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 . 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 "" 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'sadvantage by 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 or general group size effects) Fig. 1. The relationshipbetween (1) ecologicalfactors and natal philopatty (constraints,Emlen 1982, or benefits,Stacey and Ligon 1987, in press),and (2) the natal philopatty of helpers and the expressionof the stimulus-response(S-R) interaction (Jamiesonand Craig 1987). hoopoes(Phoeniculus purpureus), helpers can gain and extended this finding. Immigrants also breeding status in a new territory via cooper- sometimeskilled young birds if renestingwas ative group emigration. In this way younger, possible(Stacey and Edwards1983). These neg- subordinateallies are critically important to the ative responsesprovide importantevidence (dif- helper (Ligon and Ligon 1983).The sameis true ferent in kind) that selection has operated on for Acorn Woodpeckers(Melanerpes formicivo- the basic feeding responsein this species. rus;Koenig 1981,Hannon et al. 1985), and Ara- As pointed out earlier, indirect fitness ben- bian Babblers(Turdoides squamiceps; A. Zahavi efits have often been viewed as critical payoffs pers. comm.). In the babblersand the wood- to helpers. We have placed a few selectedco- hoopoes,helpers may compete among them- operative breeders into one of three categories selvesto feed nestlingsand young fledglings to document the variation among speciesin in- by stealingfood from each other and taking it direct fitness effects (Table 1). Additional ex- to the young birds. Feeding behavior may help amples could be added. to cement personal bonds in a manner similar Speciesin CategoryA (Table 1) fail to dem- to alloparental care and grooming in primates. onstrate a positive relationship between help- Thus,helping can producea variety of positive ers and number of related young birds pro- fitnesseffects for a helper which can be viewed duced (the first prerequisite for an adaptive, as adaptationsbased in part on the feeding re- indirect fitness interpretation of helping be- sponse. havior). Three casesillustrate this point: (1) Thus far, we have emphasized adaptive ex- Bednarz (1987) found that pairs and groups of tensions of the basic stimulus-responsebehav- Harris' Hawks (Parabuteounicinctus) showed no ior. The feeding response can be modified in differencein clutch size, number of young pro- other ways, Apparently, it can be repressedby duced per successfulnest, or number of off- selection.Stacey (1979) found in the polyga- spring fledgedper year. (2) For the Pygmy Nut- mous Acorn Woodpecker that individuals that hatch (Sitta pygmaea), Sydeman (1989: 154) joined a groupafter egglaying (thusthey could concludedthat "... helpers appear to be selec- not be parents)declined to feed the nestlings. tively neutral in relation to feeding rates and Koenig (MS) has experimentally corroborated enhancement of reproductive success."Also, October 1989] HelpingBehavior in Birds 7O3

T^BEE1. Selectedexamples of indirect fitnesseffects on helpers. Sourcesfollow scientificnames.

A. No correlation between helpers B. Correlation between presenceof C. Increasedproductivity due and number of fledglings helpers and young birds pro- to helping behaviors duced Harris' Hawk Acorn Woodpecker Parabuteo unicinctus Melanerpesformicivorus Pied Kingfisher Bednarz 1987 Stacey& Koenig 1984, Cerylerudis Koenig & Mumme 1987 Reyer 1984 Pygmy Nuthatch Sittapygmaea Stripe-backedWren White-fronted Bee-eater Sydeman1989 Campylorhynchusnuchalis Meropsbullockoides Rabenold 1984 Emlen 1984 Superb Blue Wren Malurus cyaneus Gray-backedFiscal Shrike Nias 1987; Nias & Ford MS Lanius excubitorius Zack & Ligon 1985 Feeding of nestlings. helpers do not enhance the survival of the Before this interpretation can be accepted,two breeders.(3) Similarly, in the SuperbBlue Wren other points must alsobe considered.First, this (Maluruscyaneus), "the presenceof helpersdid positive relationship may be based on a more not increasethe number of fledglingsproduced general positive group-size effect related to per nestby breedingpairs or the annual repro- predator deterfence. For example, in Florida ductive output of breeders" (Nias 1987, Nias ScrubJays (Aphelocoma c. coerulescens),all social and Ford in press).Many of the Australian categories--breeders,nonbreeding helpers, and speciesthat Dow (1980) referredto as "oppor- immatures--survive better when more birds (i.e. tunisticcooperative breeders" may alsofall into helpers)are present(Woolfenden and Fitzpat- this category.For thesespecies, the feeding of rick 1984). Rabenold (1984) found that repro- nestlingsmay not provide any measurable,in- ductive success,as measuredby fledglings pro- direct fitnessbenefits to the helpers, and this duced,was correlatedpositively with group size appearsto support the arguments of Jamieson in the Stripe-backedWren (Campylorhynchusnu- and Craig. chalis).This effect was not related to feeding Speciesin Category B (Table 1) representthe nestlings.Moreover, juvenile survival over the most common situation and the one most dif- first 6 months was unaffected by group size. ficult to interpret. In these,there is a positive Thus it may be misleadingto concludethat the relationshipbetween numbersof helpers and evolved function of feeding by helpersis for number of young fledged;however, all of these production of younger relatives. speciesare territorial and territory quality may Second,in most cooperativebreeders the ba- affect reproductive success.A causal relation- sic social unit is composedof a breeding pair ship between number of helpers (group size) and their offspringor siblings.In suchsystems, and production of young birds is therefore the only individuals available for a young bird questionable(e.g. Koenig and Mumme 1987: to interact with are its relatives, and it is difficult 165).Various studies (e.g. Zack and Ligon 1985) to identify the evolutionary basis of the ob- have attemptedto separatestatistically these ef- servedinteractions (Ligon 1983). Somestudents fects,but there is no unequivocalevidence that of cooperativebreeding have assumedthat a helpers rather than some aspectof territory positive relationship between helper numbers qualitydrive the positiverelationship between and productionof young birds was driven by group size and productivity (Staceyand Ligon kinship. However, the fact that helpersare usu- 1987). ally related to nestlingsin and of itself doesnot Many of theseexamples also illustrate another necessarilysupport a kin-selected interpreta- potentially confounding problem. If a positive tion of helping behavior.For example,Wilkin- relationshipexists between presence or number son (1988) used both empirical field data and of helpersand number of young producedper computersimulations to investigatethe effects year, a commoninterpretation is that "helpers of food-sharing (a similar form of aid-giving) help." The simple implicationof this interpre- on the probability of survival of vampire bats tation is that this is why helpers are present. (Desmodusrotundus). An intriguing outcomewas 704 LXGONAND STACEY [Auk, Vol. 106 that reciprocalaid-giving contributedmore to nomenon. As Sherman (1988) pointed out, two an individual bat's inclusive fitness than kin- explanatoryhypotheses at different levels of ship, regardlessof relatedness(i.e. cooperation analysis(here origin and current utility) can has personalbenefits apart from, or in addition both be correct. With regard to the latter, it to, genesshared by relatives).This conclusion appearsthat the relative costsand benefitsof is highly relevantto considerationsof the evo- helping behavior for both donors and recipi- lutionary significanceof avian helpers. entsvary from speciesto species,and evenfrom At least two well-studied situations demon- situationto situationwithin a species(e.g. Rey- stratea strongincrease in productionof young, er 1984). The current significanceof helping directly as a result of the food delivered by behaviorin birds cannotbe fully explainedby helpers (Table 1: CategoryC). The striking ef- anysingle adaptive model and in factfor some fect of food delivered by helperson production speciesno adaptivefunction has been identi- of young birds make two colonial species,the fied. Thus the overall significanceof helping White-throated Bee-eater (Meropsbullockoides) behaviorper sewill be understoodonly by in- and the Pied Kingfisher (Ceryle rudis), the vestigatingthe phenomenonon a case-by-case strongestcases known for an adaptive, indirect basis.Although this is not a satisfyingconclu- effectof feeding nestlings(Emlen 1984,Emlen sion, we believe that it is the one best supported and Wrege 1988, Reyer 1984). Helpers in the by current evidence. nonterritorial Pied Kingfisher fall exclusively into one of two categories,primary (closerel- ACKNOWLEDGMENTS atives[r = 0.5 or 0.25])or secondary(unrelated). We thank A. H. Brush for inviting us to write this Becausehelpers exert such a profoundeffect on essay.J. H. Brown, A. H. Brush,R. L. Mumme, R. the number of young produced and because Pierotti,S. Zack,and especiallyS. T. Emlenprovided territory quality is not a confoundingvariable, helpful commentson an earlierversion. Our studies kingfisherprimary helpers are the bestexample on cooperativebreeding have been supported by NSF of a specificadaptive, indirect effectof helping and The National GeographicSociety. behavior. In summary, as Jamiesonand Craig (1987) LITERATURE CITED suggest,placing food in the gaping mouthsof BEDNARZ,J. C. 1987. Pair and group reproductive nestlingsseems to be a basic trait of altricial success,polyandry and cooperativebreeding in birds. This view is supportedby the hundreds Harris' Hawks. Auk 104: 393-404. of speciesexploited by socialparasites and by BROWN,J. L. 1970. Cooperativebreeding and al- the many casesof interspecificfeeding. In co- truistic behavior in the Mexican Jay,Aphelocoma operatively breeding birds, nonbreedingindi- ultramarina. Anita. Behav. 18: 366-378. viduals remain in their parents' territory and 1974. Alternate routesto socialityin jays-- feed youngsters.This may be due initially to with a theory for the of altruism and physicalproximity and free accessto the stim- communalbreeding. Am. Zool. 14: 63-80. 1975. The evolution of behavior. New York, ulus of begging nestlings. According to this W. W. Norton. view, feeding by helpers is not a specially 1987. Helping and communalbreeding in evolved characteristicof cooperative breeders. birds:ecology and evolution.Princeton, New Jer- Among some cooperativelybreeding species, sey, Princeton Univ. Press. however, helping behavior appearsto have re- , & E. R. BROWN. 1981. and in- liable benefitsfor the helper at leastas often as dividual selectionin babblers.Pp. 244-256 in Nat- for the recipients.In these cases,it appearsthat ural selection and social behavior: recent re- the basicstimulus-response pattern emphasized searchand new theory (R. D. Alexanderand D. by Jamiesonand Craig hasbeen affected by nat- W. Tinkle, Eds.). New York, Chiron. ural selectionin a number of diverse ways that CLUTTON-BROcK, T. H., & P. H. HARVEY. 1979. Com- are to the helpers' benefit (via either direct or parison and adaptation. Proc. R. Soc. London B 295: 547-565. indirect fitness gains, or both). If so, the non- Dow, D.D. 1980. Communallybreeding Australian adaptive interpretation of feeding by helpers birds with an analysisof distributionaland en- as proposedby Jamiesonand Craig is usefulto vironmental factors. Emu 80: 121-140. understand the evolutionary background of EMLEN,S. T. 1982. The evolution of helping: I. An helping at the nest, but it is insufficient to ac- ecologicalconstraints model. Am. Nat. 119: 29- count for the current significanceof the phe- 39. October1989] HelpingBehavior inBirds 705

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