MINIREVIEW

The Condor 91:485-492 0 The CooperOrnithological Society I989

ON THE RARITY OF INTRASPECIFIC BROOD PARASITISM1

R. BRUCE MACWHIRTER~ Department of Zoology, Universityof Alberta, Edmonton, Alberta T6G 2E9, Canada

Key words: Brood parasitism; nestparasitism; re- features have favored the evolution of brood parasit- productivestrategy; breeding behavior. ism in waterfowl (Andersson and Eriksson 1982, An- dersson 1984) and why this phenomenon is not more prevalent in altricial birds (Yom-Tov 1980a, Lanier Brood (or nest) parasitism, wherein a female deposits 1982. Haland 1986). The imnortance of these aues- eggsin the nestsof others, is an apparently rare repro- tions’is amplified when viewed in light of Hamilton ductive strategy in birds (documented in ~2% of all and Orians’ (1965) hypothesisthat coloniality should soecies:Pavne 1977a.Yom-Tov 1980a).Parasites mav favor the occurrenceof intraspecificparasitism because lay eggs in other females’ nests or, less commonly, a parasite’s chancesof locating a suitablehost improve physically transfer eggsbetween nestsafter the eggsare considerablywith increasednumbers and proximity of laid (e.g., Trost and Webb 1986, Brown and Brown synchronouslynesting neighbors. 1988a). The conventional view has been that these The aim of this paper is to (1) present additional speciesmost often parasitize the reproductive effort of information from recently publishedstudies on the oc- other species (e.g., Payne 1977a, Yom-Tov 1980a). currence, distribution, and prevalence of intraspecific Recently, however, researchershave recognized that brood parasitism among birds, (2) evaluate methods in an increasing number of species individuals may currently used to identify and quantify intraspecific also parasitize the broods of conspecifics(see Yom- brood parasitism, and (3) provide impetus and direc- Tov 1980a, Andersson 1984 for reviews). Becausethe tion for future investigations of this subject. To this intraspecific phenomenon is less easily observed (i.e., end, I first append Yom-Tov’s (1980a) list of reported sincehost and parasite,and their eggs,are often difficult casesof intraspecificbrood parasitism with recent ac- to distinguish), the actual prevalence of intraspecific counts from the literature and categorizeeach species brood parasitism may be underestimated. Moreover, as having either altricial or precocialyoung, and wheth- despite the difficulties of detecting intrasuecificbrood er they tend to breed colonially. For those speciesthat parasitism, this alternative female reproductive strat- may breed either solitarily or colonially, categorization egy may be an important aspect of the reproductive is based upon the spacing pattern of the population biology of many avian species. from which intraspecific brood parasitism has been The presumed rarity of intraspecific brood parasit- reported. A comprehensive list of interspecific brood ism seems surprising given the potential advantages parasiticspecies does not appearin the literature, there- for the parasite and the intuitive notion that parasitic fore, usingpublished studies,I estimate the number of behavior would have more easily evolved among con- species known to parasitize other species. For com- specifics than between species. A conspecific would parison with intraspecific parasitism I list all “new” present an ideal host due to the nutritional require- (post- 1980) speciesfor which interspecific parasitism ments of the nestling parasite, the compatability of has been documented.Next, I investigatethe problem- parental behavior and egg size (Payne 1977a), and the atic nature of the various criteria used to detect par- synchrony of egg laying by the host and the parasite asitism and postulate that these limitations may pro- (Hamilton and Orians 1965). In fact, it has been sug- hibit an unbiasedassessment of the occurrenceof this gestedthat an early stagein the development of inter- behavior among and within bird species.Furthermore, specific parasitism could well have included intraspe- I make explicit those field techniques best suited for cific parasitism(Hamilton and Orians 1965, Yom-Tov detecting and measuring the extent of brood parasit- et al. 1974, Payne 1977a, Evans 1988). ism. Finally, I suggestthat researcherswho wish to Intraspecific brood parasitism has most frequently measure intraspecific brood parasitism in avian pop- been documented for noncolonial, precocial species, ulationsare behoovedto verify the efficacyofthe meth- particularly waterfowl (Anseriformes), and is assumed ods they employ if their resultsare to be deemed cred- to be rare among altricial and colonial species (e.g., ible. Yom-Tov 1980a, Haland 1986). This apparent di- chotomy has led to speculationas to what particular OCCURRENCE OF BROOD PARASITISM In his review, Yom-Tov (1980a, table 1) tabulated 53 I Received 29 September 1988. Final acceptance18 species,from eight orders,for which intraspecificbrood January 1989. parasitismhas been recorded.His list containedmainly 2 Presentaddress: Department ofZoology, The Ohio precocial, noncolonial species,particularly waterfowl State University, Columbus, OH 43210. (Anseriformes), suggestingthat intraspecificbrood par-

[4851 486 MINIREVIEW asitism is rare among altricial and colonial birds. An presumed rarity of intraspecific parasitism among al- additional three waterfowl species known to exhibit tricials and colonial breedersbe, in part, a consequence “egg dumping” were omitted by Yom-Tov, presum- of biased detectability? ably becausedocumentation was based solely on the The most frequently used method of identifying in- occurrenceof unusuallylarge clutches.However, I in- traspecific parasitism is the presence of abnormally clude those speciesas intraspecificbrood parasitesbe- large clutches(e.g., referencesin Yom-Tov 1980a, Lit- cause primary sourcesindicate that egg dumping by tlefield 1981, Dhindsa 1983a, Colwell 1986, Haland one or more females was strongly implicated in the 1986,Kendra et al. 1988, Picman and Belles-Isles1988, occurrence of clutches that were substantially larger Savard 1988, Semel et al. 1988, Young and Titman than the rangeof natural clutch-sizevariation reported 1988). Abnormally largeclutches are particularly com- for the species,or there was additional indirect circum- mon in precocial birds (e.g., waterfowl) and are as- stantial evidence. These include the Lesser ScaupAy- sumed to be the result of eggdumping by one or more thya a&zis(Vermeer 1968,Palmer 1976,Bellrose 1980) parasitic females. Given that such abnormally large Hooded MerganserLo&o&es cucullutus(Morse et al. clutchesare relatively easy to detect, it seemsprobable 1969, Johnsgird 1978;Bellrose 1980) and’Musk Duck that brood parasitism is less likely to go undetectedin Biziura lobata (Frith 1967. Johnsaard 1978). egg-dumpingspecies, than in those in which a parasitic Subsequentto Yom-To& review, intraspecificbrood female deposits one egg per host nest. Further, such a parasitism has been documented for four additional criterion becomes wholly unreliable for those species orders, and 26 new species(Table 1). It is noteworthy that remove the host’s eggbefore depositingtheir own, that of the 26 new species,19 have altricial young,and as occursin a variety of altricial speciesincluding cuc- 16 breed semi- or fully colonially. Consequently,when koos (Cuculidae; Chance 1922), European Starlings all speciesreported to exhibit intraspecificbrood par- (Sturnusvulgaris; Feare 1983, Evans 1988), Cliff Swal- asitism are considered, 3 1 (37.8%) of these are clas- lows (Hirundo pyrrhonota; Brown 1984, Brown and sified as altricial species,and at least 37% are semi- or Brown 1988b), and White-fronted Bee-eaters(Merops fully colonial. Thus, while intraspecific brood parasit- bullockoides;Wrege and Emlen 1987) or for parasite- ism remains most prevalent among precocial species, host relationships in which host females treat a para- an increasingnumber of altricial and colonial species sitic egg(s)as their own and decreaseaccordingly the are being found to exhibit this reproductive strategy. number of eggsthat they lay (Andersson and Eriksson Prior to 1980 interspecific parasitism had been docu- 1982). In short, this technique is highly insensitive to mented for 102 species(Weller 1959;Friedmann 1964; more “subtle” forms of parasitism that may be char- Hamilton and Orians 1965; Palmer 1976; Cronin and acteristic of altricial species. Sherman 1977; Payne 1977a, 1977b; Johnsgard1978; Given that most birds lay with almost constanttime Bellrose 1980; Wyllie 1981; Short and Home 1985; intervalsbetween eggs (Yom-Tov 1980a),and no species Eadie et al. 1988). As of 1980 interspecificparasitism is known to lay more than one egg per day (Sturkie was reported for only six new species,including the 1965, van Tienhoven 1983), a number of studieshave Australian Blue-billed Duck Oxyura australis(Attiwell cited an irregular sequencein the appearanceof eggs et al. 1981), Great Egret Casmerodiusalbus, Black- in a nest as an indication of parasitism (e.g., Yom-Tov crowned Night Heron Nvcticorax nycticorax(Cannel1 1980b, Erikssonand Andersson 1982, Dhindsa 1983a, and Harrington 1984), Spotted Flycatcher Muscicapa Thomas 1984, Earl6 1986a,Haland 1986, Moller 1987, striata (Achterbera and Schaefer 1985). Song Thrush Evans 1988. Picman and Belles-Isles 1988). But. while Turdusbhilomeloi(Erard and Armani 1986),&d Ver- an increase‘of two or more eggsper day in a clutch is din AuripamJIaviceps (Carter 1987). As a result,while consideredstrong presumptive evidence of parasitism interspecificbrood parasitism is apparentlymore prev- (e.g., Brown 1984; Martin 1984; Colwell 1986; Fred- alent (approximately 108 vs. 82 species),these addi- erick and Shields 1986b;Kendra et al. 1988;Lombard0 tional reports lend support to the notion that the in- 1988; Semel et al. 1988; Brown and Brown, in press), traspecific phenomenon may be more widespread, a break in egg laying is considerably problematic. It particularly among altricial and colonial species,than has been demonstratedthat interruptions in egglaying is currently believed. may occur in a variety of different bird species(e.g., Wood Duck Aix sponsa,Heusmann et al. 1980; tits, DETECTING AND QUANTIFYING Parus spp., Dhondt et al. 1983; Willow Ptarmigan La- BROOD PARASITISM gopuslagopus, Martin 1984; Common Moorhen Gal- linula chloropus,Gibbons 1986). Interruptions may Andersson( 1984) and Haland (1986) have questioned occur as a responseto adverse environmental condi- the presumed predominance of precocial birds among tions or, as Eriksson and Andersson (1982) suggest, intraspecificbrood parasites,and a number of observ- becauseof the female’s poor physical condition. Fur- ers have recognizedthe problematic nature of many of thermore, if parasiteslay just before or after the egg- the criteria used to detect and measure the frequency laying period of the host, and eggsare uniformly col- of intraspecific brood parasitism (e.g., Eriksson and ored, then brood parasitism will go undetectedand its Andersson 1982, Andersson 1984, Emlen and Wrege frequency in the population will be underestimated. 1986, Frederick and Shields 1986a, Gibbons 1986, Frederick and Shields (1986a) have shown that, as- Westneat et al. 1987, Wrege and Emlen 1987). How- suming only one parasitic eggis laid in any clutch; the ever, no one has questioned whether these problems probability of detecting brood parasitism using daily may hinder our ability to make cross-speciesgeneral- nest checks is equal to the ratio between the number izations about its distribution among birds and, con- of days on which a parasitic egg is theoretically de- sequently, an accurateassessment of the factors pro- tectable and the total number of days on which one moting this behavior. In other words, might the parasitic egg could be deposited. If the parasite does MINIREVIEW 487

TABLE 1. Additional (post-Yom-Tov 1980a) speciesreported to exhibit intraspecificbrood parasitism.

Ciconiiformes Ciconia maguari Maguari Stork altricial, colonial Thomas 1984 Eudocimus albus White Ibis altricial. colonial Frederick and Shields 1986b Galliformes Lagopuslagopus Willow Ptarmigan precocial, noncolonial Martin 1984 Gruiformes Gallinula chloropus Common Moorhen semi-precocial, Gibbons 1986 noncolonial Grus canadensis Sandhill Crane precocial, noncolonial Littlefield 1981 Fulica americana American Coot precocial, noncolonial Arnold 1987 Charadriiformes Limosa fedoa Marbled Godwit precocial, semi-colonial Colwell 1986 Phalaropustricolor Wilson’s Phalarope precocial, semi-colonial Colwell 1986 Catoptrophorus Western Willet precocial, semi-colonial Colwell 1986 semipalmatus Coraciiformes Merops bullockoides White-fronted Bee- altricial, colonial Emlen and Wrege eater 1986 Passeriformes Ficedula hypoleuca Pied Flycatcher altricial, noncolonial G. Hogstedt unpubl., cited in H&land 1986 Hirundo rustica Barn Swallow altricial, semi-colonial Moller 1987 H. pyrrhonota Cliff Swallow altricial, colonial Brown 1984 H. spilodera South African Cliff altricial, colonial Earlt 1986a Swallow Riparia riparia Bank Swallow altricial, colonial A. P. Meller unpubl., (pers. comm.) Tachycinetabicolor Tree Swallow altricial, colonial Lombard0 1988 Gymnorhinus Pinyon Jay altricial, colonial Trost and Webb 1986 cyanocephalus Pica pica Black-billed Magpie altricial, colonial Trost and Webb 1986 Troglodytesaedon House Wren altricial, noncolonial Picman and Belles- Isles 1988 Turdus migratorius American Robin altricial, noncolonial Gowaty and Davies 1986 Turduspilaris Fieldfare altricial, noncolonial Haland 1986 Sialia sialis Eastern Bluebird altricial, noncolonial Gowaty and Karlin 1984 Ploceusmanyar Striated Weaver altricial, colonial Dhindsa 1983a P. benghalensis Black-throated Weaver altricial, colonial Dhindsa 1983a Lonchura malabarica White-throated Munia altricial, colonial Dhindsa 1983b Passermelanurus Cape Sparrow altricial, noncolonial Earle 1986b

not remove a host egg, the probability of detection is equally likely to occur on any given day of a host’s decreaseswith decreasingclutch size (Frederick and egg-laying schedule. In studies where these assump- Shields 1986a). For those speciesin which parasitic tions are violated detection probabilities must be ad- females remove a host egg prior to depositing their justed, if possible, otherwise the actual frequency of own, the probability of detectingparasitism is reduced intraspecific brood parasitism will be greatly under- dramatically and, if the host specieslays eggsdaily, is estimated. reduced to zero (Frederick and Shields 1986a). Fred- Odd egg dimensions, markings, and/or color have erick and Shields (1986a) have devised a computa- frequently been used to infer intraspecific parasitism tional formula that conservatively corrects for the (referencesin Yom-Tov 1980a, Littlefield 1981, Fet- underestimation of the frequency of brood parasitism terolf and Blokpoel 1984, Colwell 1986, Earl& 1986a, due to reduced detection probabilities. Their method Gibbons 1986, Moller 1987, Evans 1988, Kendra et is most robust when the laying interval of host females al. 1988). The use of this criterion requires that egg is constant,only one parasitic eggis depositedper nest, patterns vary among individuals and are constant for parasitesdo not remove host eggs,and when parasitism each female. However, in Herring Gulls Larus argen- 488 MINIREVIEW tatus (Baerendsand Hogan-Warburg 1982) and House effects of egg markers before widespread use of these Sparrows Passerdomesticus (Lowther 1988) for ex- techniquescan be advocated. ample, odd-colored eggsmay result from pigment de- The biochemical analysis of egg albumen and yolk pletion in a singlefemale laying in a nest. Also, in some protein polymorphismsusing starchgel electrophoresis species, eggs within clutches become paler with in- has been of limited use in detectingand measuringthe creasedexposure to sunlight (Erikssonand Andersson frequencyof brood parasitism(e.g., Manwell and Baker 1982). If egg appearanceis used to estimate the fre- 1975, Fleischer 1985, Fleischer et al. 1985, Kendra et quency of intraspecificbrood parasitism investigators al. 1988). This method lacks widespread applicability must quantify the degreeofindividual variation within becauseegg albumen and yolk proteins are only suit- and between clutches.Furthermore, eggvariation must able if the embryo is unincubated(Manwell and Baker be sufficiently low within, and high between, clutches 1975). Furthermore, as a destructive technique it pro- that parasitic eggscan be unequivocally distinguished hibits an evaluation of the host or parasite’s repro- within a clutch. ductive success. Two other indirect criteria that have occasionally The identification of brood parasitism based upon been used to identify parasitism are ( 1) the appearance biochemical analysisof potential parent and offspring of new eggsafter completion of the clutch (e.g.;Colwell genotypes(e.g.. Gowatv and Karlin 1984. Wreae and 1986, Frederickand Shields 1986b. Picman and Belles- Emlen- 1987,-Evans 1988) is much less problematic Isles 1988, Semel et al. 1988), and (2), in species_ with than those based on the criteria discussedabove, but synchronousincubation, late hatchlings(e.g., Yom-Tov it too has limitations. Although the electrophoretic 1980b: Earlt 1986a. 1986b). However. in colonial analysis of isozyme variation of tissue (e.g., blood, species, where breeding is typically highly synchro- muscle) proteins is a reliable method for separating nous,such cues may rarely be manifested.For example, putative and genetickinship (Sherman 198l), it is based in White-fronted Bee-eaters,where egglaying is “mod- on parental exclusion, and as such, provides a mini- erately” synchronous,most (85%) parasiticfemales are mum estimate only (Gowaty and Karlin 1984). The capable of selectinghosts at the appropriate stage of probability of detecting parasitic offspring is limited their cycle; consequently,late eggsand hatchlings are by the degree of protein polymorphism within a pop- unlikely to occur (Emlen and Wrege 1986). This is in ulation and the extent to which putative and actual marked contrastto the egg-layinghabits of ducks,where (parasitic female and mate) parents possessdifferent eggsare frequently laid in a host’s nest well after in- genotypes. The detection of genotypic heterogeneity cubation has begun (e.g., Semel et al. 1988). Even in among individuals usinggel electrophoresisis favored specieswith synchronousincubation, hatching may be when a large number of independently segregating, delayed naturally (e.g., up to 2 days in Dead Sea Spar- polymorphic loci can be resolved, and allele frequen- row Passermoabiticus, Yom-Tov 1980b), and caution cies at those loci are not strongly skewed (Westneat et is urged in the interpretation of this criterion. For syn- al. 1987, Wrege and Emlen 1987). If, however, hosts chronous incubators,if new eggsappear after comple- and parasitesare close kin the likelihood of detecting tion of the clutch and still hatch at the same time as brood parasitism is diminished because of the in- the rest of the clutch, that may be presumptive evi- creasedprobability that the parasitic female sharesa dence for egg transfers between nests (cf. Brown and common genotype with the putative parents (e.g., Brown 1988a, 1988b). White-fronted Bee-eaters, Wrege and Emlen 1987). Clearly, the criteria consideredprovide only indirect, Wrege and Emlen (1987) and Westneat et al. (1987) circumstantial evidence for the occurrence of intra- have developed similar genetic models that incorpo- specificbrood parasitismand, consequently,results ob- rate an estimate of the probability of detectingparasitic tained from them must be interpreted with caution. offspring to generate more accurate estimates of the Further, I would suggestthat there is reasonablecause frequency of successfulbrood parasitism. If there are to believe that some ofthese criteria favor the detection additional sourcesof parental uncertainty (e.g., extra- of more “overt” instances of parasitism, such as wa- pair copulations)in a population,the useofthese models terfowl eggdumping, and that more sensitivemethods, to estimate the frequencyof brood parasitismbecomes suchas biochemical analyses(discussed below) are re- more complex mathematically, but is theoreticallypos- quired to detect more subtle forms of the behavior. sible (Westneat et al. 1987, Wrege and Emlen 1987). The use of nonintrusive markers such as fat-soluble However, even if these models are employed, gel elec- dyes (Appleby and McRae 1983) tetracycline (Hara- trophoresiswill not permit identification of the para- mis et al. 1983), and radioisotopes (Dickman et al. sitic females (Gibbons 1986). Further, although it is 1983) have been advocated, but rarely employed as a theoreticallypossible, this biochemical method has not means of ascertaininggenetic relatednessin birds. The to my knowledgebeen applied to unhatchedeggs (i.e., marker is fed or injected into an individual, and sub- dead embryos). If mortality affects parasitic eggsdis- sequentlydetected in the eggsor offspring. In general, proportionately, estimates based on the genotypesof the widespread applicability of such markers appears hatched offspring will underestimate the frequency of limited by the number of individuals that can be re- brood parasitism. liably distinguished with a given marker. More im- A recent advance in genetic analysis, the use of portantly, Eadie et al. (1987) have demonstrated that “minisatellite” DNA probes (DNA “fingerprinting” tetracycline may inhibit egg laying in birds and, con- sensuJeffreys et al. 1985) appearsto be a potentially sequently, is of limited value in obtaining an accurate powerful method of establishing biological relation- assessmentof the reproductive successof individual ships.Originallv isolatedfrom human DNA. eachprobe females. As Eadie et al. (1987) have cautioned, more consistsof a DNA segmentwhich detectsand hybrid- study is required to examine the potential deleterious izes with many hypervariable minisatellites in DNA, MINIREVIEW 489 to produce a DNA fingerprint that is completely in- sitism had occurred, yet, brood parasitism was never dividual-specific. Minisatellite probes have been ap- witnessedduring more than 15,500 hr of intensive ob- plied successfullyto wild populationsof both birds and servation. Often it may be advantageousto supplement mammals (Burke and Bruford 1987, Hill 1987, Quinn direct observationswith mounted still or motion cam- et al. 1987, Wetton et al. 1987), and although still in eras. For example, time-lapse photography has been its infancy, the technique is capable of detecting mul- usedto monitor promiscuousbehavior of shags(Phala- tiple paternity and brood parasitism where conven- crocoraxaristotelis, Harris 1982) and nest attendance tional biochemical analyseshave failed (e.g., Wetton by Pied-billed Grebes (Podilymbuspodiceps, Forbes et al. 1987). BecauseDNA fingerprintsare individual- and Ankney 1988). For thosespecies that readily accept specific(except for monozygotictwins), the probability artificial nest structures(e.g., cavity-nesters),pressure of detecting parasitism and correctly identifying indi- sensitive exposure-releasemechanisms at nest boxes vidual parasitesis great.At present,the widespreaduse may be employed to monitor the nesting activities of of this technique is hampered becauseit is relatively individually marked birds (e.g., Tree Swallows, Quin- expensive (particularly when commercial laboratories ney 1986). In assessingnatural levels of brood para- are employed) and there are often long delays in the sitism it is imperative, however, that the density and development of probes and reaction conditions that distribution of nest boxes faithfully reflect conditions produce sufficient resolution for the identification of within natural populations (discussedby Semel et al. individuals within a given study species. Unfortu- 1988). For example, Semel and Sherman (1986) ob- nately, this technique shares, with those already dis- served abnormally high levels of intraspecific brood cussed,the drawback of being unable to detect those parasitism in a Wood Duck population when artificial instancesof attempted brood parasitism in which host nestingstructures were spatially clumped and provided females discriminate against and dispose of parasitic at unnaturally high densities. Indeed, the occurrence eggs(e.g., African Village Weaverbird Ploceuscucul- of intraspecificbrood parasitism in some cavity-nest- latus, Victoria 1972; White-fronted Bee-eater, Emlen ing species’populations (e.g., EuropeanStarling, Evans and Wrege 1986; American Coot Fulica americana, 1988;Eastern Bluebird, Gowaty and Karlin 1984;Tree Arnold 1987; Barn Swallow Hirundo rustica, Moller Swallow, Lombard0 1988) may have been facilitated 1987: Euronean Starlina. Stouffer et al. 1987: Cliff by the placement of boxes in highly visible sites and Swallow, Brown and Brown, in press).The propensity in proximity to other boxes (Semel et al. 1988). The for females of certain speciesto desert their nests as use of photographyor video, while costly, may help to an adaptive countermeasureto being parasitized will circumvent problems imposed by surreptitiousbrood necessarilylimit the probability of detecting intraspe- parasites. For many studies it may be impractical to cific brood parasitism. When a nest is desertedit may monitor all nests in a population; however, it may be not always be clear whether this is a host’s responseto possible to intensively monitor an unbiased sample being parasitized, human interference, or some other that is representative of the entire study population factor. Indirect methods essentially detect only “suc- (e.g., Brown and Brown 1988b). cessful” parasitism, and an accurateindication of the Bearingthe above points in mind, a more complete prevalenceof intraspecificbrood parasitismwill be dif- understandingof the extent of intraspecificbrood par- ficult to obtain. asitism acrosstaxonomic groupsand its importance as Although time-consuming, behavioral observations an alternative female reproductive strategywithin bird may prove invaluable in studying and more fully un- populationswill best be achieved usinga combination derstandingavian parasitic behavior (e.g., Heusmann of the criteria and researchmethods discussedabove. et al. 1980;Brown 1984;Emlen and Wrege 1986;Brown I suggestthat the most fruitful studies will be those and Brown 1988b, in press). Not only is it the only that employ DNA “fingerprinting” to clarify biological reliable method of detectingattempted parasitism, but relationships in conjunction with detailed, long-term given a marked population with known genealogies, behavioral observations (both direct and indirect) of information can potentially be garneredon the identity individually marked birds. This approach permits a and characteristicsof the perpetrator (e.g., age, social comparisonof the estimatesof brood parasitism based status, kinship), behavior of host and parasite before, on biochemical and observationaldata which may re- during,and after eggdeposition, and, if followed through veal biasesin either method (Wrege and Emlen 1987). the nestling period, the subsequentsurvival and re- Furthermore, for many studies such a synergisticap- productive successof individuals employing the var- proach will be essentialfor an analysisof the adaptive ious reproductive strategies. That said, the inherent value of brood parasitism. low frequency of intraspecific parasitism within most In summary, I suggestthat the presumed rarity of populations may limit the efficiency of direct obser- intraspecific brood parasitism, particularly among al- vations. The applicability of direct observations may tricial species,may be, in part, a consequenceof meth- be further restrictedif the behavioral act of parasitism odological constraints. Most reports are based upon is highly secretiveand the females involved are incon- indirect, circumstantialcriteria that are biased toward spicuousin their actions (e.g., White-fronted Bee-eat- detecting “overt” expressionsof this behavior, as typ- ers, Emlen and Wrege 1986; Cliff Swallows, Brown ified by waterfowl; consequentlymore “subtle” forms, 1984, Brown and Brown, in press;European Starlings, likely to be exhibited by altricial species,may go un- Evans 1988). The limitation of direct observationsis detected. Furthermore, intraspecific brood parasitism illustrated by Frederick and Shields’ (1986b) study of may be an important aspectofthe reproductivebiology White Ibis (Eudocimusalbus). In one of the colonies of many avian species,despite the difficulties of de- studied, several lines of indirect, circumstantial evi- tecting its occurrence.At present, an unbiased assess- dence suggestedthat a low level of intraspecific para- ment of the distribution of intraspecific brood para- 490 MINIREVIEW sitism among birds seems improbable. Problems in CHANCE, E. 1922. The cuckoo’s secret.Sidgewick and evaluating parasitism may be circumvented by em- Jackson,London. ploying a direct (and/or indirect) observational ap- COLWELL, M. A. 1986. Intraspecificbrood parasitism proach in conjunction with biochemical pedigreeanal- in three species of prairie-breeding shorebirds. yses.Regardless of the methodsemployed it is important Wilson Bull. 98~473-475. that investigatorsjustify their use, especiallyfor those CRONIN, E. W., JR., AND P. W. SHERMAN. 1977. A studiesthat extend beyond the anecdotal and attempt resource-basedmating system:the Orange-rumped to interpret intraspecific brood parasitism in a theo- Honeyguide. Living Bird 155-32. retical or evolutionary framework. DHINDSA,M. S. 1983a. Intraspecific nest parasitism in the White-throated Munia. Notomis 30:87-92. Thanks are extended to M. Andersson, J. F. Hare, DHINDSA,M. S. 1983b. Intraspecific nest parasitism K. Martin, A. P. Meller, J. 0. Murie, B. Semel, and in two species of Indian -weaverbirds, Ploceus two anonymous reviewers for their helpful comments benahalensis and P. rnanvar. Ibis 125:243-245. on the manuscript, and to T. Herman for igniting my DHOND~, A., R. 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