Species Limits in Antbirds (Thamnophilidae)

8/13/2019 Species Limits in Antbirds (Thamnophilidae)

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SPECIES LIMITS IN ANTBIRDS (THAMNOPHILIDAE):

THE WARBLING ANTBIRD (HYPOCNEMIS CANTATOR) COMPLEXM L. I,1,3P R. I,1 B M. W2

1Department of Vertebrate ZoologyBirds, National Museum of Natural History, Smithsonian Institution,P.O. Box 37012, Washington, D.C. 20013, USA; and

2Museum of Natural Science, Louisiana State University, 119 Foster Hall, Baton Rouge, Louisiana 70803, USA

A.Six populations of Warbling Antbird(Hypocnemis cantator) currentlyconsidered subspecies are more appropriately recognized as species, given themultiplicity of vocal differences that distinguishes them. These vocal differencesare as great or greater than vocal differences documented between syntopic spe-cies-pairs in the family Thamnophilidae (Isler et al. 1998). Evidence is also providedthat two forms currently considered subspecies are syntopic and that two othersare parapatric without apparent physical barriers. Vocally, the pair of syntopic

taxa were distinguished dramatically, but solely, by common calls. The finding thatcommon calls were as diversified as songs in this species-group suggests that callsmay be as important as songs in reproductive isolation. Future field studies shouldtherefore focus on clarifying the function of different types of thamnophilid vocal-izations and elucidating their role in speciation. This is the first contribution to amultifaceted analysis of the vocalizations and genetic structure of typical antbirds(Thamnophilidae) in Amazonia. In future work, results of the vocal analysis will becompared with a parallel genetic study, aer which the two analyses will be inte-grated to suggest a phylogeny. The present study and preliminary studies of geneticdifferentiation (e.g., Bates et al. 1999) make it clear that the H. cantatorcomplex hashad a long evolutionary history that produced greater species-level diversity thanwas recognized previously. Received 15 January 2005, accepted 12 February 2006.

Key words: biodiversity, Hypocnemis, Neotropics, speciation, systematics,

Thamnophilidae, vocalizations.

Lmites de Especies en Thamnophilidae: El Complejo de Hypocnemis cantator

R.Teniendo en cuenta las mltiples diferencias en vocalizaciones quedistinguen a seis poblaciones deHypocnemis cantatorque actualmente son consideradascomo subespecies, es ms adecuado reconocerlas como especies diferentes. Estasdiferencias en vocalizaciones son iguales o mayores que las documentadas entrepares de especies sintpicas en la familia Thamnophilidae (Isler et al. 1998). Tambinse provee evidencia de que dos formas actualmente consideradas subespecies sonsintpicas, y que otras dos son paraptricas, sin barreras fsicas evidentes. Vocalmente,el par de taxones sintpicos se diferenciaron dramticamente, pero nicamente en susllamadas comunes. El hallazgo de que las llamadas comunes estn tan diferenciadascomo los cantos en este grupo de especies sugiere que las llamadas pueden ser tanimportantes como los cantos en el aislamiento reproductivo. Por lo tanto, estudiosde campo futuros deberan enfocarse en aclarar la funcin de los distintos tipos devocalizaciones de los Thamnophilidae, y en elucidar el papel que stos juegan en laespeciacin. Esta es la primera contribucin de un anlisis con mltiples facetas de

The Auk124(1):1128, 2007 The American Ornithologists Union, 2007.Printed in USA.

3E-mail: [email protected]


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V a relevant yard-stick (sensuMayr and Ashlock 1991) for esti-mating reproductive isolation and species statusof sympatric and allopatric populations of sub-oscine passerines (Isler et al. 1998, Johnson etal. 1999, Baptista and Kroodsma 2001, Helbig etal. 2002, Remsen 2005), though cautions regard-ing individual variation and clinality apply

(Isler et al. 2005). Recent studies of vocaliza-tions of the suboscine family Thamnophilidaehave documented extensive, geographically

based differentiation within some species (e.g.,Isler et al. 1997, 1999, 2001; Whitney et al. 2000;Isler and Isler 2003). Parallel to these analyses,molecular studies of antbirds have revealedhigher-than-expected levels of intraspecificgenetic structure (Capparella 1988; Hacke andRosenberg 1990; Hacke 1993; Brumfield andCapparella 1996; Bates et al. 1999; Bates 2000,2002). Questions remain, however, about theextent to which species diversity as expressed

by vocal characters is consistent with geneticdifferentiation.

Over a period of nearly two decades, wecollected recordings of vocalizations of theWarbling Antbird (Hypocnemis cantator) fromdiverse parts of its extensive range and notedsubstantial geographically related differencesamong vocalizations. More recently, explor-atory molecular studies (Bates et al. 1999;Bates 2000, 2002) have revealed high levels ofregional genetic differentiation among somepopulations of H. cantator. General concordancein these results led to the inclusion of H. canta-tor in an ongoing study of thamnophilid dif-ferentiation in Amazonia in which vocal andmolecular character sets are being developedfor populations of five widespread species-groups. Vocal and molecular characters will beemployed independently to derive estimates ofthe most appropriate taxonomy of each group.These results will be compared, an effort will

be made to understand the basis for any dis-crepancies between them, and an estimate of

phylogeny will be constructed from both datasets. Ultimately, the results of the five studieswill be integrated to provide tests of hypothesesof historical processes leading to avian diversi-fication in the Amazon basin.

Although an initial step within this long-termprogram, the results of the vocal analysis of theH. cantator complex are suffi ciently robust to

recommend modification of species limits atthis time. The analysis builds on the methodol-ogy for considering taxonomic limits in allopat-ric antbird populations established in studiescited above. The criteria are conservative, andour conclusions may be revised aer incorpo-ration of the molecular results. Additionally,

because the geographic distribution of avail-able tissue samples for H. cantator is much morerestricted than the inventory of tape recordings,we expect that determinations of distributionallimits of most populations and, by extension,taxonomic recommendations, will depend onthe results of analysis of the more robust sampleof recordings. We expect the molecular analysisto occupy a more dominant role in construct-ing a phylogeny, the balance depending on theconcordance of the vocal and molecular resultsand consideration of morphological distinctionsamong populations. Given the acceleratinganthropogenic alteration of the landscape in theNeotropics, empirically based re-evaluations ofspecies definitions are not only vital for studiesof speciation and phylogenetics, but are anurgent necessity for ecological and conservationresearch.

M

Hypocnemis cantator is distributed widely inAmazonia and the Guianan region (Zimmerand Isler 2003). Eleven subspecies wereaccepted by Peters (1951), and a 12th wasdescribed subsequently by Pinto (1966). Allwere diagnosed by plumage characters basedon specimen comparisons. We accepted existing

las vocalizaciones y la estructura gentica de los Thamnophilidae en la Amazona. Enestudios futuros, los resultados de los anlisis de vocalizaciones sern comparadoscon los de un estudio gentico paralelo, para luego integrar los dos anlisis y sugerir

una filogenia. El presente estudio, junto con anlisis preliminares de variacin gentica(e.g., Bates et al. 1999) indican claramente que el complejo de H. cantatorha tenido unahistoria evolutiva prolongada que produjo una mayor diversidad de especies que laque ha sido reconocida hasta ahora.


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Warbling Antbird Species LimitsJanuary 2007] 13

subspecies and morphological distinctions todefine a baseline taxonomy and, to simplifyexposition, we employed subspecies names

without initials as to genus or species and abbre-viated subspecies names to the first three leersin maps and tables. Because of the possibility,however, that existing, plumage-based subspe-cies definitions may not fully reflect distinctionsamong independently evolving populations asreflected in their vocalizations, we further dis-aggregated the inventory of vocal recordings tosearch for possible diagnostic vocal differenceswithin the geographic range of named subspe-cies. Twenty-six geographic clusters (Fig. 1),identified in the text as subpopulations, weredefined on the basis of existing knowledge ofgeographic limits of thamnophilid antbirds.

For example, if a major river bisecting therange of an H. cantator subspecies was knownto demarcate the ranges of sister populations ofother thamnophilid taxa, recordings obtainedon opposite sides of the river were analyzedas subpopulations. Initially, pairwise vocalcomparisons were made between subpopula-tions of currently described subspecies (e.g.,

fla1 was compared with fla2). Then, data forsubpopulations whose vocal data did not differdiagnostically were aggregated, and pairwisecomparisons were made of the vocal character-istics of all subspecies and vocally diagnosticsubpopulations. The final results provided the

basis for taxonomic recommendations, includ-ing a test of the extent of geographic congruencewith plumage-based subspecies.

Tape recordings were compiled from ourown inventories, from currently unarchivedcontributions by other individuals, and fromthe Macaulay Library (ML, at the CornellLaboratory of Ornithology), the NationalSound Archive (NSA, at The British Library),and the Florida State Museum (FSM, at theUniversity of Florida). Appendix 1 (online; seeAcknowledgments) provides a list of recordingsemployed in the study (774 recordings from 196localities) with locality names, recordists, andarchival locations. No recordings were availablefrom within the range of H. c. perflava.

We reviewed every recording to identify thenumber and sex of individuals vocalizing andto label every vocalization as to type. We identi-fied five vocalization types that we termed maleloudsong, female loudsong, common call, chirr,and chitcall. Loudsongs (following Willis 1967)

refer to the ringing series of notes delivered ina consistent paern oen described simply assong. Common calls are also multinote vocal-

izations delivered in a consistent paern but aremuch briefer than and structurally distinct fromloudsongs. Common calls are sometimes sub-

ject to individual variation (e.g., in duration orfrequency structure), but atypical common callsare almost always interspersed within lengthyseries of typical ones. Chirrs are single, vibrant,harsh notes, and chitcalls are abrupt notes thatare typically repeated rapidly in clusters of twoto four. Stereotypy of placement of spectral ele-ments within these vocal types (relative posi-tion, following Remane [1952]) allowed us toplace vocalizations into these categories witha relatively high degree of certainty that they

were homologous.CANARY, version 1.2 (Bioacoustics Research

Program, Cornell Laboratory of Ornithology),was employed to make a spectrogram of everyvocalization type delivered by each individualof either sex on every recording. Visual char-acters were obtained by examining printedcopies of all clearly delineated spectrograms(i.e., sampling was not employed). We con-sidered a character to be diagnostic visuallywhen examination of the character completelydistinguished every spectrogram of one popula-tion from another. If there was any uncertaintyin this regard, we conducted blind tests inwhich spectrograms were stripped of any iden-tification except a randomly selected code num-

ber and sorted visually into groups accordingto perceived differences. The groups were thenconsidered to differ diagnosably if they provedto be separated geographically.

We employed the following terms in visualdescriptions of note shape. Downslurredmeans that the note drops in frequency (i.e., thespectrogram trace goes from a higher to a lowerfrequency). An upslurred note goes in theopposite direction. A flat note shows lile orno change in frequency (a horizontal line on thespectrogram). A rectangular note is a flat notewith enough band width that the note appearsas a rectangle on a spectrogram at the scaleemployed here. Frequency rises and falls in aninverted U note, and the spectrogram trace isdistinctly rounded near the point of peak fre-quency. A chevron is like an inverted U butshows a sharp peak at the highest frequency,resembling an inverted V. Sometimes, inverted


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U notes or chevrons are not symmetrical;one side of the note may be more intense (asexpressed by wider band width on the spectro-gram), in which case we refer to the le-handor right-hand side of the note. Lengthydownward extensions to lower frequencies are

called le- or right-hand tails. Note shapepaern describes how the shapes of notes,including note duration, change throughouta multinote vocalization. Clear notes arerepresented on a spectrogram by distinct edges,whereas a note is said to become raspy when a

F. 1. Geographic distribution of recordings and definitions of hypothetical populations ana-lyzed in Stage 1. Recording localities are assigned to geographic sectors using methods described

by Isler (1997). Solid circles = recording locations. Heavy lines connect recording locations includedin each population and encircle other recording locations in the population. Areas outside theheavy lines contain populations for which we had no recordings. Currently defined subspecies:aff= H. c. affinis, can= H. c. cantator, col= H. c. collinsi,fla= H. c. flavescens, imp= H. c. implicata, not=H. c. notaea, och= H. c. ochrogyna,per= H. c. peruviana, sat= H. c. saturata, str= H. c. striata, and sub=H. c. subflava. No recordings were available for H. c. perflava. Numbers after abbreviations identifyhypothesized populations within subspecies ranges. Vocalizations ofper3and color subhave beenrecorded at sites in the hatched area, and labels for these populations are repeated on each sideof the hatched area to locate where the population occurs. Bothper3and subhave also been tape-recorded at the location marked A on the map. Loudsong recordings (n= 2) from Ilha de Maraj,Par, Brazil (identified in the figure as aff2), were omitted from the aggregated analysis because of

uncertainty regarding the population to which they should be referred.


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noticeable part of its edges dissolve into noise.Most raspy notes cover a wide band width andmay or may not contain a distinct solid area

of high intensity in their core. Terminal raspynotes in loudsongs were not included in descrip-tions of note shape paern because individualsoen vary the number of such notes in a seriesof songs. Visual determinations of change inpeak frequency were made in reference to ahorizontal line drawn through the peak frequen-cies of a spectrogram of a multinote vocalization.Peak frequency refers to the highest frequencyaained by the most intense trace of an indi-vidual note. Rise, flat, and fall refer tochanges of peak frequencies among the notesand signify an increase, no change, and decrease,respectively.

Quantitative measures of continuous vocalcharacters were restricted to a sample ofrecordings. Sample sizes (reflecting number ofindividual birds recorded, not number of vocal-izations measured) are provided in the Tables25 (online; see Acknowledgments). If morethan six suitable recordings were available, wesought to distribute the sample throughout theregion defined for the population. In the finalstage, aer populations were aggregated, datafor more than six individuals were availablefor most populations. To obtain quantitativemeasures, spectrograms were projected onthe screen of a Macintosh G4 computer usingdefault seings of CANARY (Charif et al. 1995),except that the display was set to smooth, over-lap was adjusted from 50% to 93.75% dependingon recording quality, and contrast was adjustedaccording to recording intensity, with caretaken to retain all elements of the vocalization.Cursor measurements were made by PRI, typi-cally at scales of 0.3 s inch1and 4.0 kHz inch1.Spectrograms shown in the figures were made

by exporting CANARY files into CANVAS,version 9.0.4 (ACD Systems, Victoria, BritishColumbia).

Whenever possible, we measured three vocal-izations of each vocalization type for six indi-viduals of every population identified in Figure1. It was not always possible to achieve this goal,

because of an inadequate number of recordingsfor some populations and because a high level ofrecording quality was required for many of themeasurements. As in the case of visual descrip-tions, terminal raspy notes were not included inmeasurements. Vocal characters were defined

on two levels. General characters included(1) number of notes, (2) duration, (3) pace, (4)change of pace, (5) note shape, (6) change in

note shape, (7) note duration, (8) change in noteduration, (9) interval duration, (10) change ininterval duration, (11) peak frequency, and (12)change in peak frequency. Specific measures(24) were assigned to general characters andincluded the number of notes; duration; over-all pace (measured from the beginning of thesecond note to the beginning of the first raspynote); durations of first, middle, and last clearnotes and the intervals (spaces) following them;ratios between note and interval durations; andpeak frequencies of first, middle, and last clearnote and ratios between them. Measures aredescribed more fully in earlier papers (Isler et al.

1998, 1999), and measurement units are providedin table legends.

In defining vocal characters that relate to spe-cies differences in antbirds, we are interested inidentifying distinct character states that havethe potential for unambiguous signal recogni-tion. Thus, rather than using standard statisti-cal tests, which would only test for differenceof means, we apply more stringent criteria thatrequire diagnostic differences in vocal char-acters to represent discrete, non-overlappingcharacter states, as described in detail in earlierstudies (Isler et al. 1998, 1999). In the case ofcontinuous variables, ranges of sample valuescannot overlap, and the means (x) and stan-dard deviations (SD) of the population with thesmaller set of measurements (a) and the popula-tion with the larger set of measurements (b) hadto meet the requirement:

xa+ taSDaxb tbSDb (1)

where ti = t-score at the 97.5 percentile of thet distribution for n 1 degrees of freedom(except for ratios, for which this statistical testis inappropriate). Visual and mensural charac-ters were selected to distinguish populationsof each pair only if they were considered inde-pendent. This required careful judgments ofwhether variation in one character could occurwithout resulting in a different outcome foranother character. If two characters appearedto be highly dependent, one was selected thatappeared most appropriate to the vocaliza-tion type. For example, because common callscomprised only a few notes that afforded a


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limited number of comparable measurements,visually defined characters were deemed moreinformative.

On the basis of vocal distinctions among con-solidated populations, we assessed their taxo-nomic status, employing guidelines developedin previous studies. We recommended speciesstatus under the Biological Species Concept forpopulations that differed diagnostically in bothvocalizations and morphology (Johnson et al.1999). Using a study of vocalizations of syn-topic, congeneric species-pairs of antbirds andsubsequent applications (Isler et al. 1998, 1999,2001) as a point of reference, vocal differences

between allopatric populations were consid-ered diagnostic at the species level if they werereflected in at least three independent vocal

characters. As noted above, current subspeciesdefinitions were accepted as representing diag-nostic morphological differences. Existing taxathat did not meet vocal requirements for con-sideration as a distinct species were maintainedas subspecies pending results of the parallelmolecular study. Future studies will describethe results of the molecular analysis, review theresults of the vocal analysis in this context, and,eventually, estimate a phylogeny for the H. can-tatorcomplex based on both data sets.

R

Diagnostic differences were identified inmale loudsongs, female loudsongs, commoncalls, and chit calls. No differences in chirrswere found between populations. Chirrs wererecorded for 17 subpopulations but not forsaturata2, peruviana1, peruviana2, peruviana4,

peruviana5, subflava, collinsi, and affi nis2. Giventhat chirrs tended to be the least frequentlyrecorded vocalization type, their absence fromthe sample of some populations repertoriesmay be a sampling artifact. However, the lack ofchirrs in the recordings of subflavaand collinsi,for which there were large samples, may proveto be taxonomically relevant.

No diagnostic vocal differences were identi-fied in pairwise comparisons of subpopulations(Fig. 1), with one exception: a difference incommon calls was found between implicata2andthe remaining subpopulations of implicata. Someother subpopulation comparisons, however, wereconstrained by small sample sizes, and althoughthere were other pairwise comparisons in which

ranges of values did not overlap, these did notmeet our statistical test. These differences will bere-examined in the future, when the results of the

ongoing genetic study are available.As a consequence of the pairwise comparisons

of subpopulations, implicata vocal data weremaintained in two populations, but data for allother subpopulations were consolidated into tenexisting subspecies (no recordings were availablefor perflava) in the following round of analysis.Although vocalizations of most subspecies dif-fered diagnostically in multiple characters, pair-wise comparisons revealed no diagnostic vocaldifferences between notaeaand cantator, saturataand peruviana, collinsi and subflava, or implicata(excluding implicata2) and affi nis. It is especiallynoteworthy that neither loudsongs nor common

calls distinguished vocalizations between mem-bers of these four pairs of taxa.

In the final stage, subspecies for which therewere no diagnosable vocal differences wereconsolidated, resulting in nine taxa, which,using the principle of priority, were desig-nated as: cantator (including notaea), flavescens (including perflava, on the basis of range andplumage characteristics), peruviana (includingsaturata), subflava (including collinsi), ochrogyna,implicata, taxon novum(= implicata2), striata, andaffi nis. Each taxon was distinguished from everyother by at least two vocal characters, except forimplicataand affi nis, which were maintained astaxa because their geographic ranges appearedto be disjunct, separated by striata. Geographicranges are depicted in Figure 2. Range bound-aries were based on specimen as well as onvocalization information and reflect resolu-tion of some ambiguities or inaccuracies (e.g.,contrary to Peters [1951], the Rio Madeira andRio Tapajs delimited the western and easternlimits, respectively, of implicata).

Table 1 provides the aggregated numbers ofdiagnostic vocal characters distinguishing pairsof taxa. Vocal characters underlying these num-

bers are provided in Appendix 2 (online; seeAcknowledgments), along with supporting data.The following descriptive summary points outsalient, primarily visual, differences in diagnosticcharacters. It uses groupings of taxa to facilitatecomparisons. These groupings do not necessar-ily reflect estimates of phylogeny, which will bedeveloped subsequently.

Male loudsongs.All populations delivereda series of clear notes ending with one or more


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raspy notes (which were omied occasionally).Measurements were confined to the series ofclear notes because of intra-individual inconsis-tency in number and structure of raspy notes.Male loudsongs (Fig. 3) fell into three groupsaccording to change in pace. Male loudsongs offive taxa (cantator, taxon novum, implicata, striata,and affi nis) accelerated (except for one individualeach of cantatorand implicata, which had aberrantsongs); those of three taxa (flavescens, peruviana,

and subflava) decelerated; and ochrogynahad rela-tively evenly paced loudsongs.

Male loudsongs of taxon novum, implicata,striata, and affi nisof southeast Amazonia beganwith a long downslurred note followed byan accelerating series of abrupt notes. Theserapidly delivered vocalizations almost alwaysconsisted of at least 7 clear notes, and usually9 or 10. Notes following the initial note weredownslurred or boxy. Within the group, only

F. 2. Geographic distributions of taxa found to differ in at least one vocal character from allother populations; vocalizations of implicata and affinis were not distinguishable. Open circles =specimen locations; open stars = recording locations, most of which are also specimen locations;1 = cantator, 2 = flavescens, 3 = peruviana, 4 = subflava, 5 = ochrogyna, 6a = taxon novum, 6b = implicata,6c = striata, and 6d = affinis. Ranges of subflavaandperuvianaoverlap in the hatched area and nearthe location labeled A where these taxa have been observed in sympatry; double lines to thenorth and south of A represent apparent altitudinal parapatry. Parapatry without any majorphysical barrier also appears to occur between flavescensand cantator in the southeastern cornerof Venezuela, located by letter B on map. Question marks identify regions lacking data where aform in the complex may occur.


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male loudsongs of striatadiffered diagnosticallyin having more abrupt notes whose frequencypeaks fell toward the end of the series.

Differences between male loudsongs of can-tator (the fih population whose notes acceler-ated) and the above southeastern Amazoniantaxa were evident visually. Notes in the cantatorloudsong could be placed in three groups: a shortinitial note, two to six notes of similar shape andpeak frequency but at a lower peak frequencythan the initial note, and an abrupt shi to athird group of one to four similar notes at aneven higher peak frequency than the initial note.

Male loudsongs ofperuvianaand subflavawerenot distinguishable from one another. The decel-erating loudsongs of these two taxa differed fromthe accelerating loudsongs of taxa in southeast-

ern Amazonia in multiple characters, but wereclosest to those of cantator. In contrast to cantatornotes, which abruptly changed shape and peakfrequency, note changes inperuvianaand subflavaloudsongs were gradual, broadening in approxi-mately even steps. In uncommon examples of

peruvianaand subflavathat had sudden shis innote shape, only a single shi occurred, ratherthan two as in cantator, and subsequent noteswidened gradually as in typical songs.

Like those of peruviana and subflava, maleloudsongs of flavescens decelerated, but shapesof initialflavescens notes were boxy, with a nar-row frequency range. Through the middle por-tion of the vocalization, notes became broader,frequency-modulated, and downslurred, endingwith distinctive long, burry, and downslurrednotes. Note peaks remained flat in frequency orgradually rose slightly while the boom of thenotes extended downward in frequency.

The final population, ochrogyna, showed theleast change of pace in male loudsong. It wasreadily distinguished from all other taxa byfrequency paern, with the peaks of its initialfour to six notes increasing gradually. Exceptfor southeastern Amazonian populations,loudsongs of ochrogyna also differed by hav-ing an initial note that was substantially longerthan the clear notes that followed. It was dis-tinguished from the southeastern Amazonianpopulations by its U-shaped notes.

Female loudsongs.Female loudsongs (Fig.4) of all populations were similar, a descend-ing series of 6 to 9 (extremes 412) notes, easilydistinguished from male loudsongs. They wereoen delivered in response to loudsongs of

T.1.Num

berofvocalcharactersdistinguishingpopulationsidentifiedasdistinctinStage1.Initialnumberisthetotalnumber

ofindepen

dentdiagnosticcharactersandisfollowedbynumberofdiagnosticcharacter

sforeachvocalizationtype.M=male

loudsongs

;F=femaleloudsongs;C=calls,includingbothcommoncallsandchitcalls.Ifaleerisomied,nodiagnostic

differencesinthatvocalizationtypewerefound.

CharactersareidentifiedinAppendix

2(online;seeAcknowledgments).

flavescens

peruviana

subflava

ochropyga

taxonnov.

implicata

striata

affinis

cantator

5/M3C2

3/M1C2

4/M1F1C2

6/M2F2C2

7/M4F1C2

8/M4

F2C2

9/M5F2C2

6/M4C2

flavescens

3/M1C2

5/M2C3

8/M2F4C2

9/M4F3C2

6/M1

F3C2

13M6F5C2

6/M2F2C2

peruviana

3/C3

4/M3F1

11/M7F2C2

7/M3

F2C2

12/M8F2C2

10/M6F2C2

subflava

9/M4F2C3

11/M8C3

6/M3

C3

13/M7F3C3

9/M5F1C3

ochrogyna

6/M3F1C2

4/M2

C2

9/M5F2C2

4/M2C2

taxonnovum

2/C2

4/M2C2

2/C2

implicata

3/M2C1

0

striata

2/M1C1


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F.3.Maleloudson

gsoftheHypocnemiscantatorcomplex

.Arrowsidentifythefirstnotesthatw

ereconsideredraspy(seetext).(A)cantator

90kmnorthofManaus,Amazonas,Brazil(WhitneyISL-BM

W.189:24).(B)flavescensFrentedelaI

slaCigarrn,Amazonas,Venezuela(S

chwartz

ML62045).(C)peruvia

naSantaRita,Loreto,Peru(WhitneyISL-BMW.187:02).(D)subflavaSana

marca,Ayacucho,Peru(WiddowsonSterling

ISL-BW&JS.1:06).(E)ochrogynaVilaBeladaSantssimaTrin

dade,MT,Brazil(WhitneyISL-BMW.190:10).(F)implicataBorba,Amazona

s,Brazil

(WhitneyISL-BMW.18

8:12).(G)taxonnovumViladoCarmo

,Amazonas,Brazil(WhitneyISL-BMW.197:17).(H)striata15kmsouthofA

ltamira,

Par,Brazil(WhitneyISL-BMW.178:06).(I)affinisSerradosC

arajs,Par,Brazil(WhitneyISL.BMW.6:12).


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F.4.FemaleloudsongsoftheHypocnemiscantatorcompl

ex.Arrowsidentifythefirstnotesthatwereconsideredraspy(seetext).(A)canta-

torBrownsbergNatureReserve,Suriname(WhitneyISL-BM

W.119:26).(B)flavescensFrentedelaIslaCigarrn,Amazonas,Venezuela(Schwartz

ML62045).(C)peruvianaYarapaReserve,Loreto,Peru(WhitneyISL-BMW.163:05).(D)subflavaSan

amarca,Ayacucho,Peru(WiddowsonSterling

ISL-BW&JS.1:06).(E)oc

hrogynaSerradosPacasNovos,Rondnia,Brazil(WhittakerISL-AW.7:23).

(F)implicataCaima,Par,Brazil(WhitneyISL-

BMW.158:17).(G)taxon

novumViladoCarmo,Amazonas,Brazil(WhitneyISL-BMW.197:14).(H)stria

taRurpolis,Par,Brazil(P.IslerML4

7910).(I)

affinisCaxiuan,Par,Brazil(ZimmerISL-KJZ.85:22).


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their mates and typically started immediatelybefore or as the male loudsong ended. Noteshapes were similar in all populations; initial

notes were usually downslurred and shadedgradually into terminal notes, which wereshaped like an inverted U. Note shapes offlave-scenswere most divergent. These were typicallyrectangular in shape, as shown in the figure, buta few individuals delivered notes resemblingthose of other populations, and, consequently,differences were not considered diagnostic.

Diagnostic differences in female loudsongswere fewer than those found in males: 44 pair-wise comparisons as compared to 132. Themost prevalent character distinguishing femaleloudsongs (Appendix 2) was a shi in note dura-tion, expressed by a ratio between durations of

initial and terminal clear notes. As is evident inthe spectrograms, females of the southeasternAmazonian taxa (taxon novum, implicata, striata,and affi nis) and, to a lesser extent, neighbor-ing ochrogyna, initiated their loudsongs with along note and ended with an abrupt note (set-ting aside terminal raspy notes). Differencesin ratios between first and last notes in canta-tor, peruviana, and subflava were diagnosticallysmaller and, at the extreme, notes of flavescensloudsongs increased in duration. Comparisonsof note duration and overall pace also provideddiagnostic differences, but they were rarer givenlarge within-taxa variances. Note that the inter-vals between notes diminished at a similar rate inall taxa, and a difference in interval duration wasdiagnostic in only one pairwise comparison.

With regard to frequency paern, peak fre-quencies gradually declined in female loud-songs of all taxa, though peaks of the first twonotes were constant or nearly so for most taxa.However, peaks of the first three notes of ochrog-

ynaascended and those of cantatordescended infrequency. Loudsongs of affi nis were lowest infrequency, diagnostically lower in initial notesthan cantatorand subflava.

We documented no diagnostic differencesin pairwise comparisons of female loudsongsamong cantator, flavescens, peruviana, and sub-

flava. Similarly, no diagnostic differences werefound among female loudsongs of taxon novum,implicata,striata, and affi nis.

Common call.Observing Warbling Antbirdsin the wild over many years has revealed thatthe common call (Fig. 5) is an important andfrequently delivered vocalization that may be

employed by both sexes and all age classes in var-ious intraspecific contexts, such as maintenanceof auditory contact between members of pairs or

families and encounters between neighbors. Itwas typically a short (usually 0.51.0 s) series oftwo to five notes. Although female calls of sometaxa tended to contain fewer notes, common callsshowed no other sex-linked differentiation, andsamples from both sexes were combined in theanalyses. Despite the variety of contexts in whichan individual may deliver this call and varia-tion in the number of notes, the great majorityof common calls were highly consistent withinpopulations. Vocal characters were defined visu-ally rather than measured because common callscontained few notes. Except in pairwise compari-sons ofperuvianaand ochrogynaand implicataand

affi nis, common calls of all populations differeddiagnostically in either note shape or frequencypaern, and both were diagnostic in 31 of 36pairwise comparisons. Thus, of all vocalizationtypes, common calls revealed the most consistentvocal differences among taxa.

Common calls of cantatorconsisted of a briefrepetitive series of two to four (most oen three)similar, clear notes having essentially level peakfrequencies (Fig. 5A). Final notes oen becameraspy, but maintained the width and spacing ofclear notes (Fig. 5B). Notes sounded upslurred

because their intensity was greatest at thebeginning of the note. Calls of peruviana, likethose of cantator, typically consisted of two tothree notes (rarely four to six) of approximatelythe same note-duration and spacing. Unlike can-tator, however, the initial two notes differed inshape, the second starting at a higher frequencythan the first and becoming more downslurred(Fig. 5E). When present, the third note was usu-ally identical to the second (Fig. 5F), but thethird note sometimes began at an even higherfrequency and became more downslurred thanthe second note (Fig. 5G). Occasionally, secondand third notes were rounded like cantator, butthe emphasis remained on the downward sideof the note (Fig. 5H). Rarely, the initial note wasreplicated in the second note. In addition, endnotes of peruviana calls rarely became raspy (2of 70 recordings), whereas cantator calls typi-cally ended in raspy notes (22 of 29 recordings).Calls of ochrogyna (Fig. 5KL) fit the paern of

peruviana in having notes following the initialnote becoming more downslurred. However,notes of peruviana calls maintained the same


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F. 5. Calls of the Hypocnemis cantatorcomplex. A through S are common calls and variants. Thelatter illustrate the range of variation and are almost always delivered within series of common calls.T and U exemplify chirrs, which were not found to distinguish taxa. V is an example of a chitcall,which was not found to differ among taxa except for subflava(W). Caption continued on next page.


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width and were almost never raspy, whereasequivalent notes of ochrogyna shortenedand usually became raspy (Fig. 5K; 14 of 20

individuals). We suspect that ochrogyna callswithout raspy endings (Fig. 5L), whose notesshortened like the raspy calls, may have beengiven by females, although notes lengthenedin one aberrant call identified as given by afemale. Without more knowledge of the sourcesof possibly overlapping calls of peruviana andochrogyna, we do not consider that calls of thesetaxa differ diagnosably at this time.

There were also no diagnosable differencesbetween calls of implicata(Fig. 5MO) and affi nis(Fig. 5S). They shared a common call consistingof a relatively long whistled note that was flat ornearly flat in frequency followed by a distinct

interval and an clear, abrupt, downslurred notestarting at a higher frequency than the first. Thesecond note was followed instantaneously by asharply descending, raspy note which typically

began at an even higher frequency (Fig. 5M, S).The abrupt, clear note before the terminal raspynote usually had no overtones. Occasionally, theraspy note was omied (Fig. 5N), and sometimesa downslurred note was inserted, producinga more distinctly three-noted call (Fig. 5O).Common calls of striata(Fig. 5QR) were similar

to those of implicata1and affi nis, though separablein 100% of blind trials. The first note was shortand usually in the shape of a shallow inverted

U (sometimes flaened), and the following notewas raspy and complex (Fig. 5Q). The second andthird notes (if present) were almost always raspy;occasionally, the second note was intermediate

between a clear and raspy note, consisting of ashort clear segment and overlapping harmonicsin a broad frequency band (Fig. 5R).

The common call of flavescens consisted of amedium-to-long, clear note followed by three tonine abrupt, sharply downslurred notes usuallystarting at a higher frequency than the first note(Fig. 5C). The abrupt notes typically maintainedthe same shape and frequency range, but short-ened in length as the series accelerated. In lon-

ger calls of four or more notes, the abrupt notesalso usually dropped in intensity toward theend. Calls of males appeared to be more rapidthan those of females, but sample sizes were toosmall to confirm this difference. Occasionally,female calls were shortened to three or even twonotes and slowed to the point where they weresimilar to those of other populations (Fig. 5D),

but these aberrant calls were always given inseries with more typical calls. No recorded callsofflavescens included raspy terminal notes.

F. 5. Continued. Examples: (A) cantator common call without raspy ending; 90 km north ofManaus, Amazonas, Brazil (Bierregaard ML 42840). (B) cantator common call with raspy ending;Iwokrama Forest Reserve, Guyana (Whitney ISL-BMW.145:31). (C)flavescenscommon call; Cao LaUrbana, Bolvar, Venezuela (Schwartz ML 62038). (D) flavescens variant given by female; P. N. N.Chiribiquete, Caquet, Colombia (M. Alvarez ISL-MAR.4:36). (E) peruviana common two-notedcall; Humait, Amazonas, Brazil (Whitney ISL-BMW.195:05). (F) peruviana common three-notedcall; Limoncocha, Napo, Ecuador (Coffey ISL-BBC.1:24). (G) peruviana variant three-noted call;Catuaba Reserva, Acre, Brazil (Whitney ISL-BMW.141:12). (H)peruvianavariant three-noted call; ElDorado, Loreto, Peru (Whitney ISL-BMW.185:10). (I) subflavacommon call; Amazonia Lodge, Madrede Dios, Peru (Zimmer ISL-KJZ.109:14). (J) subflavacommon call; Catuaba, Acre, Brazil (WhitneyISL-BMW.141:20) (It is unclear whether this call or I is more typical.) (K) ochrogynacommon call;26 km east of Vila Bela da Santssima Trindade, Mato Grosso, Brazil (Whitney ISL-BMW.190:14).(L) ochrogynavariant without raspy ending; 26 km east of Vila Bela da Santssima Trindade, MatoGrosso, Brazil (Whitney ISL-BMW.190:14). (M) implicatacommon call; 25 km west, by road, of Boim,Par, Brazil (Whitney ISL-BMW.107:30). (N) implicatavariant without raspy ending; Prainha Nova,Amazonas, Brazil (Whitney ISL-BMW.195:30). (O) implicatathree-note variant without raspy end-ing; Prainha Nova, Amazonas, Brazil (Whitney ISL-BMW.196:08). (P) taxon novum common call;Manicor, AM, Brazil (Whitney ISL-BMW.187:21). (Q) striatacommon call with raspy chirr; Portodo Meio, Par, Brazil (Whitney ISL-BMW.175:11). (R) striatacommon call with raspy overtones; SoBenedito, Par, Brazil (Whitney ISL-BMW.173:24). (S) affiniscommon call; Caxiuan, Par, Brazil(Zimmer ISL-KJZ.83:04). (T) ochrogyna example of a chirr; Florida, Santa Cruz, Bolivia (WhitneyISL-BMW.199:16). (U) cantatorexample of a chirr; Foengoe Eiland, Suriname (Whitney ISL-BMW.120:06). (V)peruviana example ofchitcall; Quebrada Sucusari, Loreto, Peru (Parker ML 29101). (W) sub-

flava example ofchitcall; Humait Reserva, Acre, Brazil (Whitney ISL-BMW.142:25).


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by D. Lebbin and W. Tori (pers. comm.), who,in studies of the avifauna of Guadua bamboo,need 27 individuals of subflava inside patches

of bamboo, whereas net lines (maintainedfor fewer hours) in nearby forest outside the

bamboo need five peruviana and no subflava.However, further study by N. Seddon and J.Tobias (pers. comm.) at this site found the habi-tat distinction to be less strict. For example, theyfound peruviana territories in the understory ofpalm swamps and in areas containing bamboo,and subflava territories in tangled riverine veg-etation and in areas lacking bamboo; and theyfound that the two forms occasionally inhabitedadjacent territories. Thus, distinctions in habi-tat preferences between the two forms remainunclearan important subject for future field

work. Syntopy of peruviana and subflava hasalso been reported in Peru from near Pozuzo(1004S, 7532W), Pasco (T. Schulenbergpers. comm.), and at Cuzco Amazonica Lodge(1233S, 6903W), Madre de Dios (T. J. Davispers. comm.), but habitat distinctions were notstudied at these sites.

Whether they inhabit adjacent territoriesor not, it appears that reproductive-isolationmechanisms between peruviana and subflavahave remained operative following secondarycontact over a fairly extensive area in the south-western corner of Amazonia. Given this rangeoverlap, and the close similarities in loudsongsand behavior of these taxa, we expect that somevery limited hybridization between peruvianaand subflava eventually may be documented,as suspected in the mixed pair observed bySchulenberg, cited above. Phenotypic distinc-tions we have been able to identify betweenthem in the field are white versus yellow throatand breast, leg color (usually bluish-gray in

peruviana, greenish-yellow in subflava), thehighly differentiated common call (Fig. 5, EHvs. IJ), the difference in chitcall, and the appar-ent absence of a chirr call in the vocal repertoireof subflava.

Parapatry of cantator and flavescens.Evidence of parapatry between these taxain southeastern Venezuela was provided

by specimens deposited in the ColeccinOrnitologia Phelps (COP). Taxon identifica-tion was substantiated by the authors usingspecimen photographs. Both taxa have beencollected on or adjacent to a plateau (knownas the Macizo de Chimant) situated between

the southwestern corner of La Gran Sabanaand the Sierra Pacaraima in the headwaters ofthe Ro Caron (region identified by B in Fig.

2). Specimens of cantatorwere collected on thewestern and northern edge of this plateau at RoCaruai (= Kariay), Ro Apcara, and Chimant-tepu. Specimens of flavescens were obtainedat Salto Arebuchi (= Aripichi?), Acopn-tepu,Ro Icabar, Santa Elena de Uairn, and Parai-tepu. In particular, the Ro Caruai (location forcantator) adjoins Acopn-tepu (location for fla-vescens) at its base. Although precise geographiccoordinates are unavailable for most of theselocalities, they do not appear to be isolated bymajor topographic features, though they mayrepresent different ecosystems. Additional fieldwork is needed to understand the biogeography

of cantatorandflavescens in this region.

D C

The number of vocal characters distinguish-ing most pairs of H. cantator subspecies wassubstantial, in most cases greater than thosedocumented for syntopic pairs of congenericthamnophilid species in an earlier study (Isleret al. 1998). All three principal types of vocaliza-tions (male loudsongs, female loudsongs, andcommon calls) differed diagnosably in 19 of 36pairwise comparisons (Table 1). Most surprisingwas the finding that calls differed diagnosablyin all but two pairwise comparisons, and aspecific result of particular interest was that thevocalizations of the only pair of subspecies nowknown to exist in syntopy (peruviana and sub-

flava) differed diagnostically only in the struc-ture of their calls. Whether these findings reflectthat calls rather than songs function in matechoice or species recognition is a question forfuture field studies using experimental designs,such as mate-removal experiments, necessaryfor understanding vocal behavior and evolutionin the Thamnophilidae.

On the basis of vocal differences describedherein and morphological differences described

by earlier authors, we recommend that the H.cantator complex be considered at this time toconsist of six species:

Hypocnemis cantator(Boddaert)Guianan Warbling-Antbird

H. c. notaeaHellmayrH. c. cantator(Boddaert)


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Hypocnemis flavescensSclaterImeri Warbling-Antbird

H. f. flavescensSclater

H. f. perflavaPinto

Hypocnemis peruvianaTaczanowskiPeruvian Warbling-Antbird

H. p. saturataCarrikerH. p. peruvianaTaczanowski

Hypocnemis subflavaCabanisYellow-breasted Warbling-Antbird

H. s. subflavaCabanisH. s. collinsiCherrie

Hypocnemis ochrogynaZimmerRondonia Warbling-Antbird

Hypocnemis striata(Spix)Spixs Warbling-Antbird

H. s. taxon novumH. s. implicataZimmer

H. s. striata(Spix)H. s. affi nis Zimmer

From the perspective of their vocalizations,we find no reason to maintain notaea, saturata,and collinsi as taxa. However, given the pos-sibility that diagnosable differences may befound between them and cantator,peruviana, andsubflava, respectively, in other suites of charac-ters, we recommend maintaining these taxa assubspecies, awaiting the completion of furthermolecular, morphological, and behavioral stud-ies. We are unable to shed light on the validityofperflava, given the absence of vocal recordings.We also recognize the possibility that furthervocal distinctions will be found within the rangesof proposed species when additional recordingsprovide improved geographic coverage.

Although recommendations regarding canta-tor, flavescens, peruviana, subflava, and ochrogynaare straightforward, the treatment of striataand its four constituent populations is moreproblematic. A paradox is posed in the rela-tionship between implicata and affi nis, whosevocalizations could not be differentiated butwhose ranges appear to be separated by that ofstriata, whose vocalizations differed from both,though striatawas found to differ vocally fromimplicata by three characters and from affi nis

by two, fewer than found in most pairwisecomparisons of taxa recommended for species

status. The importance of this vocal result isburessed by parallel morphological findingsof Zimmer (1932), who discovered minimal

plumage differences between implicata andaffi nis, even though both differed in plumagefrom the geographically intervening striata. Themost likely explanation for this paern is thatstriatahas become genetically isolated relativelyrecently, and that there remains or recently has

been gene flow between implicataand affi nis inthe essentially unstudied region south of therange of striata (identified by a question markin Fig. 2). In the interest of maintaining a con-servative stance, we recommend that implicataand affi nisbe maintained as subspecies of striatauntil further information is available from theregion and the results of molecular analysis can

be added to the data set.A second diffi culty concerns assessing the

status of taxon novum. Although differenceswere not identified in other vocalizations, dif-ferences in the calls of taxon novum and otherpopulations within striata(including affi nisandthe remainder of implicata) were substantial andcomparable to the only known vocal differences

between the syntopicperuvianaand subflava. Wemaintain taxon novumas a subspecies until it isformally described. It is noteworthy that taxonnovumand striata(sensu stricto) differed in fourvocal characters found in male loudsongs aswell as calls.

Further recommendations regarding statusof all taxa within the Warbling Antbird com-plex and estimates of its phylogeny withinthe Thamnophilidae await molecular analysesnow underway. It is now apparent, however,through conservative analysis of vocalizations,that the H. cantatorcomplex has had a long anddynamic evolutionary history, and we are con-fident that this initial revision beer reflects thetaxonomic status of populations in the complexthan current classifications.

A

Supplementary data for this study are avail-able, as Appendices 1 and 2 and Tables 25, athp://www.aou.org/suppl/auk_124_1_isler.pdf.We deeply appreciate the continuing supportof the Macaulay Library, Cornell Laboratoryof Ornithology (G. Budney); National SoundArchive, The British Library (R. Rant); andFlorida State Museum. The many recordists


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who contributed to the effort are identified inAppendix 1, and we are indebted to them all. T.

J. Davis, D. Lebbin, N. Seddon, T. Schulenberg, J.

Tobias, A. Whiaker, and K. Zimmer contributedunpublished information regarding distributionand areas of sympatry of peruvianaand subflavain Peru, and Whiaker also provided informa-tion on the distribution of taxon novumin Brazil.We appreciate the efforts of C. Rodner and C.Milensky to provide photographs of specimensand related data at Coleccin Ornitologa Phelps.

J. Bates and K. Zimmer kindly reviewed earlierdras of the manuscript, and the final manu-script was thoughtfully reviewed by N. Seddonand an anonymous reviewer. National ScienceFoundation grant no. DEB 9974104 to J. M. Batesand S. J. Hacke at the Field Museum of Natural

History helped provide computer equipmentto perform the vocal analyses. We thank FieldGuides, Inc., for support of B.M.W.s field work.

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Species Limits in Antbirds (Thamnophilidae)