected relatedness, I also eliminated nests with more than one helper, resulting in a sample size of 42 nests. When I restricted analysis to cases with yearling helpers only, the sample size was further decreased to 35. Data on actual relatedness were available for 20 families with provisioning watches, 18 of which had yearling helpers.
Helper's share of provisioning trips
The helper's share of provisioning trips to the nest (proportion of feeds) was calculated as the number of feeding trips made by the helper male divided by the total number for the helper male, breeder male, and female combined. Share of feeding trips was selected because prior studies of this population indicate that parents reduce their provisioning when helpers help (Dickinson et al., 1996). This makes share of feeding trips an extremely sensitive measure for detecting changes in helper provisioning. Furthermore, based on watches started before 1100 h (pacific standard time), share of feeding trips was less susceptible than feeding rate (feeding trips/h) to seasonal changes and temporal fluctuations within a day (J.L. Dickinson, unpublished data). In this study, statistical results based on share of feeding trips were consistent with those based on helper feeding rates (feeding trips/h). Only the tests based on helper's share of feeding trips are presented in the results.
Statistical analyses
Statistical analyses were based on planned comparisons. Proportion of feeds was angularly transformed for parametric analysis by taking the arcsine (square root of the data). Means are presented ±SEM. All tests are two-tailed. I conducted post-hoc power analysis for cases with nonsignificant results in the predicted direction by using expected, rather than observed, effect sizes, because use of observed effect sizes is incorrect (Johnson, 1999; Shaver, 1993; Steidl et al., 1997). I did not calculate power when the means for the comparison groups were equal, when differences were opposite the predicted direction, or when there was no expected effect size.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Mating system and patterns of relatedness
Incest avoidance and mate inheritance
The relative potential for direct and indirect benefits depends upon intraspecific patterns of mating, inheritance, and incest avoidance. Helper males may derive direct fitness benefits by helping at nests with unrelated females if they gain current or future access to those females and to the territories they occupy. Although helping is relatively rare in western bluebirds, male philopatry is not. Males tend to remain with their parents through their first winter and 25% of banded male nestlings eventually attempt to breed on the study area (Koenig and Dickinson, 1996
; Kraaijeveld and Dickinson, 2001). Son-mother incest was rare throughout the study and occurred only once in 662 (0.1%) unique pairings involving males born on the study area and banded as nestlings. The few previously reported cases of incest beyond this single case appeared to involve sons assisting at their mothers' nests when their fathers sired offspring, but died before the chicks hatched (Dickinson and Akre, 1998). Over 19 years, 14 males (2.1%) bred with a stepmother, after the death of the male's father. Similarly, 15 males (2.3%) inherited their brothers' mates, and only one male (0.1%) inherited his half-brother's mate. This indicates a relatively small potential for mate inheritance to select for increased feeding by helpers.
Actual versus expected relatedness
In allocating effort, helpers might use information on actual relatedness and paternity or they might simply use information on their expected relatedness, r, to the breeders at the nest. In the former case, helpers should allocate effort in proportion to their mean relatedness to nestlings, whereas in the latter they should contribute a greater share of feeding when assisting both their parents than when assisting a putative parent and a stepparent or a brother and his mate. The helper's putative father and mother are the male and female that raised him. In the absence of extrapair fertilizations, a male helping both his putative parents has a mean relatedness to the nestlings equal to 0.5, whereas a male helping a parent and stepparent or a brother and his mate will have a mean relatedness of 0.25. Helpers are only expected to base their feeding allocation on expected relatedness when it is a good predictor of actual relatedness.
Extrapair paternity reduced actual helper-nestling relatedness from the expected 0.5 and 0.25 to 0.45 and 0.23, respectively (Table 1). Because helping one rather than two first-order relatives reduced actual helper-nestling relatedness by approximately half, expected relatedness is a good relative measure of actual relatedness.
|
Does the potential magnitude of indirect benefits influence the helper's share of feeding trips?
Actual relatedness and helper's share of feeding
By using the 20 nests for which I had both molecular data and provisioning data, I performed analyses to determine whether helpers adjusted their share of provisioning with their actual relatedness to the nestlings. Mean helper-nestling relatedness was 0.30 ± 0.07 (range = 0.10–0.50, n = 20) and the mean share of feeding trips made by helpers was 32 ± 4% (range = 3–74%, n = 20). In a linear regression, there was no statistical relationship between the proportion of feeds contributed by the helper and mean helper-nestling relatedness (ß = 0.264, r 2 =.02, F1,18 = 1.3, p =.26). Similarly, I found no statistical relationship between proportion of feeds by the helper and mean helper-nestling relatedness when I included only nests with yearling helpers (ß = 0.290, r 2 =.03, F1,16 = 1.5, p =.18).
Expected relatedness and helper's share of feeding
I compared the helper's share of provisioning at single-helper nests as a function of whether they were raising apparent full siblings (r =.5) versus apparent half-siblings or nieces and nephews (r =.25). Before conducting the analysis, I first had to consider a possible age confound owing to potential correlations between helper age, share of provisioning, and helper-nestling relatedness.
As helpers age, the probability that they will have lost at least one parent increases. In a sample of nests with feeding data and apparent genealogies from color-banding, all helpers aided at least one first-order relative, but yearling helpers were more likely than were older helpers to aid two first-order relatives (Fisher exact p =.005, n = 42). Because yearling helpers also tended to assume a greater share of provisioning than did older helpers, (32 ± 3% versus 17 ± 5%, n1 = 35, n2 = 7, t = 2.5, p =.03), I restricted analysis of share of provisioning to nests with yearling helpers. Yearling helpers assisting just one first-order relative (expected relatedness = 0.25) did not feed proportionally less than did yearling helpers assisting both putative parents (expected relatedness = 0.5; 30 ± 5% versus 34 ± 4%, t = 0.52, n1 = 13, n2 = 22, p =.61, power to detect 50% reduction = 0.75).
In the three group compositions in which helpers assisted just one first-order relative (expected helper-nestling relatedness = 0.25), the mean share of feeding trips by helpers varied considerably (Table 2, A–C). The potential direct fitness benefits also varied among these groups, allowing the specific set of predictions outlined in Table 3. Two groups (Table 2, cf. A and B) differ in expected relatedness while remaining similar in the potential for helpers to benefit through current and future direct fitness benefits. Comparison of provisioning by helpers assisting both parents with provisioning by helpers assisting a mother and stepfather yields a compelling test of the importance of indirect benefits to a helper's feeding effort. Based on this comparison, helpers did not reduce their share feeding trips when raising apparent half-sibs rather than full-sibs (Table 3, power for a 50% reduction = 0.39).
|
|
Does the potential for direct fitness benefits influence the helper's share of feeding trips?
Future direct fitness benefits
I tested the prediction that helpers with an expected relatedness to the nestlings of 0.25 would make a greater share of feeding trips when they were unrelated to the breeder female (and thus had the potential for future direct fitness benefits) than when they were unrelated to the breeder male and assisted their mother, with whom they would not breed in the future (Table 2, cf. C and B). Helpers assisting at a brother's nest were excluded from this analysis, because brother-helpers had paternity in one of six nests (17%) and thus potentially derive a small direct benefit in the current year (Dickinson and Akre, 1998
). The helper's share of provisioning was not influenced by future direct fitness benefits, because helpers assisting their father and stepmother did not assume a greater share of provisioning than did helpers assisting their mother and stepfather (Table 3, "future direct fitness benefits"). Although the sample sizes are small for these two groups, the nonsignificant tendency was opposite the direction predicted if future direct fitness benefits are important (helpers tended to favor mothers and stepfathers).
Current direct fitness benefits
Current direct fitness benefits predict that helpers unrelated to the breeder female should make a greater share of feeding trips when assisting brothers than when assisting their fathers (Table 2, cf. D and C). The reason for this prediction is that helpers only had paternity when they helped brothers and not when they helped parents. Although only one of six (17%) males assisting their brothers had a share of paternity (Dickinson and Akre, 1998), this does not mean that males only rarely copulate with their brother's mate. This analysis is based on the idea that potential for copulatory access is an imperfect behavioral cue of potential paternity. The small tendency for males to sire young in the nest when helping a brother may reflect a low frequency of copulation by brother-helpers or it may reflect a bias in paternity even when both brothers have copulatory access. If the potential for current direct benefits is important to feeding decisions, then helpers assisting a brother and an unrelated female should assume a greater share of provisioning than helpers assisting a father and stepmother. This appeared to be the case based upon a sample of nine nests (Table 3, "Current direct fitness benefits").
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
The current study uses a predictive framework that can separate potential influences of direct and indirect fitness benefits in predicting the relative effort helpers should contribute to feeding young. By using this framework, it is possible to conduct planned comparisons in which just one of three potential fitness benefits (indirect [relatedness], current direct, or future direct) varies, whereas the other two remain constant. In study systems with larger samples of nests with helpers, this framework can be expanded to explore additional axes along which the benefits of provisioning vary, such as the age of the helper, the number of helpers, and costs of helping, once they are determined.
Helpers reduced their share of feeding trips as they aged, suggesting that the benefit/cost ratio decreases with helper age or with some correlate of helper age. Relatedness is inherently correlated with helper age, owing to the temporal increase in the probability that at least one parent has died. This confound may be circumvented by excluding older helpers from analysis when examining effects of relatedness or by including age as an explanatory variable in studies with large sample sizes. Failure to control for age could result in spurious support for an effect of relatedness on feeding.
Yearling helpers did not adjust their share of feeding trips in response to actual or expected reductions in their relatedness to the chicks they helped feed even when potential direct fitness benefits were similar between comparison groups. In a study of helping in meerkats (Suricata suricatta), Clutton-Brock et al. (2001) also failed to find an effect of relatedness on feeding rates when they controlled for age, foraging efficiency, brood size, group size, sex of helper, and dominance, but not potential direct benefits.
It is surprising that males did not reduce their care when feeding half-sibs compared with full-sibs, particularly because expected relatedness is a good predictor of actual relatedness. If the greater tendency for males to become helpers at nests with full- than half-sibs is based on recognition, rather than reproductive competition (Dickinson et al., 1996), this same recognition mechanism should allow helpers to fine-tune their feeding rates when they do help. Western bluebirds appear to recognize kin, because they often relocate and assist their parents or brothers after dispersing to breed. Helping is rare, however (7% of pairs have helpers), so it is possible that selection is not consistent enough to favor feeding rules that would fine-tune helping to relatedness.
The failure of helpers to reduce their share of feeding in response to a reduction in the magnitude of indirect benefits should not be misconstrued as evidence that indirect benefits are not important in this system. Early demographic analysis failed to provide any support for direct fitness benefits through enhanced survival or reproductive success of helpers, whereas indirect fitness benefits have been supported in two separate analyses (Dickinson and Akre, 1998; Dickinson et al., 1996). Evidence that helpers assess their relatedness to young and allocate effort based on the magnitude of their indirect benefits would support the importance of indirect benefits to helping, but failure to find such a pattern may simply indicate that helping is not costly or that a reduction in the level of care is not sufficiently beneficial to override the potential costs.
Helpers may fail to reduce their share of provisioning when assisting a mother and stepfather because doing so would increase parental aggression, reduce nepotism, or possibly even lead to eviction from the territory. Such costs may be important in superb fairy-wrens (Malurus cyaneus) whose helpers are thought to "pay to stay" on their natal territory (Mulder and Langmore, 1993). Although evidence for pay to stay is currently weak, there is evidence of direct fitness advantages of remaining in the natal group from studies of the Siberian jay, Perisoreus infaustus, a species without helpers (Ekman et al., 1999, 2001). In western bluebirds, however, surviving sons that do not help at all often rejoin their natal groups after breeding nearby, suggesting that eviction and other forms of parental retaliation are unlikely (Kraaijeveld and Dickinson, 2001).
Although future direct fitness benefits were not supported in the current study, the test was based upon expected rather than actual relatedness, making the assumption that indirect fitness benefits are held constant. However, taking into consideration 20% extrapair paternity of helpers and the nestlings they help raise (Dickinson and Akre, 1998), expected helper-nestling relatedness is actually 0.16 for helpers assisting a father and stepmother compared with 0.25 for helpers assisting a mother and stepfather. This difference predicts a 36% reduction in the feeding contribution of helpers aiding fathers and stepmothers compared to helpers aiding mothers and stepfathers. The sample size is small, but the difference, although not significant, is in the direction predicted if helpers were to allocate more to feeding mothers' than fathers' offspring (0.30 of feeds for helpers aiding mothers and stepfathers versus 0.19 of feeds for helpers aiding fathers and stepmothers, power = 0.42 for a 36% reduction) (Table 3). Given the low power for this analysis, I cannot rule out the possibility that indirect benefits influence share of provisioning by helpers assisting a parent and stepparent. On the other hand, the failure of helpers to reduce their provisioning of apparent half-sibs, compared with full-sibs, suggests that they would be unlikely to respond to an even smaller difference in the indirect benefit when parents breed with a male versus a female stepparent.
I found that current direct fitness benefits (potential parentage in the current nest) increased a helper's share of provisioning, whereas future direct fitness benefits had no effect. The importance of current direct fitness benefits in helping decisions is also supported by evidence from a study of white-browed scrubwrens (Sericornis frontalis), in which helpers were more likely to give aid if the breeder female was unrelated and thus a potential mate (Magrath and Whittingham, 1997). In contrast, in pied kingfishers (Ceryle rudis) unrelated secondary helpers fed less frequently than related primary helpers, an observation that is consistent with the relative inclusive fitness benefits of these two strategies (Reyer, 1984). Why wouldn't future direct benefits also be important? Given the low frequency of mate inheritance I observed, future direct fitness benefits may be sufficiently improbable that they do not act as a significant selective force. The rarity of mate inheritance in western bluebirds is in agreement with the findings for Seychelles warblers, and because it usually requires both parents to die, inheritance may be generally rare throughout cooperatively breeding birds (Komdeur and Edelaar, 2001).
This and prior studies of provisioning in western bluebirds failed to demonstrate a relationship between provisioning effort and degree of relatedness or partial paternity. These same studies have nevertheless consistently supported the notion that breeder males contribute their typical half-share of provisioning trips as long as they have some opportunity for paternity in the current nest through access to the female during her fertile period (Dickinson, 2003; Dickinson and Weathers, 1999). Similar to breeders, helpers failed to respond to variation in relatedness, per se, and elevated their share of feeding only when they had a chance of siring offspring in the nest, technically becoming cobreeders. If copulatory access or lack thereof is the main cue triggering feeding for breeder males, it may be that this same cue causes brother-helpers to assume an elevated parentlike share of provisioning, as if the bird moves abruptly from helper mode to breeder mode. The idea that there are three different feeding modes, one for males with no access to the female, one for helpers, and another for males with mating access, is consistent with prior evidence indicating that western bluebird males assess whether or not they have a chance at parentage, but do not fine tune their feeding allocation despite the availability of cues indicating wide variation in the degree of relatedness to the young.
|
ACKNOWLEDGEMENTS |
|---|
This work was performed at the University of California Natural Reserve System's Hastings Reservation and the adjacent Oak Ridge Ranch with the logistical support of the directors, faculty, and staff of the Museum of Vertebrate Zoology, University of California, Berkeley. I thank Walt Koenig, Marlene Zuk, and two anonymous reviewers for helpful comments on earlier drafts of this paper. I am indebted to a large number of field interns whose involvement in banding, nest monitoring, and behavioral observations made this study possible. I thank T. Abe, H. Abel, J. Akre, D. Barber, A. Berg, R. Bower, J. Brewer, D. Christian, K. Dean, V. Demas, M. Dietz, J. DePiero, M. Eichholz, K. Ellison, R. Etemad, E. Garcia, J. Goldstein, K. Gordon, S. Harding, M. Hemmen, M. Hoffman, K. Hondrick, B. Hahn, N. Hazle, M. Koopman, K. Kraaijeveld, F. Kraaijeveld-Smit, J. Kranz, L. Kummer, M. Lewis, A. MacGregor, L. McGraw, D. Monk, R. Morlen, G. Morse, J. Nesbitt, K. O'Connor, K. Petersen, K. Pollard, C. Riding, J. Rombouts, J. Rosenthal, D. Ruthrauff, L. Scinto, P. Shepherd, D. Shizuka, M. Stapleton, M. Stebbins, K. Truman, and L. Vogel for their dedicated efforts in the field. The Kirk family graciously allowed access to Oak Ridge Ranch. This study was supported by NSF and NIH (NRSA) postdoctoral fellowships and grants from the North American Bluebird Society, Ellis Bird Farm, the University of California's Genetic Resources Conservation Program, NSF grant IBN-9507365, and NSF grant IBN-009702.
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Boland CRJ, Heinsohn R, 1997. Deception by helpers in cooperatively breeding white-winged choughs and its experimental manipulation. Behav Ecol Sociobiol 41:251-256.[CrossRef][Web of Science]
Clutton-Brock T, 2002. Breeding together: kin selection and mutualism in cooperative vertebrates. Science 296:69-72.
Clutton-Brock TH, Brotherton PNM, O'Riain MJ, Griffin AS, Gaynor D, Kansky R, Sharpe L, McIlrath GM, 2001. Contributions to cooperative rearing in meerkats. Anim Behav 61:705-710.[CrossRef]
Cockburn A, 1998. Evolution of helping behavior in cooperatively breeding birds. Annu Rev Ecol Syst 29:141-177.[CrossRef][Web of Science]
Dickinson JL, 2003. Male feeding contribution is not influenced by actual or apparent loss of paternity in western bluebirds. Behav Ecol 14:360-366.
Dickinson JL, Akre JJ, 1998. Extrapair paternity, annual inclusive fitness, and within-group benefits of helping in the western bluebird. Mol Ecol 7:95-105.
Dickinson JL, Koenig WD, Pitelka FA, 1996. The fitness consequences of helping behavior in the western bluebird. Behav Ecol 7:168-177.
Dickinson JL, Weathers WW, 1999. Replacement males in the western bluebird: opportunity for paternity, chick-feeding rules, and fitness consequences of male parental care. Behav Ecol Sociobiol 45:201-209.[CrossRef][Web of Science]
Ekman J, Bylin A, Tegelström H, 1999. Increased lifetime reproductive success for Siberian jay Perisoreus infaustus males with delayed dispersal. Proc R Soc Lond B 266:911-915.
Ekman J, Eggers S, Griesser M, Tegelström H, 2001. Queuing for preferred territories: delayed dispersal of Siberian jays. J Anim Ecol 70:317-324.[CrossRef]
Heinsohn R, Cockburn A, 1994. Helping is costly to young birds in a cooperatively breeding white-winged choughs. Proc R Soc Lond B 256:293-298.
Heinsohn R, Legge S, 1999. The cost of helping. Trends Ecol Evol 14:53-57.[CrossRef][Medline]
Jeffreys AJ, Wilson V, Thein SL, 1985. Hypervariable minisatellite regions in human DNA. Nature 314:67-73.[CrossRef][Medline]
Johnson DH, 1999. The insignificance of statistical significance testing. J Wildl Manag 63:763-772.[CrossRef]
Koenig WD, Dickinson JL, 1996. Nestling sex ratio variation in western bluebirds. Auk 113:902-910.[Web of Science]
Komdeur J, 1992. Importance of habitat saturation and territory quality for evolution of cooperative breeding in the Seychelles warbler. Nature 358:493-495.[CrossRef]
Komdeur J, 1994. The effect of kinship on helping in the cooperative breeding Seychelles warbler (Acrocephalus sechellensis). Proc R Soc Lond B 256:47-52.
Komdeur J, 1996. Influence of helping and breeding experience on reproductive performance in the Seychelles warbler: a translocation experiment. Behav Ecol 7:326-333.
Komdeur J, Edelaar P, 2001. Evidence that helping at the nest does not result in territory inheritance in the Seychelles warbler. Proc R Soc Lond B 268:2007-2012.[Medline]
Kraaijeveld K, Dickinson JL, 2001. Family-based winter territoriality in western bluebirds: the structure and dynamics of winter groups. Anim Behav 61:109-117.[CrossRef][Web of Science][Medline]
Magrath RD, Whittingham LA, 1997. Subordinate males are more likely to help if unrelated to the breeding female in cooperatively breeding white-browed scrubwrens. Behav Ecol Sociobiol 41:185-192.
Mulder RA, Langmore NE, 1993. Dominant males punish helpers for temporary defection in superb fairy-wrens. Anim Behav 45:830-833.[CrossRef][Web of Science]
Reyer U, 1984. Investment and relatedness: a cost/benefit analysis of breeding and helping in the pied kingfisher (Ceryle rudis). Anim Behav 32:1163-1178.[CrossRef]
Richardson D S, Jury FL, Blaakmeer K, Komdeur J, Burke T, 2001. Parentage assignment and extra-group paternity in a cooperative breeder: the Seychelles warbler (Acrocephalus sechellensis). Mol Ecol 10:2263-2273.[CrossRef][Medline]
Shaver JP, 1993. What statistical significance testing is, and what it is not. J Exp Educ 61:293-316.
Stacey PB, Koenig WD, 1990. Cooperative breeding in birds: long-term studies of ecology and behavior. Cambridge: Cambridge University Press.
Seutin G, White BN, Boag PT, 1991. Preservation of avian blood and tissue samples for DNA analyses. Can J Zool 69:82-90.[CrossRef]
Steidl RJ, Hayes JP, Schauber E, 1997. Statistical power analysis in wildlife research. J Wildl Manag 61:270-279.[CrossRef]
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  A. Charmantier, A. J Keyser, and D. E.L Promislow First evidence for heritable variation in cooperative breeding behaviour Proc R Soc B, July 22, 2007; 274(1619): 1757 - 1761. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||