Rediscovery of the hummingbird Heliodoxa rubricauda ( Boddaert , 1783 ) ( Aves : Trochilidae ) in Rio Grande do Sul , southern Brazil

We report the rediscovery of the hummingbird Heliodoxa rubricauda (Boddaert, 1783) in the Brazilian state of Rio Grande do Sul after nearly 130 years without confirmed records. We captured 3 males and 1 female, and found 2 other birds (including an immature) at 3 sites in the municipalities of São Francisco de Paula and Cambará do Sul, in the northeast of the state. All records were at the top of the Southern Brazilian Plateau escarpment, at altitudes of about 900 m and near the southern limit of the Atlantic Forest.

The Brazilian Ruby Heliodoxa rubricauda (Boddaert, 1783) is endemic to the Atlantic rainforest of eastern Brazil, ranging from southeastern Bahia south through eastern Minas Gerais and Espírito Santo to Santa Catarina and northeastern Rio Grande do Sul (Schuchmann & Kirwan 2016).It inhabits tropical broadleaf and temperate mixed forests, montane thickets, banana plantations and wooded gardens from sea level to 2,100 m (Sick 1997, Ridgely et al. 2015).The species has traditionally been classified in the monotypic genus Clytolaema, although its close affinity to Heliodoxa has long been recognized (Willis 1992, Willis & Schuchmann 1993, McGuire et al. 2009).Recently, the phylogenetic relationships of Clytolaema were accessed directly (McGuire et al. 2014), confirming the previous suspicions that this genus should be merged into Heliodoxa (Piacentini et al. 2015).
In Rio Grande do Sul, the southernmost Brazilian state, H. rubricauda has been known with certainty for over a century from a single specimen obtained by Hermann von Ihering at Taquara (29°40′ S, 050°47′ W; 40 m), which was sent by him in ethanol to Count Hans von Berlepsch in Germany (Berlepsch & Ihering 1885).This specimen, an adult male, was collected on an unknown date, but doubtless between June 1882 and December 1883, when Ihering lived at Taquara and collected birds in the vicinity.
The private collection of Count von Berlepsch was acquired by the Senckenberg Museum in Frankfurt after his death (Palmer 1928).The bird collection of this museum includes a study skin of an adult male Clytolaema rubricauda (#86,989) from "Taquara do Mundo Novo" (a former name for Taquara, in use at Ihering's time), which is undoubtedly the same specimen reported by Berlepsch & Ihering (1885).The specimen label (Fig. 1) indicates that it was received from H. von Ihering in January 1883.The label also contains a note (in German) stating that the specimen was originally preserved in alcohol, having been skinned by the same person who wrote the label, presumably Berlepsch himself ("War in Spiritus conservirtvon mir abgebalgt" [sic]).
A second published record for Rio Grande do Sul is that of a male reported as having been collected north of Porto Alegre in July 1956 (Ruschi 1956).Though accepted by Belton (1984Belton ( , 1994)), this record was considered unfounded by Bencke (2001) in view of the inconsistencies between the information presented in the original source and the voucher material that was supposed to provide support for it.These inconsistencies strongly suggest that this and other Ruschi's records from Porto Alegre and surroundings lack documentation and credibility (Bencke 2001).Ruschi's record also lacks biogeographic coherence, since woodlands around Porto Alegre are relatively poor in Atlantic Forest endemics compared to forests on the adjacent escarpment (e.g., at Taquara).
Here we present recent records of H. rubricauda for Rio Grande do Sul, representing its rediscovery in the state after nearly 130 years.Records were obtained at 3 localities in the municipalities of São Francisco de Paula and Cambará do Sul, at the top of the steep escarpment leading to the highlands of the Southern Brazilian Plateau, in northeastern Rio Grande do Sul (Fig. 2).At 2 of these localities, birds were captured with mist nets during banding activities (capture permits SISBio/ ICMBio 43005-2 and 49050).Below, records are organized by locality and from south to north.Key diagnostic features used to identify the birds on site or from photographs include tail pattern, color of underwing coverts and size, among others (Grantsau 1988, Ridgely et al. 2015).
São Francisco de Paula.In late afternoon on 13 March 2010, MR observed individuals of 3 hummingbird species visiting flowers of Fuchsia regia (Onagraceae) at the edge of a late secondary forest at CPCN Pró-Mata, which is a private reserve and research station encompassing 3,100 ha of southern temperate (Araucaria) forests, second growth and grasslands, managed by the PUCRS university of Porto Alegre.Because of the rainy weather and poor light condition, it was not possible to identify a hummingbird that emitted a repetitive call while foraging.The unfamiliar voice was recorded in the background of other species' recordings (Fig. 3) and later identified as that of H. rubricauda by comparison with audio samples available for this species at the Xeno-canto website (http://www.xeno-canto.org).The site where the species was discovered (29°29′27″ S, 050°11′13″ W) is extensively forested and lies at an altitude of 900 m above sea level on the border of the escarpment that rises westward from the adjacent coastal plain.
The presence of H. rubricauda at this locality was further confirmed when an adult male (Fig. 4; Table 1) was mist-netted on 16 November 2014 by DGO, GC and PE during the third Bird Banding and Molt Analysis (BBMA) course.For this course, mist nets were placed in Araucaria forest, both oldgrowth and young secondary, and also around the main building of the research station (29°28′48″ S, 050°10′25″ W), where the bird was captured.The BBMA took place between 16-22 November, but H. rubricauda was captured only once in the morning preceding the course.The bird did not show either bill corrugations or pale spots on the head, which are juvenile characters in most hummingbird species (Ortiz-Crespo 1972, Pyle 1997), and thus was aged as "FAJ" or after-First Cycle Juvenile according to the molt-based ageing system of Wolf et al. ( 2010) and Johnson et al. (2011).This code is used when a bird can confidently be identified as non-juvenile but cannot be aged more precisely, which typically occurs when the preformative molt is complete and results in an adult-like plumage aspect (Johnson et al. 2011).
Additionally, on 16 December 2010, GAB and DBM photographed an immature H. rubricauda (Fig. 5) among a congregation of about 17 hummingbirds of 6 species around backyard feeders just south of the town of São Francisco de Paula (29°28′07″ S, 050°34′38″ W; 910 m).The bird appeared intermittently from 09:15 h on, but always for short periods, during which it was persistently harassed by male Violetcapped Woodnymphs, Thalurania glaucopis.The temperature  grassland patches.The site where the specimens were captured (29°09′40″ S, 050°04′49″ W; 900 m) is close to the head of a steep canyon that opens southeastward into the narrow coastal plain across the Rio Grande do Sul/Santa Catarina border.The area is surrounded by approximately 800 ha of humid Araucaria-dominated forest with the understory primarily consisting of tree ferns (Dicksonia sellowiana).
The presence of H. rubricauda during the spring and summer in habitats potentially suitable for breeding, along with the record of an immature bird, suggests that the species may breed locally in northeastern Rio Grande do Sul.However, with so few records, it is too early to make any inferences about its breeding status and seasonality in the state.A southward range shift of this northerly species does not seem out of the question, was relatively low for the period (late spring) and the weather remained cloudy and windy throughout the day.The species was not recorded on 6 other visits to this area in March and May 2009, March and September 2010, March 2011, and October 2015.This site lies at the top of the escarpment rising northward from the adjacent Rio Rolante valley.Surrounding areas are mostly slopes and valleys covered with secondary and disturbed forests, clearings and small cultivated fields.
Cambará do Sul.In the morning of 11 January 2016, DF and field assistants captured 2 males in mist nets during a bird monitoring survey at the Aparados da Serra National Park (Figs. 6, 7; Table 1).In addition, a female was captured on 16 October (Fig. 8).The Aparados da Serra National Park covers about 10,000 ha of Atlantic rainforest interspersed with natural  since at least 2 other hummingbird species are believed to be expanding their ranges in southern Brazil and into Rio Grande do Sul in recent years (Straube et al. 2006, Damiani 2009, Petersen & Petry 2009).
Our records were in localities situated at the top of the east-and southeast-facing slopes of the southern Brazilian highlands, in areas still extensively covered with upper mon-    tane and Araucaria-dominated mixed forests, now mostly secondary or disturbed.Because of their topographic position and proximity to the coast, these forests are often exposed to orographic precipitation and cloud formation, and are thus very humid.In fact, the average rainfall around São Francisco de Paula exceeds 2,250 mm per year and is reported to be the highest in southern Brazil, south of São Paulo (Backes 2007).
In Rio Grande do Sul, a number of bird taxa are clearly associated with the humid forests of this narrow elevation zone along the seaward border of the Southern Brazilian Plateau.These include the Atlantic Forest race of the Spectacled Owl, Pulsatrix perspicillata pulsatrix; the southern race of the Pale-browed Treehunter, Cichlocolaptes leucophrus holti; the Black-capped Piprites, Piprites pileata; the Swallow-tailed Cotinga, Phibalura flavirostris; the Serra do Mar Tyrannulet, Phylloscartes difficilis; and, to a lesser extent, the Barethroated Bellbird, Procnias nudicollis, and the Bay-chested Warbling-Finch, Poospiza thoracica (Bencke et al. 2003).Heliodoxa rubricauda may present a similar distribution pattern in the southern reaches of its range.
In addition to our records, H. rubricauda has recently been documented in the municipality of Mampituba (29°13′ S, 049° 56′ W; ca.35 m), on the border with Santa Catarina (Nunes 2015).This record along with the specimen from Taquara are so far the only records for the lowlands of Rio Grande do Sul.In southeastern Brazil, the species is believed to migrate altitudinally to lower elevations during the winter (Willis & Oniki 2002, 2003, Ridgely et al. 2015).Taquara is only about 27 km downslope from São Francisco de Paula and now mostly deforested.We speculate that H. rubricauda might have been a scarce winter visitor from the nearby highlands to this and other lowland locations of Rio Grande do Sul in the past.

Figure 1 .
Figure 1.Specimen of Heliodoxa rubricauda from the Senckenberg Museum, Frankfurt, collected by Hermann von Ihering at Taquara, Rio Grande do Sul, southern Brazil, in the early 1880s.Photo by G. Mayr.

Figure 6 .
Figure 6.Male Heliodoxa rubricauda captured and banded on 11 January 2016 at Cambará do Sul, Rio Grande do Sul.Note diagnostic tail pattern.Photo by D. Franco.

Figure 7 .
Figure 7. Male Heliodoxa rubricauda captured on 11 January 2016 at Cambará do Sul, Rio Grande do Sul.Note same distinctive features as in figures 4 and 6.Photo by D. Franco.

Figure 5 .
Figure 5. Immature Heliodoxa rubricauda photographed on 16 December 2010 at São Francisco de Paula, Rio Grande do Sul.Tail pattern and color of underwing coverts (not apparent in this photograph), in combination with the straight bill and overall body size, were useful to identify this individual.Photo by G.A. Bencke.

Figure 4 .
Figure 4. Male Heliodoxa rubricauda captured at CPCN Pró-Mata, São Francisco de Paula, Rio Grande do Sul, on 16 November 2014.The glittering red or pink gorget, in combination with the green underparts, is diagnostic in range.Photo by D. García-Olaechea.

Figure 8 .
Figure 8. Female Heliodoxa rubricauda captured on 16 October 2016 at Cambará do Sul, Rio Grande do Sul.The extensively cinnamon underparts are diagnostic in range.Photo by D. Franco.

Table 1 .
Body mass and measurements of Heliodoxa rubricauda captured in Rio Grande do Sul, southern Brazil.