Tug-of-war over reproduction in a cooperatively breeding cichlid

In group-living animals, dominants may suppress subordinate reproduction directly and indirectly, thereby skewing reproduction in their favour. In this study, we show experimentally that this ability (‘power’) is influenced by resource distribution and the body size difference between unrelated dominants and subordinates in the cichlid Neolamprologus pulcher. Reproduction was strongly skewed towards the dominant female, due to these females producing more and larger clutches and those clutches surviving egg eating better than those of subordinate females, but was not so when subordinates defended a patch. If breeding shelters were provided in two patches, subordinate females were more likely to exclusively defend a patch against the dominant female and breed, compared to when the same breeding resource was provided in one patch. Relatively large subordinate females were more likely to defend a patch and reproduce. Females also directly interfered with each other’s reproduction by eating the competitors’ eggs, at which dominants were more successful. Although dominant females benefited from subordinate females due to alloparental care and an increase in egg mass, they also showed costs due to reduced growth in the presence of subordinates. The results support the view that the dominant’s power to control subordinate reproduction determines reproductive partitioning, in agreement with the predictions from tug-of-war models of reproductive skew.     

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.     

Multiple paternity in the cooperatively breeding fish <Emphasis Type="Italic">Neolamprologus pulcher</Emphasis>

In cooperative breeders, mature males may compete for fertilizations. In this study, we measured the degree of multiple paternity in a natural population of a cooperatively breeding fish. Neolamprologus pulcher (Perciformes: Cichlidae) is a highly social cichlid endemic to Lake Tanganyika. We used highly variable microsatellite loci to survey 12 groups with an average number of 10.6 brood care helpers per group and a total of 43 offspring (mean 3.6 per brood). In 11 of 12 groups, all young were assigned to the dominant female. The dominant male sired all offspring in three groups, part of the offspring in four groups, and in five groups, he had no paternity at all. In total, 44.2% of young were not fathered by the current male territory owner. Multiple paternity was found in 5 of 12 broods (41.7 %), with 8 of 35 young (22.9 %) being sired by males other than the respective territory owners. This is an exceptionally high rate of extra-pair paternity among cooperatively breeding vertebrates. Neither helpers present in these territories during collection nor neighbouring males were unequivocally assigned to have sired these extra-pair young. However, behavioural observations suggest that male helpers may have produced these young before being expelled from the territory in response to this reproductive parasitism. We discuss these results in the light of reproductive skew theory, cooperative breeding in vertebrates and alternative reproductive tactics in fish.     

Female-biased immigration and male peace-keeping in groups of the shell-dwelling cichlid fish Neolamprologus multifasciatus

The small cichlid fish Neolamprologus multifasciatus is endemic to Lake Tanganyika and is unique among fish because it lives in complex social groups with several reproductive males and females, all of which participate in defending their territory against neighbors and intruders. Individuals use empty snail shells for breeding and shelter. Previous parentage analysis using microsatellites suggested occasional exchange of individuals between groups. In field experiments, we found that females showed a higher tendency than males to migrate into territories already occupied by a resident pair. The phenomenon and causes of female-biased immigration were further investigated in aquarium experiments: Nine of 15 females, but only 2 of 15 equally sized males, settled in territories of established pairs. Territorial males exhibited more aggression toward strange males (potential reproductive competitors) than toward strange females (potential additional mates); their females were more aggressive toward strange females (probably competitors for shells) than toward strange males. Apparently, a conflict exists between the sexes regarding the immigration of additional females. This conflict seems to be the selective basis for observed active male interference in aggressive disputes between females in the territory. Interfemale tolerance in a group was greater in the male’s presence than in his absence. Received: 1 February 2000 / Received in revised form: 2 May 2000 / Accepted: 5 May 2000     

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     

Social relationships in a cooperatively polyandrous group of tamarins (Saguinus fuscicollis)

Summary This paper presents detailed data on the social relationships among the adults, and between the adults and young, of a cooperatively polyandrous saddle-back tamarin (Saguinus fusciollis; Callitrichidae) group studied for one year. Some data are also presented from groups studied in other years. Adult males in the study groups gave more grooming than they received, while the opposite was true for females (e.g. Fig. 1). The two polyandrous males in the main study group were very rarely aggressive to each other, rarely tried to disrupt each others' copulations, groomed each other, and occasionally shared food, suggesting that their relationship was more affiliative than agonistic. Data on grooming (Fig. 2), spatial relationships, and the initiation of copulations suggest that the males of this group, may have been somewhat more responsible than the female for the maintenance of male-female relationships. Both males and females performed all forms of parental care except lactation. In the main study group each of the males groomed the offspring and remained in close proximity to them more than did the female (Figs.3 and 4). These data are compared with existing data on social relationships in bird species that exhibit cooperative polyandry.     

Age-dependent vigilance in winter aggregations of cooperatively breeding white-winged choughs (Corcorax melanorhamphos)

Summary Winter aggregation of cooperatively breeding white-winged choughs (Corcorax melanorhamphos) was examined to elucidate the advantages for different group members. Adults have higher vigilance burdens than juveniles when foraging in their regular group. Aggregation of groups in winter enables the older members to reduce vigilance and increase the time spent foraging. Vigilance was lowest and foraging time highest in aggregations of 20 individuals but the size of cooperatively breeding groups did not exceed fifteen. Despite increased foraging time, choughs did not consume more food items when aggregating.     

Social and mating system of cooperatively breeding laughing kookaburras (Dacelo novaeguineae)

DNA fingerprinting was combined with field observations over four breeding seasons to investigate the social structure and mating system of the laughing kookaburra (Dacelo novaeguineae). Groups comprised a socially dominant pair and up to six helpers of either sex. Helpers were always recruited from young hatched in the group. Territorial inheritance, which is a feature of other cooperative breeders and an oft-cited benefit of philopatry, did not occur. Helpers only attained dominant status in an established group by dispersing into a vacant dominant position in that group. However, helpers could also form new groups by excising a new territory, often through a ”budding” process. The mating system was overwhelmingly monogamous. There were no cases of extra-group parentage in a sample of 140 nestlings; within groups of three or more birds, dominance predicted parentage almost perfectly (99.2% of 129 nestlings), irrespective of whether helpers in the group were related to one or both dominant birds. This is contrary to predictions from models of reproductive skew, possibly because they currently fail to incorporate the willingness of females to share reproduction among males. Received: 15 May 1999 / Received in revised form: 2 November 1999 / Accepted: 6 November 1999     

The role of helpers in feeding chicks in cooperatively breeding green (red-billed) woodhoopoes

Summary Observations were made of ten green (red-billed) woodhoopoe Phoeniculus purpureus flocks during the breeding season in order to quantify the relationship between flock size and the amount of food delivered to chicks. The study period was kept short specifically to minimize the effects of environmental stochasticity. Neither woodhoopoe feeding visit rates nor the total amount of food brought to chicks increased with flock size. Although nonbreeders did not increase the net rate of food provisioning to chicks, they reduced parental input in chick rearing, and hence energy expenditure by the breeding pair. However, over an 8-year study period, which includes data for 144 flock years, this did not result in increased breeding frequency or enhanced survival of breeders. There is thus no evidence that helpers' feeding contributions to young per se influence the indirect fitness of helpers.     

Energy expenditure for mouthbrooding in a cichlid fish

Summary Energy costs of mouthbrooding were investigated in the East African maternal mouthbrooder Pseudocrenilabrus multicolor by measuring rates of oxygen consumption. Mothers with their brood in the mouth expended 15.7% more energy than mothers without their brood and 13.8% more than starving nonreproductive controls. After subtracting the energy expenditure of the brood, the excess is reduced to 4.7% and 3.2%, respectively, a difference that is not statistically significant. By contrast, feeding nonreproductive females expended more than twice as much energy as the other groups. We conclude that mouthbrooding is a low-cost strategy profiting from investments made during the preceding nonreproductive phase. The implications for the evolution of mouthbrooding are discussed within the context of ecological constraints.     

Alternative male mating tactics in a cichlid, Pelvicachromis pulcher: a comparison of reproductive effort and success

Pelvicachromis pulcher is a small African cichlid which breeds in holes. Males may either reproduce monogamously (pair males), polygynously (harem males), or be tolerated as helpers in a harem territory (satellite males). These helpers share in defence of the territory against conspecifics, heterospecific competitors and predators. There are two male colour morphs that are fixed for life and are apparently genetically determined. These differ in their potential mating strategy. Red morph males may become harem owners, while yellow morph males may become satellite males, and males of both morphs may alternatively pair up monogamously. We compared the reproductive effort and success of these three male reproductive strategies. Effort was measured as attack rates, time expenditure and the risk of being injured or killed when attacking competitors or predators of three sympatric fish species. Reproductive success was measured by observing how many eggs were fertilized by each male when this was possible, and by using genetic markers. The number of fry surviving to independence of parental care was used as a criterion of success. The reproductive success of harem males was 3.3 times higher than that of pair males and 7 times higher than that of the average satellite male. Dominant satellite males, however, were as successful as monogamous pair males, using the measure of fertilized eggs. To our knowledge, this has not been found previously in any fish species. Both harem and pair males had lower parental defence costs per sired offspring, however, than males using the alternative satellite tactic. Defence effort was significantly related to the risk of injury. Received: 17 January 1996 / Accepted after revision: 9 June 1997     

On the mating system of the cooperatively breeding saddle-backed tamarin (Saguinus fuscicollis)

Summary This paper reports on 5 years of observatiors of individually marked saddle-backed tamarins (Saguinus fuscicollis, Callitrichidae). Although callitrichids have long been presumed to have a monogamous social system, this study shows that the breeding structure of saddle-back tamarin groups is highly variable. Groups most commonly include two or more adult males and a single reproductive female, but occasionally contain only a single pair of adults, or less often, two reproductively active females and one or more males. Data on group compositions, group formations, intergroup movements and copulations show that the social and mating systems of this species are more flexible than those of any other non-human primate yet studied. Infants (usually twins) were cared for by all group members. There were two classes of helpers: young, nonreproductive individuals who helped to care for full or half siblings, and cooperatively polyandrous males who cared for infants whom they may have fathered. The observations suggest that non-reproductive helpers may benefit from their helping behavior through a combination of inclusive fitness gains, reciprocal altruism, and the value of gaining experience at parental care.     

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     

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.     

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.     

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.