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Home , Oropendola, Sexual dimorphism

The Auk 114(4):570-580, 1997

EXTREME SEXUAL SIZE DIMORPHISM, , AND THE FORAGING ECOLOGY OF MONTEZUMA OROPENDOLAS

MICHAEL S. WEBSTER • Sectionof Neurobiologyand Behavior, Cornell University, Ithaca, New York 14853, USA

ABSTRACT.--Sexualdifferences in body size usually are consideredto be a product of ei- ther sexualselection or ecologicaldivergence between the .I testedthe predictionsof thesehypotheses to explainextreme in sizein a Neotropicalblackbird, the MontezumaOropendola (Psarocolius montezuma). Sexual dimorphism was more pro- nouncedin wing length and relativemass, traits that appear to be important in courtship andcompetition for mates,than in bill lengthor tarsuslength. Male dominance rank, which is an indicatorof matingsuccess, was positively associated with bodysize (i.e. high-ranking maleswere larger than low- rankingmales). These results suggest that sexualselection acts to increasemale body size,and hencecontributes to sexualsize dimorphism in . Differencesin foragingbehavior and diet alsoexisted between the sexesand were related to sexualsize differences. The smallsize of femalesallowed them to forageon food resources that were difficult for the larger malesto reach(e.g. insectsin rolled leavesat the endsof branches)., though, did not appearto be restrictedfrom thoseresources exploited by males(primarily epiphytal bromeliads). Although it was not possibleto rejectthe eco- logical-divergencehypothesis, my resultssuggest that sexual foraging differences are a con- sequencerather than a causeof sexualdimorphism in sizein this species.Received 23 August 1996,accepted 18 March1997.

SEXUAL DIFFERENCES IN SIZE AND SHAPE are cubation vs. nest defense). Intersexual diver- widespreadamong , and attemptsto gencealso might arise if it reducesintersexual explainthem represent a majortheme in evo- competitionfor food resources(sexual forag- lutionarybiology that datesback to Darwin ing-nichedivergence), a processanalogous to (1871).For and ,two main hy- interspecificniche partitioning and character potheses have been proposed to explain displacement (Selander 1972, Slatkin 1984, body-sizedifferences between the sexes.The Hedrick and Temeles1989, Shine 1989). first of these,the sexual-selectionhypothesis, Thesexual-selection hypothesis has received proposesthat largebody sizein onesex (usu- a greatdeal of attentionand is widely accepted ally males)is favoredbecause it confersan ad- as an explanationfor sexualsize dimorphism. vantage in intrasexualcompetition for mates This hypothesisis supportedby both theoret- and/or becausefemales prefer large males. ical geneticmodels (Lande 1980)and interspe- ,acting throughecological cific studiesdemonstrating an associationbe- factorssuch as foragingefficiency and preda- tweensexual dimorphism and the intensityof tion, is assumed to favor the same size in both competitionamong males for mates(e.g. Clut- sexes,but sexualselection is thoughtto push ton-Brock et al. 1977, Alexander et al. 1979, malestoward larger sizes.Alternatively, the Oakes 1992, Webster 1992, Fairbairn and Pre- ecological-divergencehypothesis postulates ziosi 1994;but see H6glund 1989;Bj6rklund that foragingand/or other ecologicalfactors 1990,1991). For intraspecificstudies, this hy- favordifferent body sizesin the two sexes.For pothesispredicts that largemales have an ad- example,different sizes might resultbecause vantagein obtainingmatings, and that large the sexesdiffer in their nutritional require- male size carrieswith it an ecologicalcost. ments (suchthat they use differentfood re- Some studies of size-dimorphicbirds have sources)or in their reproductiveroles (e.g. in- demonstrateda large-malemating advantage (see Andersson 1994, Searcy and Yasukawa •Present address:Department of BiologicalSci- 1995),but severalhave not. Relatively few stud- ences,State University of New York at Buffalo, 109 ies of birds have demonstratedan ecological Cooke Hall, Buffalo, New York 14260, USA. E-mail: costof large male size.For example,some stud- [email protected] ies have demonstratedthat large maleshave 57O October1997] SexualSize Dimorphism in Oropendolas 571

lowersurvival than small males (e.g. Yasukawa malesand juvenilemales the skin patchesare pale 1987), whereas others have found no suchre- and not swollen.In addition,the outermostprimar- lationship(Weatherhead et al. 1987,BjtSrklund iesof adult malesare extremely elongated and twist- and Linden 1993, Weatherhead and Clark ed relative to those of females and juvenile males. Air rushingbetween these modified primaries pro- 1994). duces a deep "whooshing" sound used by males The ecological-divergencehypothesis is the during agonisticand courtship displays (Webster standard alternative to sexual selection (Dar- 1991). win 1871, Selander1972, Shine 1989) and is MontezumaOropendolas have been described as supportedby theoreticalmodels (Slatkin 1984). frugivorous or omnivorous(Skutch 1954, Orians Althoughmany ecological differences between 1985). Like most membersof their subfamily,oro- the sexescould lead to sexualsize dimorphism, pendolasforage for prey by "gaping" (Bee- mosttheoretical and empirical studies have fo- cher1951, Orians 1985). A gapingbird insertsits bill cusedon foragingdifferences between the - into the leavesor stemof a plant (e.g.an epiphytal es (e.g.Wallace 1974, Schoener et al. 1982,As- bromeliad)and opensits bill to pry apart the plant kins 1983, Camilleri and Shine 1990, Shine partsand exposepotential prey hiding within. Femaleoropendolas nest colonially in free-stand- 1991, Houstonand Shine 1993). Support for ing trees isolated from the surrounding forest thishypothesis requires that the sexes partition (Skutch1954, Fraga 1989,Webster 1994b). Previous food in a way that favorssize differencesin resultshave shown that the systemof the body partsassociated with foraging. MontezumaOropendola is oneof -defensepo- In this paper,I testpredictions of the sexu- lygyny(sensu Emlen and Oring 1977)characterized al-selectionand ecological-divergencehypoth- by high levelsof intrasexualcompetition between esesfor the MontezumaOropendola (Psaroco- malesfor accessto sexuallyreceptive females (Web- liusmontezuma), one of the mostsexually size- ster 1994a). Males compete for positions at nesting coloniesand, basedon the outcomeof aggressivein- dimorphicof all birds(see below). I followoth- teractions, can be ordered in a linear dominance hi- er studiesof theecological-divergence hypothesis erarchy.Top malesin this hierarchy(those winning and focuson foragingecology. To distinguish the mostaggressive interactions) physically exclude betweenthe alternativehypotheses, I examine other malesfrom nest-buildingfemales. Typically, a sexual dimorphism and the role body size single male defendsan entire colonyof 10 to 30 fe- plays in both competitionfor mates (males) males,although lower-ranking males often remain and foraging(both sexes)in this species.Be- in nearbytrees and enterthe nestingcolony when causethe relativelyinaccessible nests of Mon- higher-rankingmales are absent.Observed male tezuma Oropendolasmade it difficult to mon- mating successwithin a colonyis extremelybiased itor femalereproductive success, I do not con- toward high-rankingmales; alpha and beta males siderpotential evolutionary forces that might obtain virtually all observedcopulations (Webster 1994a).Further, genetic studies have shown that al- pushfemale size away from the ecologicalop- thoughsubordinate males obtain some fertilizations timum, suchas socialcompetition or by copulatingaway from the nestingcolony, top- selection (Rails 1977, Price 1984, Robinson ranking males(alpha and beta) sire more offspring 1985a,Langston et al. 1990). than do other males(Webster 1995). Captureand marking.--I captured a totalof 76 males METHODS and 73 femalesusing elevated mist nets(Mease and Mease1980) placed near nesting colonies and at for- Studyspecies.--The is a agingsites baited with bananas.At the time of cap- Neotropicalmember of the New World blackbird ture, I measured(flattened wing length, culmen family (Icteridae).It inhabitslowland rain foresthab- length, tarsus length), weighed, and individually itats from southern Mexico to the Canal Zone in Pan- marked birds with colored leg bands (body-mass ama, and breedsduring the dry season(January to data were not collectedin 1986).Although sample May in CostaRica; Skutch 1954). I studieda color- sizeswere small, body massdid not appear to vary markedpopulation of thesebirds during the 1986to substantiallywithin a season;three males that were 1990breeding seasons at the La SelvaBiological Sta- capturedtwice in the sameseason differed by only tion in CostaRica (seeMcDade et al. 1993). 2 to 5 g betweentheir first and secondcaptures. For Male and Montezuma Oropendolasdiffer analyses,I used mean body mass for individuals greatlyin body size but not in plumagecoloration. capturedmore than once(n = 6). Individuals of both sexeshave bare patchesof skin I determinedthe sex of capturedindividuals based in the face;in adult malesthese patches are brightly on bodysize. Measures of museumskins showed no colored and swollen to form wattles, whereas in re- overlapin tarsuslength between the sexes; male tarsi 572 MICHAELS. WEBSTER [Auk,Vol. 114

exceed60 mm in length, whereasfemale tarsi are in diameter.During the 1990season, if I encountered shorter than 60mm. Subsequentobservations of a foragingin epiphytalbromeliads (a common marked individuals revealed no cases in which an in- foodfor oropendolas;see below), I alsonoted the ap- dividual classifiedas a male behavedas a female(i.e. proximatesize of the bromeliad.I classifiedbrome- nestbuilding, incubation,feeding nestlings) or vice liadsas "small" if theywere smaller than thesize of versa.I usedthe presenceof swollenface wattles to a female(ca. one-half the body size of an adultmale), distinguishadult malesfrom juvenilemales. "medium" if they were larger than a female but Colonyobservations.--I monitored activity at a focal smallerthan an adult male,and "large" if theywere colony(La SelvaColony) during the peak of breed- largerthan an adult male.I recordedforaging data ing activityeach year (total of 1,200h), and recorded for only the first foragingobservation after an indi- colonyattendance, aggressive interactions between vidual was encountered.If I encountereda group of males,and copulationattempts during theseperi- birds foragingtogether on the samefood item, I col- ods. In addition, I visited all known colonies near the lecteddata only on the first foragingindividual of focalcolony several times throughout a season(Web- eachsex that I observedin orderto avoidproblems ster 1994a, 1994b). On each visit to one of these col- of nonindependence. onies,I notedthe malespresent and the outcomeof any aggressiveinteractions that occurred. RESULTS As an estimator of male mating success,I mea- sured male dominancerank at breedingcolonies be- Bodysize and sexual dimorphism.--Relative to causethis measurehas been shownto be a strong correlateof observedmale mating success(Webster females,male oropendolaswere approximately 1994a,1995). Males at eachcolony were assigneda 30% largerin mostof the linear measuresand dominancerank basedon the outcomeof aggressive morethan 100%larger in bodymass (Table 1). interactions(Webster 1994a). The alpha male was The distributionof body massfor adult males that male able to aggressivelydisplace all other did not overlapthat for females(Fig. 1). This males,the betamale was that maleable to displace size difference between males and females all malesexcept the alpha,and so forth. Male ranks makesthis speciesone of the most sexually seemedstable throughout the courseof a breeding size-dimorphicof all birds (Fig. 2). Juvenile season;no caseof two maleschanging relative rank males were intermediate in size between adult were recorded. Based on dominance rank, adult males and females. The size differences be- malesat the focalcolony were placed into one of two tween males and females were evident at the categories:(1) "upper" males were higher-ranking than at leasthalf of the markedmales at the colony, time of fledging (Table2). Analysesof covari- and (2) "lower" maleswere lower-rankingthan half anceindicated that both tarsuslength and sex or moreof the markedmales at that colony.For col- were independently associatedwith wing oniesthat I visitedbut did not intensivelyobserve length and body mass(although the signifi- during the season,"upper" males were marked canceof the effectof sexon masswas margin- malesobserved to win at leasthalf of their aggres- al), and therewas a significantinteraction be- sive interactions, and "lower" males were marked tweensex and tarsus length for thesemeasures malesthat lost half or moreof their aggressivein- (Table3). If tarsuslength is takenas a general teractions.Finally, "noncolony"males were those indicatorof overallbody size (seeRising and malesthat wererarely (fewer than 5% of scansmade) Somers1989, Freeman and Jackson1990), then or neverobserved at any of the nestingcolonies. Foragingobservations.--I searched for oropendolas theseresults suggest that relativemass and along foresttrails. When a foragingbird was en- wing length are greaterin malesthan in fe- countered,I recordedits sex,age class (males only), males.In contrast,the relationshipsbetween the item it was foragingon, its methodof foraging, sex and tarsuslength versusculmen length and the locationand approximatediameter of the were not significant. limb wherethe bird wasstanding. The locationof the Male size, dominancerank and mating suc- bird on the limb was notedusing a categoricalsys- cess.--Malebody mass was associatedwith tem that dividedthe limb into five zonesof approx- dominancerank category(ANOVA, F = 7.72,df imatelyequal length from baseto tip end.The ap- = 2 and 29, P = 0.002;Fig. 3A). Similar results proximatediameter of the limb was notedwith ref- erence to the bird itself: "thin" limbs were thinner were obtained using body condition (mass/ than the diameterof a male'starsus (ca. 1.5 times the tarsus,F = 5.22, df = 2 and 29, P = 0.012) and diameter of a female'starsus); "medium" limbs were tarsuslength (F = 3.74, df = 2 and 29, P = thicker than the diameter of a male'starsus, but less 0.036) as a size measure,but not using wing than approximately3.75 cm (i.e. 1.5 inches)in di- length(F = 1.54,df = 2 and 28, P = 0.233)or ameter;and "thick" limbswere greater than 3.75cm culmenlength (F = 0.39, df = 2 and 29, P = October1997] SexualSize Dimorphism in Oropendolas 573

TABLE1. Sizemeasures (œ +_ SD, n in parentheses)and dimorphismscores (œ ñ SE)of capturedMontezuma Oropendolas.All differencesbetween males (adults and juvenilescombined) and femalesare significant (t-tests,Ps < 0.001), as are all differencesbetween adult and juvenile males (t-tests,Ps -< 0.01) exceptfor culmen/tarsus (t = 0.887, P = 0.380).

Measure Females Adult males Juvenilemales Dimorphisma Mass (g) 245.8 ñ 14.4 (58) 515.9 +- 40.8 (33) 418.8 +_30.4 (14) 2.09 + 0.037 Mass•/3 6.26 +_0.12 (58) 8.01 +_0.21 (33) 7.47 + 0.18 (14) 1.28 + 0.008 Tarsus(mm) 53.71 +_1.54 (56) 67.37 _+2.27 (33) 66.03 +_1.83 (14) 1.25 _+0.009 Culmen (mm) 60.01 ñ 2.53 (54) 77.65 ñ 3.28 (33) 75.69 +_3.27 (14) 1.30 -+ 0.012 Wing (cm) 20.18 _+0.97 (50) 26.76 + 1.14 (32) 23.32 +_1.44 (12) 1.33 _+0.013 Mass/tarsus 4.58 ñ 0.21 (54) 7.64 +_0.49 (33) 6.35 + 0.48 (14) 1.67 +_0.021 Culmen/tarsus 1.12 +_0.05 (54) 1.15 +- 0.06 (33) 1.15 ñ 0.07 (14) 1.03 _+0.012 Wing/tarsus 0.38 ñ 0.02 (50) 0.40 + 0.02 (32) 0.35 _+0.03 (12) 1.06 ñ 0.011 • Dimorphismis theratio of meanvalue of adultmale to thatof female.SE estimates were made using a bootstrapmethod (Lanyon 1987). Dimorphismscores were obtained by randomlychoosing (with replacement)a subset of malesfrom the totalpool of malesand a subsetof femalesfrom the totalpool of females(the number chosen was equal to the numberin theoriginal sample), calculating a meansize measure fromthe subset for eachsex, and then calculating a dimorphism score as the male/female ratio. Values are means from 100 repetitions.

0.679).'s LSD post-hoctests showed that length(r s = -0.285, P = 0.195).Except for two all differences in size measures were due to sta- males (ranks 5 and 11), all size measuresused tistically significantdifferences (P < 0.05) be- in this analysiswere obtainedin 1988,the same tween "upper" versus "lower" and "noncol- year that dominanceranks were determined; ony" males;"lower" and "noncolony"males size measures for the other two males were ob- did not differ significantlyfrom eachother in tainedin the previousseason (1987). If the two any of the sizemeasures (P > 0.10in all cases). males whose masses were recorded in 1987 are I was able to examine male body size and excludedfrom the analysis,the correlations rank within a singlecolony, Point, in drop slightly(mass vs. rank, rs= -0.595, P = 1988 (Fig. 3B). Male dominancerank was sig- 0.057; mass/tarsus vs. rank, r•, = -0.619, P = nificantly correlatedwith body mass (rs = 0.051).The marginalsignificance in theselatter -0.661, n = 10, P = 0.024) and mass/tarsus (rs analysesmay be due to small sample sizes (n - 0.697, P = 0.018), but not with tarsus = 8 males).

34

32 [] Females(62) [] JuvenileMales (15) 30 ß AdultMales (42)

28

26-

24-

10 -'

8-

6-

4- 2- 200 300 400 500 600

Body Mass (g) FIG.1. Distributionof body massfor capturedfemale, juvenile, and adultmale Montezuma Oropendolas. Arrowsindicate mean body mass for eachgroup; sample sizes in parentheses. 574 MICHAELS. WEBSTER [Auk, Vol. 114

TABLE 2. Size measures (• + SD) of male and fe- male Montezuma Oropendolas based on five malesand six femalesat or near the age of fledg- ing.

Measure Males Females t

Tarsus (mm) 65.47 _+2.13 52.55 -+ 1.50 11.81'* Culmen (mm) 40.11 _+3.79 33.97 + 1.92 3.49* Mass (g) 252.8 _+30.0 181.2 + 19.9 4.75** *, P < 0.01; **, P < 0.001. 1.0 1.2 1.4 1.6 1.8 2•0

Male/Female Mass FIG. 2. Distribution of sexual size dimorphism ed for a substantialnumber of the foragingob- scores(male/female mass)for 97 speciesof North servations(18.3% and 15.5%of 394foraging ob- Americanpassetines for which data on male and fe- servations,respectively). male body masswere available(hatched bars; from Size and sexualforaging differences.--Males Dunning 1984)and for MontezumaOropendolas (ar- andfemales differed in the thicknessof perches row; this study). used during foraging (Fig. 4). Adult males tendedto use thick perches,whereas females Males RRR and OMO were the alpha and perchedmore on thin limbs. Perchchoice, in beta males, respectively,at the focal colony turn, was associatedwith sexual differences in during the 1987to 1989breeding seasons. To- foraginglocation along the lengthof the limb; gether,these two malesaccounted for 81 of 84 femalesforaged more than twice as often as observed copulations(Webster 1994a, 1995). malesat the thin tip end of the limb (Fig. 5). These two males also were heavier than most Femalesdid not forage toward the tips of othermales caught during this study (Fig. 3A). branchesbecause they were forcedto do soby Indeed, RRR, who accountedfor 88% of all ob- males;the distributionof foraginglocations served copulationsduring the courseof this whenfemales foraged alone did notdiffer from study,was the heaviestmale ever captured; his that when femalesforaged in the presenceof masswas nearly two standarddeviations above males (X2 = 0.59, P = 0.444). Juvenile males, who are intermediate in size between adult the mean for adult males. Generalforaging behavior and diet.•Oropen- malesand females,did not differ significantly dolas were extremely omnivorous and con- in foraging location from adult males (X2 = sumeda wide varietyof plant (bothfruit and 7.03, df = 4, P = 0.134) or females (X2 = 4.57, ),invertebrate, and vertebrateprey (Table df = 4, P = 0.335),indicating that they were in- termediate between the adults in location of 4). Individualsgaped for animalprey primarily in the leavesand rootsof epiphytes(58.2% of 261 gaping observations),particularly brome- liads(83.5% of 152observations of gapingat an TABLE3. Resultsof analysisof covarianceon size measureof male and female Montezuma Oropen- epiphyte),and in curled leavesat the end of dolas. limbs (27.6%of 261 gaping observations).Ar- thropodsand smallvertebrate prey weretaken Source F P at these sources.Occasionally, oropendolas Body mass were observedgaping open rotted wood and Tarsuslength 19.98 <0.001 twig stems,and gaping also was the method Sex 3.36 0.070 usedto openlarge fruits, suchas bananas and Tarsuslength x sex 5.20 0.025 papayas. Wing length In contrastto animal prey, oropendolasob- Tarsuslength 4.12 0.045 tained most plant foods either by plucking Sex 4.59 0.035 (pullingsmall fruits from theends of branches) Tarsuslength x sex 6.05 0.016 or nectar-drinking(inserting the bill into a Culmen length ,followed by raisingand tiltingthe head Tarsuslength 1.66 0.201 back).Although less frequently observed than Sex 0.95 0.331 gaping,plucking and nectar-drinkingaccount- Tarsuslength x sex 0.06 0.807 October1997] SexualSize Dimorphis•n in Oropendolas 575

A Malesforaged more on epiphytesthan did fe- 600' males, but the sexesdid not differ in their for- agingon otherfood resources (Fig. 6). 550' o o As was the casefor rolled leaves, small fruits o o and tended to occur near the ends of o

500' o õ branches.Therefore, it is surprisingthat males foragedon theseresources as oftenas did fe- o 8 males. However, males tended to perch on 450' thick-and medium-sizedperches while forag- o o ing on smallfruits and flowers more often than 400 did females(n = 154observations; X 2 = 6.12, df Upper Lower Noncolony = 2, P = 0.047). Males often foragedon fruit Male Rank Category from one limb while perchedon another,or distributed their mass between two or more smallbranches, suggesting that they were able 600' B to forageon fruits and flowersby taking ad- [] vantageof thickperches near the food resource. 550' Femalesdid not appearto be lessable to forage [] in bromeliadsand other epiphytesthan were [] [] males.Females gaped as oftenin epiphytesas 500 [] they did in deadleaves, and they foragedon eachof thesefood sources more often than they did on anyother food source (Fig. 6). Moreover,

[] femalesdid not forageless on largebromeliads than did males (X2 = 0.44, df = 4, P = 0.979; 450]4001 Fig. 7). 0 2 4 6 8 10 12

0tighest) Male Rank (Lowest) DISCUSSION F•c. 3. Associationbetween body massand dom- inance rank in male Montezuma Oropendolas.(A) Sexualsize dimorphismand sexualselection.- Body massof malesin differentcategories of domi- The body-massratio between male and female nance rank (see text) at all observation colonies. MontezumaOropendolas exceeds 2:1 (Fig. 2), Filled symbolsrepresent the alpha (circle)and beta whichplaces the speciesamong the mostsex- (square)males at the focalcolony. (B) Bodymass ver- ually size-dimorphicof all birds (see Rails sus dominancerank for male Montezuma Oropen- 1976).My resultssupport a critical prediction dolasat the CrocodilePoint Colony, 1988. Body mass of the hypothesisthat sexualselection is re- wasmeasured in 1988(open squares) or 1987(shad- sponsiblefor the evolutionand/or mainte- ed squares). nanceof extremesexual dimorphism in this species:body mass and tarsus length were pos- foraging (n = 60 observationsof foragingju- itively associatedwith male dominancerank, venile males). and rank is an indicator of male successin cop- Adult males and females differed signifi- ulations (Webster 1994a) and fertilizations cantlyin the amountof time they spentforag- (Webster1995) in this species. ing on rolled leavesand epiphytes(Fig. 6). Al- The hypothesisthat sexualselection is a gen- most all (67 of 72) individuals observedgaping eral causeof sexual dimorphismin size in open rolled leavesto searchfor prey blackbirdsand otherhigher is sup- were females.Normally, rolled leavesare lo- portedby interspecificstudies showing an as- catedat thevery tip of branches,where the di- sociationbetween degree of polygynyand de- ameterof the limb presumablyis too thin to greeof dimorphism,and by intraspecificstud- supportthe greaterbulk of a male.Four of the ies showingan associationbetween male size five observationsof males foraging on rolled and mating success(see Introduction).How- leaves were cases in which the male was able to ever,for severalsize-dimorphic and highly po- reachthe leaveswhile perchedon a thicklimb. lygynousbirds, the associationbetween male 576 MICHAEL S. WEBSTER [Auk, Vol. 114

TABLE4. Food items eatenby adult MontezumaOropendolas.

Fooditem Source Frequencya larvae Curled leaves High Scorpions Epiphytes Low Epiphytes High Epiphytes Moderate Orthopterans Leavesand epiphytes High Large Leavesand epiphytes High Fruits Bromeliads (Bromeliaceae) Moderate Hampeaappendiculata (Malvaceae) Moderate Miconia impediolaris(Melastomataceae) Low Topobeadurandiana (Melastomataceae) Low Cecropiasp. (Moraceae) High Coussapoapanamensis (Moraceae) High Ficusspp. (Moraceae) High Elaeisguineensis (Palmaceae) Moderate Bactrisgasipaes (Palmaceae) Moderate Zanthoxylumsp. (Rutaceae) Low Caricapapaya (Papaya, Caricaceae) Moderate Nectar Ochromalagopus (Bombacaceae) Moderate Erythrinacochleata (Fabaceae) High Fruit and nectar Musa spp. (Banana, Musaceae) High High, > 10 observations;Moderate, 5 to 10 observations;Low, < 5 observations.

size and mating successis weak or absental- tween size and mating successdifficult to de- together(Payne and Payne1977, Searcy 1979, tect in many systems. Yasukawa1981, Gibson and Bradbury 1985, Ecologicalhypotheses for sexual dimor- Weatherhead et al. 1987, Pruett-Jones and phismin size,particularly the niche-partition- Pruett-Jones1990). The latter results suggest ing hypothesis,have proven notoriously diffi- that sexualselection may not favorlarge male cult to test, primarily becauseit is difficult to size in somespecies. Alternatively, confound- determine whether observed differences in diet ing factorssuch as extrapaircopulations (e.g. between the sexes are a cause or an effect of Gibbs et al. 1990, Westneat 1993, Weatherhead and Boag1995) may make the connectionbe-

60' I1 AdultMales (80)] /•_ Females(235)I [•lAdultFemales Males(258) (99) ] 40-

30- 20- o-L,L A B C D E 10- • ' ,

Thin Medium Thick Position on Limb Limb Thickness FIG. 5. Locationof perchesused by adult male FIG. 4. Thicknessof perches(see text) used by and female MontezumaOropendolas. The sections foragingadult male and female Montezuma Oropen- of the limb run from the base(A) to its tip (E). Sam- dolas.Sample sizes in parentheses;*, P < 0.001 (X2 ple sizesin parentheses;*, P < 0.001(X 2 testscom- testscomparing males and females). paring malesand females). October1997] SexualSize Dimorphism in Oropendolas 577

Large Fruit

Females(229) Females(35) Small Fruit AdultMales(104) AdultMales(23)

Flowers

Leaves

Epiphytes

10 20 30 40 50 % of Observations Small Medium Large F•c. 6. Food resourcesexploited by adult male Size of Bromeliad and female MontezumaOropendolas. Sample sizes Fic. 7. Sizeof bromeliads(see text) foragedupon in parentheses;*, P < 0.001 (X2 tests comparing by adult male and femaleMontezuma Oropendolas. males and females). Samplesizes in parentheses. sexualdimorphism (Hedrick and Temeles 1989, 1980, Askins 1983, Holmes 1986, Noske 1986). Shine 1989).Selander (1972) arguedthat the Second,observed sexual foraging differences only reliableevidence that would supportthe appearedto resultfrom body-sizedifferences, ecological-divergencehypothesis would be a becauseadult malesused significantly thicker demonstrationthat foragingstructures are rel- perchesthan did females,and this difference ativelymore dimorphic than other body parts. wasnot a resultof malesforcing females to for- BecauseMontezuma Oropendolas search for agein suboptimalareas (as has been suggested preyby usingtheir bill to pry openvarious sub- for other species;Kodric-Brown and Brown strates,it is likelythat thebill is a primaryfor- 1978, Puttick 1981, Peters and Grubb 1983, Te- agingstructure. My resultsdo notindicate that meles 1986). Juvenilemales, which are inter- the bill is any more dimorphicin size than are mediate in size between adult males and fe- otherbody parts (Table 1). Indeed,the greatest males, also were intermediate in the amount of sexualdimorphism was found in measuresof time spentforaging at the endsof limbs.Inter- traits likely to be important in sexual compe- specificcomparisons also suggestthat large tition amongmales, i.e. wing length(the elon- sizeprevents foraging on curledleaves: Chest- gated, modified primaries of males are used in nut-headedOropendolas (P. wagleri) and Scar- agonisticand courtshipdisplays) and relative let-rumped Caciques (Cacicus uropygialis), body mass (mass/tarsus).However, using Se- closelyrelated speciesthat are sympatricbut lander's criterion is difficult because often it is smallerthan MontezumaOropendolas, search not possibleto know which morphological for in curled leaves more often than do traits are importantin foraging(i.e. for oropen- Montezuma Oropendolas(Orians 1985, pers. dolas,structures other than thebill maybe im- obs.).Indeed, most bird speciesthat specialize portant), and the test is highly conservative on foragingin aerialleaf litter andleaves at the (Shine1989, 1991). ends of limbs are extremely small (Greenberg Two criticalpredictions of theforaging-niche 1979, 1987; Gradwohl and Greenberg1984; divergencehypothesis were supportedin this Remsenand Parker1984). Together, these ob- study. First, males and femalesdiffered signif- servationsindicate that the greater mass of icantlyin the microhabitatsexploited for food maleoropendolas prevents them from reaching resources,with femalesforaging more often in the rolled-leafresources used by females. leavesat the end of limbs and males taking Althoughthe small size of femaleoropen- moreanimal prey by gapingin epiphytalbro- dolasappears to allow themto exploitfood re- meliads. Similar sexual foraging differences sourcesin rolled leaves, it is not clear whether havebeen reported in the Russet-backedOro- largesize assists males in foragingon their pri- pendola (P. angustifrons;Robinson 1985b) as maryfood resource, epiphytal bromeliads. It is well as in other birds (Selander1966, Williams conceivablethat beinglarge and havinga long 578 MICHAELS. WEBSTER [Auk, Vol. 114 bill is beneficialwhen foraging in larger,deep- However,I couldnot rejectthe ecological-di- er bromeliads.However, females foraged on vergencehypothesis completely. These possi- bromeliadsapproximately as often as they did bilitiesrequire further study in this and other in curledleaves, suggesting that they did not sexuallydimorphic species. specializeon leavesat the expenseof reduced ability to foragein bromeliads,and malesdid ACKNOWLEDGMENTS not forageon larger bromeliadsthan did fe- males.Interspecific comparisons suggest that I thank S. T. Emlen, P. W. Sherman, and L. K. Sterk large size is not necessaryto foragingby gap- for advice and encouragement throughout this ing in bromeliads:most avian species that use study.For assistanceand goodhumor in the field, I epiphytalbromeliads, including smaller spe- thankI. Ayub, J.Guild, K. Y.A. Merg,E. Phillips,and L. Sterk.A pilot versionof this studywas conducted ciesof oropendolasand caciques that forage by with the assistance of students from OTS Course gaping, are smallerthan femaleMontezuma 88-1; I thank them for their interestand suggestions Oropendolas(Orians 1985, Nadkarni and Mat- for improvement.Valuable discussion and/or com- elson 1989,pers. obs.).Indeed, the Jamaican ments on an earlier draft were provided by C. Blackbird(Nesopsar nigerrimus), a speciesless Aquadro, M. Bj6rklund, S. Emlen, R. Hoy, R. Irwin, than half the sizeof the MontezumaOropen- T. Martin, C. Murphy,E H. Pough,S. Pruett-Jones,P. dola, foragesalmost exclusively by gapingin Sherman,and two anonymousreferees. The Orga- bromeliads (Wiley and Cruz 1980, Orians nizationfor TropicalStudies and JessieSmith Noyes 1985).Therefore, although additional studies Foundationprovided critical financial and logistic are neededto makefirm conclusions,large size support.Further generous support was provided by probably does not assistmales in obtaining the following organizations:American Museum of foodfrom bromeliadsor otherepiphytes. Natural History (Frank M. ChapmanFund), Cornell University,National Institute of Mental Health, Na- The aboveresults suggest that the observed tional Science Foundation (NSF Graduate Fellow- foragingdifferences between male and female ship), Organizationfor American States,and Sigma Montezuma Oropendolasare a consequence Xi (Grant-in-Aid-of-Research).Finally, I thankthe La ratherthan a causeof sexualsize dimorphism. Selvadenizens, and the many CostaRican residents However, the results are not conclusive and who allowedme to work on their lands,for making must be considered with two caveats. First, as this studypleasant as well aspossible. During prep- discussedabove, detailed studiesof foraging aration of the manuscriptI was supportedby the efficiencyon different food resourcesare need- University at Buffalo and a National ScienceFoun- ed to determinewhether large males are better dation CAREER Award. able to forage in bromeliadsthan are small males or females.Second, ecological differ- LITERATURE CITED encesbetween the sexesother than foraging may favorsexual size dimorphism. For exam- ALEXANDER,R. D., J. L. HOOGLAND, R. D. HOWARD, K. M. NOONAN, AND P. W. SHERMAN. 1979. Sex- ple, differentparental roles, risk of predation ual dimorphismsand breedingsystems in pin- (if differentpredators prey on the two sexes), nipeds,ungulates, , and .Pages or parasitism (if niche separationreduces 402--435in Evolutionarybiology and so- transmissionrates) could lead to sexual size di- cial behavior:An anthropologicalapproach (N. morphismeven if competitionfor food re- A. Chagnonand W. Irons, Eds.).Duxbury Press, sourcesdoes not. These alternativesrequire North Scituate, Massachusetts. furthertesting. ANDERSSON, g. 1994. Sexual selection. Princeton In summary,my resultsshow that sexualse- University Press,Princeton, New Jersey. lectionis at leastpartially responsiblefor the ASKINS,R. A. 1983. Foragingecology of temperate- extremesexual size dimorphismin Montezu- zone and tropical .Ecology 64: 945-956. ma Oropendolas,and that the sexesdiffer in BEECHER,W.J. 1951. Adaptationsfor food-gettingin the microhabitatsthat theyexploit for animal the American blackbirds. Auk 68:411-440. prey.These results also suggest that sexual for- BJORKLUND,M. 1990. A phylogeneticinterpretation agingdifferences are a consequencerather than of sexual dimorphism in body size and orna- a causeof sexualsize dimorphism in this spe- ment in relation to mating systemin birds. Jour- cies,and that sexualforaging differences rep- nal of EvolutionaryBiology 3:171-183. resent an ecologicalcost of large male size. BJ•)RKLUND,M. 1991. Evolution, phylogeny,sexual October1997] SexualSize Dimorphism in Oropendolas 579

dimorphismand matingsystem in the grackles birds: Male-female differences. Wilson Bulletin (Quiscalusspp.: Icterinae). Evolution 45:608-621. 98:196-213. BJ•RKLUND, M., AND M. LINDgN. 1993. Sexual size HOUSTON, D., AND R. SHINE. 1993. Sexual dimor- dimorphismin the GreatTit (Parusmajor) in re- phism and nichedivergence: Feeding habits of lationto historyand currentselection. Journal of theArafura filesnake. Journal of AnimalEcology EvolutionaryBiology 6:397-415. 62:737-748. CAMILLERI, C., AND g. SHINE. 1990. Sexual dimor- KODRIC-BROWN,A., AND J. H. BROWN. 1978. Influ- phism and dietary divergence:Differences in ence of economics,interspecific competition, trophicmorphology between male and female and sexualdimorphism on territorialityof mi- .Copeia 1990:649-658. grant Rufous . Ecology 59:285- GLUTTON-BRocK, t. H., P. H. HARVEY, AND B. RUD- 296. DER.1977. Sexualdimorphism, socionomic sex LINDE, g. 1980. Sexualdimorphism, sexual selec- ratio and body weightin primates. 269: tion, and adaptationin polygeniccharacters. 797-800. Evolution 34:292-305. DARWIN, C. 1871. The descent of and selection LANGSTON, N. E., S. FREEMAN, S. ROHWER, AND D. in relation to sex.John Murray, London. GORI. 1990. The evolutionof femalebody size DUNNING,J. B., JR. 1984. Bodyweights of 686 Spe- in Red-wingedBlackbirds: The effectsof timing ciesof NorthAmerican birds. Eldon Publishing, of breeding,social competition, and reproduc- Cave Creek, Arizona. tive energetics.Evolution 44:1764-1779. EMLEN,S. t., ANDL. W. ORING.1977. Ecology,sexual LANYON,S. M. 1987. Jacknifingand bootstrapping: selectionand the evolutionof mating systems. Important"new" statisticaltechniques for or- Science 197:215-223. nithologists.Auk 104:144-146. FAIRBAIRN,D. J., AND g. E PREZIOSI.1994. Sexual se- MCDADE, L. A., K. S. BAWA, H. A. HESPENHEIDE,AND lectionand the evolutionof allometryfor sexual G. S. HARTSHORNE.1993. La Selva:Ecology and size dimorphismin the water strider,Aquarius naturalhistory of a Neotropicalrainforest. Uni- reiniBis.American Naturalist 144:101-118. versityof ChicagoPress, Chicago. FRAGA,R. M. 1989. Colony sizes and nest trees of MEASE,D., ANDE. MEASE.1980. Aerial net assembly. Montezuma oropendolasin Costa RiGa.Journal North American Bird Bander 5:138-139. of FieldOrnithology 60:289-295. NADKARNI, N.M., AND t. J. MATELSON. 1989. Bird FREEMAN, S., AND W. M. JACKSON. 1990. Univariate use of epiphyteresources in Neotropicaltrees. metricsare not adequateto measureavian body Condor 91: 891-907. size. Auk 107:69-74. NOSKE,R. A. 1986. Intersexualniche segregation GIBBS,H. L., P. J. WEATHERHEAD,P. t. BOAG, B. N. amongthree bark-foraging birds of eucalyptfor- WHITE, L. M. TABAK,AND D. J. HOYSAK. 1990. ests.Australian Journal of Ecology11:255-267. Realized reproductive successof polygynous OAKES,E. J. 1992. Lekkingand the evolutionof sex- Red-wingedBlackbirds revealed by DNA mark- ual dimorphism in birds: Comparative ap- ers. Science 250:1394-1397. proaches.American Naturalist 140:665-684. GIBSON,R. g., AND J. W. BRADBURY.1985. Sexual se- ORIANS, G. H. 1985. Blackbirds of the Americas. lectionin lekkingSage : Phenotypic cor- Universityof WashingtonPress, Seattle. relatesof malemating success. Behavioral Ecol- PAYNE,g. B., AND K. PAYNE. 1977. Social organiza- ogy and Sociobiology18:117-123. tion and mating successin local song popula- GRADWOHL,J. A., AND g. GREENBERG.1984. Search tions of Village Indigobirds, Vidua chalybeata. behavior of the Checker-throated Antwren for- Zeitschriftffir Tierpsychologie45:113-173. aging in aerial leaf litter. BehavioralEcology and PETERS,W. D., AND t. C. GRUBB.1983. An experi- Sociobiology15:281-285. mental analysisof sex-specificforaging in the GREENBERG,g. 1979. Body size, breedinghabitat Downy ,Picoides pubesGens. Ecology and winter exploitationsystems in Dendroica. 64:1437-1443. Auk 96:756-766. PRICE, T. D. 1984. The evolution of sexual size di- GREENBERG,g. 1987. Seasonalforaging specializa- morphismin Darwin'sfinches. American Natu- tion in the Worm-eating Warbler. Condor 89: ralist 123:500-518. 158-168. PRUETT-JONES,S. G., AND M. A. PRUETT-JONES.1990. HEDRICK,A. V., AND E. J. TEMELES.1989. The evo- Sexualselection through female choice in Lawes' lution of sexual dimorphism in animals: Hy- Parotia,a lek-matingbird of paradise.Evolution pothesesand tests.Trends in Ecologyand Evo- 44:486-501. lution 4:136-138. PUTTICK, G. M. 1981. Sex-related differences in for- HC•GLUND,J. 1989. Size and plumagedimorphism in aging behaviour of Curlew .Ornis lek-breeding birds: A comparative analysis. Scandinavica 12:13-17. American Naturalist 134:72-87. RILLS,K. 1976. Extremesof sexualdimorphism in HOLMES,R. T. 1986. Foraging patterns of forest size in birds. Wilson Bulletin 88:149-150. 580 MICHAELS. WEBSTER [Auk, Vol. 114

RALLS,K. 1977. Sexualdimorphism in mammals: WALLACE,R. A. 1974. Ecologicaland social impli- Avian models and unanswered questions. cationsof sexualdimorphism in five melaner- American Naturalist 111:917-938. pine woodpeckers.Condor 76:238-248. gEMSEN,J. V., JR., AND t. A. PARKER,III. 1984. Ar- WEATHERHEAD,P. J., AND P. t. BOAG. 1995. Pair and borealdead-leaf-searching birds of theNeotrop- extra-pair mating successrelative to male qual- ics. Condor 86:36-41. ity in Red-wingedBlackbirds. Behavioral Ecol- RISING, J. D., AND K. g. SOMERS.1989. The mea- ogy and Sociobiology37:81-91. surement of overall body size in birds. Auk 106: WEATHERHEAD,P. J., AND R. G. CLARK. 1994. Natural 666-674. selectionand sexualsize dimorphismin Red- ROBINSON,S. K. 1985a. Benefits, costs, and deter- winged Blackbirds.Evolution 48:1071-1079. minants of dominancein a polygynousoriole. WEATHERHEAD,P. J., H. GREENWOOD,AND R. G. Animal Behaviour 34:241-255. CLARK. 1987. Natural selection and sexual se- ROBINSON,S. K. 1985b.The Yellow-rumped lection on body size in Red-wingedBlackbirds. and its associatednest pirates. Pages 898-907 in Evolution 41:1401-1403. Neotropicalornithology (M. S. Buckley,M. S. WEBSTER,M. S. 1991. The dynamicsand conse- Foster, E. S. Morton, R. S. Ridgely, and E G. quencesof intrasexualcompetition in the Mon- Buckley,Eds.). Ornithological Monographs No. tezumaOropendola: Harem-polygyny in a Neo- 36. tropicalbird. Ph.D. dissertation, Cornell Univer- SCHOENER,t. W., J. B. BLADE,AND C. H. STINSON. sity,Ithaca, New York. 1982. Diet and sexualdimorphism in the very WEBSTER,M. S. 1992. Sexualdimorphism, mating catholiclizard ,Leiocephalus of the Baha- systemand body size in New World blackbirds (Icterinae). Evolution 46:1621-1641. mas.Oecologia 53:160-169. WEBSTER,g. S. 1994a. Female-defencepolygyny in SEARCY,W. g. 1979. Male characteristicsand pair- a Neotropicalbird, the Montezuma Oropendola. ing successin Red-winged Blackbirds.Auk 96: Animal Behaviour 48:779-794. 353-363. WEBSTER,M. S. 1994b.The spatial and temporal dis- SEARCY,W. A., AND K. YASUKAwA.1995. Polygyny tribution of breeding female Montezuma Oro- and sexual selectionin Red-winged Blackbirds. pendolas: Effects on male mating strategies. PrincetonUniversity Press,Princeton, New Jer- Condor 96:722-733. sey. WEBSTER,g. S. 1995. The effects of female choice SELANDER,R. K. 1966. Sexualdimorphism and dif- andcopulations away from the colony on the fer- ferential niche utilization in birds. Condor 68: tilization successof male MontezumaOropen- 113-151. dolas. Auk 112:659-671. SELANDER,R. K. 1972. Sexual selection and dimor- WESTNEAT,D. E 1993. Polygynyand extrapair fer- phismin birds.Pages 180-230 in Sexualselec- tilizations in eastern Red-winged Blackbirds tion and the descentof man (B. Campbell,Ed.). (Agelaiusphoeniceus). Behavioral Ecology 4:49- Aldine,Chicago. 60. SHINE,R. 1989. Ecologicalcauses for the evolution WILEY, g. H., AND A. CRUZ. 1980. The Jamaican of sexualdimorphism: A reviewof theevidence. blackbird:A "naturalexperiment" for hypoth- Quarterly Review of Biology64:419-461. eses in socioecology.Evolutionary Biology 13: SHINE,R. 1991. Intersexualdietary divergenceand 261-293. the evolutionof sexualdimorphism in snakes. WILLIAMS,J. B. 1980. Intersexualniche partitioning American Naturalist 138:103-122. in Downy Woodpeckers.Wilson Bulletin 92:439- SKUTCH, A. F. 1954. Life histories of Central Amer- 451. ican birds. Pacific Coast Avifauna No. 31. YASUKAWA,K. 1981.Male qualityand female choice SLATKIN,M. 1984. Ecologicalcauses of sexual di- of mate in the Red-wingedBlackbird (Agelaius morphism.Evolution 38:622-630. phoeniceus).Ecology 62:922-929. TEMELES,E. J. 1986. Reversed sexual size dimor- YASUKAwA,K. 1987. Breedingand nonbreedingsea- phism:Effect on resourcedefense and foraging son mortality of territorial male Red-winged behaviorsof nonbreedingNorthern Harriers. Blackbirds(Agelaius phoeniceus). Auk 104:56-62. Auk 103:70-78. Associate Editor: T. E. Martin