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The Long-Billed Lark Complex: a Species Mosaic in Southwestern Africa

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The Long-Billed Lark Complex: a Species Mosaic in Southwestern Africa The Auk 116(1):194-208, 1999 THE LONG-BILLED LARK COMPLEX: A SPECIES MOSAIC IN SOUTHWESTERN AFRICA PETER G. RYAN •,3 AND PAULETTE BLOOMER •'2 •PercyFitzPatrick Institute of AfricanOrnithology, University of CapeTown, Rondebosch 7701, South Africa; and 2Departmentof Zoologyand Entomology, Pretoria University, Pretoria 0001, SouthAfrica ABSTi•ACT.--TheLong-billed Lark (Certhilaudacurvirostris) is a geographicallyvariable species.Thirteen subspecies have been described, and at leastthree phenotypically well- definedgroups exist. We use concordantpatterns of genotypicand phenotypicvariation to recognizecryptic species within this complex.Genotype information was obtainedby se- quencingpart of themitochondrial DNA cytochrome-bgene. Three taxa are genetically high- ly distinct,differing from each other by 6 to 9% sequencedivergence. One of thesetaxa com- prisesthree phenotypically distinct taxa that differ from eachother by 2% sequencediver- gence.These values far exceedthe variationwithin describedsubspecies (0.2 to 0.4%)and approachthe distanceto the presumedsister taxon, the Short-clawedLark (C. chuana;8 to 10%).Well-defined morphological and plumage differences exist between all taxaexcept ben- guelensisand northernpopulations of subcoronata.We proposethat the complexconsists of five species:the closelyrelated C. curvirostris,C. brevirostris,and C. semitorquata,and the more distantly related C. subcoronataand C. benguelensis.Comparison of male display songs providesadditional support for the recognitionof five species,but samplesizes are small. The positionof C. chuanarelative to the five speciesnoted aboveis not resolved.Species' rangesare allopatric,but more work is neededto elucidatethe distributionallimits of taxa in northernNamibia and Angola.These findings have implications for biodiversityconser- vation,and they suggestthat considerablediversity has been overlooked in wide-ranging, sedentarylark species.Received 19 December1997, accepted22 June1998. THE LARKS(FAMILY ALAUDIDAE) are a pre- deserts,and mesicmontane grasslands (Dean dominantlyOld World family whoseaffinities et al. 1992, 1997). Being sedentary(Dean and within the passerinesare poorly understood Hockey1989; Dean et al. 1992,1997) apparently (Sibley and Monroe 1990). Most speciesare has promoted the evolutionof marked geo- found in Africa, where there are two main cen- graphicalvariation in plumageand morpholo- ters of diversityassociated with the northeast- gy. Theseregional differences have been inter- ern and southwestern arid zones. These re- preted as adaptationsto local conditions.For gionsare characterizedby highlevels of ende- example,upperpart coloration matches the lo- mism,with manyspecies having small ranges. cal substratum color (Macdonald 1952), and Recentresearch suggests that superficially sim- long bills and hind clawsoccur in birds living ilar allopatricpopulations, which have been on soft, sandy soils (Clancey1957). lumped together in polytypic species,may This geographicvariation has led to consid- have been isolatedfor considerableperiods of erable debate about the species'taxonomy. time (e.g. Ryan et al. 1998). Thirteen taxa have been described (Clancey The Long-billed Lark (Certhilaudacurviros- 1980,Dean et al. 1992),which havebeen split tris) is restricted to southwesternAfrica from into as many as four species(Roberts 1940), southernAngola throughwestern Namibia to and even placed in separategenera (Sharpe SouthAfrica. It formsa superspecieswith the 1904). However, the current consensusis to Short-clawedLark (C. chuana),which replaces lump all forms into a single polytypic species the Long-billedLark in arid acaciasavannas in (Clancey 1957, Dean et al. 1992,Maclean 1993). easternBotswana and adjacentSouth Africa This is despitea recentreview of the speciesin (Dean et al. 1992, 1997; Fig. 1). Long-billed South Africa that concludedthat the species Larksoccur in a wide rangeof habitats,includ- perhapsshould be viewed as a superspecies ing coastaldunes, open plains, rocky slopes, with at least three allospecies(Quickelberge 1967). E-mail: [email protected] Here, we use geneticsequence data to help 194 January1999] Long-billedLark Species Complex 195 25S 3O S curvirostris 35 S bre viros tris 15 E 20 E 25 E 30 E FIG.1. The distributionof speciesin the Long-billedlark complex,including the presumedsister taxon, Short-clawedLark (Certhilaudachuana), based on examinationof specimensand atlasdata from Dean et al. (1997).Open squaresdenote collection localities of birds whosemtDNA was sequenced. resolvethe evolutionaryrelationships among mM Tris pH 7.6, 100 mM NaC1, 1 mM NaEDTA pH taxa within the Long-billedLark complex.We 8.0, 0.5% SDS, i mg/mL proteinaseK) overnightat sequencedpart of the mitochondrialcyto- 37øC. Following RNAse treatment, total genomic chrome-bgene, which has provedvaluable in DNA was extractedtwice with phenol,once with chloroform:isoamylalcohol(24:1), and precipitated resolvingrelationships at the specieslevel in with 2M ammonium acetate and 100% ethanol. Pu- larks and otherbirds (e.g.Shields and Helm- rified mtDNA was extractedfrom three specimens Bychowski1988, Smith et al. 1991,Helbig et al. (Table1) followingthe methods of Essopet al. (1991). 1996, Ryan et al. 1998).We also reanalyze geo- A 500 base-pair(bp) fragment of the mtDNA cyto- graphicvariation in plumageand morphology chrome-bgene was amplifiedusing primersL14990 in relation to the geneticallydefined taxa and (L14841;Kocher et al. 1989)and H15499 (CBINT; Av- make recommendationsabout the taxonomyof ise et al. 1994).Double-stranded amplifications were the complex. performed in 50-p,L volumes using 2.5mM MgC1v 2mM dNTPs,25 pmol of eachprimer, and 1.5 units METHODS of Taq DNA polymerase(Promega). Reaction mix- tures were subjectedto 35 cyclesof denaturationat Samplingand DNA analysis.--BetweenOctober 94øC(30 s), annealingat 48 to 50øC(1 min), and ex- 1994and July1997, we collected19 birds from 17 lo- tensionat 72øC(1 min).The first cycle was preceded calities(Table 1, Fig. 1). Individuals were assignedto by an initial denaturationof 3 min at 94øC,and the taxabased on plumagecharacters and locality(see last cyclewas followed by a final extensionof 10min below).We dissectedout the heart, liver, and pec- at 72øC.PCR productswere purified through 2% toral muscletissues and preservedthem in a satu- low-meltingpoint agarose gels (MS8; Whitehead Sci- rated NaCI/20% DMSO solution (Amos and Hoelzel entific)and recoveredusing the QIAEX II gel extrac- 1991). tion kit (Qiagen).Both light andheavy strands were In the laboratory,tissue samples were digested (50 sequencedby dideoxy sequencing(Sanger et al. 196 RYANAND BLOOMER [Auk,Vol. 116 TABLE1. Collectionlocalities and subspecificdesignation of the 19 birds in the Long-billedLark complex whosecytochrome-b gene was sequenced(one per site,except for UniabRiver). Taxon Locality Coordinates falcirostris Port Nolloth 29ø15'S,16ø50'E falcirostrisa GroenrivierMouth 30ø50'S,17ø35'E curvirostris Paternoster 32ø48'S, 17ø55'E brevirostris Roodekleigat(20 km W of Robertson) 33ø50'S,19ø40'E brevirostris Bredasdorp(15 km NE) 34ø25'S,20ø10'E semitorquata Cradock(25 km NW) 32ø08'S,25ø24'E semitorquata Stutterheim(20 km NW) 32ø23'S,27ø42'E semitorquata NottinghamRoad (15 km W) 29ø22'S,29ø54'E transvaalensis Wakkerstroom(10 km SE) 27ø22'S,30ø12'E gilli Toorberg(35 km E of Murraysburg) 32ø03'S,24ø08'E gilli Middlestevlei(40 km N of Laingsburg) 32ø55'S,20ø57'E subcoronata• Bloubosfontein(40 km NW of Prieska) 29ø24'S,22ø38'E subcoronata Dikpens (100 km NW of Brandvlei) 30ø10'S,19ø32'E bradshawia Pofadder 29ø10'S, 19ø22'E bradshawi Nieu-Tsaus (40 km S of Aus) 27ø00'S,16ø12'E kaokensisb Uniab River (100 km W of Kamajab) 19ø54'S,13ø59'E chuana Pietersburg 29ø20'S,29ø25'E Sequencesfrom purifiedmtDNA (seeMethods). btI --3. 1977)with the Sequenaseversion 2 enzymesystem have been depositedin GenBankunder accession (United StatesBiochemicals). The two PCR primers numbers AF033249-58. and two internal primers (H15 298 [Kocheret al. Morphometricsand plumage.--PGRmeasured 414 1989]and L15245[Palumbi et al. 1991])were usedfor Long-billedLarks and Short-clawedLarks; 400 were generating sequences.Sequences were aligned by from skins housed in the Durban, East London, Na- eye, and no insertionsor deletionswere found. mibian, South African, and Transvaal museums, and A matrix of pairwise nucleotidesequence diver- 14 were birds measured in the field. Measurement gencesfor neighbor-joininganalysis (Saitou and Nei protocolsfollow Ryan et al. (1998).Tail lengthand 1987) was calculated in MEGA version 1.01 (Kumar wing length(flattened chord) were measured to the et al. 1993)using the Kimura two-parametercorrec- nearest1 mm. Tarsuslength, bill length(distal edge tion (Kimura 1980). This model accountsfor the of naresto bill tip), andbill depth(depth at proximal higher rate of transitional substitutionsin animal edgeof nares)were measuredto the nearest0.1 mm. mtDNA and usesa 2:1 TV:TI ratio; no gammacor- Bill lengthfrom the nareswas preferred to the stan- rection was applied to correct for possibleamong- dard measureof bill length(from the baseto the tip) site rate variation. Maximum-parsimonyanalysis becausemolt and damageto museumskins make it was performed using PAUP 3.1.1 (Swofford 1993). difficult to consistentlymeasure standard bill length Phylogeneticsignal was assessedby analyzingtree- (seeGrant et al. 1985). Coefficientsof variation with- lengthdistributions of 1,000random trees (Hillis and in taxainvariably were smaller using bill lengthfrom Huelsenbeck1992).
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