Delayed dispersal as a potential route to cooperative breeding in ambrosia beetles

Xyleborini are a species-rich tribe of ambrosia beetles, which are haplodiploid and typically mate among siblings within their natal brood chamber. Several characteristics of this tribe would predict the evolution of higher levels of sociality: high genetic relatedness within galleries due to inbreeding, high costs of dispersal and the potential benefit of cooperation in brood care within the natal gallery (e.g. by fungus gardening, gallery extension, offspring feeding and cleaning). However, information on the social system of these beetles is very limited. We examined the potential for cooperative breeding in Xyleborinus saxeseni by monitoring dispersal in relation to brood size and composition. Results show that adult female offspring delay dispersal despite dispersal opportunities, and apparently some females never disperse. The females’ decision to stay seems to depend on the presence of eggs and dependent siblings. We found no indication that female offspring reproduce in their natal gallery, as colonies with many mature daughters do not contain more eggs than those with few or no daughters. There is a significant positive relationship between the number of females present and the number of dependent siblings (but not eggs), which suggests that cooperative brood care of female offspring raises colony productivity by improving survival rates of immatures. Our results suggest that cooperative breeding is likely to occur in X. saxeseni and possibly other xyleborine species. We argue that a closer look at sociality within this tribe may yield important information on the factors determining the evolution of cooperative breeding and advanced social organization.     

Sex ratio,monogamy and breeding success in the Midas cichlid (Cichlasoma citrinellum)

Summary The Midas cichlid (Cichlasoma citrinellum) is a large, aggressive monogamous fish from the Great Lakes of Nicaragua. It lives in an ecosystem where breeding sites are at a premium and where breeding success can be low. I tested the strength of the pair bond by manipulating the sex ratios in captive groups, using ratios of 1:1, 2:1, 4:1, 1:2 and 1:4 (:). No polygamy was seen at any of the ratios. Departure from a ratio of 1:1 decreased breeding success for those pairs that formed. Both sexes appeared to enforce the pair bond but did so in different ways: females attacked males and females equally but males attacked other males significantly more than they did females. These results, coupled with field observations, indicate the Midas cichlid is obligated to monogamy by the demands of competition for breeding sites, the need for two parents to protect the fry and by energetic constraints.     

Family insurance: kin selection and cooperative breeding in a solitary primate (Microcebus murinus)

Lactation imposes substantial physiological costs on mothers and should therefore not be directed towards foreign offspring. Such allonursing, however, is common in mammal species that share roosts. Hypotheses to explain allonursing among such plural breeders include misdirected parental care, milk evacuation, brood parasitism, reciprocity, and kin selection. The necessary behavioral data, in combination with data on kinship and kin recognition, have rarely been available to distinguish among these explanations, however. In this study, we provide evidence for cooperative nursing and adoption by plural-breeding females in a nocturnal primate, the gray mouse lemur (Microcebus murinus), in which females forage solitarily during the night, but form day-time sleeping groups with one to two other females. We observed 34 resident females in an 8 ha study area in Kirindy Forest, Madagascar, over three consecutive annual breeding seasons and determined genetic relationships among all members of this population. Five sleeping groups of adult females were filmed inside their roosts during one breeding season after females gave birth. The composition of groups changed substantially across years, but they always consisted of close maternal relatives. All females within a group gave birth to one to three infants. They regularly transferred only their own offspring among roosting sites, demonstrating an ability to discriminate between their own and other’s offspring, but they regularly groomed and nursed related offspring other than their own and adopted related dependent young after their mother’s death. Kin selection may therefore be the main selective force behind cooperative breeding among these closely related females with a high mortality risk, providing each of them with family insurance.     

Delayed breeding in the cooperatively breeding Florida scrub-jay (Aphelocoma coerulescens): inhibition or the absence of stimulation?

To determine whether fundamental differences exist in the reproductive physiology of breeder and nonbreeder Florida scrub-jays (Aphelocoma coerulescens), we compared plasma levels of testosterone (T) and luteinizing hormone (LH) in males, and estradiol (E₂) and LH in females. Although male breeders had higher overall T and larger testes, nonbreeders’ T paralleled that of breeders, and their testes were more than an order of magnitude larger than regressed testes. Breeder and nonbreeder males had equivalent baseline LH, and equivalent changes in LH following a gonadotropin-releasing hormone (cGnRH-I) challenge. The T, LH and GnRH challenge data indicate that nonbreeder males have functional hypothalamo-pituitary-gonadal (HPG) axes. We found no hormonal evidence of inbreeding suppression in males: nonbreeders that did not live with their mothers and those that did had similar T. Male nonbreeders that were exposed to E₂-implanted females had higher T than did controls, suggesting that the lack of within-pair stimulation is a key factor in whether an individual delays breeding. Female nonbreeders had E₂ titres equal to or higher than breeders and neither basal LH nor LH following GnRH challenge differed by breeding status. Nonbreeders’ ovarian follicles were smaller than breeders’, but were larger than they would be during the non-breeding season. These data suggest that nonbreeders were primed for breeding and were simply waiting for an opportunity or a required stimulus. Female nonbreeders that lived in a territory with an unrelated male breeder had significantly higher E₂ than those that remained with their fathers. Similarly, nonbreeders that were captured away from their home territories had elevated E₂. However, nonbreeders that lived with their fathers had E₂ that was equivalent to breeding females, suggesting that inbreeding avoidance may not be the primary factor leading to delayed breeding in females. Received: 13 June 1995 /Accepted after revision: 27 April 1996     

Sociality and cooperative breeding of red-cockaded woodpeckers,Picoides borealis

Summary Thirty groups of red-cockaded woodpeckers (Picoides borealis) were studied from 1976–1982 to (1) determine the demographic structure of groups, (2) identify the role helpers play in reproductive activities, and (3) investigate the selective pressures promoting sociality and helping behavior. Groups had only 1 mated pair and 0–2 helpers. Approximately half of all groups had helpers and a given group had helpers some years but not others. Helpers, with rare exception, were males 1 or 2 years old and progeny of 1 or both members of the breeding pair. As a result of higher nestling survival, groups with helpers fledged significantly more young per year than unassisted pairs ( , SD=0.97,n=43 vs. , SD=1.01,n=50). Nesting success was also associated with size and quality of nesting period home range, but evidence suggested that the increased number of young fledged resulted directly from the action of helpers. There was a significant positive correlation between reproductive success and experience of breeding females among unassisted pairs but a significant negative correlation among pairs with helpers. In groups with experienced females, helpers were assisting both their mothers and fathers and, therefore, were related to the offspring on the average by 0.50. In groups with inexperienced females, helpers were assisting their fathers and unrelated females and were related to the offspring by 0.25. The red-cockaded woodpecker's unique habit of excavating nest and roost cavities in living pines and the extended period of time required for excavation may be an important ecological constraint that promotes the retention of helpers. Because helpers are related to the offspring they help rear, kin selection and gains in indirect fitness may provide a partial explanation of why red-cockaded woodpecker helpers help. However, the negative correlation between the efficacy of helping behavior and the helpers' relatedness to the offspring they help rear implies that helpers are least effective in producing offspring which would represent greatest gains to indirect fitness. This raises questions about the relative importance of kin selection and indirect fitness in the evolution of helping behavior among red-cockaded woodpeckers.     

Reproductive sharing and proximate factors mediating cooperative breeding in the African wild dog (Lycaon pictus)

Although dominant African wild dogs (Lycaon pictus) are generally believed to be the sole breeders within a pack, earlier behavioral and endocrine data suggest that reproduction could be shared with subordinates. We performed an extensive behavioral, demographic, and genetic evaluation of a wild dog population in South Africa to examine the level of such sharing and the proximate mechanisms influencing reproductive contributions of each sex. While a majority of pups were born to dominants because of a lack of subordinate potential breeders, we discovered a substantial portion of reproductive sharing between dominants and subordinates. Compared with alpha females that mated annually, subordinate beta females bred in 54.5% of years whereas thetas never bred. The three top-ranking males all sired pups (56.0%, 32.0%, and 12.0%, respectively) when three or more adult males were present. With only two pack males, alpha and beta individuals shared reproduction nearly equally (55.2% and 44.8%, respectively), and litters of mixed paternity were discovered on eight of 15 (53.3%) occasions. A skewed adult sex-ratio and frequent alpha mortalities for females and behavioral aggression in males allowed most individuals to attain dominant status in their lifetime, creating a constantly shifting social hierarchy. Genetic parentage results corresponded to reported hormone profiles, suggesting physiological suppression in some lower-ranked individuals of both sexes. Thus, a combination of demographic, behavioral, and hormonal proximate factors mediates reproductive partitioning in wild dogs. We conclude that reproductive sharing can be significant in this species, especially for males that have less robust suppressive mechanisms than females.     

The behavioral regulation of monogamy in gibbons (Hylobates muelleri)

Summary Responses of mated individuals to playbacks of the songs of solitary females and males permit evaluating the behavioral mechanisms maintaining monogamy in gibbons. When female songs are played back from the centers of their ranges, mated female gibbons typically initiate duets and group approaches toward playback sites. Female songs played back from range boundary locations elicit duetting responses. Responses to solitary female songs do not differ from responses to song duets used by established mated pairs to mediate patterns of intergroup spacing. Mated males lead silent group approaches toward the sites of male song playbacks. These results suggest that range defense by female gibbons forces males into accepting monogamous mating relationships and that monogamy in gibbons is regulated by intersexually-supported, intrasexual aggression.     

Male's return rate, rather than territory fidelity and breeding dispersal, explains geographic variation in song sharing in two populations of an oscine passerine (Oreothlypis celata)

Males of some oscine passerines learn and share songs of neighboring males. This process can lead to the formation of song pattern neighborhoods or microhabitat song dialects. The degree to which song sharing occurs between populations and the spatial scale over which neighboring males share songs, however, can vary widely, and interpopulation comparisons have suggested that song sharing is more common in residents than in migrants. Here, we examine two populations of the orange-crowned warbler (Oreothlypis celata) to quantify patterns of song sharing at the northern (long-distance migrant) and southern (short-distance migrant) edges of the breeding distribution and to test if return rate, territory fidelity, and breeding dispersal explain the patterns found in the two populations. The southern population (O. celata sordida breeding on Santa Catalina Island, California; 33°N) had a higher annual return rate to their territories and exhibited higher song sharing in neighborhoods than their counterparts (O. celata celata breeding in Fairbanks, Alaska; 64°N). Year-to-year patterns of territory fidelity and breeding dispersal distances were similar between populations. Our results suggest that if migratory distance generally covaries with the proportion of returning males, this could explain different levels of song sharing between the short- and long-distance migrants.     

Sex and status in a cooperative breeding fish: behavior and androgens

Among taxonomically widespread cooperatively breeding vertebrates, those with non-breeding helpers-at-the-nest provide an excellent opportunity to understand the proximate mechanisms underlying care and allocare. In this study, we examined androgen levels in relation to care behavior in a cooperatively breeding cichlid fish, Neolamprologus pulcher, from Lake Tanganyika. We concentrated on androgens, as these hormones have been linked to the defense behavior, and the defense of young is a common form of parental care in fishes. N. pulcher dominant female breeders performed the most care and also displayed the highest levels of plasma testosterone (T) compared with other individuals within the social group. We also found that dominant male breeders provided a similar amount of care as did the subordinate helpers, but breeding males had the highest levels of 11-ketotestosterone (11KT), an important androgen in fish. Breeders had higher levels of both androgens (T and 11KT) compared to helpers. There was a weak but significant positive correlation between T levels and the frequency of care regardless of sex and status. Our results suggest that androgens may promote defense of young and are in contrast to the commonly reported trade-off between androgen and parental care.     

The relationship between ecology and the incidence of cooperative breeding in Australian birds

Summary Australia has many cooperatively breeding species of birds. These tend to occur in eucalypt and semi-arid woodlands rather than in rainforests or deserts. They tend to be insectivores that pursue rather than sit and wait for their prey, and tend to forage on the ground rather than above it. We propose that environments where resources do not show marked seasonal fluctuations are those in which cooperative breeding is most likely to evolve. Under these conditions birds might experience difficulty acquiring the extra food necessary to breed, especially if inexperienced. When adult survival was high, young and inexperienced birds could delay breeding. Unpredictable environments may also favor cooperative breeding, but our data do not strongly support this. Groupliving would be favored further if young birds are particularly vulnerable to predators when alone. They should therefore remain in the family group and delay their dispersal unitl a suitable breeding vacancy becomes available. These hypotheses are not mutually exclusive, but are complementary. Both may be required to ensure that at least some year-old birds do not breed and also do not disperse. We believe that they give rise to predictions, which can be tested in future field studies.     

Predator stimuli and calling behavior of Carolina chickadees (Poecile carolinensis), tufted titmice (Baeolophus bicolor), and white-breasted nuthatches (Sitta carolinensis)

Evidence from different chickadee species (Poecile genus) indicates that birds can modify the note composition of their “chick-a-dee” calls in the presence of predator stimuli. Here, we tested the effects of predator models and the distance of those models on calls of three species foraging together at feeding stations: Carolina chickadees (Poecile carolinensis) and tufted titmice (Baeolophus bicolor), both members of the Paridae family, and white-breasted nuthatches (Sitta carolinensis), a member of the Sittidae family. Model and distance affected seed-taking rates in all three species. “Chick-a-dee” calling rates were higher in the predator context for both chickadees and titmice, but we detected no predator context effects on “quank” call rates for nuthatches. Predator and distance contexts affected acoustic parameters of notes of the “chick-a-dee” calls of chickadees and titmice; no such effects were detected for nuthatch “quank” calls. These results suggest species differences in encoding of information in the primary social calls of these three species that commonly occur in multi-species flocks. Chickadees and titmice are “nuclear” species and nuthatches are “satellite” species, and these different roles might be related to the differences in vocal signaling that we detected.     

Natal dispersal in Belding's ground squirrels (Spermophilus beldingi)

Summary Dispersal from the natal site was documented in two populations of Belding's ground squirrels (Spermophilus beldingi) living at different altitudes in the Sierra Nevada of North America. Distance dispersed and age at dispersal were monitored by a combination of observation, trapping, radio telemetry, and examination of road kills. Dispersal was sexually dimorphic in both populations (Tables 1 and 2). All surviving males emigrated before they were 55 weeks of age, with most dispersing midway through the juvenile summer (Fig. 1). By contrast, most females remained within the boundaries of their mothers' home range (Fig. 2 and 3). Those very few females that did emigrate moved distances from their natal burrows similar to those travelled by dispersing males (200–450 m; Table 2), but females tended to disperse at a slightly older age. Significant differences between the study populations were found in distances moved by juveniles of both sexes (Fig. 2). Body weights of juvenile male dispersers were significantly greater than were those of juvenile males of equivilent ages that had not yet dispersed (Fig. 4). The results were considered in light of Shields' (1982) discussion of dispersal and inbreeding. I concluded that if dispersal is related to reproductive success, then dispersal distances selected for use in tests of evolutionary hypotheses should be measured just prior to the subject animals' first reproduction. Finally, although not tested in the present study, the evolutionary hypothesis most consistent with my data suggests that dispersal in S. beldingi may function to minimize nuclear family incest.     

Social monogamy and extra-pair fertilization in an Australian lizard, Tiliqua rugosa

This study investigates social monogamy in the Australian sleepy lizard, Tiliqua rugosa. At a 70-ha site near Mount Mary, South Australia, we radio tracked 55 adult female and 39 adult male lizards during their spring activity periods. Each lizard was observed in 1–5 years. Females were observed with a single male partner on an average of 10.8 days per year, although in 17.3% of cases, females were observed on 2 or fewer days with a male. The most intense pairing period each year was 15 September–15 November when females were with male partners on an average of 36% of observation days. Partnerships lasted an average of 43.3 days each year. After mating in early November, the pairs separated. Observations of females pairing with other males were rare. Most males (82%) were also consistently monogamous, although 7 were observed pairing with 2 females within one season. To investigate paternity, we allowed 21 gravid females to give birth to 42 offspring in the laboratory. We determined genotypes at five polymorphic microsatellite DNA loci for the females, their male partners and their offspring. Four litters (19%) and 6 of the offspring from those litters (14.3%) showed evidence of extra-pair fertilization (EPF). Although the sample sizes are small, females of polygynous males were more likely to experience EPF. Received: 22 February 1998 / Accepted after revision: 23 May 1998     

Fitness costs of dispersal in red foxes (Vulpes vulpes)

The costs of dispersal are an important factor promoting natal philopatry, thereby encouraging the formation of social groups. The red fox, Vulpes vulpes, exhibits a highly flexible social system and one that is thought to represent a possible stage in the evolution of more complex patterns of group-living. Although the potential benefits accruing to philopatric offspring have previously been studied in this species, the potential costs of dispersal have received less attention. We contrasted survival rates, nutritional status, injuries and reproductive output of dispersing and non-dispersing male and female foxes in an urban population to assess the relative costs of dispersal versus natal philopatry. Mortality rates were not significantly higher for dispersing foxes, either in the short- or long-term. There was no evidence of increased nutritional stress in dispersing individuals. Dispersing individuals did, however, exhibit greater levels of wounding, although this did not appear to affect survival. Dispersing females were more likely to miss a breeding opportunity early in their reproductive lifespan. In contrast, both dispersing and non-dispersing males were unlikely to breed in their first year. We conclude that the major fitness component in females affected by dispersing is age at first reproduction.     

Positive correlation between helpers at nest and nestling immune response in a cooperative breeding bird

In cooperatively breeding species, helpers may contribute to the success of the brood by increasing the number of independent offspring, but also, they may affect offspring condition and, hence, their survival and recruitment into the breeding population. This second type of benefits is rarely included in theoretical models or assessed in field studies. Immune response is a good proxy of individual quality and fitness, and there is good evidence that the performance of the immune system of chicks during the nestling phase is related to their chances of survival and future reproduction. However, no study has so far explored whether helpers at the nest might contribute to enhance immune functioning of nestlings in species with a cooperative breeding system. Here we investigate this issue in the azure-winged magpie (Cyanopica cyanus) and found for the first time a positive correlation between the number of helpers at nest and the cell-mediated immune response of nestlings. This effect was not explained by a general improvement of body condition of chicks because it was independent of individual variation in body mass or tarsus length. Our results suggest that helping can have subtle effects on the quality of offspring that may influence their survival and future reproduction.     

Natal dispersal and philopatry in prairie voles (Microtus ochrogaster) in relation to population density,season, and natal social environment

Summary We used intensive livetrapping to examine natal dispersal and philopatry in prairie voles (Microtus ochrogaster). The majority of male (70.0%) and female prairie voles (75.1 %) remained at the natal nest until death. Those males and females that did disperse left home at about the same age (45–55 days) and moved similar distances (28–33 m). Dispersal was more common (1) from small natal groups than from large natal groups, (2) following disappearance of parents, (3) during the breeding period than during the nonbreeding period, and (4) at low population densities than at high densities. Dispersal was not associated with level of competition for mates within natal groups, and dispersers did not differ from nondispersers in body weight. Our data do not support competition for mates or resources as important factors influencing natal dispersal in prairie voles. The absence of sex differences in dispersal tendency or distance, and our fording that more than half of dispersers had become reproductive before leaving the natal nest, lead us to suggest that inbreeding avoidance is not a primary function of dispersal in this species. Dispersal was, however, more common when potential mates within the natal group were relatives than when they were nonrelatives. Although not tested here, if family members avoid mating with one another through patterns of mate choice, then some animals may leave home in search of mates. The precise benefits associated with philopatry in prairie voles remain to be identified. Correspondence to: B. McGuire at her present address     

Colonial breeding and nest defence in Montagu's harrier (Circus pygargus)

We assessed whether colonial breeding allows individuals to decrease their investment in predator defence, by presenting decoys of owls, foxes and crows to Montagu's harrier, Circus pygargus. Decoy detection increased with colony size, as did the number of individuals mobbing the decoy. The number of mobbers was greater for predators potentially risky for the adults (owl or fox) than for non-dangerous predators (crow). Recruits (breeding neighbours, fledglings and non-breeders) were present a lower percentage of the time, and attacked and alarm called less frequently than tested individuals. Nevertheless, the overall attack rate on the predator increased with the number of mobbers. When the size of the mobbing group increased, individuals were more likely to attack predators that represented a risk for adults, but did so less intensively and with a lower frequency of close dives. Thus, coloniality decreased the individual costs of defence in terms of risk taken, whilst enhancing defence efficacy. Birds alarm called more intensively when presented with dangerous predators than with the crow. The number of recruits significantly increased with increasing alarm rate of the tested individuals, even when taking colony size into account. Furthermore, the alarm rate of the tested birds also had a significant effect on the proportion of recruits that engaged in attacks against dangerous predators but not against the crow. The higher recruitment and attack rates for dangerous predators were thus apparently modulated through alarm calling. We discuss whether tested birds may manipulate recruits' behaviour to lessen their own risk.     

Forced dispersal of juvenile guanacos (<Emphasis Type="Italic">Lama guanicoe</Emphasis>): causes,variation, and fates of individuals dispersing at different times

We examined adult-juvenile conflict in the guanaco (Lama guanicoe). During spring, territorial males become increasingly aggressive toward all juveniles born the previous year and begin expelling them from family groups. In an apparent effort to reduce aggression, juveniles display submissive crouches when being observed, approached, or attacked by the territorial male. Therefore, we assessed the influence of juvenile submissive behavior on the timing of dispersal and also examined if dispersal time was related to survival and reproductive performance as adults. We also evaluated hypotheses regarding the evolution of juvenile mammalian dispersal in the context of if and how each may favor the forced dispersal of juvenile guanacos by territorial males. Juveniles generally dispersed in late spring and early summer, and a nearly equal proportion of females (n=46; 48%) and males (n=49; 52%) dispersed. More-submissive animals generally dispersed later than less-submissive animals. Juvenile sex and dispersal time were not related to survival. In contrast, juvenile sex and dispersal time were related to reproductive performance. The probability of reproducing was highest when juveniles dispersed early and decreased with increasing time in family groups prior to dispersal. The largest proportion of juveniles was forced to disperse during a 2-week interval following the peak of the breeding season. Competition for food resources is likely very intense at this juncture and territorial males may force older juveniles to disperse in order to divert food resources to younger neonates. Additionally, juveniles may be forced to disperse after territorial males mate their mothers to prevent lost mating opportunities, because females leave territories when their offspring disperse and possibly prior to mating with males. We conclude that the forced dispersal of juvenile guanacos by territorial males is ultimately driven by competition for food resources on territories. The timing of dispersal, however, may be tempered by the chronology of matings between territorial males and particular adult females, and/or genetic relatedness between territorial males and juveniles.     

Carbofuran induced changes in breeding of a freshwater fish,Labeo rohita (Hamilton)

The effect of carbofuran, a carbamate pesticide, on the breeding performance of the freshwater fish Labeo rohita (Hamilton) has been investigated in the present study. Breeding of L. rohita was conducted after treatment with three sublethal concentrations, i.e. 0.06, 0.15 and 0.30 mg L^?1 of carbofuran for 96 h. The present investigation showed that the number of total eggs and total amount of eggs (litre per kg body weight) decreased significantly (p < 0.01) at all concentrations of carbofuran in comparison to controls, while the reduction in fertilization percentage at all concentrations of carbofuran was not significantly different from controls. The reduction in hatching percentage, the expected number of hatchlings, and the expected number of hatched larvae were significantly (p < 0.01) different between treated and control groups at all carbofuran concentrations. No significant differences for the 96 h survivability of hatched larvae were reported at all concentrations of carbofuran.