Siblicide in the cooperatively breeding laughing kookaburra (Dacelo novaeguineae)

I describe siblicide in the laughing kookaburra (Dacelo novaeguineae), a reverse size-dimorphic, cooperatively breeding kingfisher. Clutches were usually of three eggs, and nestlings hatched asynchronously, with intervals of 2–72 h between successive eggs. Siblicide occurred in two temporally and mechanistically distinct episodes. The youngest nestling died in one-third of all nests within days of hatching as a result of aggression from its elders. Kookaburra nestlings attacked each other using a hook on their upper beak – a rare example of a morphological specialisation for sibling rivalry. In one-fifth of all nests, the youngest nestling starved to death much later, without overt aggression, when nestling growth rates were highest. I examined the effects of food availability and competitive disparities between nestlings on the incidence of both types of siblicide. The probability of late, starvation-mediated mortality was negatively correlated with the number of male helpers. Early, aggressively mediated siblicide occurred in nests characterised by a suite of correlated variables that I call the ”kookaburra siblicide syndrome”: (1) no male helpers attended the nest, (2) the third-hatched nestling was much smaller than the second-hatched nestling, (3) the first and second nestling to hatch were male and female, respectively, and (4) there was a short hatch interval between the first two nestlings. The kookaburra siblicide syndrome variables could be inter-correlated if they were all related to the female’s condition at the onset of incubation. Females in poorer condition may be less likely to have male helpers, more likely to lay small third eggs, and more likely to hatch the first two eggs relatively synchronously because of nutritional constraints during the onset of incubation. These females may further promote siblicide by modifying the sexes of the first two nestlings. If a female hatches soon after an older but eventually smaller brother, dominance between the first two nestlings could be destabilised. I suggest this leads to escalated aggression in the nest and the death of the third nestling, which is least able to defend itself. Received: 17 December 1999 / Received in revised form: 8 May 2000 / Accepted: 20 May 2000     

Relatedness, polyandry and extra-group paternity in the cooperatively-breeding white-browed scrubwren (Sericornis frontalis )

We used DNA fingerprinting to examine the genetic parentage and mating system of the cooperatively breeding white-browed scrubwren, Sericornis frontalis, in Canberra, Australia. Our analyses revealed a remarkable variety of mating tactics and social organization. Scrubwrens bred in pairs or multi-male groups that consisted of a female and two or more males. Females were always unrelated to the pair male or alpha (dominant) male. Among multi-male groups we found three different mating tactics. Firstly, when alpha and beta (subordinate) males were unrelated, they usually shared paternity in the brood. This resulted in both males gaining reproductive benefits directly. Secondly, when beta males were not related to the female but were related to the alpha males, beta males sired offspring in some broods. In this situation, beta males gained reproductive benefits both directly and potentially indirectly (through the related alpha male). Thirdly, when beta males were related to the female or both the female and alpha male, they remained on their natal territory and did not sire any offspring. Thus beta males gained only indirect reproductive benefits. Overall, when group members were related closely, the dominant male monopolized reproductive success, whereas when the members were not related closely the two males shared paternity equally. This positive association between monopolization of reproduction and relatedness is predicted by models of reproductive skew, but has not been reported previously within a single population of birds. Other cooperatively breeding birds with both closely related and unrelated helpers may show a similar variety of mating tactics. Finally, we found that extra-group paternity was more common in pairs (24% of young) than in multi-male groups (6%), and we discuss three possible reasons for this difference. Received: 21 May 1996 / Accepted after revision: 14 December 1996     

Offspring number in pygmy marmosets, Cebuella pygmaea *, in relation to group size and the number of adult males

In many species of birds and mammals with a co-operative breeding and rearing system, offspring survival is positively related to the number of helpers. In the New World callitrichine primates (marmosets and tamarins), adult males are considered as particularly valuable helpers, and female reproductive success may depend strongly on the males' contribution to infant care. We analysed the number of offspring (infants, juveniles) in groups of wild pygmy marmosets, Cebuella pygmaea (Callitrichinae, Cebidae, Primates), in relation to the number of adult males and to the number of adult and subadult group members. In contrast to other callitrichines with a co-operative system of infant care, no relationship was found between the number of adult males and the number of infants and offspring. However, there was a significant positive relationship between the number of juveniles and the number of adult and subadult group members. The lack of a relationship between infant and adult-male number is interpreted as resulting from the reduced importance of adult males as helpers in pygmy marmosets in comparison to other callitrichines, probably due to the reduced costs of infant care. The relationship between the number of juveniles and the number of adult and subadult group members is in accordance with increased offspring survival in larger groups, as observed in other primates. Received: 1 February 1999 / Received in revised form: 5 June 1999 / Accepted: 29 June 1999     

Subordinate males are more likely to help if unrelated to the breeding female in cooperatively breeding white-browed scrubwrens

Subordinates in communally breeding groups of birds usually help to provision nestlings, but in some species helping-at-the-nest is facultative. In species in which groups usually contain relatives, subordinates either always feed young or are more likely to do so when breeding dominants are close relatives, suggesting that benefits of helping collateral kin are important. In other species, adult group members are unrelated to each other and males may only feed young if they have gained paternity, showing that cooperation is related to the mating system. The white-browed scrubwren, Sericornis frontalis, is a communally breeding species in which most groups consist of a simple pair or a dominant pair with a subordinate male. Subordinate males either fed nestlings in a given nest at a rate comparable to the dominants, or did not feed them at all. Breeding groups usually formed through natal philopatry of males, so that about 80% of subordinates were closely related to one or both members of the dominant pair. However, because of death and dispersal, 54% of subordinates were unrelated to the resident female. Although subordinates with their mother fed nestlings in 48% of cases, they fed offspring in 75% of cases if their mother had been replaced by an unrelated female, suggesting that their decision to help is influenced by the opportunity to mate with the female. Supporting this conclusion, relatedness to the dominant male did not affect subordinate behaviour, and genetic studies showed that subordinates often gained paternity if unrelated to the female. Thus, paradoxically, provisioning nestlings is related to the opportunity for mating in a society in which there is natal philopatry and subordinates are usually related to one or both members of the dominant pair. Received: 25 January 1997 / Accepted after revision: 1 May 1997     

Determinants of male mating success in the red bishop (Euplectes orix)

We studied sexual selection in the red bishop, Euplectes orix, a colonial, polygynous weaverbird widely distributed over sub-Saharan Africa. Male reproductive success measured in terms of the number of nests accepted by females and the number of eggs and nestlings in all the nests on a male's territory varied considerably. The standardized variance (variance/mean²) in male reproductive success ranged from 0.505 to 1.737 in different years, indicating a high potential for sexual selection in this species. An analysis of genetic parentage for 432 nestlings by non-radioactive, multilocus DNA fingerprinting confirmed that male reproductive success (number of young sired on the territory) in this species can be reliably estimated by the measures introduced above. In all 4 study years there was a strong positive correlation between male mating success and the total number of nests that males built in their territories. The number of nests built can be partitioned into the number of weeks a male held a territory and his nest-building performance. Both factors exert a significant positive effect on male mating success and in combination explained between 53.3 and 86.3% of the variation in male reproductive success. Male morphological characters were found to be of no importance. Males that established a territory in the following season built more nests and held their territories for longer than males that did not establish a territory in the following season, suggesting that these measures might be indicators of male condition and quality. Male nest-building performance (number of nests built per week) seems to be unrelated to male condition or quality. Received: 8 January 1999 / Received in revised form: 7 June 1999 / Accepted: 13 June 1999     

Parent blue-footed boobies suppress siblicidal behavior of offspring

Behaviorally dominant nestlings routinely kill sibling nestmates in blue-footed booby (Sula nebouxii) broods during periods of food shortage. Previous work demonstrated that these dominant, first-hatching “A-chicks” regulate the lethality of their behavior towards subordinate, second-hatching “B-chicks,” showing tolerance towards B-chicks except during chronic food shortages. Siblicide by A-chicks usually occurs after the hatchling stage. Results of an interspecific cross-fostering experiment indicated that A-chicks also attempt siblicide shortly after hatching, but parents apparently exert control over these attempts, and thwart them, when chicks are young. Theory predicts selection for such regulation in siblicidal birds that are likely to experience genetic parent-offspring conflict over the value of subordinant nestlings; our evidence of post-hatching parental regulation is consistent with that prediction. Received: 6 June 1998 / Accepted after revision: 12 July 1998     

Helpers-at-the-nest have the same provisioning rule as parents: experimental evidence from play-backs of chick begging

Despite the success of kin selection in explaining helping-at-the-nest among communally breeding birds, we know almost nothing about how helpers regulate their chick-feeding effort. This is especially interesting given how much we now know about parental provisioning `rules-of-thumb' and the evolution of chick begging as an honest signal of `need'. This study explores the provisioning rules of helpers and parents in Arabian babblers (Turdoides squamiceps), using tape play-backs to supplement chick-begging signals and increase apparent brood demand. In all eight groups tested, both helpers and parents fed older, noisier broods at higher rates. Total provisioning rates to nests increased during begging play-back days compared to control days. Absolute provisioning rates by helpers and the scale of their responses to play-backs were statistically indistinguishable from those of parents. In both helpers and parents, increases in nest visits during play-backs were associated with reductions in foraging distance from the nest and increases in size of prey delivered. Older birds of both sexes delivered slightly larger prey items, possibly reflecting differences in foraging ability due to experience. These results are consistent with the idea that, like the parents, helpers-at-the-nest in Arabian babblers provision nestlings as part of a strategy of investment, irrespective of helper age, dominance status or sex. In this species, high relatedness within groups may provide parents and helpers with similar kin-selected fitness benefits, although the mutualistic advantages to helpers from simply augmenting group sizes cannot be ruled out. Received: 17 June 1997 / Accepted after revision: 28 February 1998     

Deception by helpers in cooperatively breeding white-winged choughs and its experimental manipulation

White-winged choughs (Corcorax melanorhamphos) are obligate cooperative breeders, living in groups which may contain up to 20 birds. Although breeding is dominated by a single pair, all birds contribute to rearing young, including the provisioning of nestlings. However, some birds which have carried food to the nest, even to the point of placing the food in the gaping mouth of a nestling, consume the food themselves rather than provision the nestlings. Birds which fail to feed nestlings are typically young, and are only likely to fail to deliver food when they cannot be observed by other group members. Birds which have just failed to deliver food are more likely to engage in alternative helping behaviours such as allopreening the nestlings than are helpers which have just delivered food in the conventional manner. Failure to deliver food is almost eliminated when foraging constraints are experimentally reduced by supplemental feeding of the group. Collectively these observations suggest that young white-winged choughs act deceptively by simulating helping behaviours without sacrificing food supplies. Received: 24 January 1997 / Accepted after revision: 6 June 1997     

Ectoparasites of house sparrows (Passer domesticus): an experimental test of the immunocompetence handicap hypothesis and a new model

Conspicuous secondary sexual traits may have evolved as handicap-revealing signals or as badges of status. We present results of an experiment using males of the sexually dimorphic house sparrow (Passer domesticus), that support the idea that the male-specific bib can be both a handicap-revealing signal and a reliable badge indicating the physical condition of the bird. In a test of the immunocompetence handicap hypothesis, wild-caught adult male house sparrows were studied in captivity. Birds implanted with elevated doses of testosterone were more dominant, had higher circulating levels of both testosterone and corticosterone and they also harboured relatively larger ectoparasite loads. Higher parasite loads were also associated with individuals showing lower immunocompetence and larger changes in bib size. A new model for immunocompetence effects in sexual selection is introduced, integrating actions that the hypothalamopituitary axis exerts on gonads, adrenals and the thyroid gland. The ”integrated immunocompetence model” synthesizes both the ”handicap” (i.e. survival-decreasing) and ”badge of status” (i.e. survival- enhancing) models for evolution of secondary sexual traits. Received: 15 May 1999 / Received in revised form: 2 November 1999 / Accepted: 6 November 1999     

Social system and reproduction of helpers in a cooperatively breeding cichlid fish (Julidochromis ornatus) in Lake Tanganyika: field observations and parentage analyses

It is suggested that some fish of the genus Julidochromis, substrate-brooding Tanganyikan cichlids with biparental care, breed cooperatively with helpers. We studied the social system of J. ornatus in the wild and analysed genetic parentage using microsatellites. Within the studied population three patterns of social system were identified: monogamous pairs (61%, 44 of 72 groups), pairs with helpers (29%, 21), and polygamous harems with helpers (controlled by either a large female or large male owner; 10%, 7). In cooperatively breeding groups, the number of helpers at each nest ranged from 1 to 6 (median 1), and male helpers were more numerous than female helpers. In both sexes, the body size was different among individuals of different social status (harem owner > breeder > helper). Helpers and harem owners of both sexes exhibited brood defence although its frequency was low. The molecular analysis revealed that (1) the helpers were mostly unrelated to dominant breeders, (2) many helpers of both sexes contributed genetically to the next generations, (3) male helpers had high siring success (41% of young in total), and (4) large young unrelated to group members were detected at 30% of observed nests, which may be due to breeder (or helper) replacements and immigration of young. We discuss the implications of these results for understanding the complex social system of this species, especially the low reproductive skew in comparison with other cooperatively breeding cichlids.     

The effects of helpers in cooperatively breeding purple gallinules

Summary The effects of helpers in a population of cooperatively breeding purple gallinules (Porphyrula martinica) were examined. All young birds past the age of 2 months helped feed and protect subsequent broods of chicks and participated in territorial defense. Most helpers remained on their natal territories for approximately 1 year. The number of helpers varied both among and within breeding groups. Clutch production and chick survival were related positively to the number of helpers in the group. The increase in chick survival was independent of several measures of territory quality. Helpers possibly aided chick survival by provicing extra food for the chicks and decreasing predation risk. Helpers were necessary in order for a breeding pair to keep a territory long enough to produce more than one clutch of eggs. A change in the number of helpers (increase or decrease) often was followed by a similar change in territory size. These results suggest that purple gallnule helpers can increase the reproductive success of the breeding group and may be vital for the continued maintenance of a breeding territory.     

Low paternity in the hornet Vespa crabro indicates that multiple mating by queens is derived in vespine wasps

Queen mating frequency was studied in the European hornet, Vespa crabro, by analyzing four DNA microsatellite loci in 20 workers from each of 14 nests. Queens were found to be predominantly singly mated (9/14), although double (4/14) and triple mating (1/14) also occurred. For most multiply mated queens, paternity was significantly biased with the majority male fathering on average 80% of the female offspring. The population-wide effective mating frequency was therefore low (1.11), and sister-sister relatedness high (0.701 ± 0.023 SE). Low effective mating frequency in Vespa, in combination with data from other vespines, suggests that high paternity frequency is derived in the group. Some problems with the non-detection of fathers, where the queen was not sampled or shared alleles with males, are analyzed. Received: 16 November 1998 / Received in revised form: 29 March 1999 / Accepted: 12 April 1999     

Effects of helpers on breeder survival in the red-cockaded woodpecker (Picoides borealis)

Helpers can gain future indirect fitness benefits by increasing the survival of breeders that produce offspring related to the helper. Helping augments group size through the helper's presence and, in some cases, by increasing fledging success. Breeders may then experience enhanced survivorship because of the benefits of living in large groups. Helping may also reduce the workload of the breeder, which in turn may increase the likelihood that the breeder will survive to breed again. We used Cox's proportional hazards model to examine whether breeders' survival in two populations of the red-cockaded woodpecker (Picoides borealis) was enhanced when group size was increased in the presence of (1) the helper itself, or (2) "extra" fledglings (fledglings produced by the breeder because of helping behavior). We found that in the presence of helpers, the risk of a breeder dying declined by 21–42% for males and 0–14% for females. Our results suggest reduced breeder workload as one mechanism to explain reduced breeder mortality in the presence of helpers: breeders spent less time incubating and provisioning nestlings when assisted by helpers. The risk of a breeder dying declined by 16–42% in males and 26–43% in females in the presence of "extra" fledglings. We speculate on possible mechanisms by which fledglings might affect breeder survival. Our results support the hypothesis that helpers gain future indirect benefits by reducing breeder mortality. Electronic Publication     

Maternal energy expenditure does not change with flight costs or food availability in the pied flycatcher (Ficedula hypoleuca): costs and benefits for nestlings

We manipulated parental work load without changing brood size in a population of pied flycatchers Ficedula hypoleuca by removing two primaries (7 and 9) from each wing of females, thus reducing wing area and increasing flight costs. At other nests, we offered supplementary food in the form of live mealworms (10–20 g daily from hatching) to reduce brood demand and thus parental foraging costs. Other nests were left as controls. The daily energy expenditure of females feeding 12-day-old nestlings was measured with doubly labelled water D₂ ¹⁸O. Females in both treatments expended the same amount of energy, fed at the same rate and had similar body masses to birds in the control group. No effect of treatment on male mass and feeding effort was detected. More nestlings, however, died in nests of handicapped females. Nestlings of handicapped females had significantly lower body mass and haematocrit values than nestlings in food-supplemented nests, with nestlings in control nests occupying an intermediate position. The effects of both treatments on nestling mass, haematocrit values and mortality rates were only noticeable in nests infested with mites. Maternal energy expenditure is apparently constrained and offspring pay the costs imposed by reduced provisioning rate or increased demand caused by ectoparasites, while receiving benefits when food supply improves. The presumption that avian reproductive costs derive from changes in a flexible energy output may not be met in many cases. Received: 24 October 1998 / Received in revised form: 15 March 1999 / Accepted: 26 April 1999     

Cooperative breeding by the Galápagos mockingbird,Nesomimus parvulus

Summary The costs and benefits of helping behavior were analyzed for 36 pairs of the Galápagos mockingbird, Nesomimus parvulus, and their associates. Helping at the nest is usually done by sons or males suspected to be offspring of the breeders. Costs and benefits to breeders were assessed by comparison of pairs with and without helpers, and costs and benefits to helpers were assessed by comparison of birds which help and those which establish themselves as novice breeders.Helping behavior benefits breeders by increasing fledging success and by reducing the adult energy load in territory defense and feeding of nestlings. Breeders assisted by helpers may also benefit by decreased nest predation. Helpers enhance their inclusive fitness by helping, and gain directly by increasing their chances of securing a territory. Helpers do not appear to gain any fitness advantage from the experience of assisting, nor do they increase their survivorship by remaining on natal territory.Ecological and demographic features such as saturated territories and low territory turn-over rates due to high adult survival may be primarily responsible for the evolution of the helping behavior, with kinselection reinforcing it. Associated features of this system are a male-biased population sex ratio, a greater energetic benefit to breeding males than to breeding females in having helpers, earlier dispersal and breeding by females than by males, and much more frequent helping by males than by females. These are interpreted as consequences of brothersister aggression that indirectly minimizes the chances of inbreeding.     

Sexual selection on mature male parr of masu salmon (Oncorhynchus masou): does sneaking behavior favor small body size and less-developed sexual characters?

In many salmonid species, males exhibit morphological dimorphism associated with alternative mating behaviors. ”Precocious males” have a small body size with little or no development of sexual characters and adopt sneaking to gain access to females, while ”migratory males” of large body size and well-developed secondary sexual characters fight. We quantified selection on precocious male parr of masu salmon (Oncorhynchus masou) under simulated natural conditions to examine the contribution of morphology to sneaking success. In contrast to the prediction that sneaking behavior favors small body size, we detected selection favoring relatively large body size for sneaking success. This selection pressure was caused by the dominance hierarchy within parr and may have been facilitated by indifference of dominant migratory males to parr. Unlike the secondary sexual characters exhibited by migratory male salmon, such as the hooked snout and humped back, no morphological characters other than body size contributed to the reproductive success of masu salmon parr. This non-contribution may have been responsible for the lack of development of sexual characters in precocious males. Received: 15 November 1999 / Accepted: 20 May 2000     

Old endemics and new invaders: alternative strategies of passerines for living in the Australian environment

Life history parameters of ”old endemics” and ”new invaders” among the Australian passerines were compared, controlling for phylogeny by using current, phylogenetic research methods. Old endemics were found to have significantly smaller clutches and demonstrated significantly more cooperative breeding than the new invaders, whose fledging periods are significantly longer than those of the old endemics. We argue that breeding under conditions of a small annual food increment during the breeding season, as is probably the situtation in Australia, is possible only when clutch size is small, or while breeding cooperatively, or by extending the fledging period. Our data show that the old endemics use the first two options, while the new invaders employ the third. Received: 10 February 1999 / Received in revised form: 10 November 1999 / Accepted: 20 November 1999     

Influence of kinship on helping behavior in Galápagos mockingbirds

Summary The social organization of the Galápagos mockingbird (Nesomimus parvulus) in unusual in that groups frequently include more than one breeding pair (plural breeding), and helping behavior is flexible: some birds neither breed nor help, while others do both. To investigate the influence of kinship on helping behavior, I categorized each bird as a helper or non-helper with respect to each nest within its group where it had an opportunity to help. The incidence of helping varied with relatedness: more birds helped when nestlings available to be fed were close relatives than when not. This result was independent of a higher incidence of helping among males than among females and of variation with age among males. Proportionally more nonbreeding than breeding males helped, but breeding and nonbreeding females helped equally infrequently; breeders helped most often after their own nests failed. The incidence of helping was highest among birds with opportunities to feed offspring of breeders that had fed the potential helper as a nestling, suggesting a mechanism for kin discrimination based on associative learning. Juveniles with opportunities to choose among alternative recipients preferentially fed closely related nestlings, but insufficient information was available to determine if adults also did so. Kinship did not influence the rate at which nestlings were fed by helpers. Juveniles fed nestlings at lower rates than did adult helpers, but helping effort was otherwise unaffected by age, sex, or relatedness. Limitation of help to former feeders functions as a mechanism for directing aid to relatives in a plural breeding system where degrees of kinship vary among potential recipients within the same group.     

Cooperative breeding in purple gallinules: the role of helpers in feeding chicks

Summary The participation of breeders and helpers in the feeding of 21 broods of chicks was studied in a population of cooperatively breeding purple gallinules (Porphyrula martinica). In the breeding group, all birds over the age of 2 months fed chicks. Female breeders fed chicks at the highest rate, followed by male breeders and adult helpers, old juvenile helpers, and young juvenile helpers. The amount of food breeders fed chicks was independent of the number of helpers in the breeding group. However, breeders made fewer feeding visits when they had helpers. Male and female breeders spent similar amounts of time feeding chicks. Helpers spent significantly less time feeding chicks than did breeders. As helpers grew older they fed chicks at a faster rate, made more feeding visits and spent more time feeding chicks. Analysis of variance was used to determine which variables explained the variation in the brood feeding rate (amount of food delivered to an entire brood during one observation). Age of chicks had a significant nonlinear effect, and size of brood and number of helpers had significant linear effects on the brood feeding rate. Chicks in groups with helpers received more food and were accompanied for longer periods of time than chicks in groups without helpers; either or both of these factors may have led to increased chick survival.     

Paternal care in the European starling,Sturnus vulgaris: nestling provisioning

The extent to which male birds in polygynous species with biparental care assist in nestling feeding often varies considerably between nests of different mating status. Both how much polygynous males assist and how they divide their effort between nests may have a profound effect on the evolution of mating systems. In this study we investigated how males in the facultatively polygynous European starling Sturnus vulgaris invested in their different nests. The amount of male assistance affected the quality of the offspring. Polygynous males invested as much as monogamous males, but divided their effort asymmetrically between nests, predominantly feeding nestlings of first-mated (primary) females. Although females partly compensated for loss of male assistance, total feeding frequency was lower at primary females’ nests than at monogamous females nests. Secondary females received even less assistance with nestling rearing, and the extent to which males assisted decreased with the length of the interval between the hatching of the primary and secondary clutches. These results are contrasted with those from a Belgian populations of starlings with a much more protracted breeding season and thus greater opportunities for males to attract additional mates during the nestling rearing period. The results show that both the “defence of male parental investment model” and the “asynchronous settlement model” have explanatory power, but that their validity depends on the potential length of the breeding season. Received: 21 July 1995/Accepted after revision: 13 July 1996