INTRA-ISLAND THE VARIATION MASCARENE ZOSTEROPS BORBONICA FRANK ORNITHOLOGICAL WHITE-EYE B GILL MONOGRAPHS PUBLISHED THE AMERICAN NO 12 BY ORNITHOLOGISTS' UNION IN INTRA-ISLAND THE VARIATION MASCARENE IN WHITE-EYE ZOSTEROPS BORBONICA BY FRANK ORNITHOLOGICAL B GILL MONOGRAPHS PUBLISHED THE AMERICAN NO BY ORNITHOLOGISTS' UNION 12 •,A.L k Color forms of Zosterops borbonica on Reunion Island (top to bottom): gray morph; highland brown-headed brown morph; lowland brownheaded brown morph; gray-headed brown morph ORNITHOLOGICAL MONOGRAPHS This series,publishedby the American Ornithologists' Union, has been established for major paperstoo long for inclusionin the Union's journal, The Auk Publicationhas been made possiblethroughthe generosityof Mrs Carll Tucker and the Marcia Brady Tucker Foundation,Inc Correspondence concerningmanuscriptsfor publicationin the series shouldbe addressedto the incomingEditor, Dr John W Hardy, Moore Laboratoryof Zoology,OccidentalCollege,Los Angeles,California 90041 Copiesof Ornithological Monographsmay be orderedfrom the Treasurer of the AOU, Burt L Monroe, Jr., Box 23447, Anchorage,Kentucky40223 (See price list on insideback cover.) OrnithologicalMonographs,No 12, vi + 66 pp Editor, Robert M Mengel SpecialEditor for OrnithologicalMonographsNo 12, Marion Anne Jenkinson Issued May 4, 1973 Price $2.00 prepaid ($1.60 to AOU Members) Library of CongressCatalogueCard Number 73-78162 Printedby the Allen Press,Inc., Lawrence,Kansas66044 CONTENTS ACKNOWLEDGMENTS INTRODUCTION REUNION ISLAND vi 1 FIELD STUDIES • BIOLOGY OF ZOSTEROPS BORBONICA COLOR V•U•L•T•ON IN ZOSr•ROeS Spec•en exm•ation sORSOWICA 12 12 Basis of the color variation Back coloration 12 14 Head colorationin brown morphs 21 Underart 30 MtNS•L coloration V•T•ON S•c•en 39 measurements 39 Statistics •alysis DmCUSS•ON 40 41 44 V•iafion in cont•ental white-eyes 44 T•onomy of Zosterops borbonica 48 Relation of Zosterops borbonica mauritiana to •e Re•ion Isl•d forms 49 Evolutiona• history of Zosterops borbonica 49 Ch•acter variation and adaptation Character divergence • natural populations SUMM•Y L•Ts• •so Arrs•g I ArrsNDg II 51 52 56 59 62 65 ACKNOWLEDGMENTS This studywas made possibleprimarily throughthe cooperationof the governmentand citizensof France,Departmentde la R•union In particular, I am gratefulto V Robin,DirecteurdesAffairsG•n•rales,for handlingthe many administrativeformalitieswith maximum dispatch,and to Armand Barau, ConseilerG•n•ral de la R•union, Harry Gruchet, Conservateurdu Museum d'I-IistoireNaturelie de Saint Denis, and ChristianJouaninof the MuseumNational d'HistoireNaturelie in Paris, who were a sourceof advice, encouragement, and assistance.Several private landownerson Reunion Island, includingMessrs.A Barau (Bols Rouge), G Barau (Beaufonds, Ste.Marie), I Boyer (La Possession), P Lougnon(La PetiteFrance), J de Villineuve (Grand Fond), and the Banquede la R6union,permittedme to studyand collectwhite-eyeson their properties.The frequentcooperation of the Servicedes Eaux et For•ts de la R•union, and in particularMessrs Moulin, Miguet, and Soroquereis also gratefully acknowledged.Messrs Malick and Laidet of the Service M•t•orologique de la R•nnion placed climatological data from R6unionat my disposal,and M ThereseanCadet generously providedmostof the plant identifications mentionedin this study In Ann Arbor, Michigan,the membersof my doctoralcommittee,Morris Foster,Robert W Storer,HarrisonB Tordoff, and Warren H Wagner,providedmany a stimulatingsuggestion.I am indebtedalso to R B Bartels of the Universityof MichiganComputingCenterfor making availablethose facilitiesandto William Lnnk who paintedthe colorillustration I have benefitted from discussions with J Alan Feduccia, Theodore H Fleming, John P Hubbard, William C Preston,and Donald R Tinkle Acknowledgment and thanksare due especiallyto my wife, Frances,for her many contributions to this study This studywas supportedby a National ScienceFoundationPredoctoral Fellowshipin 1967 and 1968 and a National ScienceFoundationGrant (GB 3366) to T H Hubbellat The Universityof Michiganfor researchin Systematic and EvolutionaryBiology vi INTRODUCTION Geographicvariationreflectsthe geneticdivergenceof conspecificpopulationsthroughnatural selection;it therebyservesas primary evidenceof the evolutionaryprocess.Althoughevery local populationdiffers from adjacent populations with respectto the frequencyof somecharacteristics, conspicuous phenotypicdifferentiationon a microgeographic scale is evidentprimarily in terrestrialand relativelysedentaryanimal groups Geographicvariation in highly mobile organismssuch as birds, however, tends to involve great distanceso.relseconspicuous isolation The characteristicuniformityof most localbird populations seemsto reflectgeneticunitythat is the combinedresult of gene flow betweenadjacentdemesand the resistanceof coadaptedgene poolsto fragmentation by disruptiveselection(Mayr, 1963:296, 361) Yet, the preciseness of avian adaptationto climaticgradients(James, 1970) and the surprisingrapidityof populationcharacterdivergence in Passerdomesticus (Johnstonand Selander,1964) continueto emphasizethe overridingimportanceof natural selectionas the primary determinantof patterns of geographicvariation A birdpopulationon a smalloceanicislandischaracteristically homogeneous in color and size Althoughinter-islanddifferentiationis common,intra-island variation is exceptional Until the discoveryof four apparent races of a white-eye,Zosteropsborbonica,on Reunion Island (Storer and Gill, 1966), Jamaicawas the smallestisland (4,540 squaremiles) known to have geographicallyseparatedbird populationssufficientlydistinct to be considered subspecies ReunionIslandis only about1,000 squaremilesin area No other islandwith an area of lessthan 10,000 squaremilesis known to have a polytypic speciesin its avifauna On the other hand, many larger islandshave differentiatedbird populations,the number of which tends to increasewith island size But even on islandsas large as Madagascar(240,000 square miles) and Borneo (290,000 squaremiles), only one or two specieshave as many as four races Thus island size seemsto impose some constraintson geographic variation This studyexaminesthe patternsof phenotypicvariation in Zosteropsborbonicaon Reunion Island and considerstheir evolutionary origin and maintenance REUNION ISLAND Reunion Island is one of the MascareneIslands,a group of three oceanic islandsof volcanicorigin in the westernIndian Ocean Reunion is situated approximately500 mileseastof Madagascar(Figure 1) at latitude21ø Off S andlongitude55 ø 30' E, is ellipticalin shape,39 mileslong by 29 mileswide, and encompasses about 1,000 squaremiles It is both the largestof the three MascareneIslands and the highest,reachingan elevationof 10,068 feet ORNITHOLOGICAL MONOGRAPHS NO 12 Mauritius -20 $ R•union -25 $ INDIAN FretroE Location of the Mascarene OCEAN islands of Reunion and Mauritius in the western Indian Ocean The third Mascarene island, Rodriguez, is located 250 miles to the east Reunion'sfaunalrelationships are with Madagascarand the otherislandsin the westernIndian Ocean The islandwas colonizedprimarilyfrom Madagascar(Moreau, 1957:399) although.,judgingfrom the similarityof their faunas,irtterchange betweenMauriflusandReunionislandsmusthaveoccurred quitefrequently.At least8 speciesof birdsbecameextinotshortlyafter man's arrivalon Reunionin 1663 Todaythe land bird avifaunaincludes11 indigenous and 16 introducedspecies.Discussions of thesespeciesare available in Milon (1951), Berlioz (1946), and Watsonet al (1963) Topographically ReunionIslandis an extremelyruggedisland,risingsteeply 1973 GILL: VARIATION IN ZOSTEROPS BORBONICA ALTITUDE PIT GRA ST N D N NEIGES ST LEUI BENOIT FIGURE Cross-section of Reunion Island Original vegetation above St Leu as follows (from sea level): savanna,evergreen forest, tamarin forest, heath from the seawith little roomfor co.astal plains(Figures2 and 3) It is composedof two overlappingshieldvolcanos(Upton and Wadsworth,1966:3): Piton de la Fournaise(also called le Volcan; 8,342 feet), an active volcano forming the southeasternthird of the island, and Piton des Neiges (10,068 feet), an extinct volcano in the northwest The latter, as a result of "extremedevelopment of amphitheatre-headed valleyerosion"(Upton and Wadsworth,1966:5), is dissected up to depthsof 2,500 metersby deepgorges and threehugebasin-like"cirques." The youngestlavaseruptedfrom Piton des Neigesbetween100,000 and 350,000 years ago in the late Pleistocene (Chamalaunand McDougall, 1966) The locationof ReunionIslandat the southernedgeof the tropicsensures a rather stable,mild climatewhichis dividedinto a warm rainy seasonfrom Novemberto April, and a cool dry seasonfrom May to October Midsummerdaysaveragetwo and one-halfhourslongerthan winter days and five to six degrees centigrade warmer Averagemonthlyrainfallon the windward sideof the islandis about 100 cm higherin the wettestmonth, March, than in the driestmonth,August The differenceon the island'sdry sideis about 15-20 cm ReunionIsland'sruggedrelief promotesmarkedlocal variationin temperature and rainfall (Figure 4) The averagerainfall on the west coast,which i.sin a rain shadow,is lessthan 100 cm a year, whereason the easternwindward slopesit reaches800 cm a year Temperaturedecreasesabout 7øC with each1,000 metersaltitude,or about2øC per 1,000 feet Highlandsover 2,000 metersare 14ø to 16ø colderthanthe coast,wheretemperatures average about 22øC in the summer Rainfall data and temperaturerecordsin the form of ten-yearsummaries for 112 and 30 Reunionlocalities,respectively, were made availableby the ORNITHOLOGICAL MONOGRAPHS NO 12 ST DENIS I Pos ?eBr•l• :hicots ST PAUL ST.BENOIT • CIRQUE Ja Petite • France • DE SALAZIE Piton • des Neig,• ROSE ForGt du BGbour For•t DE Mourouvin Piaine des Cartes ST TSvelave Blanc LE Etarig Sal•_•_ les Bains •,• ST LOUIS liv St Etienne ST PI ,o s, i? kilometers PHI L I P PE ST JOSEPH FIOURE Reunion Island localities ServiceM6t6orologiquede la R6union For a few additional localities for whichrecordshave beenkept only a few years,I computedaveragesfrom the annual "BulletinsClimatologiques"pubh'shedby the same service Many of my collectinglocalitieswere sufficientlyfar from an actualmeteorological station that I usedrainfall valuesfrom isohyeticalchartsbasedon the ten-year summaries andcalculatedtemperatures regressed from existingaltitudinalcorrelations.Two temperatures have beenusedin this studyfor each locality: the mean maximum of the warmest month of the year (either January or February) and the meanminimumof the coldestmonth of the year (usually August) Altitudeswerefixed to the nearest20 meterseitherfrom existing altitude markers or from a 1:50,000 topographicalmap publishedby the MinistbredesTravaux Publicset desTransports(Institut GeographiqueNational) of France Corresponding to variationin localclimatesis a diversityof habitats.The indigenousvegetationis describedby Rivals (1952) and its distributionon the islandbefore the arrival of man is illustratedin Figures2 and The 1973 GILL: VARIATION IN ZOSTEROPS BORBON1CA 53 Furthermore,the importanceof geographicisolation,or disruptionof the continuityof populations,seemsundeniableas a factorpromotingevolutionary divergence(Mayr, 1970:296-330) However, the probability and rate of geneticdivergencedependsalsoon the magnitudeof the selectioncoefficients in the differentenvironments.The relationshipbetweenthesetwo factors must be examined to ascertain the basis of differences or the lack thereof betweenpopulations Direct measuresof selectioncoefficientsin natural populations,basedon temporal fluctuationsin the proportionsof genotypes(Clarke and Murray, 1962; Gershenson, 1945; Merrell and Rodell, 1968), relativeviability (Ford, 1964:50, 62; SheppardandCook, 1962; Fisher,1939), or differentialcapture by predators(Kettlewell, 1961a, 1961b), are availablefor only a few well studiedpopulationsof moths, butterflies,snails,and small mammals The selectioncoefficients indicatedby thesestudiesrangefrom to as high a.s90 per centrelativeadvantageof one genotypeover another In two studiesthe selectioncoefficientsrequiredto offsetthe effectsof dispersalin natural casesof clinal variation have been computed;the computed selectioncoefficients were very low 0.1 per cent in Peromyscus pMionotus (Haldane, 1948:284) and 004 per cent in Amathesglareoxa(Kettlewell and Berry, 1961) andwerewell belowthe actualintensitiesof selectionthought to be operating The mathematicalrelationshipsbetween natural selection and dispersal (= gene flow) and the distancesover which these two forces interact to produceclinal variation have been treated by Haldane (1948) and Fisher (1950) for simplegeneticsystems.Haldane'smethodassumesthe following: 1) the specieslivesin an areawhichis plane and infinite, i.e., it must be large enoughthat regionsexist where there is no polymorphism;2) the density is equal throughoutthe area; 3) the animalsdisperseat random; 4) they have one annual generation; 5) mating is at random betweenthe different types; 6) the populationis in equilibrium; 7) an autosomaldominantand its allelomorphunderlie the polymorphism;and 8) the plane is sharply dividedby a straightboundaryinto two halves Assumptions1 thru are acceptablewithoutmajor violationfor Zosterops borbonica Assumption5 may not be completelyvalid, however The presence of helpersandcommunalfeedingof youngin the nestmightbe taken as indirect evidenceof inbreeding,as such behavior would be selectively advantageous to the participatingindividualsif the parentsand helperswere relatedgenetically(Lack, 1968:80) Allochronicdifferencesin the onsetof breedingmay reducealtitudinalgene flow even further and reinforcethe geographicisolation between lowland populations Finally, any tendency toward differential habitat selection, for which there is some evidence (see p 17), will alsoreducegeneflow 54 ORNITHOLOGICAL MONOGRAPHS NO 12 The underlyinggeneticbasesof the polymorphismin this white-eye (Assumption7) arenot clear However,othersimilarcasesof colorpolymorphism in birds (Cooke and Cooch, 1968:299; Munro et al., 1968; Hrubant, 1955: 229) appearto be controlledby two alleleswith one being dominantand with modifiersbeingresponsible for the intermediateplumagetypes The requirementof a sharpboundary(Assumption8) is violatedby our situation However,Haldane (1948:284) recognizes that in manycasesenvironmental conditions changegraduallyandhe thinksthat in thesecasesthe computed selectioncoefficientshouldat leastindicatethe order of magnitudeof selection neededto maintain a cline, i.e., whether selectiveintensitiesof the order of 10 or 01 per cent are involved The measurements involvedin Haldane'sformula (1948:283 ) are the interquartiledistance(d), which is the linear distancebetweenthe two.localities at whichthe frequencies of oneof the phenotypes are 25 and 75 per cent,and the averagedispersaldistance(m) from hatchingsite to first breedingsite The intensityof selectionin the interquartileregionis then considered to be m2/2d There are no directmeasuresof dispersaldistancesfor Zosteropsborbonica Mean distancesof dispersalhave, however, been measuredfor severalocher bird species.The SongSparrow (Melospiza melodia) dispersesabout 400 meters (Johnston, 1961) The Wrentit (Chamaea fasciata), an inhabitant of densebrush and chaparral,might disperseabout 600 to 700 meters (Miller, 1947) The mean dispersaldistanceof the Great Tit (Parus major) is also about 600 meters (Kluijver, 1951: 14) I would estimate,therefore,that the meandispersaldistancein Zosteropsborbonicais about500 meters However, the highly social nature of borbonica'syear-roundactivities,includingthe apparentlack of territoriality,must promotethe formationof local and perhapsinbred populations In order to compensatefor this, as well as for the earlierstatedpossibleviolationsof Assumption5, I have consideredthat the effectivedispersaldistancemight be as little as 250 meters This seemslike an absoluteandprobablyexaggerated minimumpossibility for a highlymobile bird At the other extreme, I doubt that Zosteropsborbonicais much more mobile than someof the other speciesmentionedabove,and would set 1,000 metersas the upperlimit to its meandispersaldistance UsingHaldane'sformula,then,I haveestimatedthe interquartileselection coefficients for four of the five clinesin the ratio of brown and gray morphs whichI sampledon ReunionIsland Separatevalueswere computedassuming mean dispersaldistancesof 250, 500, and 1,000 meters (Table 12) The resultingselection coefficients rangefrom a low of 0.06 per centto a maximum oœ5.5 per cent These calculated selection coefficients are not intended to be actual measures of selectionon ReunionIsland,but they provideestimatesof the approxi- 1973 GILL: VARIATION IN ZOSTEROPS TABLE BORBONICA 55 12 INTENSITY OF SELECTION REQUIRED FOR MAINTENANCE OF CLINES IN THE RATIO OF GR•Y AND BROWN MORPHS 1N Zosterops borbonica Calculation Transect • A Locality number with 25 per cent gray morphs Locality number with 75 per cent gray morphs Distance (d) between the two localities (in km) Selection coefficient With m -250 meters With m -500 meters With m = 1,000 meters B C D 33 74 62 41 71-73 64 4 06 25 19 78 35 1.40 19 78 1.02 3.10 5.50 3.10 • A, St Benoit to Plaine des Carres; B, St Denis to Plaine des Chicots (locality is adjacent to but not actually on this transect); C, Petite France to Piton des Epinards; D, gtang Sa16 les Bains to Piton des Epinards (see Figure 11) •The selection coefficient (K) =m•/2d •, where m is the assumed mean dispersal distance and where d is the distance as defined above (after Haldane, 1948) Values indicated are per cent relative advantage of a morph on that part of the cline where it comprises more than half of the population mate minimummagnitudeof selectionthat seemsto be operating From them it is apparent.that a small selectiveadvantageis sufficientto maintain steepclinal variationin simplemorph or allelic frequenciesin a mobile small bird Studiesof natural populationsincreasinglyare revealingdemal structures and selectioncoefficientscapableof evolvingmarkedlocal populationdifferencesdespitehigh dispersalrates (Ehrlich and Raven, 1969) There are, of course,lower limits to the sizeof a geographical area within which a given speciescan differentiate,but theseare well below the actualrangesfor most species.Also, geneticmarkersrevealdifferences that are muchmore localized than are the differencesin external morphologywhich classicallyhave been usedto describegeographic variation It is importantto recognize,therefore, that geneflow per se (i.e., the resultingtendencytowardsgeneticsimilarity) has probablybeen overemphasized as a factor preventingthe divergenceof conspecificpopulations Rather, character uniformity over large areas probably reflects a generalizedphenotypethat adaptively compromisesa varietyof opposingselectiveforces Characteruniformitymay alsoreflecta species'inability to evolve locally adaptedpopulationsbecauseof genetic homeostasis(see Mayr, 1963:289) In strong contrast to the clinal situationsfound in the highland areas on ReunionIsland, in the lowlandscolor forms of Zosteropsborbonicachange abruptly acrossobviousgeographicalbarriers (river beds and a lava flow) 56 ORNITHOLOGICAL MONOGRAPHS NO 12 For example,the coas{alrangesof gray-headedand brown-headedbrown morphsare separatedby the gravelbedsof the Rivibredes Galets and the Rivibre St Etienne, but the transition between these two forms above 1,400 meterson the eastsideof ReunionIslandis steeplyclinalwithoutany apparent barrier In fact, all altitudinal transitions between color forms are clinal, whereas all coastal contacts involve a barrier Furthermore, the coastal transitionstake place in the absenceof conspicuous environmentalchange One might conclude,therefore,that the selectioncoefficientsaffectingthe altitudinaldistributionof genotypes are largeenoughto maintaingeographic differenceswithout the restrictionof gene flow, whereasthe selectioncoefficientsin the lowlandsare lower Geographictransitionsbetweengenotypes in the lowlands,therefore,require some restrictionof gene flow A delicatebalancebetweengeneflow and opposingselectionforcesmustbe involved Finally, in analyzingthe forcesaffectingthesecharacterdivergences,the nature of Reunion Island itself must be considered Few small islands are as high as ReunionIsland or containcomparablerangesof environmental extrem.eswithin their confines Furthermore, a tropical or subtropicallocation maximizesclimatic diversitybecausea very high island can includeboth tropical lowlandsand alpine mountain{ops Few small tropical islands,but several subtropicalislands,includingReunion, Hawaii, Maul, Bali, and Lombok, are that high Characterdivergencein birds on theseother islands shouldbe lookedfor The essentialabsenceof visualpredatorsfrom Reunion Island may alsohave beenan importantfactor in the evolutionof Zosterops borbonica,sincereleasefrom a need for protectivecolorationmay have increasedthe evolutionaryflexibilityof borbonica'splumagecoloration.Taken together these considerationssuggestthat the marked differentiation in Zosteropsborbonicaon ReunionIslandresultedfrom and was made possible by severalfactorswhich in themselvesare not unusualbut which are rarely found in combination in such a small area SUMMARY Zosteropsborbonica,a white-eyeendemicto the MascareneIslandsin the westernIndian Ocean,is characterized by complexpatternsof plumagecolor and size variation within the confinesof Reunion Island, a remote volcanic islandabout 1,000 squaremilesin area and 3,000 metershigh Z borbonica appearsto be the secondof the two indigenouswhite-eyesto colonizethis island and has lost the carotenoidpigmentationand white eye-ring characteristicof most of its relatives However,it is still a typicallysocialwhiteeyethat hasa generalized diet and preferencefor edgeand disturbedhabitats One aspectof the colorvariationin Z borbonicainvolvesthe presenceo.r absenceof phaeomelanins in the feather barbs of the back plumage,which 1973 GILL: VARIATION IN ZOSTEROPS BORBON1CA 57 produces brownand graycolormorphs,respectively.The offspringof mixed matings between morphswereobserved; the genetic basisof backcolorseems to involvea simplepair of alleleswith somemodifiers Thesetwo color forms are extensivelysympatric,but the ratio of the two varies clinally with altitude from 100 per cent brownmorphpopulations occurringin the lowlandsto predominately gray morphpopulationsoccurringin the highlands.Linear distances betweenlocalitiesat whichgraymorphscomposed 25 per centand 75 percentof thepopulation variedfromthreeto sevenkilometers.The minimum intensityof selectionrequiredto maintainsuchsteepaltitudinalclines in theproportions of the twomorphsis estimated to be on theorderof per centrelativeadvantage of onemorphoverthe other A secondaspectof the colorvariationinvolvesdifferencesin the head color of brownmorphsonly Threecategories of brownmorphheadcolorvariants canbe distinguished: an all gray-headed form whichis characteristic of the wet northernand easternlowlandsbelow 1,380 meterselevation;an all brownheadedform whichis foundon the dry westernslopesand in the highlands above1,400 meterselevation;and a brown-naped intermediate whichis the form characteristic of the southern coast Lowland contacts between these differentbrownmorphsare abrupt,coinciding with the Rivigredes Galets (gray headsvs brownheads),the RivigreSt Etienne (brown headsvs brown napes),andrecentlavaflowsnearBoisBlanc(brownnapesvs grayheads) In contrastthe altitudinaltransitionbetweenthe gray-headedand brownheadedforms on the easternslopesof ReunionIsland is continuousand steeplyclinalover a distanceof aboutfive km; samplesfrom this contactzone includea largenumberof purebrown-or gray-headed formsaswell as intermediatephenotypes The intensityof eumelanindepositionin the feathersof the underparts variesin relationto altitudein all colorforms,the underpartschangingfrom whitishin lowlandsto dark gray in the highlands.Extremesof this color variationare more strikinglydifferentthan is the casein mostmainlandsubspecies of Zosteropswhichexhibitthisvariation The highlysignificantcorrelationsof thisvariationwith altitudeandthe absence of significant visualpredaters on ReunionIsland suggestthat the differenceshave physiologicalvalue in termsof absorption of radiantenergy.In brown-headed brownmorphsthe intensityand extent of phaeomelanindepositionon the underpartsalso increasesin relationto increasingaltitudeand rainfall Size characteristics vary betweencolor forms and in relationto altitude Wing length of brown morphs increasesabout one millimeter per 1,000 meters of elevation Bill and tarsal lengthsalso increasewith altitude in brown-headedbrown morphs Bill length decreaseswith altitude in gray morphs Gray-headedbrown morphshave longer bills than lowland brownheadedbrownmorphs,but aboutthesamelengthbillsaslargehighlandbrown 58 ORNITHOLOGICAL MONOGRAPHS NO 12 morphs.Lowlandgray-headed brownmorphsand highlandgraymorphsshow sexualdimorphismin bill length The following sequenceof possibleevolutionaryeventsis envisionedas beingresponsible for the presentsituation.The brown morphfirst appeared as a mutantform in the originalgray morph populationsof ReunionIsland They graduallyreplacedgray morphsin the lowlandsbut not the highland heath zone and evolved head color and associated differences while isolated in disjunctpocketsof suitable"edge"habitat,e.g., brown-headed brownmorphs in the savannaof the arid westcoast,gray-headed brownmorphsalongrivers and streambedsin the east,and brown-napedbrownmorphsin youngforests at the baseof the activevolcanoin the south It is possiblethat the brownnapedbrownmorpharosethroughhybridization betweenthe othertwo forms The presentday pattern of geographicdistributionof thesecolor forms reflects range expansionsand secondarycontactsthat resultedfrom human destructionof indigenousforests Associatedaltitudinal range expansions havebroughtbrownand graymorphstogetherand clineshavedevelopedrefleetingthe relativeadaptationof the morphsto the lowlandsand highlands The expansions alsohaveled to the development of steepprimaryclinesin the intensityof melanindepositionand sizewithin the past250 years The highly localizeddifferentiationof populationsof Z borbonicaappears to havebeenthe inevitableresultof severalfactors,e.g.,its socialand sedentary habits,which,however,are not exceptionalor even extreme,its ties to disturbedand edgehabitats,the climaticdiversityof ReunionIsland,and perhaps increasedadaptiveflexibility resultingfrom releasefrom someselectiveagents usuallypresenton continents,suchas visualpredators In themselveseach of thesefactorsis not very unusual,but they are rarely found in combination within the confines of a small oceanic island 1973 GILL: VARIATION IN ZOSTEROPS LITERATURE BAILEY, N T.J BORBON1CA 59 CITED 1959 Statistical methods in biology London, The English Uni- versities Press Ltd BArl)W•N,S P., H C OBEVa-IorSER, ANl) L G WORrE¾ 1931 Measurementsof birds Sci Publs Cleveland Mus Nat Hist., Vol BERrIOZ,J 1946 Faune de l'empire franqais IV Oiseaux de la R6union Paris, Librairie LaRose BOWERS,D E 1956 A study of methods of color determination Syst Zool., 5: 147-160 BOWERS, D E 1960 Correlation of variation in the Wrentit with environmental gradients Condor, 62: 91-120 BROWN,J H., AND A K LEE 1969 Bergmann'sRule and climatic adaptation in woodrats (Neotoma) Evolution, 23: 329-338 CHAMArAUN,F H., Am) I McDouanrr 1966 Dating geomagnetic polarity epochs in R6union Nature, 210: 1212-1214 CLAmrE,B., Am) J MURRAY 1962 Changesin gene-frequencyin Cepaea nemoralis (L.); 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II Seasonal and annual changes in the frequencyof black hamsters Genetics,30: 233-251 GILL, F B 1971 Ecology and evolution of the sympatric Mascarene white-eyes, Zosteropsborbonicaand Z olivacea Auk, 88: 35-60 HArl)ANE,J B.S 1948 The theory of a cline J Genetics, 48: 277-284 HAMILTON,T.H 1961 The adaptivesignificancesof intraspecifictrends of variation in wing length and body size amongbird species.Evolution, 15: 180-195 HAMILTON, W J., III, AND F H HEPPNER 1967 Black pigmentation: adaptation for concealment or heat conservation Science, 158: HAm•IsoN,C J.O 1341 1965 Allopreening as agonisticbehaviour Behaviour, 24: 161- 204 HARTLAUB,G 1877 Die Voegel Madagascars und der benachbarten Inselgruppen Halle, Drnck and Verlag yon H W Schmidt HEPPNER,F 1970 Metabolic significanceof differential absorptionof radiant energy by black and white birds Condor, 72: 50-59 HRUBANT,H.E 1955 An analysisof the color phasesof the eastern ScreechOwl, Otus asio, by the gene frequency method Amer Nat., 89: 223-230 60 ORNITHOLOGICAL JAMES,F.C MONOGRAPHS NO 12 1970 Geographicsize variation in birds and its relationshipto climate Ecology, 51: 365-390 JOHNSON, N.K 1966 Morphologic stability vs adaptivevariation in the Hammond's Flycatcher Auk, 83: 179-200 JOHNSTON,R.F 1961 Population movements of birds Condor, 63: 386-389 JOHNSTON,R F., AND R K SELANDER.1964 House Sparrows: rapid evolution of races in North America Science, 144: 548-550 JOHNSTON, R F., AND R K SELANDER 1971 Evolution in the House Sparrow II Adaptive differentiation in North American populations Evolution, 25: 1-28 KETTLEWELL, H B D 1961a Selection experiments on melanism in Amathes glareosa Esp (Lepidoptera) Heredity, 16: 415-434 KETTLEWELL,H B D 1961b The phenomenon of industrial melanism in Lepidoptera Ann Rev Entomol., 6: 245-262 KETTLEWELL,H B D., aND R J BERRY 1961 The study of a cline Heredity, 16: 403-414 KLUIJVER,H.N 1951 The population ecologyof the Great Tit, Parus rn major L Ardea, 39: 1-135 LACK,D 1968 Ecological adaptations for breeding in birds London, Methuen and Co., Ltd LUSTICK,S 1969 Bird energetics: effects of artificial radiation Science, 163: 387- 390 LUSTInK, S MAY•, E 1971 Plumage color and energetics Condor, 73: 121-122 1956 Geographicalcharactergradientsand climatic adaptation Evolution, 10: 105-108 MAY•, E 1963 Animal speciesand evolution Cambridge, Belknap Press MAY•, E 1970 Population, species,and evolution Cambridge, Belknap Press MERRELL,D J., AND C F RODELL 1968 Seasonal selection in the leopard frog, Rana pipiens Evolution, 22: 284-288 MILLER, A H 1941 Speciationin the avian genusJunco Univ California Publs Zool., 44: 173-434 MILLER,A.H 1947 Panmixia and populationsizewith referenceto birds Evolution, 1: 186-190 MILON, P 1951 Notes sur l'avifaune actuelle de File de la R6union Terre et la Vie, 98: 129-177 MOREAU,R E 1957 Variation in the western Zosteropidae (Aves) Bull British Mus (Nat Hist.), Zoology, 4: 312-433 MoaEAu, R E 1967 [Family Zosteropidae, African and Indian Ocean taxa.] Pp 326-337 in Check-list of birds of the world, vol 12 (R A Paynter, Jr., Ed.) Cambridge, Massachusetts,Mus Comp Zool MUNRO, R E., L T SMITH, AND J J KUPA 1968 The genetic basis of color differencesobservedin the Mute Swan (Cygnus olor) Auk, 85: 504-505 NEWTON,A., ANDE NEWTON 1888 Notes on some speciesof Zosterops Ibis (Fifth Series) 6: 474-476 PAci•nm), G C 1967 House Sparrows: evolution of populations from the Great Plains and Colorado Rockies Syst Zool., 16: 73-89 POLLEN, F P L., AND D.C VAN DAM 1868 Recherches sur la Faune de Mada- gascaret de ses d6pendences,d'apres les decouvertesde F P L Pollen and D.C van Dam Pt Mammiferes et Oiseaux Leiden POWER,D.M 1969 Evolutionary implicationsof wing and size variation in the Redwinged Blackbird in relation to geographicand climatic factors: a multiple regressionanalysis Syst Zool., 18: 363-373 1973 GILL: RAND,A.L VARIATION IN ZOSTEROPS BORBON1CA 61 1936 Results of the Archbold Expedition No 12 Altitudinal variation in New Guinea birds American Mus Novit., no 890 RIVALS,P 1952 Etudes sur la vegetation naturelie de l'ile de la R6union Travaux Laboratoire Forestier Toulouse Tome V, Geographie forestiere du monde, Vol I, Art II SCHOLA•qDER, P.F 1955 Evolution of climatic adaptation in homeotherms Evolu- tion, 9: 15-26 SHEPPARD,P.M., AND L M COOK 1962 The manifold effects of the medionigra gene on the moth Panaxia dominula and the maintenanceof a polymorphism Heredity, 17: 415-426 Sm6EL, S 1956 Nonparametric statisticsfor the behavioral sciences.New York, McGraw-Hill Book Co STORER, R.W 1968 The cotypesof ZosteropsE Newtoni Hartlaub Auk, 85: 127 STOR•R, R W., AND F B GILL 1966 A revision of the Mascarene white-eye Zosterops borbonica (Aves) Occ Papers Mus Zool Univ Michigan No 648 UPTON,B G J., ANDW J WADSWORTH 1966 The basalts of Reunion Island, Indian Ocean Bulletin Volcanologique, 29: 7-24 WATSON,G E., R L Zus•, ANt) R W STOR•R 1963 Preliminary field guide to the birds of the Indian Ocean Washington, Smithsonian Inst 62 ORNITHOLOGICAL MONOGRAPHS APPENDIX SUMMARY Locality number Altitude (meters) OF REUNION km SSE le Brill6 km SSE le Brill6 5.7 km SSE le Brill6 km S le Brill6 7.7 km S le Brill6 5.2 km E Dos d'Ane 3.3 km E Dos d'Ane 20 km NNE St Joseph 10 1,000 820 11 12 13 14 15 16 90 220 10 200 560 680 17 18 19 20 21 22 23 24 1,100 1,530 1,940 1,160 920 1,350 1,570 1,400 I Name Number of specimens Val Fleuri Mamode Camp Rav Rivi•re 14 14 8 km SSW St Denis 5.3 km ESE la Possession des Remparts Chemin Arnoux Piton d'Orange 11 13 km S St Denis 3.5 km S Ste Marie 2.7 km E Ste Marie 5.2 km NE Salazie 1.5 km SSE Salazie km ESE Gd Islet Ravine du Butor Beaufonds Ravine Chevres Bras de Caveme Salazie Rivi•re Fleurs Jaunes 10 17 13 km NE Gd Islet km SSW Gd Islet km W Hellbourg Grand Islet Col Bemale Col de Fourche 11 11 km W Hellbourg Ravine Farla 10 km W Hellbourg km S Hellbourg 2.2 km SW Hellbourg 3.8 km NE Hellbourg Rivibre du Mat Terre Plate Plateau de Belouve Trou de Fer 10 10 Plaine des Chicots (gite) Plaine des Chicots Plaine d'Affouche Plaine d'Affouche 25 640 km SW St Benoit Ravine Mathurin 11 26 27 1,010 1,180 12 km SW St Benoit km WNW P1 des Palmistes (1 er) Takamaka Plateau Duverney 11 10 28 1,360 7.5 km W P1 des Forgt du B6bour Forgt du B6bour 15 Plaine des Salazes 10 Bras Grand 11 Palmistes (1 er) 29 1,350 30 1,720 6.5 km WNW P1 des Palmistes (1 er) 9.2 km W P1 des Palmistes ( 1er) 31 720 32 860 33 1,060 34 170 km NE P1 des Palmistes (1 er) 2.7 km NE P1 des Palmistes (1 •r) 1.5 km SSW P1 des Palmistes (1 or) 3.5 km NNE St Joseph 351,250 4.2 km SW P1 des Piton Piton Camp de Tgte P1 des Palmistes (2 eme) Rivi•re des Remparts Palmistes 36 1,250 4.7 km SW P1 des 37 1,620 km SE P1 des 10 Palmistes Palmistes 12 ISLAND LOCALITIES Location 1,000 1,100 1,580 1,780 1,910 1,650 1,460 1,700 NO Rampe de la Grande Mont6e 1973 GILL: VARIATION IN ZOSTEROPS APPENDIX Locality number Altitude (meters) 38 1,600 39 2,300 BORBONICA 63 I (continued) Location 5.5 km le VingtSepti•me km ENE Pas de Name Plaine des Carres Number of specimens Pas de Bellecombe Piton de la Plaine des Cafres Nez de Boeuf Bellecombe 40 1,400 km WNW P1 des Palmistes 41 2,060 4.5 km E le VingtSepti•me 7.5 km ENE le VingtSepti•me km SSE le VingtSepti•me 42 2,300 43 2,300 44 45 46 520 500 47 48 60 100 49 1,060 50 20 51 40 km NE l'Etang 52 1,380 Piton 16 de Sable Plaine des Remparts lgtang du Gol 13 ForSt Mourouvin Forgt Mourouvin Grand Brill6 Grand Brill6 12 11 12 11 17 km N St Joseph Rivi•re des Remparts 12 km Ravine 2.5 km WSW St Louis km WSW Ste Rose 4.2 km S Ste Rose km SSW Bois Blanc 10.2 km SSW Bols Blanc ESE St Pierre des Cafres Forgt Dominale 11 Sa16 les Bains 3.5 km NNE Plaine Bols Court Petite Serr6 11 10 37 10 10 des Cafres 53 270 8.7 km NNE 54 55 340 300 km N St Louis 6.5 km SSE Cilaos St Louis Bras de Patate Le Pavillon 56 57 58 59 60 61 1,000 1,380 1,400 2,000 2,460 1,080 km SSE Cilaos 4.5 km S le Brill6 km N Cilaos km NNE Cilaos km NE Cilaos km N T6velave Bras de Benjoin 62 1,440 2.5 km NNE ForSt Soumise des ForSt du Gd Matarum Petit Matarum Cavern Dufour For•t Soumise des Bernards (PK 2) T•velave 21 Bernards (PK 7) 63 1,700 km NNE T•velave For•t Soumise des 29 Bernards (PK 10+) 5.7 km NNE T•velave 64 1,980 65 66 180 10 67 68 120 km WSW Trois Bassins 2.5 km S St Gilles 2.5 km NNE St Paul 5.5 km SE le Port 69 160 km SE le Port Ravine Ravine des Avirons Chauve Souris l•tang St Paul Rivi•re des Galets 10 (south side) 70 71 72 73 74 75 1,660 1,800 1,400 2,200 1,550 20 11 km ESE St Paul 11.7 km ESE St Paul 9.5 km ESE St Paul 14.2 km ESE St Paul 10.5 km ESE St Paul km WSW St Paul Rivigre des Galets (north side) Ligne Dominiale Camp Dennemont (PK 5) Piton Maido (PK 7) Ravine Jacques 10 14 13 64 ORNITHOLOGICAL APPENDIX Locality number Altitude (meters) 76 20 MONOGRAPHS 12 I (continued) Location km WSW NO Name St Denis NE la Possession Rav de Grande 0 20 !km 78 40 I km SSE la Possession Grande 79 80 900 500 1.7 km W Cilaos 9.5 km SW St Benoit Cilaos (Bras Rouge) Grand Etang 81 82 83 84 85 30 10 20 20 km SSE St Benoit km SSE Ste Anne Ste Rose 5.2 km SE Ste Rose km NNE Bois Blanc Ravine S&he Ste Anne Monument Piton $te Rose Pointe Cascades 86 500 6.5 km W St Philippe Brfil• du Baril 87 88 89 90 70 I0 1,360 680 Jardin Boyer Mare Longue Plaine d'Affouche Morne de l'Etang 91 10 92 20 4.5 km WNW 93 90 4.2 km E St Louis 94 95 96 300 640 740 Ravine St Pierre (Oratorio) St Pierre 1.5 km NW les Avirons 1.7 km W T•velave I km SE le Brfil• Chaloupe Camp Magloire 77 km SE le Port 2.5 km$E St Philippe 4.6 km NE Dos d'Ane 4.7 km NE P1 des Palmistes (! •') 1.7 km W St Pierre Number of specimens 0 11 0 10 16 0 0 Riv St Etienne (south side) Ravine des Avirons Ravine des Avirons Ravine Butor 97 98 1,080 1,330 7.6 km ESE St Paul 1.8 km NNE T•velave (Le Brill6) La Petite France For•t Souraise des 99 380 6.6 km SW St Benoit Chemin de la 11 1! I0 10 10 I0 Bernards (PK 5.5) Grand I00 1,740 I01 1,940 102 280 I1 Fond km NNW le VingtSepfi•me 7.7 km NNE le VingtSeptibme Plaine des Carres km E Ste Rose Riv de l'Est Coteau Maigre 10 ! All specimens were taken in 1967, except those for localities I00 and I01, which were taken in 1964 1973 GILL: VARIATION IN ZOSTEROPS APPENDIX BORBON1CA 65 II UNDERPARTGRAY COLORVARIATIONIN Zosterops borbonica ON REUNION ISLAND Locality ARitude number (meters) Sample size Underpart gray Mean 1,000 1,100 1,580 1,650 1,700 1,000 index Standard deviation 14 11 11 4.6 4.8 6.5 5.8 6.2 3.1 1.50 1.83 1.13 0.45 1.75 1.37 10 820 11 3.3 1.19 11 12 14 16 90 220 200 680 10 13 13 2.7 2.5 4.0 3.9 1.25 0.87 1.22 18 1,530 11 5.5 1.44 19 20 1,940 1,160 10 10 6.0 6.2 1.05 1.31 23 24 1,570 1,400 10 10 5.3 5.9 1.42 1.41 1.44 25 640 4.1 1.25 26 27 29 1,010 1,180 1,350 11 10 10 5.1 5.3 5.5 30 1,720 6.5 1.30 0.67 1.35 0.84 31 720 11 5.0 1.79 33 1,030 5.5 1.76 34 170 10 1.1 0.73 39 40 41 2,300 1,400 2,060 24 6.3 6.4 5.6 1.30 0.78 1.10 44 45 13 12 11 12 11 1.7 3.3 4.4 2.7 2.4 0.87 1.37 46 47 48 520 500 80 100 49 1,060 12 4.8 1.75 51 53 55 40 270 300 17 7* 2.4 2.1 2.3 0.87 0.69 0.72 56 57 58 60 61 62 63 1,900 1,380 1,400 2,460 1,080 1,440 1,700 38 10 15'* 25 4.6 5.4 6.0 6.5 2.6 3.5 5.4 0.53 1.06 1.37 1.08 1.30 1.12 1.34 1.21 1.37 1.86 64 1,980 5.7 1.83 68 120 10 1.4 0.71 70 72 1,660 1,400 2,200 4.4 4.5 1.94 1.34 14 6.3 1.24 73 ORNITHOLOGICAL 66 APPENDIX Locality number Altitude (meters) MONOGRAPHS NO II (continued) Sample size Underpart gray Mean index Standard deviation 74 1,550 13 6.7 1.55 85 86 87 93 94 95 96 20 320 70 90 300 640 740 10 12 10 10 2.7 1.0 2.6 0.5 1.9 2.5 3.3 0.95 0.89 0.79 0.55 0.60 1.08 1.25 97 98 1,080 1,330 6** 3.6 4.0 0.69 2.11 99 380 3.1 2.04 * Gray morphs excluded ** "Brown-napes" excluded 12 ORNITHOLOGICAL No MONOGRAPHS A Distributional Studyof theBirdsof BritishHonduras, byStephen M Russell.195pp.,2 colorplates.1964.Price$4.50($3.60to AOU members) No A Comparative Studyof Some Social Communication Patterns in the Pelecaniformes, by GerardFrederickvan Tets 88 pp., text figures.1965 Price$2.00 ($1.60 to AOU members) No The Birdsof Kentucky,by RobertM Mengel.Clothbound,xiv+ 581 pp., colorplatesplustextfiguresandvignettes 1965 Price $10.00 ($8.00 to AOU members) No Evolutionof SomeArcticGulls (Larus): an ExperimentalStudy of IsolatingMechanisms, by NealGriffithSmith.99 pp., 62 text figures.1966 Price$2.50 ($2.00to AOU members) No A Comparative Life-history Studyof FourSpecies of Woodpeckers, by Louise deKirilineLawrence 156pp.,33 textfigures.1967.Price $3.75 ($3.00 to AOU members) No Adaptations for Locomotion andFeeding in theAnhinga andthe Double-crested Cormorant,by OscarT Owre.138pp.,56 textfigures 1967 Price $3.50 ($2.80 to AOU members) No A DistributionalSurveyof the Birds of Honduras,by Burt L Monroe,Jr 458 pp., 28 text figures,2 colorplates.1968 Price $9.00 ($7.20 to AOU members) No AnApproach totheStudy of Ecological Relationships among Grassland Birds,by JohnA Wiens.93 pp.,30 textfigures.1969 Price $2.50 ($2.00 to AOU members) No.9 MatingSystems, Sexual Dimorphism, andtheRoleof MaleNorth AmericanPassefineBirds in the NestingCycle,by JaredVernerand MaryF Willson.76 pp 1969.Price$2.50($2.00to AOUmembers) No.10.TheBehavior of Spotted Antbirds, byEdwin O.Willis, vi + 162pp.,3 colorplates, 27textfigures.1972.Price$6.00($4.75to AOUmembers) No.11.Behavior,MimeticSongs and SongDialects,and Relationships of the ParasiticIndigobirds(Vidua) of Africa, by RobertB Payne, vi + 333pp.,2 colorplates, 50 textfigures, 40 audiospectrographs 1973 Price $8.00 ($6.40 to AOU members) No 12 Intra-island Variation in the Mascarene White-eye Zosterops borbonica,by FrankB Gill, vi + 66 pp., colorplate,31 textfigures 1973 Price $2.00 ($1.60 to AOU members) Like all otherAOU publications, Ornithological Monographs are shipped prepaid.Makechecks payable to "TheAmerican Ornithologists' Union."For the convenience of thosewho wish to maintaincompletesetsof Ornithological Monographs andto receive newnumbers immediately uponissue, standing orders will be accepted Orderfrom: Burt L Monroe,Jr., Treasurer,AmericanOrnithologists' Union, Box 98447,Anchorage,Kentucky4099• ... Somevariationbetween counts,dueprimarilyto sampling error,is present 16 ORNITHOLOGICAL MONOGRAPHS NO 12 o o 19 0 5O •9 2125 626, 18 "•27 200 0 12 ½ i0 16 27 9O 47 31 02 0TM 61 I0 KILOMETERS 0 Fioum• The... 79, 58, 59, 60 in sequence) 20 ORNITHOLOGICAL MONOGRAPHS NO 12 90 -•- a 70 r• 60 r• 50 c.) 40 '• 3o •o o IO 12 14 16 lB 20 22 24 26 ALTITUDE(meters /100) FleURE 12 Altitudinal relationshipsof... temperaturerecordsin the form of ten-yearsummaries for 112 and 30 Reunionlocalities,respectively, were made availableby the ORNITHOLOGICAL MONOGRAPHS NO 12 ST DENIS I Pos ?eBr•l• :hicots ST PAUL ST.BENOIT