The Classification of Avian Species and Subspecies

The classification of avian species and subspecies

A lucid presentation of the baseson which speciesare lumped or split

John T. Ratti

INTRODUCTION (1971:99) reported that ornithologists evidencethat these two indigo birds have "universallyadopted" the biologi- locally behave as distinct biological ECENTLY,THERE HAVE BEENa cal speciesconcept, defined by Mayr species"(Payne 1973:175). number of changesin the classifica- (1969:20) as "groups of interbreeding tion of bird speciesapproved by the natural populations that are reproduc- ISOLATING MECHANISMS Committee on Classification and No- tively isolatedfrom other suchgroups." menclature (American Ornithologists' Strictly and simply, this definition states N THEPARAGRAPH above I referred Union Check-List Committee 1973, that if two populationsoccur in the same to "isolating mechanisms." This con- 1976). Nearly all changesinvolve two or region (sympatric) and do not inter- cept should be discussedbefore con- more closelyrelated species or subpopu- breed, they are separate species sidering evolution of species.Popula- lations of a species.Thus, the systema- regardlessof phenotypic(appearance), tions of birds that occur in the same tist rarely has difficulty separating morphological, or ecological similari- generalregion, yet fail to interbreed,are speciesfrom different orders or families, ties. On the other hand, if two sympatric said to have isolating mechanisms-- and challengesin proper classification or adjacentpopulations frequently inter- "propertiesof individualswhich prevent usually involve populations of the same breed, they are the same species(con- interbreeding" (Mayr 1970:56). Mayr genus or species.Such changesare cas- specific)regardless of phenotypic, mor- (1970) classifiedisolating mechanisms as ually referred to as "lumping" (combin- phological, or ecological differences. "premating" or "postmating." Premat- ing two or more speciesinto a singlespe- Consequently, "reproductive isolation" ing isolating mechanisms include cies) or "splitting" (separating a species is the key to the biological speciescon- seasonaland habitat isolation, behavior- into two or more species) and often cept. However, this does not mean that al isolation, and mechanical isolation. generate confusion and misunderstand- closely related valid species never Postmatingmechanisms include gametic ing among amateur ornithologists and hybridize. Isolating mechanisms are mortality, zygotic mortality, hybrid in- some professional biologists. To often imperfect, and Mayr (1951:102) viability, and hybrid sterility. Avlan ehmlnate this confusion one must study noted that "I understand the occasional isolating mechanisms are commonly and considerpast and present concepts interbreeding of two otherwise well- reported to be behavioral premating of speciation.The following brief review delimitedsympatric species. There is no mechanisms associated with speciesmay be helpful in this regard. Some conceptual difficulty in regard to this specificrecognition of song, color pat- readersmay wish to review the glossary type of hybridization." Speciationis re- terns, courtship displays, and similar of technicalterms in the Appendix. gardedas essentiallycomplete if, during mechanismsthat may be reinforced by sympatry, interbreedingis reducedto a conditioningor imprintingby newlyhat- THE SPECIES CONCEPT level that preventsgenetic swamping by ched chicks (Beach and James 1954, the parent species(Mayr 1959, Bigelow Marler 1957 and 1961, Hinde 1959, Im- OSTSPECIES OF BIRDScurrently 1965).An examplemay be helpful at this melmann 1975a and 1975b). recognized were described on a point. Because two speciesof indigo Smith (1966) found contrastingcolor morphological basis, i.e., classification birdsof Africa, Vidua chalybeataand V. patternsnear the eyeand wingtippattern of speciesaccording to consistent size, purpurascens, were morphologically in- to be the isolatingmechanisms among structure, and color differences. When distinguishable,their status as separate four speciesof gulls (Larus spp.). Jehl dealing with extinct species and fossil species was questioned (White' 1962, and Bond (1975) describeda similarsitu- records, we are forced to base classifica- Payne 1973). To clarify the problem, ation with murrelets of the genus En- tion on morphological characteristics. Payne (1973) studied the degreeof re- domychura and suggestedthat facial However, most modern systematistsdis- productive isolation; pair observations patternsnear the eye and bill shapeboth favor the morphological speciesconcept revealed 71 chalybeata x chalybeata, 5 function as isolating mechanismsbe- becauseit may lead to incorrect classifi- chalybeatax purpurascens,and 73 pur- tween theseclosely related species.Song cation (of subspecies or failure to purascens x purpurascens. Although a and/or call notes have been identified as recognize the separate speciesstatus of small number of hybrids was observed, isolatingmechanisms for syrupatticmea- slbhngspecies). These problemswill be thesedata, along with phenotypicdiffer- dowlarks (Sturnella spp.), Australian discussedlater with examples. Selander ences,were reported to provide "direct Wedgebills(Psophodes spp.), flycatch-

860 AmericanB•rds, November 1980 ers (Empidonax spp.), and indigo birds occasionallyinterbreed. If hybridization the Galapagos Islands and Hawaiian of the sub-genusHypochera (Szijj 1966, is frequent, the populationswill quickly Honey Creepers(Drepanididae) are dra- Ford and Parker 1973, Stein 1963, and lose any differences evolved during iso- maticexamples of founderspecies. Mayr Traylor 1966, respectively).Combina- lation, and their speciesstatus will be (1951:9•)suggested that foundersmay tions of song and color pattern have unchanged.However, if isolatingmech- speciateby double invasion. Where "an been identified as isolating mechanisms anisms prevent interbreeding, or only island is repeatedlyinvaded by colonists by Gill and Murray (1972) and Brown allow for occasionalhybridization, then from a distant mainland, it may happen (1967) while Payne (1973) reportedthe a new specieswill have evolved (Dobz- that the descendants of the first wave of combination of songand behavior. hansky 1937, Lack 1944, Miller 1947, colonists have changed so much that Selanderand Giller's (1961:77) study Mayr 1951 and 1970, Sibley 1961, they are reproductively isolated from of the Great-tailed (Quiscalus mex- Selander 1971, Stebbins 1971, and Bush new arrivals." tcanus)and Boat-tailed grackles(Q. ma- 1975). Speciationis usually a long-term jor) reported the primary isolating processand likely involvesthousands of SUBSPECIES mechanismto be female recognition of years of evolution. Figure 1 was con- male "behavioral differences, both at structed to offer a graphic review of ECAUSESPECIATION issuch a long- term process,some populations can- the time of nest site selection and at time geographicspeciation. not be classifiedas simply belongingto of mating." Many other isolatingmech- At this point one shouldcarefully con- one speciesor another. Certain popula- anisms are reported, including habitat sider the following note of caution. tions are in intermediatestages of specia- (Brewer 1963) and seasonal isolation Divergenceand developmentof isolating tion or have specialmorphological char- (Smith 1966). mechanisms are not mutually depen- acteristics(Mayr 1951, 1963, and 1970, An important part of isolatingmecha- dent; many populations are known that Selander 1971, Stebbins 1971). msms and speciation is reinforcement have diverged morphologically in allo- The taxonomiccategory of subspecies (Mayr 1970). For example, a population patty but possessno isolating mechan- is assignedto distinct subpopulationsof having color patterns as an isolating isms in zones of sympatry. These popu- the same species.This category ranges mechanism may have a fractional por- lations are usually called subspecies. from populationshaving barely percep- tion of members that will readily Conversely, some populations evolve ef- tible morphologicaldifferences to those hybridize. However, if the hybrid off- fective isolating mechanisms, become that appear sufficiently distinctive to spring(Fl) expressan intermediatecolor sympatric, but fail to diverge mor- have been classifiedas separatespecies. pattern, they may be selectedagainst by phologically or in general appearance. In each case, the populations so classi- the majority in their attempt to find a Such populations are called sibling fied have discrete geographic ranges, mate. This negative selection will even- species. have morphologically diverged, but have tually minimize or completelyeliminate Mayr (1970:278) noted that, given the not developed sufficient isolating hybridization. overwhelmingacceptance of geographic mechanisms to maintain reproductive speciation, "the basic problem of THE SPECIATION PROCESS isolation should their ranges overlap. speciation consists in explaining the Consequently, most bird populations AYR(1970:247-277) discussed various origin of the gaps between sympatric that undergogeographic speciation like- modesof speciationwith examples species."With the exceptionof founder ly evolve through a period when they from several taxonomic groups (birds, species(to be discussed),extrinsic bar- would be recognized as subspecies plants, insects, etc.), but ornithologists riers promoting speciation result from (Figure 1). Hence, we do not expect to agreethat geographicdivergence best ex- large-scale environmental change, such observe subspeciesthat are sympatric plains this evolutionary process for as continental drift, glaciation, or (especially during the reproductive birds. climate shifts (Selander 1965, Cracraft season) becausesubspecific characters Geographic, or allopatric, speciation 1973, Croizat et al. 1974). A commonly will quickly be lost via frequent inter- is a processthat typically involves the proposedgeologic event responsiblefor breeding, i.e., subspeciesby definition subdivisionof a large, widely distributed recent North American avian speciation cannot be sympatric. parent population (species)into two or is Pleistocene glaciation. Evidence or Canada Geese (Branta canadensts) more populations.The sub-populations hypothesesfor speciationby Pleistocene provide one of the well-known casesof are isolated geneticallyfrom each other glaciationare presentedby Rand (1948), avian subspeciationin North America. by some extrinsic barrier, e.g., an ocean Sibley (1950), Brewer (1963), Selander There are 10 subspeciesof Canada Geese or mountain range. While separated,the (1965), Mengel (1970), Heusmann recognized by the American Ornitholo- populations diverge either randomly or (1974), and many others. On a more re- gists' Union. Each subspecificpopula- via selectiveforces of their respectiveen- gional scale,the emergenceof mountain tion has isolatedbreeding grounds (Hlne vironments. Divergence by the respec- ranges or the transition of a grassplain and Schoenfeld 1968) and the birds tive populationsmay yield differencesin to desert could easily segregatewidely range in size from the 3 1/2-pound one or severalfactors, such as color pat- distributed populations. Cackling Canada Goose (B.c. minima) tern, size and structure, song, feeding A special form of geographic specia- to the 12 l?2-pound Giant Canada habits, habitat selection, and behavior. tion has been called founder effect. The Goose (B.c. maxima) (Bellrose These or other divergent factors may founder effect is explained as a small 1976:141). Although the subspecific function as isolating mechanismswhich number of birds ("founders") becoming populations have evolved significant will prevent widespread interbreeding established in an area highly isolated morphological differences, there is no when and if the populationsexpand and from the parent population, such as an evidenceto indicatethey have developed overlap. Initially, the populations may island. Darwin's finches (Lack 1947) of isolating mechanisms.

Volume 34, Number 6 861 ParentPopulation•

Population A Geographic Population B Separation I I I I I I I I I I I I I

Divergence I I I Populationswhich have I I separation, but which have l '•1divergednot developedduringisolatinggeographicl I mechanisms,areclassified Isol•ating I as subspecies Mechanisms I- Develop I IPopulation becomeSympatr,cAand.B I

If frequent interbreeding llreproductive isolation occurs in sympatry, A and is maintainedin sympatry,A B are the same species andBare separate species

Figure 1. A graphicillustration of eventsleading to geographicspeciation.

862 AmericanB•rds, November 1980 THE SPECIES-SUBSPECIES CON- Severalhypotheses have been propos- DISCUSSION TROVERSY ed to explain the occurrenceof hybridization. Prevett and Macinnes (1973) ANY OF THE RECENTspecxes PPLICATIONOFTHE SUBSPECIES con- suggestedthat the probable factor caus- changes by the American Orm- cept creates some controversy ing hybridization between Blue Geese thologists' Union Check-List Commxttee among systematists.Stebbins (1971:99) (Anser caerulescens)and Canada Geese have been reviewedby Arbib (1973). In noted "there are many allopatric, com- (Branta canadensis) is egg-dumping. the following paragraphsI will comment pletely separated populations which are This resultsin chicks hatched by, and on only a few of the recent changesand obviously related to each other, but be- relate them to the previousdiscussion of tween which no intermediate individuals imprintedto, geeseof the other species. When reproductivelymature, thesebirds concepts. exist. These populations have never had are probable candidates to seek At this point, it should be fairly ob- a chance to take the 'test of sympatry' membersof the other speciesfor mates, vious why some of the classificationsof and so could be either speciesor subspe- and thus, hybridize. Severalgroups of avian specieshave been changed and cies." The problem is somewhat birds, such as waterfowl, experience why more changes will occur in future paradoxical in that speciesevolve during "brood mixing" when broods from years. The biological species concept geographic isolation, yet cannot be separatespecies meet during useof com- demands years of careful field study to classified as species(via the biological mon habitat. Occasionallychicks end up determine the relationship of popula- concept) until they lose their isolation with the wrong parent of a different tions. Recalling that I began this paper and become sympatric with their parent species,which providesan opportunity noting that most speciespresently recog- species.When "allopatric populations for imprinting to the wrong species,as nized were classifiedon a morphologxcal are so different morphologically or with egg-dumping.When a rare species basis, it should be understandable that otherwisethat reproductiveisolation be- inhabitsthe rangeof a common,closely errors from this approach will be dxs- tween them can be assumed" they are related species,hybridization is likely to closed. classified as superspecies (Mayr occur. Sibley (1961:76) hypothesized Two well-known speciesof warblers, 1970:286, also see Areadon 1966). Mayr that when conspecificmates are in short the Myrtle Warbler (Dendroica cor- (1970) noted that over 30 percent of the supply "the intrinsicmating drive even- onata) and Audubon's Warbler (D. breeding birds in North America meet tually overcomesthe inhibitory effect of audubom), have been merged into a the classificationcriteria of superspecies. incorrectspecies recognition signals and singlespecies, the Yellow-rumped Warb- Therefore, often with "allopatric popu- a mixed pair is formed." ler (D. coronata). The two populatmns lations, phenetic data are evaluated and were originally considered to occupy a predictionis made asto whetheror not Hybridizationamong somespecies is separate ranges and to show distinctly toterbreeding would occur if the forms well known. The Golden-wingedand different color patterns. However, study were in contact" (Selander 1971:100). It Blue-winged warblers (Vermivora of overlappingpopulations has revealed is quite understandable that "predic- chrysoptera and V. pinus) have widespreadinterbreeding--evidence that tions" will lead to disagreement, con- recognized hybrid forms known as the Brewster's and Lawrence's warblers sufficient isolatingmechanisms have not troversy, and error. Equally understand- evolved to consider these forms as able is Mayifs (1970) contentionthat the (Parkes 1951, Gill and Murray 1972). separatespecies (Hubbard 1969). b•ologicalspecies concept, when applied Trauger et al. (1971) reported that to syrupattic populations, is "unam- hybridization is so common among Several speciesof flickers, known to biguous." Snow (Chen h. hyperborea) and Ross' hybridize for nearly a century, have geese(Chen rossit) that approximately recently lost their species status. The HYBRIDIZATION 1400 hybrids have been produced an- Yellow-shafted Hicker (Colaptes aura- nually in recentyears. In one or both of tus), Red-shaftedFlicker (C. cafer), and SOLATINGMECHANISMS seldom are these cases, hybridization may become the Gilded Flicker (C. chrysoides)are perfect between closely related spe- more frequent and systematistsmay now considered to be the same species, and the breakdown of isolating consider"lumping," consistentwith the cies-the Common Flicker (C. auratus). mechanisms results in hybridization. biologicalspecies concept. However, in Again, widespread interbreeding by Hybridization was defined by Mayr numerous cases, hybridization is occa- overlapping populations indicated that (1970:69) as "the crossingof individuals sional or stable, and does not threaten classification as separate specieswas an belongingto two unlike populationsthat speciesstatus of the respectivepopula- error (Short 1954). The three popula- have secondarily come into contact." tions. Numerous other accountsof hy- tions are now consideredsubspecies Unlike populations usually refer to bridization are discussedby Short A third example of "lumping" re- populations that are separated by dis- (1969). A full reviewof avian hybridiza- volves the Tufted Titmouse (Parus crete, contrastingcharacters such as col- tion is beyond the limits of this manu- bicolor) and the Black-crestedTitmouse or pattern, and are separatespecies. Hy- script, and the following list of selected (P. atricristatus).Head markingsare the bridization occurscommonly; Mayr and referencesof reportedavian hybridiza- chief differences between the two forms Short (1970) noted that 10 percent ("at tion is certainly incomplete: Dixon (Dixon 1954). "The evidence suggests least 52") of North American nonma- (1955), Sibley(1957), Johnsgard(1960), that these forms diverged from a com- rine avian specieshave been reported to Selander (1964), Smith (1966), Szijj mon ancestor, but that the morphologi- hybridize. Mayr (1970) was careful to (1966), Gurr (1967), Short (1969), In- cal changes which developed were not point out the "erroneous" notion golfsson(1970), Mayr and Short(1970), accompanied by the evolution of amongmany naturaliststhat hybridsare Patten and Weisbrod (1974), and Jehl mechanisms which would ensure repro- always "sterile mules." and Bond (1975). ductive isolation. Since free inter-

Volume34, Number 6 863 breeding between Black-crested and of two or more genetically different eye, bill color, and flank color. The Tufted titmice occurs, the suggestionis classesin the sameinterbreeding popula- Western Grebe has been classified as a made that they be consideredconspeci- tion." The geneticsof polymorphism polymorphic species(Mayr and Short fic" (Dixon 1954:190). In 1976 this sug- will not be discussedhere, but are well 1965). However, three years of recent gestionwas adopted and both forms are presentedin moststandard genetics texts field study (Ratti 1979) have shownthat now considered to be the Tufted Tit- (Srb et al. 1965, Levine 1969, Gardner sympatric populations of dark- and mouse(P. bicolor). 1975). The objective here is to note how light-phaseWestern Grebesrarely inter- Each of the above errors was due to polymorphismis diagnosedin an avian breed. Surveysof mated pairs in 1975, earlier classifications based on mor- population and to provide some ex- 1976, and 1977 from California, Ore- phology in the absenceof' information amples. Studies of polymorphism in gon, and Utah revealed577 dark x dark on interbreeding. The morphological birds frequently deal with phenotypic pairs, 432 light x light pairs, and only 5 differences were considered to reflect polymorphism, or what Mayr (1970:89) dark x light hybrid pairs. Thesedata •n- reproductiveisolation and the presence defined as "the occurrence of several dicate that dark- and light-phase of effective isolating mechanisms.Simi- strikingly different discontinuousphe- Western Grebes are separatebiological lar errors, based on the same morpho- notypes within a single interbreeding species. logical approach, have been disclosed population." One well-known example In conclusion, many avian species resultingin "splitting" of severalspecies of polymorphism is the red-phaseand have been "lumped" or "split" because into two separate species.An excellent grey-phase Screech Owl (Otus asio). recent field studieshave providedsuffi- example is the Boat-tailed Grackle and Mayr (1963) and Traylor (1966) reported cient information to disclose errors •n the Great-tailed Grackle. Prior to the that polymorphismis best demonstrated classification. Future research will cer- 1973 changes,the Great-tailed Grackle by random interbreedingand by both tainly generateadditional changes,and was consideredto be a subspeciesof the color types occurringin a singlenest. this knowledgeshould be welcomed,for Boat-tailed Grackle. "These two Among recent changes in classifica- it furthers our understandingof awan gracklesare so similar morphologically tion are two speciesthat were lumped evolution. that museum systematistshave generally when polymorphismwas demonstrated. acceptedwithout questiontheir designa- The Great White Heron is now consid- ACKNOWLEDGMENTS tion as subspecies"(Selander and Giller ered conspecific with the Great Blue 1961:29). However, study of a 100-mile- Heron (Ardea herodias). This change Sincerethanks to the followingpeople wide zone of sympatryshowed that they was made after Meyerriecks (1957) re- who providedhelpful criticismand sug- failed to interbreed and are separate ported interbreedingby the heronsand gestions on various portions of the species. both color types occurring in the same manuscript: D. Amadon, K. Dixon, S. Species such as the Boat-tailed and nest. Hubbard, R. Linder, J. Kadlec, T Modde, L. Ratti, G. Sloane,L. Smith, Great-tailed grackle are called sibling One of the best-known cases of a col- species.Sibling speciesare populations L. Wells, and J. Wentz. or phase of a polymorphic speciesmas- that are morphologicallyvery similar, or querading as a separate speciesis the identical, yet are reproductivelyisolated. APPENDIX blue phase of the Snow Goose (Chen Sibling speciesare often sympatric, and caerulescens).Blue and snow phasesof The following selectedterms and defini- because they are nearly indistinguish- the Lesser Snow Goose were considered able, they go unrecognizedas separate tions are from the glossaryin Mayr to be separatespecies prior to a studyby biological species. Mayr (1970:23) (1970:413). Cooch (1961). The two color phases acknowledgedthe importance of sibling were found to readily interbreed and speciesfor they permit "us to test the mixed color. phase broods were ob- ALLOPATRIC. Of populationsor spe- vahdity of the biologicalversus the mor- served. Cooke and Cooch (1968) have cies, occupyingmutually exclusive phological species concept." Five studied the geneticsof this polymor- (but usually adjacent) geographical speciesof flycatchersof the genusEm- phismand reportedthe color phasesrep- areas. ptdonax are classifiedas sibling species resent a single pair of alleles, the blue ALLOPATRIC SPECIATION. Geo- in North America. The speciesare only phase being BB or Bb and the snow graphicspeciation. recognizedin the field with certainty by phasebeing bb. Other casesof polymor- BIOLOGICAL SPECIES CONCEPT. their song, and the song is consideredto phism in birds were reportedby Cooke A concept of the speciescategory be the primary isolatingmechanism and and Ryder (1971), Johnson and Brush stressingreproductive isolation and means of the speciesrecognition (Stein (1972), and Bengstonand Owen (1973); the possessionof a geneticprogram 1963). In 1973, the Traill's Flycatcher Mayr (1970) noted that over 100 cases effecting suchisolation. (Empidonax traillit) was reclassifiedas are known of morphs originally con- CONSPECIFIC. Individualsor popula- two sibling species populations; the sideredseparate species. tions of the samespecies. Willow Flycatcher(E. trail!it) having the Although numerouscases of polymor- ETHOLOGICAL. Behavioral, partic- vocalization "fitz-bew," and the Alder phism were unrecognized for many ularly with reference to species- Flycatcher (E. alnorum) having the years, some speciesmay have been pre- specificcomponents of behavior,the vocalization "fee-bee-o." maturely classified as polymorphic. phenotypic expressionof which is Another phenomenon causing Dark- and light-phase Western Grebes largely determinedgenetically. changesin the classificationof avian (Aechrnophorusoccidentalis) have been ETHOLOGICAL BARRIERS. Isolat- speciesis polymorphism.Gardner (1975) describedby Storer (1965) with the main ing mechanismscaused by behavioral defined polymorphism as "the existence differencesbeing color pattern near the incompatibilitiesof potentialmates.

864 American Btrds, November 1980 F 1. Firstfilial generation. tions. blue-snowgoose complex. Auk 78:72-89. FOUNDER PRINCIPLE. The principle SPECIES RECOGNITION. The ex- COOKE, F. and F.G. COOCH. 1968. The that the founders of a new colony (or genetics of polymorphism in the goose change of appropriate (species- Anser caerulescens. Evolutton population) contain only a small specific) stimuli and responsesbe- 22:289-300. fraction of the total geneticvariation tweenindividuals (particularly during and J.P. RYDER 1971.The geneticsof of the parental population (or courtship). polymorphism in the Ross' goose(Anser species). SUBSPECIES. An aggregate of local rossit). Evolution 25:483-496. GAMETES. Functional germ cells (= popu!ationsof a speciesinhabiting a CRACRAFT, J. 1973. Continental dr•ft, eggsand spermatozoa). geographicsubdivision of the range paleoclimatology,and the evolution and GEOGRAPHIC BARRIER. Any ter- of the species and differing tax- biogeography of birds. J. Zool. Lond rain that preventsgene flow between onomically from other populations 169:455-545. CROIZAT, L., G. NELSON, and D.E populations. of the species. ROSEN. 1974. Centers of origin and GEOGRAPHIC SPECIATION. The SUPERSPECIES. A monophyletic related concepts.Syst. Zool. 23:265-287 acquisitionin a population--while it group of entirely or essentially DIXON, K.L. 1955. An ecologicalanalys•s of is geographicallyisolated from other allopatric speciesthat are either mor- the interbreeding of crested titmice •n populationsof its parental species-- phologically too different to be in- Texas. Univ. Calif. Publ. Zool. 54:125-197. of characters that promote or cluded in a single speciesor demon- DOBZHANSKY, Th. 1937. Genetics and the guarantee reproductive isolation strate their reproductive isolation in a origin of species.Columbia Univ. Press after the external barriers break zone of contact. New York. 364 pp. down. SYMPATRY. The occurrence of two or FORD, J. and S.A. PARKER. 1973. A sec- HYBRIDIZATION. The crossingof in- cond species of wedgebill? Emu more populations in the same area; 73:113-118. dividuals belonging to two unlike more precisely, the existence of a GARDNER, E.J. 1975. Principles of ge- natural populations that have secon- population in breeding condition netics. John Wiley & Sons, Inc., New darily come into contact. within the cruising range of individ- York. 622 pp. IMPRINTING. A process of rapid uals of another population. GILL, F.B. and B.G. MURRAY, JR. 1972 learning of highly specific informa- Discrimination behavior and hybridiza- ZYGOTE. A fertilized egg; the cell tion of the blue-winged and golden- tion (like the parent image) during a (individual) that resultsfrom the fer- winged warblers. Evolution 26:282-293. critical period in the life cycle. tilization of an egg cell. GURR, L. 1967. Interbreeding of Larus ISOLATING MECHANISMS. Proper- novaehollandiae scopulinus and Larus bulleri in the wild in New Zealand. Ibis ties of individuals that prevent suc- LITERATURE CITED 190:552-555. cessfulinterbreeding with individuals HEUSMANN, W. 1974. Mallard-black duck that belongto different populations. AMADON, D. 1966. The superspeciescon- relationshipsin the northeast. Wildl Soc. cept. Syst. Zool. 15:245-249. Bull. 2:171-177. MECHANICAL ISOLATION. Repro- AMERICAN ORNITHOLOGISTS' UNION HINDE, R.A. 1959. Behavior and spec•atmn ductiveisolation owing to mechanical COMMITTEE. 1973. Thirty-secondsup- in birds and lower vertebrates. Biol. Rev incompatibility of male and female plement to the American Ornithologists' 34:85-128. genitalicstructures. Union check-list of North American HINE, R.L. and C. SCHOENFELD (Eds) birds. Auk 90:411-419. MORPHOLOGY. The descriptionand 1968. Canada goose management. Dem- AMERICAN ORNITHOLOGISTS' UNION bar Educational Research Serwces, study of structural characteristics, COMMITTEE. 1976. Thirty-third sup- Madison, Wisconsin. 195 pp. particularlythose on the surfaceof plement to the American Ornithologists' HUBBARD, J.P. 1969. The relationshipand the body. Union check-list of North American evolution of the Dendroica coronata com- birds. Auk 93:875-879. PHENOTYPE. The totality of charac- plex. Auk 86:393-432. ARBIB, R. 1973. Hail, great-tailed grackle! IMMELMANN, K. 1975a. Ecological sig- teristics of an individual (its ap- Baltimore oriole, farewelll Audubon nificance of imprinting and early learn- pearance)as a result of the interac- Magazine, 75(6): 36-39. ing. Annu. Rev. EcoL Syst. 6:15-37 tion betweengenotype and environ- BEACH, F.A. and J. JAMES. 1954. Effects __ 1975b. The evolutionary significanceof ment. of early experiencein the behavior of early experience. Pages 15-17 in G POLYMORPHISM. The simultaneous animals.Psychol. Bull. 51:239-263. Baerends, C. Berr, and A. Manning, eds BELLROSE, F.C. 1976. 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The splitting of a phy- JOHNSGARD, P.A. 1960. Hybridizatmn •n ductiverelationships of black-cappedand the Anatidae and its taxonomic imphca- letic line; the processof the multipli- Carolina chickadees. Auk 80:9-47. tions. Condor 62:25-33. cation of species; the origin of BROWN, R.G. 1967. Speciesisolation be, JOHNSON, N.K. and A.H. BRUSH. 1972 discontinuitiesbetween populations tween the herring gull Larus argentatus Analysis of polymorphism in the sooty- caused by the development of and lesserblack-backed gull L. fuscus. capped bush tanager. Syst. Zool Ibis 109:310-317. 21:245-262. reproductiveisolating mechanisms. BUSH, G.L. 1975.Modes of animal specia- LACK, D. 1944. Ecological aspects of SPECIES. A reproductively isolated tion. Ann. Rev. Ecol. Syst.6:339-364. species-formationin passefinebirds Ibis aggregate of interbreeding popula- COOCH, G. 1961. Biologicalaspects of the 86:260-286.

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