ORNITOLOGIA NEOTROPICAL 16: 347–359, 2005 © The Neotropical Ornithological Society

INDEPENDENT EVOLUTION OF TWO DARWINIAN MARSH- DWELLING OVENBIRDS (FURNARIIDAE: LIMNORNIS, LIMNOCTITES)

Storrs L. Olson1, Martin Irestedt2, 3, Per G. P. Ericson2, & Jon Fjeldså4

1Division of , National Museum of Natural History, Smithsonian Institution, P.O. Box 37012, Washington, DC 20013-7012, U.S.A. E-mail: [email protected] 2Department of Vertebrate Zoology and Molecular Systematics Laboratory, Swedish Museum of Natural History, P.O. Box 50007, SE–104 05 Stockholm, Sweden. E-mail: [email protected] & [email protected] 3Department of Zoology, University of Stockholm, SE–106 91 Stockholm, Sweden. 4Vertebrate Department, Zoological Museum, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen Ø, Denmark. E-mail: [email protected]

Resumen. – Evolución independiente de dos horneros de pantano (Furnariidae: Limnornis, Limnoc- tites). – La Pajonalera Pico Curvo (Limnornis curvirostris) y la Pajonalera Pico Recto (Limnoctites rectirostris) son dos especies de hornero de pantano colectados por primera vez por Charles Darwin en . Ambas tienen una distribución limitada a Uruguay, el sur de Brasil y el norte de , área en la cual ocupan hábitat muy diferentes. Descritas originalmente como congéneres debido a sus similitudes en plu- maje, las dos especies han sido consideradas parientes cercanas a pesar de diferencias estructurales obvias entre ambas. Analizamos secuencias de ADN de tres genes de estas dos especies y las comparamos con una amplia variedad de otras especies de Furnariidae y varios grupos externos. Limnoctites rectirostris perte- nece al grupo de especies tradicionalmente agrupadas en Cranoleuca, estando más cercanamente relacio- nada al Curutié Ocráceo (C. sulphurifera) entre las especies muestreadas. Estos resultados están respaldados por vocalizaciones y nidificación. Limnornis curvirostris forma un clado con el Junquero (Phleocryptes mela- nops); este clado tiene al Macuquiño (Lochmias nematura) como grupo hermano. Una relación cercana entre Limnornis y Phleocryptes es respaldada por el color azul de los huevos y la arquitectura del nido, la cual es apa- rentemente única en estos dos géneros. Abstract. – The Curve-billed Reedhaunter (Limnornis curvirostris) and the Straight-billed Reedhaunter (Lim- noctites rectirostris) are marsh-dwelling ovenbirds that were first collected by Charles Darwin in Uruguay. Each has a limited distribution in southernmost , Uruguay, and northern Argentina, within which the birds occupy very distinct habitats. Originally described as congeners because of overall similarity of plum- age, the two have been treated as close relatives through most of their history despite obvious structural differences. We analyzed DNA sequences from three different genes of these species, compar- ing them with a wide variety of other species of Furnariidae and several outgroup taxa. Limnoctites rectirostris belongs among the species traditionally placed in Cranioleuca, being most closely related to the marsh- dwelling Sulphur-throated Spinetail (C. sulphurifera) among the species we sampled. This is supported by vocalizations and nidification. Limnornis curvirostris forms a clade with the Wren-like Rushbird (Phleocryptes melanops), with the Sharp-tailed Streamcreeper (Lochmias nematura) as a rather distant sister-taxon. A close relationship between Limnornis and Phleocryptes is supported by the apparently unique nest architecture and blue-green egg color. Accepted 5 April 2005. Key words: Furnariidae, Limnoctites, Limnornis, molecular systematics, nidification, ovenbirds.

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INTRODUCTION We decided to test this hypothesis by review- ing the information on morphology, ecology, Charles Darwin was the first naturalist to col- and nidification, and by comparing this with lect two paludicolous species of ovenbirds new molecular evidence. that are now known to be of very limited dis- tribution in southeastern . SYNOPSIS OF MORPHOLOGY AND These were obtained in June 1833 (Steinhe- NOMENCLATURAL HISTORY imer 2004; not 1832 as per Vaurie 1980: 211) in what is now the province of Maldonado in Both reedhaunters are plain brownish or dull the Republica Oriental del Uruguay. When rufous above, with rufous tails, dull whitish John Gould (1839: 80–81, pll. 25–26) identi- undersides, and no adornment apart from a fied and described the birds from the voyage whitish superciliary stripe. Limnornis curviros- of H. M. S. Beagle, he created a new , tris is a reasonably robust (26.7–33.3 g, Limnornis, for these two species, calling the mean 29.0 g, n = 10, according to USNM first L. rectirostris, for its very straight, pointed specimen data; mean of 21 eggs 24.6 x 17.9 bill, and the second L. curvirostris, for its bill mm, according to Narosky et al. 1983) with a with a more typically curved tip. In English longish, rounded tail and a stout, curved bill. these species are now called the Straight- It has very much the appearance of a drab billed and the Curve-billed reedhaunters, version of one of the smaller species of Fur- respectively. narius. Limnoctites rectirostris is a much slighter Both species were said by Darwin (in bird (15.6–24.5 g, mean 19.2 g, n = 5, accord- Gould 1839:80–81) to live in the same habitat ing to USNM specimen data [the heaviest was “amongst the reeds on the borders of lakes” a very fat laying female]; mean of 3 eggs 20.3 and that he was “unable to point out any dif- X 15.3 mm, according to Ricci & Ricci 1984) ferences” in the habits of the two. This mis- with an extremely long, straight, slender bill, taken impression probably colored much of and a shorter, graduated tail with very the subsequent thinking about these birds. pointed, usually worn, rectrices. The nomen- Apart from the supposedly shared habitat, the clatural history of the two species has main similarity between the two reedhaunters revolved around whether to emphasize their is in general coloration and plumage pattern. similarities or their differences. This is doubtless what lead Gould (1839) to Gould (1839) did not designate a type his original decision to place them both in the species for Limnornis and Gray (1840) subse- same genus and also why Vaurie (1980) rather quently selected L. curvirostris as the genotype. vigorously defended this course. On the other Sclater (1889) overlooked Gray’s action and hand, there are manifest differences between applied a new name, Limnophyes, to L. curviros- the two, so that they have most often been tris, reserving the name Limnornis for L. rec- placed in separate monotypic genera (Limnor- tirostris. But Limnophyes was preoccupied by a nis and Limnoctites). Regardless, the two genus of Diptera, so Oberholser (1899) pro- reedhaunters first collected by Darwin have posed Thryolegus as a replacement. Hellmayr long been regarded as each other’s closest rel- (1925) pointed out Gray’s (1840) type desig- ative. This also appeared to receive support nation, returned curvirostris to Limnornis, and from a phylogenetic analysis of nest structure proposed the new generic name Limnoctites (Zyskowski & Prum 1999) in which Limnornis for L. rectirostris. Since then, most authors and Limnoctites were said to form a group with have maintained the two species in monotypic the Wren-like Rushbird (Phleocryptes melanops). genera, usually placing them next to one

348 EVOLUTION OF TWO MARSH-DWELLING OVENBIRDS another. Argentina, by W. H. Hudson (Sclater & Salvin The first exception appears to be Esteban 1868). Durnford (1877: 182) found the spe- (1949), who advocated removing Limnoctites cies common in the same province and was rectirostris to the subfamily Synallaxinae near “at a loss to understand how this bird could Certhiaxis, presumably leaving Limnornis curvi- have escaped the observation of naturalists till rostris in the Philydorinae, where both were Mr. Darwin’s visit to South America.” Addi- placed by Sclater (1890). Peters (1951) also tional specimens were obtained in Uruguay dissociated the two, placing Limnornis immedi- (Sclater & Hudson 1888, Sclater 1890, Hell- ately after Furnarius, with 12 genera between it mayr 1925), Sanborn’s (1929) assertion that and Limnoctites, which was placed between Cer- his 1926 specimens from Uruguay were the thiaxis and Poecilurus/Cranioleuca. Although first since Darwin being erroneous. By 1899, Meyer de Schauensee (1966) followed Peters’ the range of the species was extended to Rio sequence almost exactly, one of his few depar- Grande do Sul, Brazil (Ihering 1899). tures was to place Limnoctites immediately after Although Darwin stated (in Gould 1839) Limnornis. Vaurie (1971, 1980) and Sibley & that the two reedhaunters occurred together Monroe (1990) returned to the original Goul- and Vaurie (1980: 212) asserted that “L. rec- dian nomenclature and combined both spe- tirostris shares the same habitat [as L. curviros- cies in Limnornis. Other authors (e.g., Ridgely tris], but its requirements are less rigid,” this is & Tudor 1994) have preferred to emphasize not, in fact, the case. Ridgely & Tudor (1994: differences by recognizing two genera for the 61) note that the two species “appear never to reed-haunters, although still maintaining their occur together in the same marsh.” Belton close association. Remsen (2003) maintained (1984: 622) shows no overlap in range them as adjacent in his linear sequence but between the species in Rio Grande do Sul, noted that differences in tail structure, nesting Brazil. Olson has experience with L. curviros- materials, and egg color called into question tris in Argentina, and with both species their proposed sister relationship. through much of Uruguay, and has not yet visited a site where both species might be DISTRIBUTION AND HABITAT expected to occur in proximity. Limnoctites rectirostris typically occurs in For nearly a century, Darwin’s original two marshes. Although a variety of may specimens of L. rectirostris were the only ones occur in such sites, particularly at the edges, known. Sanborn (1929) next obtained the the bird is found only where the spiny cara- species at another locality in Uruguay in 1926. guatá, Eryngium spp., dominates. In the orni- Gradually, its range was extended from the thological literature this has erroneously provinces of Entre Rios and Buenos Aires, been referred to as a sedge (e.g., Ridgely & Argentina, to Rio Grande do Sul and Santa Tudor 1994, Remsen 2003: 226, but correctly Catarina, in southernmost Brazil, and the spe- as an “apiaceous herb” on 261) or a grass cies was also found more extensively in Uru- (Gerzenstein & Achaval 1967, Vaurie 1980, guay (Daguerre 1933, Pereyra 1938, Esteban Babarskas & Fraga 1998). It is actually a dicot 1949, Escalante 1956, Gerzenstein & Achaval that belongs in the carrot family (Apiaceae or 1967, Zorilla de San Martin 1963, Alda do Umbelliferae). Ricci & Ricci (1984: 205) cor- Rosário 1996, Babarskas & Fraga 1998). rectly describe the plants as growing in “bro- After Darwin’s original collection, Limnor- meliad-like rosettes,” the leaves of which are nis curvirostris was next collected from 1866 to beset with sharp spines that make the pursuit 1868 at Conchitas, Buenos Aires Province, of birds in this habitat a decided challenge to

349 OLSON ET AL. the ornithologist’s flesh and clothing. The basis of their supposedly building a domed species that have been mentioned in connec- nest with “a small awning over the nest tion with Limnoctites are Eryngium horridum entrance” (p. 899). The nest of Limnornis curvi- (Belton 1984, Remsen 2003), E. pandanifolium rostris is described by von Ihering (1902) and (Gerzenstein & Achaval 1967, Babarskas & Belton (1984); that of Limnoctites rectirostris by Fraga 1998, Remsen 2003), and E. eburneum Daguerre (1933), Ricci & Ricci (1984) and (Ricci & Ricci 1984). The ranges of these Sick (1993); and those of both species in Vau- plants are given as southern Brazil to NE rie (1980) and Narosky et al. (1983). Included Argentina, with the last two extending to Par- here are all the references cited by Zyskowski aguay (Cabrera 1965). & Prum (1999), plus some others, but none That the birds are tied to the plant and mentions an awning over the entrance of the not necessarily to marshy environments is nest of Limnoctites. This error came about shown by their occurrence at 200 to 250 m in from misinterpretation (K. Zyskowski pers. rocky scrub forest where Eryngium pandanifo- com. to Olson, June 2004) of photographs of lium occurs in 5 to 20 m wide patches along the nest of Phylloscartes ventralis in the article streams (Gerzenstein & Achaval 1967). That preceding the paper by Ricci & Ricci that L. rectirostris occurs as high as 1100 m (Ridgely were erroneously captioned as Limnoctites. & Tudor 1994, BirdLife International 2000, Zyskowski (pers. com. ibid.) has since found Remsen 2003) is presumably based on the and photographed a nest of L. rectirostris in populations in Aparados da Serra National Uruguay and confirmed that it does not have Park mentioned by Belton (1984: 621), an awning. Remsen (2003) took his descrip- though no substantive documentation of their tions of the nests of both reedhaunters as occurring so high appears to exist. having awnings from Zyskowski & Prum Although also a marsh bird, L. curvirostris (1999). is found in extensive reedbeds, especially of The first mention of an “awning” being the giant sedge or pajonal (Scirpus giganteus), constructed by Limnornis curvirostris appears to the grass known as espadaña (Zizaniopsis bona- be that in one of two nests of described by riensis), and also cattails (Typha). Although its Narosky (in Vaurie 1980: 213). Later, Narosky briefly stated range from Rio Grande do Sul et al. (1983: 36) confirmed that the nest of L. to Buenos Aires is the same as that of L. rec- curvirostris “possesses, like that of the junquero tirostris, within that area it is much the more Ph[leocryptes] melanops, a 3 cm projection or abundant and widespread of the two species eave above the mouth of the entrance” (our because of the greater extent of its habitat. translation). In summary, although the distributions of On the other hand, it does seem that the the two reedhaunters are superficially similar, basic nest structure of Limnornis and Phleo- they are adapted to distinct habitats and are cryptes is similar, best exemplified by Narosky’s probably never syntopic. descriptions in Vaurie (1980). Phleocryptes pre- sents a presumably more derived condition in NIDIFICATION covering its nest with mud. The vast majority of species of Furnari- Nest structure in the Furnariidae is extremely idae have pure white eggs, although the eggs diverse and has been used to devise a phylog- in a few species of Synallaxis may have a light eny of the family (Zyskowski & Prum 1999). bluish, greenish or yellowish cast (Schönwet- In this phylogeny, Limnornis and Limnoctites ter & Meise 1967: 12, Sick 1993: 428). In con- were grouped with Phleocryptes melanops on the trast, the eggs of Limnornis curvirostris and

350 EVOLUTION OF TWO MARSH-DWELLING OVENBIRDS d d d d d d d d d d d d d d d d d d d al History; G3PDH r ding to ding to two AY590097 AY590065 AY590066 AY590078 AY590081 AY590076 AY590077 AY590072 AY590070 AY590073 AY590069 AY590068 AY590063 AY590080 AY590088 AY590093 AY590087 AY590092 AY590095 AY590096 r a c a a a a a a a a a a a a a a a d d d b Myoglobin AY064255 AY065756 AY065755 AY065758 AY065757 AY065765 AY065761 AY065766 AY065764 AY065763 AY065772 AY065768 AY065771 AY065776 AY065774 AY065773 AY590054 AY590058 AY590053 AY065770 AY065769 AY065769 b c a a a a a a a a a a a a a a a a d d d b AY064279 AY065700 AY065699 AY065702 AY065701 AY065709 AY065705 AY065710 AY065708 AY065707 AY065715 AY065711 AY065712 AY065714 AY065718 AY065717 AY065716 AY590044 AY590048 AY590043 AY065713 Cytochrome amily designations are given acco amily are given designations rk; NRM = Swedish Museum of Natu Museum of Swedish NRM = rk; Voucher no. Voucher ZMUC S220 ZMUC S439 ZMUC S428 ZMUC S150 ZMUC S292 ZMUC S540 NRM 966772 NRM 937251 NRM 937334 NRM 966903 NRM 966910 NRM 966821 NRM 956643 NRM 937258 NRM 966930 NRM 966847 NRM 976662 NRM 967031 ZMUC S2577 ZMUC S2053 USNM B2735 USNM B2734 ZMUC 125590 ZMUC 124797 USNM B17199 USNM B14895 AMNH RTC467 . (2005). et al et Fjeldså d in the study. Family and subf Family in the study. . (2002), seum of Natural History, Yo New History, seum Natural of et al Classif. by Remsen (2003) Remsen by Classif. Furnariidae: Furnariinae Furnariidae: Furnariinae Furnariidae: Furnariinae Furnariidae: Furnariinae Furnariidae: Philydorinae Furnariidae: Philydorinae Furnariidae: Philydorinae Furnariidae: Philydorinae Furnariidae: Synallaxinae Furnariidae: Synallaxinae Furnariidae: Synallaxinae Furnariidae: Synallaxinae Furnariidae: Synallaxinae Furnariidae: Synallaxinae Furnariidae: Synallaxinae Furnariidae: Synallaxinae Furnariidae: Synallaxinae Furnariidae: Synallaxinae Furnariidae: Furnariinae Furnariidae: Philydorinae Dendrocolaptidae Dendrocolaptidae Dendrocolaptidae Dendrocolaptidae Formicariidae Rhinocryptidae Rhinocryptidae Ericson c . (2002, in press) . (in press), press), . (in et al et al Irestedt b Classif. by Irestedt Irestedt by Classif. Furnariidae: Furnariinae Furnariidae: Furnariinae Furnariidae: Furnariinae Furnariidae: Furnariinae Furnariidae: Furnariinae Furnariidae: Furnariinae Furnariidae: Furnariinae Furnariidae: Furnariinae Furnariidae: Furnariinae Furnariidae: Furnariinae Furnariidae: Furnariinae Furnariidae: Furnariinae Furnariidae: Furnariinae Furnariidae: Furnariinae Furnariidae: Furnariinae Furnariidae: Furnariinae Furnariidae: Furnariinae Furnariidae: Furnariinae Furnariidae: Sclerurinae Furnariidae: Sclerurinae Furnariidae: Dendrocolaptinae Furnariidae: Dendrocolaptinae Furnariidae: Dendrocolaptinae Furnariidae: Dendrocolaptinae Formicariidae Rhinocryptidae Rhinocryptidae . (2001), et al (*) Irestedt iseicapillus iseicapillus a 1. Specimen 1. data and Genbank accession numbers for samples used Species fuscus Cinclodes Furnarius cristatus Furnarius leucopus Upucerthia jelskii Automolus leucophthalmus Lochmias nematura atricapillus Philydor flammulatus Thripadectes Anumbius annumbi cactorumAsthenes Coryphistera alaudina Cranioleuca albicapilla Cranioleuca pyrrhophia Cranioleuca sulphurifera ruficapillaSynallaxis Limnocites rectirostris Limnornis curvirostris Phleocryptes melanops tenuirostris Geositta Sclerurus scansor Drymornis bridgesii Xiphocolaptes major Dendrocincla tyrannina gr Sittasomus meruloides Chamaeza Pteroptochos tarnii Scytalopus spillmanni TABLE Acronyms: classificationalternative AMNH = American schemes. Mu USNM = National Museum Smithsonian of NaturalInstitution; History, ZMUC = Zoological Museum of theof University Copenhagen. References:

351 OLSON ET AL.

Phleocryptes melanops are a deep greenish-blue herein) and the woodcreepers (Irestedt et al. (Schönwetter & Meise 1967: 12; Vaurie 1980). 2002, Chesser 2004, Fjeldså et al. 2005). Serv- We reviewed the egg color of at least 32 gen- ing as outgroups are three representatives of era of Furnariidae, mainly based on the col- the proposed sister clade of Furnariidae lections of the British Museum (Michael (Irestedt et al., 2002, Chesser 2004): Pteropto- Walters, pers. com. to Olson, June 2004) and chos tarnii and Scytalopus spillmanni (family Rhi- scattered references in more recent literature nocryptidae) and Chamaeza meruloides (family and found no exceptions to the preceding Formicariidae). Sample identifications and observations. Thus, the decidedly greenish GenBank accession numbers are given in blue eggs of Limnornis curvirostris and Phleoc- Table 1. ryptes appear to be unique within the Furnari- We sequenced the complete myoglobin idae, a similarity noticed at least as early as intron 2 (along with 13 bp and 10 bp of the Pereyra (1938). flanking regions of exons 2 and 3, respec- In contrast, the nest and eggs of Limnoc- tively), the complete glyceraldehydes-3-phos- tites rectirostris have been likened to that of phodehydrogenase (G3PDH) intron 11 Cranioleuca. “The [white] eggs and nest more (along with 36 bp and 18 bp of exons 11 and closely resemble those of C. sulphurifera than 12, respectively), and 999 bp from the cyto- those of L. curvirostris, whose eggs are bluish chrome b gene (see Ericson et al. 2002, green and the nest [of L. curvirostris], although Irestedt et al. 2002, and Fjeldså et al. 2003, spherical with a lateral entrance, is more con- 2004, for primer sequences and procedures). spicuous for being constructed at consider- Positions where the nucleotide could not be able height (up to 1.6 m), and is without much determined with certainty were coded with differentiation between the external material the appropriate IUPAC code. Due to the and the lining” (translated from López-Lanús low number of insertions in the introns, et al. 1999: 63). the combined sequences could easily be Within the Furnariidae the white eggs and aligned by eye. All gaps in the myoglobin and less elaborate nest of L. rectirostris are proba- the G3PDH sequences were treated as miss- bly plesiomorphic states, or relatively so in the ing data in the analyses. No insertions, dele- case of the nest, the apparently unique tions, stop or nonsense codons were awninged nest and blue-green eggs of L. curvi- observed in any of the cytochrome b rostris and Phleocryptes are derived conditions sequences. that argue for a sister-group relationship for ModelTest 3.06 (Posada & Crandall 1998) these two taxa. in conjunction with PAUP* (Swofford 1998) was used to evaluate the fit of the data to dif- MOLECULAR SYSTEMATICS ferent models for nucleotide substitutions. The GTR+I+Γ model has the best fit for the Materials and methods. Twenty species of oven- combined data set and for the cytochrome b birds and four woodcreepers were selected partition, while GTR+G was selected for for the molecular analysis. In addition to Lim- both the myoglobin intron 2 and the G3PDH nornis and Limnoctites, we included representa- intron 11 partitions. These models were tives of all major clades of furnariids used in the analyses of the individual genes, as identified by Fjeldså et al. (2005), as well as the well in the analysis of the combined data set. genera Sclerurus and Geositta, which form the The posterior probabilities of trees and sister group to a clade consisting of all the parameters in the substitution models other ovenbirds (called “core ovenbirds” were approximated with Markov chain

352 EVOLUTION OF TWO MARSH-DWELLING OVENBIRDS

TABLE 2. Descriptive statistics for the observed pairwise, uncorrected sequence divergencies (p-distances) between selected groups of taxa. Larger distances suggest higher rates of nucleotide substitutions.

Cytochrome b Myoglobin intron 2 G3PDH intron 11 Mean Min. Max. Mean Min. Max. Mean Min. Max. Within core ovenbirds 12.63 2.4 15.62 2.3 0.29 3.62 5.16 0.76 7.73 Core ovenbirds vs woodcreepers 14.53 12.21 17.12 4.17 2.96 5.16 6.84 4.59 8.83 Core ovenbirds vs Sclerurus/Geositta-clade 15.57 13.51 18.12 3.77 2.8 4.92 7.71 4.53 9.63 Core ovenbirds vs Outgroups 17.7 15.84 20.32 7.09 5.67 8.6 9.31 6.68 11.54

Monte Carlo and Metropolis coupling using myoglobin intron 2 and G3PDH intron 11 the program MrBayes (Huelsenbeck & Ron- sequences requires postulation of a few inser- quist 2001, Ronquist & Huelsenbeck 2003). tions and deletion events (indels) among the We ran two analyses of 500,000 genera- core ovenbirds, most of which involve only a tions for each gene with trees sampled every single basepair (singletons) and/or are found 100 generation. The parameter estimates from only in a single taxon (autapomorphic). the two separate MCMC runs for each data The phylogenetic trees obtained from the set were compared and found to be very simi- Bayesian analyses of the individual genetic lar, thus allowing an inference from the con- markers, as well as of the combined data set, catenated output. Posterior probabilities for are generally similar (Figs 1A-C and 2). The the individual genes were based on a total of analyses also agree well on the systematic 9000 trees saved after discarding the trees positions of Limnornis and Limnoctites, which saved during the “burnin phase” (as estimated clearly are not sister taxa. Most major group- graphically) in each analysis. The analysis of ings of ingroup taxa are recovered by all data the combined data set was conducted in the partitions and receive generally high supports same manner as for the individual genes (Table 3). Monophyly of the ingroup is except that the number of generations in each strongly corroborated, as is the basal position run was two millions. The 50% majority-rule of Geositta and Sclerurus relative to the core consensus trees were identical in the runs and ovenbirds and woodcreepers, which in turn the posterior probabilities are based on a total are recovered as sister groups. All data parti- of 390,000 saved trees. tions except cytochrome b also support a basal position among the core ovenbirds of a Results. The concatenated sequences became clade consisting of Automolus, Thripadectes and 2164 basepairs long after alignment. Within Philydor. Although the cytochrome b data set the ingroup (all ovenbirds and woodcreepers) also recognizes monophyly of this clade, it the lengths of the myoglobin sequences range leaves the group unresolved in relation to the from 677 in Philydor to 701 bp in Geositta, and other core ovenbirds. The remaining core the lengths of the G3PDH sequences range ovenbirds are divided into two clades that from 349 in Dendrocincla to 401 bp in Xiphoco- receive strong support in the analyses of laptes. The myoglobin intron is the least varia- most data partitions. Limnornis groups with ble among the three genetic markers studied Phleocryptes with 100% posterior probabilities herein (Table 2). The observed substitution in the analyses of both myoglobin and the rate is larger in the mitochondrial cytochrome genes combined. The analyses of cytochrome b gene, in accordance with previous studies b and G3PDH also suggest a Limnornis-Phleo- (Irestedt et al. 2004). The alignment of the cryptes clade, albeit with weaker support.

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FIG. 1. Majority-rule consensus trees obtained from Bayesian analyses of three genetic markers: A. cyto- chrome b, B. myoglobin intron 2, C. glyceraldehydes-3-phosphodehydrogenase (G3PDH) intron 11. Pos- terior probabilities are indicated at the nodes.

Cinclodes, Lochmias, Upucerthia and the two Asthenes, Anumbius and Coryphistera. Limnoctites species of Furnarius are the other members falls well within the Cranioleuca clade, but of this larger group of core ovenbirds. it groups with different species of Cranio- The other group consists of the three leuca depending on which genetic marker is species of Cranioleuca, Limnoctites, Synallaxis, studied.

354 EVOLUTION OF TWO MARSH-DWELLING OVENBIRDS

FIG. 2. Maximum-likelihood tree calculated from the combined data set (cytochrome b, myoglobin intron 2 and glyceraldehydes-3-phosphodehydrogenase intron 11). Posterior probabilities from the Bayesian analysis are indicated at the nodes.

DISCUSSION and within the sample we tested was closest to the Sulphur-throated Spinetail C. sulphurifera. DNA sequence data unambiguously show This is another marsh-inhabiting species with that Limnornis curvirostris and Limnoctites rectiros- a distribution similar to the two reedhaunters, tris are not particularly closely related. Limnoc- except that it also occurs farther inland and to tites falls out among the species of Cranioleuca the south in Argentina (Remsen 2003). As

355 OLSON ET AL.

TABLE 3. Posterior probabilities for selected nodes obtained in analyses of different data partitions.

Combined Cytochrome b Myoglobin G3PDH 11 data set intron 2 Monophyly of Furnariidae (ovenbirds and 100% 100% 100% 100% woodcreepers) Basal position of a Sclerurus/Geositta-clade 100% 98% 100% 90% Monophyly of core-ovenbirds 100% 100% 100% 100% Basal position of Automolus, Thripadectes and 100% No support, but 92% 93% Philydor among core-ovenbirds no contradition Monophyly of a Cranioleuca spp. and Limnoc- 100% 99% 100% 100% tites clade Sister group relationship between Limnoctites 100% 100% 100% Alternative and Cranioleuca sulphurifera tree topology suggested Sister group relationship of Limnornis and 100% 76% 100% 61% Phleocryptes recounted above, Esteban (1949) advocated sulphurifera, which gives a vocalization of simi- putting Limnoctites in the Synallaxinae. lar length (between 2.5 and 3.5 s) but with a Gerzenstein & Acheval (1967), followed by wider frequency range (between 1 and 6.5 Ricci & Ricci (1984), noted its general similar- kHz) and a greater and more complex quan- ity in appearance to Cranioleuca sulphurifera. tity of elements” (translated from López- López-Lanús et al. (1999) concurred and also Lanús et al. 1999: 62). considered that the vocalizations, nest, and In our molecular phylogeny Limnornis is eggs of Limnoctites were more similar to C. sul- well separated from Limnoctites and its closest phurifera than to Limnornis curvirostris. relative among the taxa we sampled is the In the straight bill and in tail and rectrix Wren-like Rushbird Phleocryptes melanops, with shape, Limnoctites agrees better with Cranio- the Sharp-tailed Streamcreeper Lochmias ne- leuca than with Limnornis. The juvenal plumage matura as the closest outlying sister group. of C. sulphurifera, which lacks the breast There is nothing in the external morphology streaks and yellow throat of the adult, is like of these three genera that suggests a particu- that of Limnoctites in every respect except for larly close relationship. An obligate inhabitant its rufous and black pattern in the wing. of streams in dense forests (Remsen 2003 ), Similarities extend to vocalizations as well. Lochmias differs strikingly from the other two “L. rectirostris gives a hissing trill Ti-ti-ti-ti- in its habits. titititritriiiii, accelerating at the end. This is Phleocryptes, like Limnornis, inhabits marshy maintained at a stable frequency of between 4 reedbeds and the two may occur together in and 6.5 kHz, lasting about 2.5 and 3.5 s, com- the same marsh, although Phleocryptes is much posed of 14 to 18 elements, varying up to 22 more widely distributed, from Pacific Ecua- ... . The territorial advertising vocalization of dor to Chile and east across parts of Bolivia, this species is well differentiated from that of Paraguay, most of Argentina, Uruguay and L. curvirostris, whose song sounds rough and southern Brazil (Remsen 2003). It is a smaller faltering. On the other hand, it could be con- bird with a much more variegated plumage founded by an untrained ear with that of C. than Limnornis. Apart from DNA sequences,

356 EVOLUTION OF TWO MARSH-DWELLING OVENBIRDS the best evidence for a relationship between hypothesis is corroborated by the similar nest these two genera comes from the nests and structure, egg coloration, and to some extent eggs, as outlined above. by the similarity in microhabitat. These two taxa otherwise appear to be sufficiently dis- CONCLUSIONS tinct from one another morphologically and molecularly to justify the recognition of sepa- The available molecular, morphological, and rate monotypic genera. behavioral data all indicate that Limnoctites rec- tirostris belongs among the species currently ACKNOWLEDGMENTS included in the genus Cranioleuca, within which it appears to be most closely related to For assistance in the field in Argentina and another marsh-dwelling species, C. sulphurifera. Uruguay, we are greatly indebted to Joaquin Thus it appears possible that Limnoctites rec- Aldabe, J. Phillip Angle, Luis Chiappe, Miguel tirostris may be a large, paedomorphic (in Clara, Santiago Claramunt, Christina Geb- plumage) derivative of C. sulphurifera that hard, and Christopher Milensky. Jorge moved out of reedbeds and became adapted Cravino, Director, Departamento de Fauna, to marshes of Eryngium, where its long, Montevideo was instrumental in providing straight bill is possibly an adaptation for permits and critical information as well as extracting prey from the spiny rosettes of that arranging for accommodations for fieldwork plant, as suggested by Ricci & Ricci (1984). on numerous estancias in Uruguay, to whose It would be premature, however, to make generous owners we are most grateful. any taxonomic or nomenclatural recommen- George and Janet Winter provided a sumptu- dations until the systematics of the entire ous base of operations for fieldwork in Uru- genus Cranioleuca has been undertaken. guay in 2002. J. V. Remsen, Michael Walters, Zyskowski & Prum (1999) indicate that there and Kristof Zyskowski provided much useful are two distinct groups within Cranioleuca information and references. Field work in based on nest structure, which they designate Argentina and Uruguay was supported by the as the albiceps group and the pyrrhophia group. Virginia Y. Hendry Fund and the Alexander Limnoctites and C. sulphurifera belong to the Wetmore Endowment Fund, Smithsonian pyrrhophia group. The type species of Cranio- Institution, respectively. Samples owned by leuca is C. albiceps and there does not seem to the Swedish Museum of Natural History were be any previously recognized generic name collected in Paraguay in collaboration with the available for the pyrrhophia group (Hellmayr Museo Nacional de Historia Natural del Para- 1925). Thus, if this group were to be sepa- guay, San Lorenzo. The Swedish Research rated generically from Cranioleuca, the 8 spe- Council (grant no. 621-2001-2773 to P.E.) cies now in it would presumably have to take funded the laboratory work. We thank J. V. the name Limnoctites, which would certainly be Remsen and Frank Steinheimer for many use- an ironic turn of events. Another possibility is ful comments on the manuscript. that L. rectirostris and C. sulphurifera may be sufficiently distinct as to be separated in Lim- REFERENCES noctites, so that the rest of the pyrrhophia group would require a new name. Alda do Rosário, L. 1996. As aves em Santa Catar- Our molecular evidence indicates that the ina: distribuição geográfica e meio ambiente. previous intimation of a relationship between Fundação do Meio Ambiente-FATMA, Flori- Limnornis and Phleocryptes is correct. This anópolis, Brazil.

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