Cooperative (communal) breeding: Helpers sacrifice their intelligence for breeders

Eusociality can be considered an extreme of cooperative breeding systems being based on irreversible caste determination. However, many vertebrate species possess more flexible social systems which are based on facultative division of labour and temporal limits on breeding for some members of communities. In cooperative breeding vertebrates, a dominant pair usually produces the majority of the offspring, whereas the cost of caring for offspring is shared by non-breeding subordinates. In certain cooperative breeding animals one or a few dominant females are the only capable of breeding; the subordinates don't have the proper hormone levels to be fertile although they are physiologically equipped for the task.

There is still a great controversy in literature about to what extent cooperative breeding can be explained in terms of kin selection theory. Results so far are mixed: while some studies have produced evidence supporting the association between kinship and contributions for cooperative activities, others have found no consistent association between contributions to helping behaviour and variation in relatedness (for reviews see: Clutton-Brock et al., 2000, 2002).

Cognitive aspects of cooperative breeding are intriguing and have not been studied enough. Serving as helpers for the “royal family” young animals gain experience that can be useful for them in future when they establish their own families. Nevertheless, in many cases helpers have no chance to have their own offspring. Somehow or other, cooperative breeding system enables helpers to sacrifice their intelligence for other members of the community. It is possible that helping individuals accomplish a wider variety of tasks and under more risky circumstances than those who have the opportunity to raise their young being given every support by helpers. Several examples will give us an impression of how division of labour occurs within communities which are based on communal breeding.

In birds about 3 percent (approximately 300 species) of species are known as cooperative breeders. Helpers (also called auxiliaries) at the nest were first described by Skutch in 1935. It was not until the mid-1960s, however, with the advent of modern behavioural ecology, that widespread attention began to focus on cooperatively breeding species (see: Emlen, 1991, 1995).

Cooperative systems often appear to arise when environmental constraints force birds into breeding groups because the opportunities for younger birds to breed independently are severely limited. Limitations may include a shortage of territory openings, a shortage of sexual partners, and unpredictable availability of resources. That cooperative breeding is a common strategy in arid and semiarid portions of Africa and Australia lends strong support to this line of reasoning. For some species the role of ecology is not completely clear

(Arnold and Owens, 1999).

Cooperative breeding may be viewed primarily as a means by which young adults put off the start of their own breeding in order to maximize their lifetime reproductive output, and in the process occasionally promote genes identical with their own via kin selection. There are two types of cooperative arrangements: those in which mature nonbreeders help protect and rear the young, but are not parents of any of them, and those where there is some degree of shared parentage of offspring. Cooperative breeders may exhibit shared maternity, shared paternity, or both.

The best-studied North American cooperative breeders, the Scrub-Jay, Gray-breasted (Mexican) Jay, Groove-billed Ani, and Acorn Woodpecker provide good examples of communal breeding (see: Ehrlich et al., 1988).

Scrub jays in Florida reside in permanent, group-defended territories. Woolfenden and Fitzpatrick (1984) have found that groups consist of a permanently bonded monogamous pair and one to six helpers, generally the pair's offspring of previous seasons. About half the territories are occupied by pairs without helpers, and most other pairs have only one or two helpers. Although pairing and breeding can occur after one year spent as a helper, birds often spend several years as non-breeding auxiliaries. Males may remain in this subsidiary role for up to six years; females generally disperse and pair after one or two years of helping. Helpers participate in all non-sexual activities except nest construction, egg lying, and incubation. Pairs with helpers are more successful - they fledge one and a half times younger than pairs without helpers.

Like the Florida Scrub-Jays, the closely related Gray-breasted Jays live in permanent group-defended territories, and breeding adults are monogamous. Brown (1970. 1974) has shown that the cooperative system of this species is more complex than that of its southeastern relative in several ways. Gray-breasted Jay groups are much larger, ranging from 8 to 18 individuals; thus, they usually include offspring from more than just the preceding year. Within each group, two and sometimes three breeding pairs nest separately but simultaneously each season, and some interference among them often occurs. Interference usually involves theft of nest-lining materials, but can include tossing of eggs from nests by females of rival nests. Although the laying female does all the incubating, she is fed on the nest both by her mate and by auxiliaries. Nestlings receive more than half of their feeding from auxiliaries.

Acorn Woodpecker group of communal breeders is composed from up to 15 members whose territories are based on the defence and maintenance of granaries in which they store acorns (Stacey and Koenig, 1984, 1990, see also: Koenig and Dickinson eds., 2004). Groups consist largely of siblings, their cousins, and their parents. Some of the sexually mature birds are non-breeding helpers. Within each group, up to four males may mate with one (or occasionally two) females, and all eggs are laid in a single nest. Thus paternity and sometimes maternity of the communal clutch is shared.

In mammals more than 100 species have been described as cooperative breeders, and among them are cooperative carnivorous, mongooses (meerkats, dwarf mongooses), primates (marmosets and tamarins), as well as several species of rodents and shrews. As it was noted before, some rodent species possess facultative communality in dependence of their habitat and many ecological factors.

The painted hunting dog (African wild dog) Lycaon pictus provides a good example of obligate cooperative breeding. These dogs live in packs of up to 20 adults, in which most of the time only the alpha pair breeds. The remaining adults are reproductively suppressed and help to raise the pups; they must wait to breed until their circumstances improve, either through the death of a higher-ranking female or by finding a mate with an unoccupied territory (Burrows, 1992; Fuller et al., 1992). Baby sitting is a costly task and this includes: watching pups to prevent loss, alerting them to danger (lions, hyenas), protecting them from smaller predators or alien dogs, and moving them under cover in heavy rain. Other members of the pack are also involved in caring for common babies: they feed pups with regurgitated meat when return from successful hunting. Baby sitting is not an obligatory load for pack members, as they can choose between hunting and guarding young. Researchers observed situations where a dog returned to a den to baby-sit after encountering a predator close by (Malcolm and Marten, 1982). At the same time, Lycaon hunt cooperatively and baby sitting draws a member of a pack away from hunting where both efficiency and the risk to lose prey for kleptoparasites depend on the size of the party (Gorman et al., 1998). It is worth to note that in contrast to queens in eusocial communities that are specialised baby-machines, the breeding female in wild dogs, as in other cooperative carnivorous, is often an experienced hunter, and her presence in the hunting pack may increase efficiency of enterprise. Besides, there is a threshold for the group size to survive. Smaller packs need to hunt more often to feed their pups, especially when using a pup guard (Courchamp et al., 2002).

Another impressing example of obligatory communal breeding in mammals comes from small arboreal monkeys, marmosets and tamarins of the family Callitrichidae endemic to the Northern half of South America. Within the family, cooperative breeding strategies are widespread and virtually all species are characterised by small territorial groups of approximately 4-15 individuals, where reproduction is monopolised by one or a small number of dominant individuals. Typically one dominant female breeds, normally producing dyzigotic twins. An important role of helpers in the group is to assist in the care of the dominant female’s offspring. This is principally by sharing the burden of carrying the relatively bulky twin infants around their arboreal habitat. Each group member helps rear the young, which involves food sharing, caring and defence against predators (Snowdon and Soini, 1988; McGrew and Feistner, 1992).

Life history of Callitrichidae can serve as an example of cooperative breeding in groups consisting both of related and unrelated individuals. Helping behaviour in these primates is thus possibly governed by mechanisms of reciprocal rather than kin altruism. This raises a question to what extend cognitive abilities allow these small primates to calculate reciprocity in their groups. Hauser et al. (2003) have conducted experiments on food sharing within groups of cotton-top tamarins (Saguinus oedipus) concentrating on psychological mechanisms of reciprocity. The design of experiments was based on animals’ tool-using abilities (see Part VI). The apparatus consisted of a tray with an inverted L-shaped tool. When food was on the actor’s side, pulling the tool’s stem brought the food within rich. Similarly with experimental paradigm used in many experiments on social learning (see Part VIII) where researchers trained several animals to be the demonstrators of new skills, here again stooge “altruists” and “defectors” were specially trained to pull pieces of food to their partners or to themselves. Results clearly showed that tamarins discriminate between altruistic and selfish actions, identify and recall conscpecifics by their cooperativeness and give more food to those who give food back. Special series of experiments also demonstrated that tamarins give food to genetically unrelated conspecifics even though they obtain no immediate benefit from doing so. Tamarins therefore have the psychological capacity for reciprocally mediated altruism.

The ability to estimate partner’s cooperativeness and remember the history of inter-individual relationships is particularly important for those communal breeders that incorporate both kin and non-kin into their communities, and whose altruistic acts are costly. This is well illustrated by experiments of Clutton Brock et al. (2000) on individual contributions to babysitting in a cooperative mongoose, Suricatta suricatta.

Meerkats (suricates) are desert - adapted animals living in groups of 3-25 animals that typically include a dominant female that is responsible for more than 75% of all breeding attempts, a dominant male that fathers most of the offspring born in the group and a number of helpers of both sexes. A dominate female controls the presence of subordinate adult females in the group. During the first month of pup’s life babysitters usually remain at the burrow with young for a full day while the rest of the group is foraging and feed little or not at all during their period of babysitting (Clutton-Brock et al., 1999; Doolan and McDonald, 1999). Clutton-Brock et al. (2000) have shown how costly baby sitting is: helper suffer substantial weight losses. It is important that large differences in contribution exists between helpers. These differences are correlated with such characteristics of group members as age, sex, and weight, but, surprisingly, not with their kinship to the young raising. In field experiments researchers regularly provided some group members with food (boiled eggs) matching them with controls of the same sex and age. It turned out that feeding essentially increased contribution of helpers to babysitting. So a regular salary may increase and equalise individual contributions of co-operators. However, in natural situations meerkats cannot rely on donations from above, they rather depend on their ability to distinguish between more and less conscientious cooperators (Fig. X-8).