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Cooperative Behaviour in Cooperative Breeders: Costs, Benefits, And Behavioural Processes 76 (2007) 100–105 Commentary Cooperative behaviour in cooperative breeders: Costs, benefits, and communal breeding a,b, Jason S. Gilchrist ∗ a School of Life Sciences, Napier University, 10 Colinton Road, Edinburgh EH10 5DT, UK b Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK Received 11 December 2006; accepted 12 December 2006 In this issue, Bergmuller¨ et al. (2007) have provided a valu- one to do something), esp. by sharing the work, cost, or burden of able review paper, re-establishing cooperative breeding within something”. The term “alloparental care”, defined simply as pro- a theoretical framework in field studies of cooperative breeding viding care for offspring of other individuals carries less baggage vertebrates. I am in agreement with the authors in their outlook (Jennions and Macdonald, 1994). and suggestions. In this critical review, I wish to (1) review the Bergmuller¨ et al. (2007) comment that in studies of coopera- costs and benefits approach previously taken in the field, (2) tive breeding, researchers have mainly focussed on the outcomes evaluate communal breeding species with regard to the game- of helping. Historically, studies of cooperative breeding have theoretical approach promoted by Bergmuller¨ et al. (2007), and been concerned with whether alloparental care in cooperative (3) consider the reasons why empiricists researching cooper- breeding species is adaptive, with two principal questions: (1) is ative breeding have generally side-stepped a game-theoretical care costly to the donor, and (2) is care beneficial to the recipient. approach. The adaptive nature of alloparental care is then determined by There is no doubting the great interest in cooperative breed- whether the end inclusive fitness benefits to the carer exceed the ing systems, in particular which individuals care for young, costs of care, with benefits to carers potentially accrued along and the distribution of costs and benefits to care to determine two axes: direct–indirect and present–future (Brown, 1983). whether and how individuals accumulate evolutionary fitness Numerous studies have found evidence that “helpers” directly (Heinsohn and Legge, 1999). However, as Bergmuller¨ et al. improve the survival and present or future reproductive success (2007) point out—this has proceeded relatively independently of breeders (Emlen, 1991). However, some studies have failed of game-theoretical approaches to cooperative behaviour. to detect benefits of the presence of “helpers” to breeders or their reproductive success (Leonard et al., 1989; Magrath and Yezerinac, 1997; Packer et al., 1992; Zahavi, 1990) or have even 1. Alloparental care: costs and benefits shown a negative effect of “helpers” on the fitness of breeders (e.g. Legge, 2000; Woodroffe and Macdonald, 2000). This casts Whilst Bergmuller¨ et al. (2007) are clear in their definition doubt on whether “help” is necessarily adaptive and whether of cooperative breeding systems, characterised by individuals “helpers” actually “help”. In such cases alloparental care may contributing care to offspring that are not their own (Cockburn, represent unselected or even maladaptive misplaced parental 1998; Solomon and French, 1997a; Stacey and Koenig, 1990), care (Jamieson, 1989, 1991). It is important to keep this in mind they are less clear in their use of the terms “helper” and “help- when we consider cooperation and cooperative breeding—we ing”. The use of the terms “helping” and “helper” in cooperative should not simply assume that cooperative behaviour is adaptive. breeding literature is often unfortunate. These terms are loaded In order for a behaviour to qualify as true “help” it must be and implicitly suggest an active altruistic behaviour: a cost to (1) conducted by individuals directly to individuals that are not helper and benefit to recipient. According to the Collins Concise their offspring (otherwise such behaviour is simply accounted Dictionary, the primary definition of “help” is “to assist (some- for as parental behaviour), (2) costly to the individual conducting the behaviour, and (3) beneficial to the receiver (Clutton-Brock et al., 1998). Alloparental care has been shown to be costly in ∗ Correspondence address: School of Life Sciences, Napier University, 10 a variety of studies, both in terms of conditional costs (Arnold, Colinton Road, Edinburgh EH10 5DT, UK. E-mail address: [email protected]. 1990; Clutton-Brock et al., 1998; Heinsohn and Cockburn, 1994; 0376-6357/$ – see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.beproc.2006.12.013 J.S. Gilchrist / Behavioural Processes 76 (2007) 100–105 101 Taborsky, 1984) and survival (Rabenold, 1990; Reyer, 1984). reproductive skew) in their consideration of cooperative breed- Additionally alloparental care has been shown to benefit breed- ing species. Throughout the review, Bergmuller¨ et al. (2007) ers in a variety of studies. Helpers can increase the condition refer to breeders and helpers with the implicit assumption of (Hatchwell, 1999) or survival of the young they rear (Emlen reproductive role division. However, reproductive skew is indeed and Wrege, 1991). Alternatively helpers can reduce the work- a continuum (Sherman et al., 1995; Vehrencamp, 2000), and load of the parents they help through “load lightening” (Crick, there are a number of cooperative breeding species in which 1992). This can increase the probability that the parents sur- it is the norm for breeders to contribute care to offspring that vive to breed again (Koenig and Mumme, 1987; Reyer, 1984; are not their own, e.g. banded mongooses (Mungos mungo) and Russell and Rowley, 1988), or increase their future productiv- grey mouse lemurs (Microcebus murinus)(Eberle and Kappeler, ity, by decreasing inter-birth interval or increasing productivity 2006; Gilchrist, 2004). per litter, e.g. the grey crowned babbler Pomatostomus tempo- The majority of cooperative breeding species exhibit high ralis (Brown et al., 1978), pine vole Microtus pinotorum (Powell reproductive skew, where reproduction is monopolised by one and Fried, 1992), dwarf mongoose Helogale parvula (Creel or a few of the adult group members, and most adults do not et al., 1991), stripe-backed wren Camphylorhynchus nuchalis reproduce but help to rear the breeder’s offspring (Solomon and (Rabenold, 1990) and splendid fairy wren Malurus splendens French, 1997a; Stacey and Koenig, 1990). However, at the oppo- (Rowley and Russell, 1990). site end of the continuum from high skew species are plural Bergmuller¨ et al. (2007) acknowledge that alloparents com- breeding species, with low reproductive skew, where subordi- monly accrue indirect fitness benefits, and briefly summarise the nates commonly breed. Cooperative breeding systems of this principal hypothesised direct fitness benefits to contributors of kind include communal breeders (or “joint-nesting plural breed- alloparental behaviour. Individuals may contribute alloparental ers”, Brown, 1987), in which more than one female lays eggs or care as a payment of rent (pay-to-stay), to increase group size gives birth to young in the same nest or den. For a full discussion (group augmentation), or as an advertisement of status (pres- of the problems and inconsistencies of terminology in the litera- tige or competitive altruism) (see reviews by Clutton-Brock, ture surrounding cooperatively breeding birds and mammals see 2002; Cockburn, 1998; Emlen, 1991). An additional possibility Solomon and French (1997b). Communal breeding is particu- is that individuals contribute alloparental care to gain experi- larly rare. Within mammals it occurs at a high frequency only ence of parental care. Such experience can improve their own in the banded mongoose (Cant, 2000; Rood, 1975) and some future success as parents (Brown, 1987; Heinsohn, 1991; Skutch, rodent species, for example, the house mouse (Mus musculus 1961). Evidence that helpers improve their reproductive success domesticus), Norway rat (Rattus norvegicus) and various cavies from experience gained by helping is available for some species (Hayes, 2000; Solomon and Getz, 1997). Within birds, com- (Komdeur, 1996; Rowley and Russell, 1990). Notably, within munal breeding is typical in only a few species, including the a species alloparents may gain fitness along different axes, e.g. groove-billed ani Crotophaga sulcirostris (Koford et al., 1990), in the pied kingfisher primary helpers gain indirect fitness and pukeko Porphyrio porphyrio (Craig and Jamieson, 1990) and secondary helpers “queue” for a mate (Reyer, 1986). Guira cuckoo Guira guira (Macedo, 1992). It is also notable that in some “cooperative” species, appar- Whilst it is simpler to consider cooperative breeding sys- ent “helpers” may gain personal reproductive success, as for tems with distinct differentiation between the role of breeder male stripe-backed and white-browed scrubwrens Sericornis and (non-breeding) helper (as in systems with high reproductive frontalis (Magrath and Whittingham, 1997; Whittingham et al., skew), this overlooks the interesting dynamics within systems 1997), and male callitrichids (Tardif,1997). Indeed some authors with low reproductive skew where the roles of breeder and helper regard direct access to parentage as an adaptive reason for “help” (or carer) are not clearly differentiated (Lewis and Pusey, 1997). (e.g. Cockburn, 1998), when such examples are perhaps better In communal breeding systems the majority of individuals may regarded as parental care, with
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