ELEVATIONAL CORRELATES OF SPECIATION AND INTRASPECIFIC GEOGRAPHIC VARIATION IN PLUMAGE IN ANDEAN FOREST BIRDS GARY R. GRAVES • Departmentof BiologicalScience, Florida State University, Tallahassee, Florida 32306 USA ASSTRACT.--Intraspecificvariation in plumage was used to test the null hypothesesthat geographicvariation in 280 speciesof elevationallyrestricted Andean forestbirds is inde- pendent of elevation and is not a function of patchy geographicdistribution. Both null hypotheseswere rejected. At most taxonomiclevels, geographicvariation in plumage was correlatedpositively with both the mean of its elevationaldistribution and the size of its geographicrange. Vertical amplitude of elevational distribution was not a significantpredictor of geographicvariation in plumage in most taxa. Independent of these elevational correlates,patchily distributed speciesshowed significantly more geographicvariation than continuouslydistributed species. Theseresults show that geographicvariation and presumablyongoing speciation phenom- ena are greaterat higher elevations.The decreasedspecies richness at high elevationsmay be attributable to a higher rate of extinction from catastrophicdisturbance as well as to ecologicalfactors that limit sympatryin newly formed species.Received 6 August1984, ac- cepted26 December1984. IN this paper I examine the relationship be- of potential new species. Second, there are tween elevational distribution and possible adaptivepeaks; the morenumerous these peaks, speciationphenomena in Andean forestbirds. the greaterthe numberof potentialnew species. Two initial observationsare pertinent. First, on Predictions--(1)The frequencyof fragmented an elevationalgradient in Peru, Terborgh(1977) populations and incipient speciation increases found a negativecorrelation between elevation with elevation. (2) Intraspecific geographic and bird speciesrichness, canopy structure, and variation increases with elevation. (3) Extinc- number of plant strata. Second, geographic tion ratesof isolatedpopulations are greater at barriersto dispersaland gene flow increasewith higher elevations.(4) The range of speciesmor- elevation. Catastrophic vicariant events (e.g. phologiesand the diversity of foragingbehav- glaciation,landslides, vulcanism, forest frag- ior within ecological assemblagesdecreases mentationby climatic events)are more preva- with increasing elevation in correspondence lent in the physiographicallycomplex Andean with the decrease in resources and habitat com- highlands than in the adjacent foothills and plexity. Amazonian lowlands. I investigatedthe first two predictionsby ex- I proposea simple model of speciation(see amining geographicvariation in plumage char- Mayr 1963,Pielou 1979)that incorporatesthese actersin Andean birds. I began with two basic observations,predicts a pattern of geographic assumptions:bird speciationis largely allopat- variation correlated with elevation, and ac- ric, and plumage differentiation is related to countsfor the decreasein speciesrichness with speciation. I tested the null hypothesis that elevation. Two factors control the number of geographicvariation is independent of eleva- potential speciesalong the elevational gradi- tion and a subsidiary hypothesis that geo- ent. First, parent speciesare fragmentedby vi- graphic variation is not a function of patchy carlant events into a number of mutually iso- geographicdistribution. lated demes. The more fine-grained the fragmentationpattern, the greaterthe number STUDY AREA AND METHODS Studyarea.--Humid Andean forest extendsnearly uninterrupted from Venezuela southward along the • Present address: Division of Birds, National Mu- easternslope of the Andesto centralBolivia. My study seum of Natural History, SmithsonianInstitution, area included the portion of the easternslope of these Washington, D.C. 20560 USA. mountains from the Rio Marafi6n in northern Peru 556 The Auk 102:556-579. July 1985 July1985] SpeciationinAndean Birds 557 south to the Bolivian border (Fig. 1). This region was chosenbecause of the relativehomogeneity and even distribution of humid Andean forests (ONERN 1976); the linear distribution of Andean forest bordered by pdramoand punaon the west and lowland rain forest on the east, which facilitated mapping geographic ranges and locating contact zones and gaps in the distribution of montane bird species;and the avail- ability of specimensfrom a seriesof mostly unpub- lished post-1965 expeditions [Louisiana State Uni- versity Museum of Zoology (LSUMZ), Princeton University (specimensdeposited in the American Museumof Natural History, AMNH), and the Field Museum of Natural History (FMNH)] to the eastern slopeof the PeruvianAndes. Although the study area spansca. 10ø latitude, there is little regional differ- ence in forest physiognomycorrelated with latitude. Exceptfor outlying spursof the EasternCordillera, the undulating ribbon of humid Andean forest is backedby high-elevation pdramoor puna.The entire Fig. 1. Distribution of middle- to high-elevation elevational slope measured from the Amazonian humid Andean forest (ca. 1,200-3,400 m) along the lowlands (<500 m elevation) to timberline is rarely easternslope of the PeruvianAndes (adaptedfrom more than 30-50 km. The area and quality of pres- ONERN 1976). Note the deeply dissectedcontours ent-day montane forest at any contour interval is associatedwith river canyonsand timberline. Forest unknown becauseof heavy cloud cover and inacces- on the lower slopes(600-1,200 m) is continuousand sibility. Large-scalemaps indicate that the area more evenly distributed. between the 500-m and 1,500-mcontour lines is per- haps twice as large as the area in the 1,500-m to 4,000-m contour interval. Humid Andean forest above and genera suggestsa long occupancyin the region 1,500 m elevation often is restricted to narrow cor- and an autochthonousorigin of the Andean forest ridors or is patchy at the heads of several deeply avifauna.Species residing in other habitatshave dif- convoluted,dry intermontanevalleys (e.g. upper Rio ferent evolutionary histories(Haffer 1969, 1974). For Huallaga, upper Rio Apurimac, Rio Huari Huari). this reason,species not restricted to humid Andean Humid forest of the Andean foothills (600-1,200 m forest are excludedhere. Examplesof excluded hab- elevation) is continuouslydistributed. Precipitation itats and speciesare: (1) puna-pdramograssland (e.g. data from Andean forest in Peru are incomplete,but Asthenesfiammulata, Phrygilus unico!or); (2) Polylepis annual precipitationranges from 2 to 16 m (ONERN woodlands above timberline (e.g. Oreomanesfraseri, 1976, Simpson and Haffer 1978). A distinct wet sea- Xenodacnisparina); (3) intermontane deciduousforest son occursfrom November to May, but rainlesspe- (e.g. Pachyramphusalbogriseus, Tangara viridicollis); (4) riods of more than a few days are rare year-round. montane streams(e.g. Cinclusleucocephalus); (5) agri- Four distinct vegetation zones (lowland rain forest, cultural areasand scrub (e.g. Troglodytesaedon); and montane rain forest, cloud forest, and elfin forest), (6) lowland forest (primarily <500 m elevation;e.g. usually are present along the continuousphysical Piaya cayana). gradientfrom the Amazonian lowlands to timberline I alsoexcluded several species recorded from only (see Terborgh 1971). The term "Andean forest" (ca. one transect block (see Geographic range), repre- 600-3,500m elevation)refers collectively to montane sentedby insufficientspecimen material (e.g. Accip- rain forest, cloud forest, and elfin forest (sensuTer- iter collaris,Gallinago imperialis, Aegolius harrisii), or tax- borgh 1971). Excellent descriptionsof the humid for- onomically problematic (Scytalopus,Elaenia). The est of the Peruvian Andes can be found elsewhere remaining 280 speciesand superspeciesoccurring in (Tosi 1960; Terborgh 1971, 1977; Terborgh and Dud- the studyarea and includedin the analysesare listed ley 1973;Terborgh and Weske 1975;ONERN 1976). in the Appendix. The compositionof families follows Specieslist.--Of the 1,678species recorded from Peru Morony et al. (1975). (Parkeret al. 1982),about 320 exclusivelyinhabit An- Geographicrange.--To facilitate the measurementof dean forest on the Amazonian side of the continental geographicrange, the studyarea was partitioned into divide. The habitatfidelity of this heterogeneousas- 15 blocks (Fig. 2). This was an attempt to reduce the semblage(30 families)is supportedby literally thou- effectsof coarsesampling (Pielou 1979) without sac- sandsof observationsspanning 70 yr (e.g. Chapman rificingaccuracy by excessivesubdivision of the study 1917, 1926; Weske 1972). Although fossil evidence is area. Each block was delineated to include at least not yet available,the large number of endemicspecies one major collecting locale (>250 specimens), and 558 GARYR. GRAVES [Auk, Vol. 102 A B GEOGRAPHICRANGE C'D 200 km o 2 ;5 4 5 6 ? 8 9 I0 II 12 I;5 14 15 NUMBER OF BLOCKS Fig. 3. Histogram of geographic range values for all species(n = 280). Speciesoccurring in only one H J block were omitted. I M studyarea (Fig. 3). This resultsfrom estimatingrange from a segmentof the Andes that restrictsthe upper value to 15 (equivalent to 15 or more) transectblocks. Geographicrange values indicate only the number Fig. 2. Division of the study area into 15 transect blocks. of blocksin the study area in which a speciesis be- lieved to occur.Range 15 valuesimply that a species is found throughoutthe study area;values less than 15 can have continuous or discontinuous distribu- representativecollecting