Short Communications and Commentaries

The Auk 111(3):703-710, 1994

Serrate Tomia: An for Nectar Robbing in ?

JtJAN FRANCISCOORNELAS Departmentof Ecologyand EvolutionaryBiology, University of Arizona, Tucson, Arizona 85721, USA

Hummingbirds are distinguished from all other straight or curved mandibles. Bill serrationsare very groups of birds by the range of bill-shape and bill- conspicuouson both tomia in Androdonand Rampho- length variation.Such bill configurationsare thought don,but in Glaucisand Sapphoserrations were detected to match particular floral morphologies(e.g. Grant only on the maxillary tomium. The serrationsare and Grant 1968, Stiles 1978, Brown and Kodric-Brown presentonly on one-thirdto one-halfof the bill start- 1979, Stein 1992). Considerable research has been ing at the tip. Thosetoward the tip usuallyare longer conductedon bill shapeand length variation;in con- and slant posteriorlyat an angle of 45ø . trast, serrations have not received much attention. In In the 24 genera lacking hooked bill tips but having their extensivereview of the literature dealing with serratedtomia, the serrationsat the tip of the bill are bills (and tongues)of nectarivorousbirds, Paton and not as enlarged as in the previous group. Sixteen Collins (1989) make no mention of bill serrations. Bill generahave serrationsonly on the maxillary tomium serrations,a variable feature among hummingbirds, and 8 generahave serrationson both tomia (seeTable have been studied only in a few species.Only two 1). genera, Androdonand Ramphodon,have been consis- Given the condition of many older specimensat tently reportedas having bills with distinctlyserrated museums,it was often impossibleto count accurately edges(e.g. Ridgway 1890,1911, Johnsgard 1983, Hilty the number of serrations.However, most genera have and Brown 1986).According to Ridgway(1911), how- about 20 to 30 serrations along the cutting edge of ever, this characteris present in other genera, and it the bill; serrationsare most abundant distally and consists of a variable number of minute serrations in diminish proximally. A unique situation prevails in the terminal portion of the maxillary and mandibular Schistesgeoffroyi in which serrationswere mainly ob- tomia. In this paper I describebill serrationsin hum- served at the middle of the bill. Individuals of An- mingbirds at the generic level and discusstheir func- drodonand Ramphodonmay have more than 50 very tional significance. long and conspicuousserrations (Fig. 1). In Chrysu- Methods.--I studied skin collections at five muse- ronia,Cynanthus, Goldmania, Oreonympha, Taphrolesbia, ums (see Acknowledgments),examining skin speci- and in somespecies of Chlorostilbon,bill serrationsare mensof 107 genera(98% of total of 110 genera)and weakly developed when present (seeTable 1). In such 311 species(92% of total of 320 known species)of cases,the existenceof serratetomia must be regarded hummingbirds. I checked at least 10 specimensof with uncertainty. each speciesfor bill serrationsusing a stereomicro- The shape of the bill is variable even among hum- scope and/or a hand lens. Most museum skins are mingbirds that lack a hooked tip. Most of the hum- prepared with the mouth closed (often tied shut). mingbirds with serrations have very pointed bills. When this was the case,I opened the bills carefully This very sharp cutting edge resemblesa needle in for examination. I recorded the following informa- Doryfera,Augastes, Chrysolampis, and Damophila.In two tion: (1) shapeof bill tip (e.g. hooked,wedge shaped); genera the terminal portion of the bill is very much (2) the number and shapeof serrations(when pres- compressed(i.e. wedge shaped; Heliothryxand Au- ent); and (3) the distribution of the serrationsalong gastes;Ridgway 1911). The bill of the Fiery-tailed the bill (e.g. serrationsonly on maxillary tomium). Awlbill (Avocettula recurvirostris) is upturned with ser- Results.--Twenty-eightgenera (23% of humming- rationson both tomia (Fig. 1). bird genera) have specieswith serratedbills (a total Discussion.--The parallel bill structures in Andro- of 69 species;Figs. 1 and 2). Four of thesegenera also don,Glaucis, Ramphodon, and Sapphoand 24 other gen- have hooked bill tips (Table 1). In the Tooth-billed era have not been exploredcarefully. In the following (A ndrodonaequatorialis), both the upper sections,I propose two possible functional explana- and lower bill (maxilla and mandible) are hooked, tions for such morphological characteristicsin hum- and the edge of both tomia finely toothed (ca. 50 mingbirds. serrationsalong 10 ram) or fringed near the tip (Ridg- It has been hypothesizedthat the function of bill way 1911, Johnsgard1983; Fig. 1). The genera Ram- serrationsis to facilitate the holding of insects(Ridg- phodon,Glaucis, and Sapphohave hooked maxillasbut way 1890, Johnsgard1983, Hilty and Brown 1986, 7O3 704 ShortCommunications andCommentaries [Auk,Vol. 111

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I I •rnm Fig. 1. Serratetomia in lateralview. Drawingswere madeby examiningseveral museum specimens (see Acknowledgments).Left (unhookedbills): (A) Colibricoruscans; (B) Anthracothoraxprevostii; (C) Thalurania furcata;and (D) Avocettularecurvirostris. Right (hookedbills): (E) Androdonaequatorialis; (F) Glaucisaenea; (G) Sapphoshanganura; and (H) Ramphodonnaevius. Note changes in size(data available only for unhooked),shape, and orientationof serrationsamong species in both groups.

Gosner1993). The hook and bill serrationsmay form habitats(open canopyand forestinterior, respective- part of a feeding structureof hummingbirds that spe- ly; Ch•vez-Ramlrezand Dowd 1992,Chavez-Ramirez cialize on hard-bodied arthropods.Such a morpho- and Tan 1993). This suggeststhat an associationof logical device may serveto secureprey by increasing bill setrationswith foragingtechnique and/or habitat the coefficientof friction when catching or holding type is unlikely. prey. Little is known about how hummingbirds handle Most hummingbirdsroutinely consumearthropods different types of arthropod prey. In aviaries, hum- asa sourceof protein (Young 1971,Remsen et al. 1986, mingbirdsseem incapable of manipulatingprey items Ch•vez-Ramlrez and Dowd 1992, Ch•vez-Ramlrez and with the bill or even holding them for more than a Tan 1993). Mobbs (1979) describedfive methodsused few seconds(pers. obs., Thompson 1974). Mobbs (1979) in captivity among hummingbirds when capturing observedthat "when a hummer capturesan insectin insects and attributed such variation to habitat dif- flight (hawking), its forward movement forces the ferences (e.g. open areas vs. forest interiors) or to prey so far to the rear of the gape that it is already substrate (usually or bark). tech- swallowed." It is possible,however, that highly in- niques include flycatching and gleaning from flow- sectivoroushummingbirds use the bill serrationsfor ers,leaves, and spiderwebs (Young 1971,Mobbs 1979). manipulating food items. Two specieswith setrationson both tomia, the Green- Gosner(1993) suggestedthat scopatetomia in birds throated Carib (Sericotesholosericeus) and Purple- (i.e. brushlike ridges on cutting edgesof mandibles) throated Carib (Eulampisjugularis; Table 1), use dif- are adaptationsfor handling hard-shelledprey. If this ferent arthropod foraging methods (flycatching and is true, one would expect that hummingbirds with flower gleaning,respectively) and foragein different serratedbills should feed on aerial hard-bodiedprey. July1994] ShortCommunications andCommentaries 705

A TABLE1. Generaof hummingbirdswith minute ser- rations on tomia.

Serrations Known Only Both to rob ! • 1• Genera Hook maxilla tomia nectar Aglaiocercus B Androdon X Anthracothorax x Augastes A vocet tula Chalybura Chlorostilbon x i i 1ram Chrysolampis Chrysuronia X a ½ Colibri x Cynanthus Damophila Doryfera Elyira x • 1 lmm Eulampis x Eupherusa x x D Glaucis X x Goldmania X" Heliothryx x x Polytmus Oreonympha X" Ramphodon X • • lmm Sappho X x Sericotes x E Schistes x Taphrolesbia x- Thalurania x x Trochilus x x

ßSerrate tomia. when present,weakly developed(see text).

I i lmrn of hummingbirds,those with serratedbills specialize on hard-bodied arthropods, nor that when hum- Fig. 2. Photographsshowing only upper mandi- mingbirdsforage they useconsistently the sametech- bles. Smooth tomia: (A) Campylopterushemileucurus nique and/or forageon the samesubstrata. A detailed (UA, 8 972). Serrate tomia: (B) Cohgricoruscans (U^, studyis neededof the kind of arthropodsconsumed 13 897); (C) Thaluraniaridgwayi (UA, 8 025); (D) An- by bothhermits and nonhermits.The arthropod-feed- thracothoraxprevostii (UA, 13 010); and (E) Colibrico- ing hypothesisfor serratetomia and hookedbills can tuscans(UA, 13 898). be evaluated as information accumulates on (1) dif- ferencesin arthropoddiets of hummingbirds,and (2) Hummingbirdswith a hookand/or setrationson their differencesin arthropod-foragingtechniques. bills would be capturingand holding different types Nectar robbing is a behavior exhibited by various of prey and usingdifferent foraging techniques(e.g. speciesof hummingbirds and passerinebirds. Nectar gleaning vs. flycatching)than birds without hooksor is obtained through holes made near the basesof the setrations on their bills. Little is known about the corolla tubes, in a manner generally circumventing types of arthropods hummingbirds consume, but contactwith the sexualparts of the flowers (Inouye Remsen et al. (1986) found that hermits take a much 1983).I hypothesizethat bill serrationsmay enhance higher proportionof soft-bodiedspiders than do most the exploitation of resourcessuch as long-tubed co- nonhermits.Based on this possiblepattern, one would rollas and tough-tissuecorollas by facilitating: access expectto find bill serrationsdistributed mostly among to protectednectaries; the graspingof toughand waxy nonhermit species.This seemsnot to be the case. blooms;and the cutting of flower tissue. Accordingto the classificationof Sibley and Monroe There are several morphological similarities be- (1990), 25% of the genera in each group of hum- tween passerine flower-piercers (Diglossa)and the mingbirds have serrated bills (6.8% of all hermit spe- hummingbirds that have serrate tomia. The maxilla ciesand 23.1%of all nonhermit species). of a typical speciesof Diglossasweeps slightly up- There is no evidence then that, among either group wardsfrom its baseand endsin a distinct stronghook 706 ShortCommunications and Commentaries [Auk, Vol. 111

T^I•I.•2. Nectarrobbing in the family Trochilidaeand plantsutilized by nectar-robbinghummingbirds.

Hummingbird species species(reference') Primary nectar robbers Anthracothoraxnigricollis Tabebuiaserratifolia (3) A. viridis Malvaviscus arboreus(9) Chlorostilbonmaugaeus Erythrinaberteroana (9), Neurodolphiavolubilis (5), Malvaviscusarboreus (9), Pitcairniaangustifolia (9), P. bromeliifolia(5), Tabebuiahaemantha (5), T. rigida(9), T. schumanniana(5) C. mellisugus Plant not identified (7) C. ricordii Barlena cristata(9), Tabebuiarosea (9) Colibri thalassinus Salviaspp. (8) Eulampisjugularis Plant not identified (9) Eupherusaeximia Plant not identified (13), Justiciaaurea (2), Malvaviscuspalmarus (2), Dry- moniarubra (2), Drymoniaconchocalyx (2), Raziseaspicata (2), Poikilacan- thus macranthus(2) Heliothryxbarroti Erythrinasp. (10), Aphelandragolfodulcensis (6), Raziseasp. (12), Heliconia spp. (13) Thaiuraniaridgwayi Plant not identified (8) Trochiluspolytmus Plant not identified (9) Secondary nectar robbers Panterpeinsignis Plant not identified (11), Centropogontalamancensis (1) Nectar thieves Calliphloxevelynae Plant not identified (9) Heliodoxajacula Marcgraviaspp. (12) Lesbiasp. Brugmansiasp. (4) Phaethornislonguemareus Plant not identified (14), Aphelandragolfodulcensis (6), Justiciaaurea (6) Selasphorusfiammula Centropogonvalerii (1) Threnetes ruckeri Calatheaspp. (13) • References:(1) Colwell et al. 1974;(2) Feinsingeret al. 1987;(3) ffrench 1973;(4) Gould 1861;(5) Kodric-Brownet al. 1984;(6) McDadeand Kinsman1980; (7) Meyer de Schauenseeand Phelps1978; (8) pets.ohs.; (9) Quesada-Tyrrelland Tyrrell 1990;(10) Skutch1973; (11) Stiles1983; (12) Stiles 1985; (13) Stiles and Skutch 1989; (14) Wetmore 1968.

(Vuilleumier 1969, Bock 1985) as in Androdon,Glaucis, piercing by short-billed hummingbirds(Beal 1880, Ramphodon,and Sappho.Immediately behind the hook, Ridgway1890, Grant 1952, Skutch 1954, Colwell 1973, there is a notch in the maxillary tomium that is fol- Gentry1974, Janzen 1975, Ingels 1976, Feinsinger and lowed by two to four setrationsin Diglossa(but these Colwell 1978,Snow 1981,Inouye 1980a,1983; for more are weak or almostabsent in somespecies; Bock 1985). references, see Table 2). Similarly, among hummingbirds,28 genera have the Four behavioral categoriesamong nectar robbers edge of the tomia finely toothed near the tip, so that can be recognized(after Inouye 1980b):(1) highly the tip of the bill resemblesthat of a flower-piercer specializedprimary nectarrobbers perforate the base bill (pets. obs., Ridgway 1890). of long-tubedcorollas (gamepetalous corollas) polli- The hook and setrations of the upper jaw, the flat nated mainly by other hummingbirds;(2) secondary cutting edge of the mandibular tip, and the incom- nectar robbers utilize flowers perforated by other plete mandibulartube in Diglossaspecies are all parts hummingbirdsor passefineflower-piercers; (3) nectar of a specializedadaptive complex associatedwith the thieves use the opening utilized by pollinators but, unusual method of nectar feeding used by flower- without biting or making holes, collect nectar from piercers (Bock 1985). The bird robs nectar first by flowersmorphologically adapted for pollinationby a holding the side of the flower with its hooked upper different classof visitors;and (4) baseworkers obtain jaw and cutting through the corolla wall with the nectarby reachingbetween the .This behavior mandibular tip. With the corolla held in place, a lon- is performed to flowers with polypetalouscorollas, gitudinal slit is cut into its near wall with the man- thereby bypassingthe opening used by pollinators dibular tip. Finally, the bird's tongue is protruded and gaining more direct accessto the nectary at the through this slit into the flower to obtain nectar baseof the corolla.For example, Ch•vez-Ramlrez and (Skutch 1954, Vuilleumier 1969). Dowd (1992) observedDominican caribsprobing be- The Diglossaflower-piercers are perhaps the best- tween the petals(polypetalous corolla) to take nectar. known examples of nectar robbers among birds The observation indicates that caribs, which have ser- (Skutch 1954,Lyon and Chadek 1971, Colwell et al. rated tomia, fit the definition of base workers (after 1974, Snow 1981, Kodric-Brown et al. 1984, Arizmen- Inouye 1980b);however, carlbs also exhibit behaviors di 1994), but several studies have reported flower of a nectar thief, as observedby Ingels (1976). Ac- July 1994] ShortCommunications and Commentaries 707

cording to Inouye (1980b), however, a base worker An obvious prediction is that serrated tomia should would not cut the flowerswith its bill, but the open- be more prevalentamong short-billed hummingbirds ing usedby pollinatorsis not usedeither. Carlbsap- than long-billed hummingbirds. parently do not cut the flowers with their bills, but There are several immediate benefits to the cheater would be better able to probebetween petalsdue to when it performsthis behavior. First, nectar robbing the serrated tomia on their bills. Sometimes these is potentially more energy efficient than legitimate hummingbirds would collect nectar that has leaked flower visitation (Darwin 1889). Furthermore, it has between the petals. been demonstratedwith beesthat the costof foraging Someprimary nectarrobbers (after Inouye 1983) decreasesif nectar is obtained by circumventingthe are mostlyreferred to in the literature as"marauders" flower entrance(Weaver 1956, Free 1968,Inouye 1980a; (seeFeinsinger and Colwell 1978),and secondary nec- but see Sober6n and Martinez del Rio 1985). Second, tar robbersand nectarthieves are consideredas par- nectar robbers have accessto highly rich resources asitoids.However, I follow the categorizationmade (i.e. nectarin long-tubed corollas)that otherwise are by Inouye (1980b) to minimize confusion. Because restrictedonly to long-billed pollinators.This behav- nectarthieves probably do not greatly influencethe ior is advantageousto nectar robberswhen their le- activitiesof pollinators(Inouye 1980b,Stiles 1985),I gitimate accessto nectar in short-tubed corollas is do not include them in further discussion. restricted(e.g. by competition,or by scarcityof ac- Hummingbirds exert strong selectivepressures on cessible flowers). corollamorphology. For example,Fenster (1991) sug- One trade-offfor beingopportunistic (i.e. obtaining gestedthat corollalength is a floral specializationdue nectarby bypassingthe opening usedby pollinators) to competition for pollinators. By increasingcorolla is rarity (Brian 1957, Stiles 1975, Kodric-Brown and length, plantsare discriminatingamong a set of pol- Brown 1979, Sober6n and Martinez del Rio 1985). linators (i.e. long-billed hummingbirds)that would Individuals of a third speciestake advantageof mu- evolve as highly specializedon commonlyrich-nec- tualisticpartnerships and becomedensity dependent tar, long-tubed corollas(e.g. Wolf et al. 1976). on the mutualistic interaction. Rarity among nectar Once a mutualistic relationship has arisen, there is robberswould be the evolutionary outcomeof plant a high probability that a third speciesmight evolve specializationon a particular set of true pollinators to take advantageof mutualistic partnerships(Bou- (e.g. long-billed hummingbirds) and the improve- cher et al. 1982,Inouye 1983,Sober6n and Martinez mentof the robbingtechniques of the excludednectar del Rio 1985).Nectar robbersare probablythe best- exploiters (i.e. hummingbirds with short, serrated documentedexample of behavior (Sober6n bills). As predicted, nectar-robbing hummingbirds and Martinez del Rio 1985) deriving benefitsfrom seemto be rare in nature (Stiles1985, Hilty and Brown flowers without pollinating, while competingwith 1986)and/or erraticon a regionalscale. When present the pollinatorsfor nectar(McDade and Kinsman1980, at a smaller scale,however, nectar robbersare fairly Arizmendi 1994). Some hummingbird flowers are common(pers. obs., Stiles 1985, Hilty and Brown1986, structurallyprotected against nectar robbers (Inouye Feinsinger et al. 1987, Collar et al. 1992, Ornelas in 1980b),but most are unprotectedand are regularly press). exploitedby nectarrobbers, which significantlyaffect Since nectar robbing lets the nectar exploiter be- the amountof nectaravailable to the pollinators(Snow come essentiallyindependent of floral morphology 1981,Arizmendi 1994). However, the ecologicalim- (Stiles 1985), some behavioral attributes should be pact of nectar robbing on both plant reproductive associatedwith this behavior.For example,Stiles (1983) fitnessand pollinators'foraging efficiencyremains observed that Fiery-throated Hummingbirds (Pan- controversial (Hawkins 1961, Heinrich and Raven terpeinsignis) utilize flowers perforated by passefine 1972, Koeman-Kwak 1973, McDade and Kinsman 1980, flower-piercers and may follow the flower-piercer Sober6n and Martinez del Rio 1981, Roubik 1982, from flower to flower, usingthe flower-piercers'holes Inouye 1983, Kodric-Brown et al. 1984, Arizmendi to extract the nectar. This observationsuggests that 1994). an inherent difference in behavior should exist be- It has been assumedthat short-billed humming- tween this nectar robber and a nonnectar-robbing birds cannot feed on flowerswith long corollas(Col- species(Brian 1957). In contrastto most humming- well et al. 1974),but thesespecies often obtain nectar birds that visit flowers by the obvious and correct from flowers with long corollasby making perfora- entrance,nectar robbersshould be expectedto have tions at the base (Darwin 1889, Skutch 1973). This a more plasticand lessstereotyped set of behaviors. behaviorindicates that flowerswith long corollasse- In contrastto most legitimate visitors,nectar robbers crete nectar attractiveto short-billed hummingbirds need to keep track of the flowersthat have been punc- solong asthey are ableto extractit (e.g.Kodric-Brown tured by the flower-piercers and have to deal with, and Brown 1979, Inouye 1983, Koctric-Brownet al. for example,flowers with well-protectednectaries such 1984, Feinsinger et al. 1987). Hummingbirds may as mostbromeliads. This suggeststhat nectarrobbers pierce the base of flowers with long corollaswith a shoulddiffer from legitimatevisitors in their tenacity short,serrate, hooked, and/or exceptionallysharp bill. and observationalskills when obtaining food. An- 708 ShortCommunications andCommentaries [Auk,Vol. 111

other differencebetween these two groupsof hum- brles-plantasy el ladr6nde n•ctar Diglossa baritula mingbirds is that individuals of most nectar robbers (Passeriformes: Aves). Tesis Doctorado, Univ. foragealone, and rarely defend territories(Wetmore Nacional Aut6noma de M•xico, M•xico, D.F. 1968,ffrench 1973,Meyer de Schauenseeand Phelps BEAL,W.J. 1880. Fertilization of flowers by hum- 1978, Stiles 1985, Hilty and Brown 1986, Stiles and mingbirds. Am. Nat. 14:126-127. Skutch1989). Typically, nectar robbers do not estab- Boche,W.J. 1985. Is Diglossa(?Thraupinae) mono- lish territories,but they are notablybellicose; they phyletic?Pages 319-332 in Neotropicalornithol- are able to withstand attacks of most territorial hum- ogy (P. A. Buckley,M. S. Foster,E. S. Morton, R. mingbirds (Stiles 1985, Stiles and Skutch 1989). S. Ridgely, and F. G. Buckley,Eds.). Ornithol. The rhamphothecalfeatures of the flower-piercers Monogr. 36. are adaptationsfor nectarivoryon flowerswith long BOUCHER,D. H., S. JAMES,X•qD K. H. KEELER. 1982. corollas(Bock 1985). However, the flower-piercing The ecologyof .Annu. Rev.Ecol. Syst. method of nectar feeding on flowers with deep co- 13:315-347. rollas is not restrictedto the flower-piercersamong Bmx•, A.D. 1957. Differences in the flowers visited passerines,but is found in two other genera (Coereba by four speciesof bumblebeesand their causes. and Conirostrum)and in severalgenera of humming- J. Anim. Ecol. 26:71-98. birds (e.g. Skutch 1954, Bock 1985, Stiles and Skutch BROWN, J. H., AND A. KODRIC-BRowN. 1979. Con- 1989;see Table 2). This suggeststhat the complexof vergence,competition, and mimicry in a tem- featuresof the bill for nectarrobbery has evolved perate community of hummingbird-pollinated more than oncein birds with suchmorphology. Al- flowers.Ecology 60:1022-1035. though a phylogenyof the Trochilidaeis not yet CHAVEz-RAMIREZ, F., AND M. DOwD. 1992. Arthro- available, the existence of serrated tomia in otherwise pod feeding by two Dominican hummingbird dissimilarhummingbird species leads me to suggest species.Wilson Bull. 104:743-747. that this feature has evolved severaltimes indepen- CHAVEZ-RAMiREZ, F., AND S.S. TAN. 1993. Habitat dently within the family. separationand arthropod resourceuse in three With the evidencepresented above, it appearsthat LesserAntillean hummingbirds.Condor 95:455- bill serrationsare an adaptationin somehumming- 458. birds for nectar robbing, but further supportfor this COLLAR,N. J., L. P. GONZAGA,N. KRABBE,A. MADROiqO ideais requiredfrom ontogenetic,phylogenetic, and NIETO, L. G. NARANJO,T. A. PARKERIII, AND D. behavioral studies. C. Wœc;œ. 1992. Threatened birds of the Amer- Acknowledgments.--Ithank Felipe Chfivez-Ramirez, icas.The ICBP/IUCN red databook, 3rd ed.,part W. Mark Roberts,Gary D. Schnell,and LarryL. Wolf 2. International Council for Bird Preservation, for helpful discussionand review of the manuscript. Cambridge,United Kingdom. Lucinda McDade, Stephen M. Russell, Peter Scott, COLWELL,R. K. 1973. Competition and coexistence SusanWethington, and Yaron Ziv provided invalu- in a simple tropicalcommunity. Am. Nat. 107: able suggestionsconcerning earlier versionsof the 737-760. manuscript.I thank the following curatorsfor allow- COLWELL,R. K., B. J. BETrS, P. BUNNELL,F. L. CAR- ing me to examine specimens under their care: G. }'ENTER,AND P. FEINSIIqGER.1974. Competition Barrowclough(American Museum of Natural Histo- for the nectarof Centropogonvalerii by the hum- ry, AMNH); P. Escalanteand L. Navarijo (Colecci6n mingbirdColibri thalassinus and the flower-piercer Ornito16gicadel Instituto de Biologlade la Univer- Diglossaplumbea, and its evolutionaryimplica- sidadAut6noma de M•xico, IBUNAM); T' HueIs(Uni- tions. Condor 76:447-452. versity of Arizona, UA); A. Navarro (Museo de Zool- DARWIN, C. 1889. The effects of cross and self-fer- ogia de la Facultad de Ciencias de la Universidad tilization in the vegetablekingdom. D. Apleton, Aut6noma de M•xico, MZFC); and A. T. Petersonand. New York. D. Willard (Field Museumof Natural History, FMNH). FEINSINGER,P., AND R. K. COLWELL. 1978. Commu- Kris Sondereggerprepared the illustration.Funding nity organization among Neotropical nectar- wasprovided by scholarship56254 from ConsejoNa- feeding birds. Am. Zool. 18:779-795. cionalde Cienciay Tecnologla(CONACyT-M•xico), FEnqSINGER,P., J. H. BEACH,Y. B. LINHART,W. H. BUSBY, and by a grant from the Universityof Arizona Re- AND G. MURRAY. 1987. Disturbance,pollinator searchTraining Group (RTG) in the Analysisof Bi- predictability,and successamong ological Diversification. CostaRican cloud forest . Ecology 68:1294- 1305. FENSTER,C.B. 1991. Selectionon floralmorphology by hummingbirds.Biotropica 23:98-101. LITERATURE CITED FmlENCH,R. 1973. A guide to the birds of Trinidad and Tobago.Livingston Publishing Co., Winne- ARIZMENDI,M. C. 1994. Interacciones eco16gicas wood, Pennsylvania. mfiltiples: E1 caso del sistemamutualista coli- FREE,J.B. 1968. Thebehavior of beesvisiting runner July1994] ShortCommunications andCommentaries 709

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The Auk 111(3):710-713, 1994

Divergence in the Mitochondrial DNA of Empidonax traiIIii and E. alnorum, with Notes on Hybridization

• WINY•R • Academyof Natural Sciences,Benjamin Franklin Parkway, Philadelphia, Pennsylvania 19103, USA

The Empidonaxflycatchers represent a morpholog- pleton 1989)are remarkablywell developed.Perhaps, ically conservativespecies assemblage. This conser- however, it is our inability to recognize Empidonax vatismhas made recognition of specieslimits difficult, hybrids, rather than their true rarity, that leads to and there hasbeen a recenttrend toward recognizing their apparent scarcity.Two of the five recognized separatespecies among populationsformerly consid- tyrannid hybrids (seeShort and Burleigh 1965, Phil- ered conspecific(e.g. Stein 1958,1963, Johnson 1980, lips 1966, Phillips and Short 1968) are intergeneric, Johnsonand Marten 1988).Empidonax flycatchers rep- suggestingthat congenerichybrids are being over- resent a group where molecular systematicscan ad- looked.Further, because individuals of the genusEm- dressa variety of heretofore unanswered questions, pidonax(including E. traillii) have produced hybrids especiallythose regarding degreesof distinctivehess with heterospecifics(see Short and Burleigh 1965, and gene flow between populationsor species(see Phillips 1966), hybridization might be predicted be- alsoHewitt 1988,Avise and Ball 1991).Sibling species tween the closely related E. traillii and E. alnorum. such as the Willow Flycatcher(E. traillii) and Alder Seutin and Simon (1988) arrived at the same conclu- Flycatcher(E. alnorum)are particularlyinteresting with sion in a different manner, suggestingthat the close regard to the evolution of intrinsic isolating mecha- phenotypic similarity and habitat preferencesof E. nisms,an important component of the speciationpro- alnorumand E. traillii,together with the extensivezone cess.The degreeto which intrinsic reproductiveiso- of sympatry,makes hybridization betweenthem like- lating mechanisms(i.e. ability to discriminatebetween ly. These authors failed to find evidence of hybrid- con- and heterospecifics,resulting in assortativemat- ization, however, and concluded that these species ing) have arisenbetween two allopatricpopulations were reproductivelyisolated in southeasternCanada. will affecthow distinctthese gene poolswill remain They sought evidence of hybridization using allo- following secondarycontact. zyme electrophoresis,although this technique had A scarcityof recognizedhybrids among Empidonax already revealed no fixed allelic differencesbetween flycatcherssuggests that, althoughthey are morpho- the two speciesin Minnesota(Zink and Johnson1984). logically conservative,their intrinsic reproductive Without a fixed-allelicdifference, the ability to detect isolatingmechanisms (or cohesionmechanisms; Tern- hybrids is compromised.Another problem with the study was that it did not include traillii from allopatric populations. * Present address: National Museum of Natural His- My study consistedof three parts:(a) estimating tory, Division of Birds, SmithsonianInstitution, the level of divergencein the mitochondrialDNA Washington,DC 20560, USA. (mtDNA) of E. traillii and E. alnorum;(b) finding spe-