On the Significance of Helping Behavior in Birds
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ON THE SIGNIFICANCE OF HELPING BEHAVIOR IN BIRDS J. DAVID LIGON AND PETERB. STACEY Departmentof Biology,University of New Mexico,Albuquerque, New Mexico87131 USA ABSTR•CT.--Incooperatively breeding birds, the feedingof nestlingsby nonbreedinghelp- ers may be derived from a general stimulus-responseinteraction, widespread among altricial species.It hasbeen suggested that adaptationistshave overinterpretedthis helping behavior. Two distinct points can be recognized here: evolutionary origin and current functional significance.The significanceof helping behaviorto the helper appearsto vary on a species- to-speciesbasis. However, the evidenceoverall does not supporta unitary,nonfunctional or nonadaptiveinterpretation of avian helping behavior.Received 1 February1989, accepted 2 June 1989. THEIMPETUS for this essaywas a paper by Ian aspectsof avian reproductive biology, which Jamiesonand John Craig (1987), "Critique of are basedon male-female and parent-offspring helping behavior in birds: a departure from interactionsand can be accountedfor solely by functional explanations."More recently,Jamie- direct gains in inclusive fitness. son (1989) reiterated and qualified Jamieson's In contrast,Jamieson and Craig (1987) argue and Craig's major arguments. Jamiesonand that the feeding of nestlings by helpers basi- Craig make someimportant and previously un- cally is no more than a manifestationof a gen- statedpoints that merit the attention of the or- eral trait among altricial birds, namely an "au- nithological community. Their nonadaptive or tomatic" response(placing food) to a stimulus "unselected"explanation of helping behavior (the gaping mouth of a vocalizing nestling). in cooperativelybreeding birds, specificallythe They point out that nonbreeding birds of a va- feeding of nestlings by nonbreeders,requires riety of species(including individuals too young a responsefrom function-oriented studentsof to be "hormonally primed") will respondto this avian cooperativebreeding. Jamieson and Craig stimulus. Other lines of evidence also support addresstwo major issues.We present each of a stimulus-responseinterpretation of feeding these issues as a direct statement and offer re- behavior. For example,many casesof interspe- plies to them. cific feeding of nestlings have been recorded 1. Feedingnestlings by nonbreedinghelpers is not (Shy 1982), and a wild bird even fed fish (see a uniquebehavior that sets cooperative breeders apart Welty and Baptista1988: fig. 17-7). Perhapsthe from other avian species.--Theview that avian best evidence for the stimulus-responsenature cooperativebreeding is a subjectapart from oth- of feeding nestlings comesfrom the phenom- er areas of ornithology is based both on the enon of avian brood parasitism.Certain species, existenceof nonbreeding helpers and on the such as many cuckoosand the Brown-headed interpretationof their significance.Nonbreed- Cowbird (Molothrusater) in North America,spe- ing helpers define cooperativebreeding, and cialize in exploiting the generalgaping-feeding early in the modern study of this subject,em- interaction.These points led Jamiesonand Craig phasiswas placed on the conceptof "altruism" to propose "that the feeding of nestlings in by helpers(e.g. Brown 1970,1974, 1975). Brown communalbreeders is maintained by the same and Brown (1981) and Brown (1987) later urged stimulus-responsemechanism that results in caution in the use of the term "altruism." How- parentsfeeding their own young or hostspecies ever, the perceptionhad been establishedthat feeding parasitic young.... "(Jamieson and feeding behavior by nonbreeding helpers was Craig 1987: 80). a costly behavior in terms of personal repro- Jamiesonand Craig argue that the feeding of ductive successand that helperswere repaid by nestlings by nonparents is not a uniquely gain in the indirect component of their inclu- evolved character that distinguishescoopera- sive fitness. This dichotomy--specieswith al- tively breeding speciesfrom other birds. Rath- truistic helpers and specieswithout helpers-- er, it is the nondispersalof young birds that tended to foster the view that avian cooperative provides these nonbreederswith accessto the breeding is fundamentally distinct from other stimulusof begging nestlings(also see Wool- 7OO The Auk 106: 700-705. October 1989 October1989] HelpingBehavior in Birds 701 fenden and Fitzpatrick ! 984:345). Jamiesonand lings and therefore have accessto them. This Craig conclude that no evolutionary change factor probably is shared by all cooperative based on selection for helping behavior per se breeders (Fig. 1). However, developments sub- has occurred in cooperative breeders. By this sequentto this common starting point are the view, cooperativebreeding is no more than the onesof specialinterest to most studentsof ad- outcomeof ecologicallybased natal philopatty, aptation(e.g. "... adaptationshould be defined which provides the opportunity for the stim- by its effectrather than by its causes... ," Clut- ulus-response feeding interaction between ton-Brockand Harvey 1979,also see Mayr 1983). nonbreeding helpers and nestlings. As Sherman (1988) pointed out, hypotheses A question that arises is whether Jamieson about the evolutionaryorigin of a trait and its and Craig have confounded two separateissues: current significanceare at different "Levels of origin of a trait and currentutility or functional Analysis" and thus are not alternatives. Few significanceof that trait (Tinbergen 1963, Sher- students of cooperative breeding have con- man 1988). This leads to their second and more founded origin of helping with its current func- controversial point. tional effects (contraJamieson 1989). 2. It is inappropriateto interprethelping behavior It is likely that no adaptivebenefit to helpers, in cooperativebreeding systems in anadaptive frame- direct or indirect, will be detectable in each and work ("We therefore advocate a complete de- every cooperatively breeding species.We are parture from increasedfitness-type arguments looking at a variety of birds through a single to explain the occurrenceof so-calledhelping slice in time; and the time elapsed since the behavior." Jamieson and Craig 1987: 92).-- initiation of group-living via natal philopatry, Jamiesonand Craig'sview of helping behavior as well as the ecology and intensity of subse- as a single stimulus-responseinteraction has a quent selection,almost certainly will vary from certain appeal in that it hypothesizes a single speciesto species(Fig. 1). In caseswhere co- explanation for the feeding of nestlings. For operativebreeding hasbeen the rule for a long example,in a variety of cooperativelybreeding time, we may be able to documenta benefit of species,no positive effect of feeding behavior somesort to the helpers. This provides a feed- on reproductive successor survival of group back system that can reinforce the feeding be- members has been observed;in some coopera- havior and fine-tune the entire nestling-helper tively breeding species,helpers unrelated to the interaction. young occur regularly; and in somewell-stud- If helping behavior is costly to the helper, ied cooperative breeders, there is no relation- and if it persists,we would expect a compen- ship between degree of genetic relatednessand sating benefit. However, with one possibleex- feeding effort by helpers (e.g. Rabenold 1984, ception(Reyer 1984),no costof helping in terms 1985;Emlen and Wrege 1988).At one level these of direct fitness has been detected for any co- facts appear to support Jamieson'sand Craig's operative breeder. In addition, the stimulus-re- unitary, nonadaptive explanation of helping sponsefeeding behavior probably will nearly behavior. However, this diversity of observa- always be maintained by natural selectionbe- tionsalso suggests an alternative interpretation. causeof its overwhelming importance in pa- The relevant data on cooperative breeders rental care (Jamieson 1989), because all birds suggeststo us that Jamieson and Craig have hatch with the possibility of becomingparents overextendedtheir nonadaptive view of the (i.e. the costof respondingto a nearby gaping helping phenomenon. Although we agree that mouth rarely will exceed its benefits), and be- early in the study of cooperativebreeding too causeproduction of offspringis by far the pri- much emphasis was placed on kinship or in- mary means of maximizing individual fitness. direct fitness as an adaptive explanation for Interactionswith nestlings (e.g. feeding and helping, we believe also that the way to un- grooming)can potentially increase the director derstand helping behavior is to recognize and personalfitness of helpers.Because of the large appreciate the variation among cooperative numberof socialrelationships that maybe mod- breeders in both the circumstances and the ef- ified to the helper's advantageby virtue of its fects of helping. We concur with Jamiesonand feeding and other cooperativebehavior, devel- Craig that the feeding responseof helpers prob- opmentor strengtheningof personalbonds with ably occursin a proximate sensebecause non- the youngbirds canbenefit greatlyboth helper breedersare in closeproximity to begging nest- and nestlings. For example, in Green Wood- 702 LIGON^ND ST^CEY [Auk, Vol. 106 EcologicalFactors Natal(SetsPhilopatrystage for: ) Evolutionary (unselectedS-Rfeeding behavior) Functional Consequence SpeciesA SpeciesB SpeciesC (Nodetectable fitness benefit to (Weakfeedback benefits tohelper; (Strongfeedback benefit to helper} herper} oftenconfounded with variation in territoryquatity