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Breeding biology of the Cipo Cinclodes Cinclodes espinhacensis, a micro-endemic furnariid of the southeastern Brazilian mountains

Breeding biology of the Cipo Cinclodes Cinclodes espinhacensis, a micro-endemic furnariid of the... Revista Brasileira de Ornitologia 27(2): 63–69. ARTICLE June 2019 Breeding biology of the Cipo Cinclodes Cinclodes espinhacensis, a micro-endemic furnariid of the southeastern Brazilian mountains 1,4 1 1 Lílian Mariana Costa , Guilherme Henrique Silva de Freitas , Pedro Henrique Vieira Braga Pereira da Silva , 2 3 1 Leonardo Cotta Ribeiro , Marcelo Ferreira de Vasconcelos & Marcos Rodrigues Laboratório de Ornitologia, Departamento de Zoologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil. Laboratório de Ecologia de Populações, Departamento de Genética, Ecologia e Evolução, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil. Museu de Ciências Naturais, Pontifícia Universidade Católica de Minas Gerais, Belo Horizonte, MG, Brazil. Corresponding author: lilian.mcosta@gmail.com Received on 08 August 2018. Accepted on 21 June 2019. ABSTRACT: The Cipo Cinclodes Cinclodes espinhacensis is a recently described furnariid endemic to the campos rupestres of Serra do Cipó, southern Espinhaço Range, southeastern Brazil. It is an “Endangered” species and its natural history is poorly known. We studied the Cipo Cinclodes breeding biology at Serra do Breu, where we found six nests on rock outcrops in 2009 and 2012. At least one nest was reused in different years. Breeding season was from September (nest building) to January (dependent juveniles). Nests were shallow cups or beds placed in chambers at the end of earthen and/or rocky tunnels or crevices on rock outcrops. Clutch size was 2–3 eggs. It exhibited biparental care during all nest stages. We demonstrated that the nesting habits of Cipo Cinclodes agree with those reported for other species of the genus, although some details differ from what is known for the closely related species, the Long-tailed Cinclodes Cinclodes pabsti. KEY-WORDS: cavity nest, campos rupestres, egg, fledgling, Furnariidae, nest, nestling, reproduction. INTRODUCTION since its description (Freitas et al. 2012). About its breeding biology, it is only known that it nests in cavities The Cipo Cinclodes Cinclodes espinhacensis is a recently (Freitas et al. 2012), which is a common pattern within described furnariid endemic to campo rupestre vegetation the genus (Zyskowski & Prum 1999, Remsen-Jr. 2019). mosaic from the highest mountaintops of Serra do Cipó, However, a variety of cavity types are used by members southern Espinhaço Range, Brazil (Freitas et al. 2012 & of the genus, existing some evidence of species-specificity 2019). The species is isolated by more than 1000 km from and also intra-specific differentiation (Hahn et al. 2005, its closest relative, the Long-tailed Cinclodes Cinclodes Ojeda 2016). pabsti from the Serra Geral, southern Brazil (Freitas et Recognizing the importance of breeding data not al. 2008 & 2012, Chaves et al. 2015). Cipo Cinclodes only to species conservation, but also to investigate is included in the Brazilian Red List as “Endangered” ecological and evolutionary hypotheses (Zyskowski & (MMA 2014), and the Long-tailed Cinclodes as “Near- Prum 1999, Hahn et al. 2011), we present information Threatened ” (ICMBio 2014). The global Re d List about the breeding biology of Cipo Cinclodes, including considers the Long-tailed Cinclodes, including the Cipo data on its nest, nest site, clutch size, egg, nestling, Cinclodes as subspecies, as “Near-Threatened ” (BirdLife fledgling, bree ding season and parental care. International 2019). A recent study investigated the population and spatial ecology of Cipo Cinclodes, improving our understanding METHODS of their basic biology and distribution and supporting the designation as “Endangered” on the Brazilian Red List We studied a Cipo Cinclodes population at Serra do (Freitas et al. 2019). Beyond that, nothing else has been Breu, Santana do Riacho municipally, state of Minas published about the natural history of Cipo Cinclodes Gerais, from 2009 to 2017. The study area comprises Breeding biology of the Cipo Cinclodes Costa et al. small Eriocaulaceae, and green mosses, but also from ~295 ha of campo rupestre – a high altitude complex animals, like mammals' hair and feathers from other bird mosaic of vegetation (see Alves et al. 2014, Silveira et al. species. The nests were placed inside chambers that were 2016) – where quartzite outcrops predominate within grasslands, traversed by several streams bordered by low preceded by narrower entrances that frequently had a riparian vegetation. We marked birds and searched for small amount of the same nest materials, notably large flight feathers. The entrances were mainly tunnels in soil nests by following the adults during nine visits (4–7 among the rocks (n = 4) or rocky crevices or gallery (n = days each): two in 2009 (November and December), six 2). The chambers with nests were always positioned a bove in 2012–2013 (July, September, October, December, January and February), and one in 2017 (January). Birds the opening of the entrances, so tunnels were inclined were captured with mist nets and marked with color and upwardly. The narrow entrances communicated with the exterior directly (i.e., the openings were visible to an metallic numbered leg bands, and with radio transmitters external observer; n = 2), or, most frequently, it opened (Biotrack Pip Ag393; details in Freitas et al. 2019). inside a rocky shelter or cave (i.e., the openings were We measured with a metric tape (to the nearest 0.5 cm) the following nest and nest site attributes: height hidden to an external observer; n = 4). The substrates of the entrance above ground, distance of the entrance delimiting the chambers and entrances (i.e., their walls, ceilings, and floors) were t he quartzitic rock itself and to the top of the bank/hillside, width and height of the the dark, moist, peat soil with some fine roots of the entrance, length of the tunnel or crevice (distance from above plants emerging. The nest shape and site of Cipo the entrance to nest cup) and total length of the cavity (distance from the entrance to the end of the chamber; Cinclodes can be described as cups or beds placed in “burrow depth” sensu Hansell 2000), inclination (angle ground hole/cavity (sensu Hansell 2000), and classified as cavity/with-tunnel/low cup (or cavity/with-tunnel/ of inclination of the tunnel or crevice, measured with a simple/platform) with an inclined tunnel (sensu Simon protractor); width and height of the chamber containing & Pacheco 2005). Nests are individually described below the nest; nest external and internal diameter and depth (“nest diameter”, “cup diameter”, and “cup depth”, (see Fig. 1 & Table 1). respectively, sensu Hansell 2000). We weighted (Pesola The clutch size was three (n = 2 nests) or two (n = 1 nest) eggs. Eggs were white with overall (varying) spring scales to the nearest 0.1 g) and measured (with a oval shape (Fig. 2C, Table 1). At hatching, nestlings had Mitutoyo caliper to the nearest 0.1 mm) eggs (width and closed eyes, pinkish skin and tarsus, gray natal down height), nestlings (tarsus, total culmen, bill width at gape, total body length and total head length – from the tip feathers (neossoptiles), brown nails with whitish tips, of the bill to the occiput) and fledglings (body length) orange bill with brownish tip and an egg-tooth, vivid orange inner mouth and light yellow enlarged gape (Baldwin et al. 1931). flanges (Fig. 2D). At fledging, the black-colored bill and Some nests and its contents were not reachable the overall plumage appearance were similar to the adults, (neither visible) inside their cavities to be measured, and the nest stage was inferred from the adults' behavior (e.g., but the enlarged yellow gape and some neossoptiles at the staying long periods inside the nest or taking food). For tips of some feathers were retained, the flight feathers (still growing) were shorter, and the breast had a scaled nest shape, site and attachment descriptions we follow appearance (Fig. 2E). Those features were still o bserved the terminology of Simon & Pacheco (2005) and Hansell in the post-fledgling period but were gradually being lost, (2000). being the scaled breast the most persistent feature (Fig. 2F). Both parents were seeing entering into the nest cavity RESULTS during all nest phases, carrying nest material during nest building and incubation, and taking food to nestlings. In some occasions, both parents were observed inside the We found six nests, four in the breeding season of 2009 and two in 2012. One of those nests found in 2009 was nest cavity simultaneously. active again in 2012. Nesting period extended from The nest one was found on 18 November 2009 with three eggs. It was built inside a chamber at the end of a September, when we observed nest building activity, tunnel at the ceiling of a rocky cave (Fig. 1A), c. 2.6 m through November and December, when eggs and from the cave entrance, that was 1.4 m wide. The tunnel nestlings were found. Juveniles dependent on parental were observed in December and January. had its superior part composed of rock and the inferior All nests were found within cavities on rocky outcrops of soil (Fig. 1B). The chamber containing the nest was entirely composed of soil, with fine roots emerging. There (Fig. 1) and consisted of a shallow cup made of fragments were many worn feathers from other bird species and of thin and pliable material, with some soil among them other nest materials lining the tunnel and loosely placed (Figs. 2A & B). Nest materials were mostly from plants, such as dry grass-like narrow leaves, inflorescences of at the ground of the cave below the tunnel entrance, Revista Brasileira de Ornitologia 27(2): 2019 Breeding biology of the Cipo Cinclodes Costa et al. Table 1. Attributes of the Cipo Cinclodes Cinclodes espinhacensis nests, eggs, nestling and fledglings found from 2009 to 2012 at Serra do Breu, Serra do Cipó, Brazil. Entrance type: tunnel on soil (T), rocky crevice or gallery (S); entrance opening: hidden (H), visible (V). Eggs 1–3 and all nestlings were from nest one; eggs 3–6 from nest 3 (egg 6 was rotten); eggs 7–8 and all fledglings from nest 4. Identification numbers of measured unities Nest Sites Entrance 1 2 3 4 5 6 n Mean SD Min Max Type/opening T/H T/V T/H T/V S/H S/H Height above ground (cm) 90.0 210.0 292.0 133.0 239.5 195.0 6 193.3 72.8 90.0 292.0 Distance to top (cm) - 34.0 40.0 28.0 - - 3 34.0 6.0 28.0 40.0 Opening width (cm) 16.0 18.0 5.0 13.0 44.0 - 5 19.2 14.7 5.0 44.0 Opening height (cm) 7.0 20.5 13.0 11.0 56.0 19.5 6 21.2 17.8 7.0 56.0 Length of the tunnel or 48.0 70.0 12.0 17.0 84.5 114.0 6 57.6 39.7 12.0 114.0 crevice (until nest; cm) Total length of the cavity 63.5 90.0 36.0 87.0 101.5 - 5 75.6 26.1 36.0 101.5 (including chamber; cm) Inclination (°) 43.0 20.0 55.0 - 45.0 - 4 40.8 14.8 20.0 55.0 Chamber with nest Width (cm) 19.0 - 21.0 - - - 2 20.0 1.4 19.0 21.0 Height (cm) 14.0 - 20.0 - - - 2 17.0 4.2 14.0 20.0 Nests 1 2 3 4 5 6 External diameter (cm) - - 15.0 24.0 - - 2 19.5 6.4 15.0 24.0 Internal diameter (cm) - - 10.0 12.0 - - 2 11.0 1.4 10.0 12.0 Depth (cm) - - 4.0 2.5 - - 2 3.3 1.1 2.5 4.0 Eggs 1 2 3 4 5 6 7 8 Width (mm) 21.6 21.5 21.6 21.1 20.9 - 20.5 19.4 7 20.9 0.8 19.4 21.6 Height (mm) 27.2 28.0 27.0 28.4 27.6 - 26.4 27.5 7 27.4 0.7 26.4 28.4 Mass (g) 6.1 5.9 6.0 6.0 5.6 5.3 5.2 5.1 8 5.7 0.4 5.1 6.1 Nestlings (0–1 day) 1 2 3 Body mass (g) 6.7 4.8 9.1 3 6.8 2.2 4.8 9.1 Body length (mm) 53.0 47.0 53.5 3 51.2 3.6 47.0 53.5 Tarsus length (mm) 11.4 10.5 12.0 3 11.3 0.8 10.5 12.0 Total culmen length (mm) 9.8 8.7 9.8 3 9.4 0.6 8.7 9.8 Bill width (mm) 12.0 9.7 12.1 3 11.3 1.4 9.7 12.1 Total head length (mm) 19.1 21.3 2 20.2 1.6 19.1 21.3 Fledglings (0 day) 1 2 Body mass (g) 51.2 52.2 2 51.7 0.7 51.2 52.2 Body length (mm) 150.0 165.0 2 157.5 10.6 150.0 165.0 apparently dropped from it. One of the birds attending paired birds was banded in 2009 (and disappeared in this nest was observed energetically shaking and mashing 2012), it is possible that at least one member of the pair a flight feather from other species with t he mandibles was the same at both breeding attempts. On 10 December before taking it to the nest. On 22 November 2009, three 2012, the marked bird was feeding a juvenile outside the nestlings were born (Fig. 2B) and on 16 December 2009, nest. After four years, on 04 January 2017, the nest was the nest was empty. not active, but the pile of nest materials below the tunnel Three years later, on 09 September 2012, this nest entrance was still there, where we found white eggshell was active again. Two birds were carrying narrow straws fragments. and gray mammal hairs to the nest, one non-marked and The nest two was discovered on 20 November 2009, another banded in July 2012. Given that just one of the apparently with eggs. It was inside a long tunnel – so deep Revista Brasileira de Ornitologia 27(2): 2019 Breeding biology of the Cipo Cinclodes Costa et al. Figure 1. Nest sites of the Cipo Cinclodes Cinclodes espinhacensis at Serra do Breu, southern Espinhaço Range, Brazil. For each nest two pictures show the overall (left) and close-up (right) location of the nest cavities (red arrows indicate entrances). Nest 1 (A & B), nest 2 (C & D), nest 3 (E & F), nest 4 (G & H), nest 5 (I & J), and nest 6 (K & L). Photo author: G.H.S. Freitas. Revista Brasileira de Ornitologia 27(2): 2019 Breeding biology of the Cipo Cinclodes Costa et al. Figure 2. Shallow cupped nests inside (A) and removed from the cavity (B), eggs (C), hatchlings (D), fledglings (E), and a dependent juvenile (F) of the Cipo Cinclodes Cinclodes espinhacensis at Serra do Breu, southern Espinhaço Range, Brazil. At (B), approximately 30 cm of a metric tape is apparent; at (C) and (D), part of a caliper with 1 mm graduation is apparent. Photo author: G.H.S. Freitas (A & C–F) and L.M. Costa (B). that the content was not accessible – at the border of a juveniles fledged w hen we approached the nest. Those rocky outcrop (Fig. 1C). The cross section of the tunnel were captured and collected (paratypes described in was triangular, with one rocky wall and the remaining Freitas et al. 2012; Fig. 2C). One was a male and the sides of soil with rootlets (Fig. 1D). The floor was lined other a female, both heavier than adults (c. 45 g). with feathers and thin dry grass-like leaves. Both adults The nest five was detected on 09 December 2012, were observed entering the tunnel. On 17 December with nestlings. Adults were seen taking food to the nest 2009, we witnessed an adult carrying food to the nest that and nestlings begging calls were heard. The nest was apparently contained at least one well-developed nestling. placed at the end of a long rocky gallery (Fig. 1J) that The nest three was found on 19 November 2009 opened inside a small cave located in the middle of a with three eggs, being one of them rotten. The nest was mountain slope (Fig. 1I). within a chamber of soil, after a tunnel with rock and soil The nest six was found on 13 December 2012, that opened inside a rocky crevice, c. 45 cm of the outside probably with eggs. The nest was unreachable inside (Figs. 1E & F). In the tunnel, we found feathers and thin a rocky crevice at the end of an extensive and narrow grass leaves near the nest. We observed one adult taking crevice between two large boulders (Figs. 1K & L). Two nest material into the nest cavity. On 16 December 2009, adults visited the nest, sometimes carrying nest material the nest was empty. in the beak. The nest four was first observed on 21 November 2009 with two eggs. It was located in a rocky outcrop bordering a stream (Fig. 1G). The entrance was a short, DISCUSSION not inclined, roughly triangular tunnel, with one rocky wall and the other sides were soil (Fig. 1H). There was a The Cipo Cinclodes is socially monogamous with biparental care during all nest stages. The bree ding small hole on the opposite side of the cavity containing the nest. Twenty-five days later, on 16 December, two season length was at least four to five months, from Revista Brasileira de Ornitologia 27(2): 2019 Breeding biology of the Cipo Cinclodes Costa et al. early September (nest building) to January (dependent Cipo Cinclodes following the standardized classification juveniles). The habitat used for nesting was rock schemes (Hansell 2000, Simon & Pacheco 2005) we outcrops, the typical environment of the campos rupestres found some difficulties. One of them was to classify landscape that occurs among grasslands, in slopes or the nests without typical tunnels preceding it as cavity/ bordering streams. Although Cipo Cinclodes uses all without-tunnel, because their entrances did not open habitat types available in our study area, including rocky directly to the exterior (like the Fig. 4A in Simon & outcrops, grasslands, and riparian areas, a recent habitat Pacheco 2005), but were always preceded by narrowing selection analyses revealed the importance of riparian rock entrances; so we kept it as cavity/with-tunnel. A areas for foraging (Freitas et al. 2019), while the present further doubt we have was about the elementary nest study evidenced the importance of the rocky outcrops to standard. Due to the imprecision of the terms, we think complete the Cipo Cinclodes life cycle. that the nests could be classified both as low cups and The breeding biology of the Cipo Cinclodes is overall as simple/platforms (sensu Simon & Pacheco 2005), or similar to that reported (observed or presumed) for its its equivalents cups and beds (sensu Hansell 2000). Cups congeners. There are at least minimal information about were suggested as the Cinclodes nest type by Simon & the breeding of all of the ~16 species recognized in the Pacheco (2005) and Zyskowski & Prum (1999). Those genus (Cawkell & Hamilton 1961, Sick 1973, Narosky last authors, in their nest-based phylogenetic analysis et al. 1983, Belton 1984, de la Peña 1987 & 2019, Graves of the Furnariidae, hypothesize that platforms and cups & Arango 1988, Bertolero & Zavalaga 2003, Greeney et are two ordered derived states of nests built in cavities, al. 2011, Salvador & Salvador 2012, Avalos & Gómez showing the putative importance in distinguishing 2014, Salvador 2015, Ojeda 2016, Vizcarra et al. 2018, between these nest types. We observed a thick platform Remsen-Jr. 2019). The Cipo Cinclodes' sister species, the with a prominent depression in the middle, which is Long-tailed Cinclodes, nests at end of tunnel excavated dissimilar to those nests of Olrog's Cinclodes (C. olrogi) in soil banks (some with rocks), frequently at roadcuts, or and Cordoba Cinclodes (C. comechingonus) as can be in roof beam within farm-house attics (Sick 1973, Belton seen on photographs in Salvador & Salvador (2012) that 1984). While for some species there are records of nest are distinctly cup-like and composed of less fragmented only in earthen banks (the Chestnut-winged Cinclodes C. material, mostly by broader straw-like grasses. albidiventris, the Cream-winged Cinclodes C. albiventris, Here, we provide the first detailed information on and the Stout-billed Cinclodes C. excelsior; Graves & many aspects of the breeding biology of Cipo Cinclodes. Arango 1988, Greeney et al. 2011, Salvador 2015), However, more information is required for a complete others seem to breed exclusively in natural rocky crevices understanding of the breeding ecology of Cipo Cinclodes, (the Royal Cinclodes C. aricomae, the Surf Cinclodes such as the duration of the nest stages, nestling and C. taczanowskii, and the White-bellied Cinclodes C. fledgling development, and reproductive success. We palliatus; Bertolero & Zavalaga 2003, Avalos & Gómez demonstrated that it agrees with those reported for other 2014, Vizcarra et al. 2018, Remsen-Jr. 2019). However, species of the genus, although some details differ from this differentiation can be due to a lack of adequate what is known for the closely related species, the Long- sampling, since for the remaining species of the genus tailed Cinclodes. The rock outcrop habitat of the campos there are records for both types of cavities, with some rupestres could be key to the breeding of Cipo Cinclodes, species nesting also in other kinds of burrows, such as tree as also documented for the other furnariid endemic to the holes (Cawkell & Hamilton 1961, Narosky et al. 1983, de campos rupestres, and sympatric at our study area, the Cipo la Peña 1987 & 2019, Salvador & Salvador 2012, Ojeda Canastero Asthenes luizae, despite their distinct nesting 2016). Cipo Cinclodes lies within that third group since habits (Costa et al. 2019). Investigating the availability the nests can be placed in natural holes among the rocks of suitable nesting sites for Cipo Cinclodes may elucidate or at the end of tunnels in an earthen substrate, although possible restrictions on their occupancy. Detailed studies the tunnels were always bordering a rock. Although we on the breeding biology of other Cinclodes are needed, did not observe the birds actively excavating tunnels as allowing to detect intra-generic and intra-specific others did for congeneric species (e.g., Sick 1973, Graves differentiation, and to better understand the evolution of & Arango 1988, Greeney et al. 2011), we suspect that the breeding strategies in Furnariidae. this occurred in some nests, since the burrows seemed to be recently made, with rootlets visible. ACKNOWLEDGEMENTS The nest ar chitecture of the Cipo Cinclodes was a shallow, flattened cup, composed of very fragmented and pliable material. The nests of the Long-tailed Cinclodes We thank the Fundação Grupo Boticário de Proteção à also differ by having some sticks within the soft cushion Natureza (0885_20102), CAPES, CNPq and FAPEMIG (Sick 1973). 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Breeding biology of the Cipo Cinclodes Cinclodes espinhacensis, a micro-endemic furnariid of the southeastern Brazilian mountains

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Revista Brasileira de Ornitologia 27(2): 63–69. ARTICLE June 2019 Breeding biology of the Cipo Cinclodes Cinclodes espinhacensis, a micro-endemic furnariid of the southeastern Brazilian mountains 1,4 1 1 Lílian Mariana Costa , Guilherme Henrique Silva de Freitas , Pedro Henrique Vieira Braga Pereira da Silva , 2 3 1 Leonardo Cotta Ribeiro , Marcelo Ferreira de Vasconcelos & Marcos Rodrigues Laboratório de Ornitologia, Departamento de Zoologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil. Laboratório de Ecologia de Populações, Departamento de Genética, Ecologia e Evolução, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil. Museu de Ciências Naturais, Pontifícia Universidade Católica de Minas Gerais, Belo Horizonte, MG, Brazil. Corresponding author: lilian.mcosta@gmail.com Received on 08 August 2018. Accepted on 21 June 2019. ABSTRACT: The Cipo Cinclodes Cinclodes espinhacensis is a recently described furnariid endemic to the campos rupestres of Serra do Cipó, southern Espinhaço Range, southeastern Brazil. It is an “Endangered” species and its natural history is poorly known. We studied the Cipo Cinclodes breeding biology at Serra do Breu, where we found six nests on rock outcrops in 2009 and 2012. At least one nest was reused in different years. Breeding season was from September (nest building) to January (dependent juveniles). Nests were shallow cups or beds placed in chambers at the end of earthen and/or rocky tunnels or crevices on rock outcrops. Clutch size was 2–3 eggs. It exhibited biparental care during all nest stages. We demonstrated that the nesting habits of Cipo Cinclodes agree with those reported for other species of the genus, although some details differ from what is known for the closely related species, the Long-tailed Cinclodes Cinclodes pabsti. KEY-WORDS: cavity nest, campos rupestres, egg, fledgling, Furnariidae, nest, nestling, reproduction. INTRODUCTION since its description (Freitas et al. 2012). About its breeding biology, it is only known that it nests in cavities The Cipo Cinclodes Cinclodes espinhacensis is a recently (Freitas et al. 2012), which is a common pattern within described furnariid endemic to campo rupestre vegetation the genus (Zyskowski & Prum 1999, Remsen-Jr. 2019). mosaic from the highest mountaintops of Serra do Cipó, However, a variety of cavity types are used by members southern Espinhaço Range, Brazil (Freitas et al. 2012 & of the genus, existing some evidence of species-specificity 2019). The species is isolated by more than 1000 km from and also intra-specific differentiation (Hahn et al. 2005, its closest relative, the Long-tailed Cinclodes Cinclodes Ojeda 2016). pabsti from the Serra Geral, southern Brazil (Freitas et Recognizing the importance of breeding data not al. 2008 & 2012, Chaves et al. 2015). Cipo Cinclodes only to species conservation, but also to investigate is included in the Brazilian Red List as “Endangered” ecological and evolutionary hypotheses (Zyskowski & (MMA 2014), and the Long-tailed Cinclodes as “Near- Prum 1999, Hahn et al. 2011), we present information Threatened ” (ICMBio 2014). The global Re d List about the breeding biology of Cipo Cinclodes, including considers the Long-tailed Cinclodes, including the Cipo data on its nest, nest site, clutch size, egg, nestling, Cinclodes as subspecies, as “Near-Threatened ” (BirdLife fledgling, bree ding season and parental care. International 2019). A recent study investigated the population and spatial ecology of Cipo Cinclodes, improving our understanding METHODS of their basic biology and distribution and supporting the designation as “Endangered” on the Brazilian Red List We studied a Cipo Cinclodes population at Serra do (Freitas et al. 2019). Beyond that, nothing else has been Breu, Santana do Riacho municipally, state of Minas published about the natural history of Cipo Cinclodes Gerais, from 2009 to 2017. The study area comprises Breeding biology of the Cipo Cinclodes Costa et al. small Eriocaulaceae, and green mosses, but also from ~295 ha of campo rupestre – a high altitude complex animals, like mammals' hair and feathers from other bird mosaic of vegetation (see Alves et al. 2014, Silveira et al. species. The nests were placed inside chambers that were 2016) – where quartzite outcrops predominate within grasslands, traversed by several streams bordered by low preceded by narrower entrances that frequently had a riparian vegetation. We marked birds and searched for small amount of the same nest materials, notably large flight feathers. The entrances were mainly tunnels in soil nests by following the adults during nine visits (4–7 among the rocks (n = 4) or rocky crevices or gallery (n = days each): two in 2009 (November and December), six 2). The chambers with nests were always positioned a bove in 2012–2013 (July, September, October, December, January and February), and one in 2017 (January). Birds the opening of the entrances, so tunnels were inclined were captured with mist nets and marked with color and upwardly. The narrow entrances communicated with the exterior directly (i.e., the openings were visible to an metallic numbered leg bands, and with radio transmitters external observer; n = 2), or, most frequently, it opened (Biotrack Pip Ag393; details in Freitas et al. 2019). inside a rocky shelter or cave (i.e., the openings were We measured with a metric tape (to the nearest 0.5 cm) the following nest and nest site attributes: height hidden to an external observer; n = 4). The substrates of the entrance above ground, distance of the entrance delimiting the chambers and entrances (i.e., their walls, ceilings, and floors) were t he quartzitic rock itself and to the top of the bank/hillside, width and height of the the dark, moist, peat soil with some fine roots of the entrance, length of the tunnel or crevice (distance from above plants emerging. The nest shape and site of Cipo the entrance to nest cup) and total length of the cavity (distance from the entrance to the end of the chamber; Cinclodes can be described as cups or beds placed in “burrow depth” sensu Hansell 2000), inclination (angle ground hole/cavity (sensu Hansell 2000), and classified as cavity/with-tunnel/low cup (or cavity/with-tunnel/ of inclination of the tunnel or crevice, measured with a simple/platform) with an inclined tunnel (sensu Simon protractor); width and height of the chamber containing & Pacheco 2005). Nests are individually described below the nest; nest external and internal diameter and depth (“nest diameter”, “cup diameter”, and “cup depth”, (see Fig. 1 & Table 1). respectively, sensu Hansell 2000). We weighted (Pesola The clutch size was three (n = 2 nests) or two (n = 1 nest) eggs. Eggs were white with overall (varying) spring scales to the nearest 0.1 g) and measured (with a oval shape (Fig. 2C, Table 1). At hatching, nestlings had Mitutoyo caliper to the nearest 0.1 mm) eggs (width and closed eyes, pinkish skin and tarsus, gray natal down height), nestlings (tarsus, total culmen, bill width at gape, total body length and total head length – from the tip feathers (neossoptiles), brown nails with whitish tips, of the bill to the occiput) and fledglings (body length) orange bill with brownish tip and an egg-tooth, vivid orange inner mouth and light yellow enlarged gape (Baldwin et al. 1931). flanges (Fig. 2D). At fledging, the black-colored bill and Some nests and its contents were not reachable the overall plumage appearance were similar to the adults, (neither visible) inside their cavities to be measured, and the nest stage was inferred from the adults' behavior (e.g., but the enlarged yellow gape and some neossoptiles at the staying long periods inside the nest or taking food). For tips of some feathers were retained, the flight feathers (still growing) were shorter, and the breast had a scaled nest shape, site and attachment descriptions we follow appearance (Fig. 2E). Those features were still o bserved the terminology of Simon & Pacheco (2005) and Hansell in the post-fledgling period but were gradually being lost, (2000). being the scaled breast the most persistent feature (Fig. 2F). Both parents were seeing entering into the nest cavity RESULTS during all nest phases, carrying nest material during nest building and incubation, and taking food to nestlings. In some occasions, both parents were observed inside the We found six nests, four in the breeding season of 2009 and two in 2012. One of those nests found in 2009 was nest cavity simultaneously. active again in 2012. Nesting period extended from The nest one was found on 18 November 2009 with three eggs. It was built inside a chamber at the end of a September, when we observed nest building activity, tunnel at the ceiling of a rocky cave (Fig. 1A), c. 2.6 m through November and December, when eggs and from the cave entrance, that was 1.4 m wide. The tunnel nestlings were found. Juveniles dependent on parental were observed in December and January. had its superior part composed of rock and the inferior All nests were found within cavities on rocky outcrops of soil (Fig. 1B). The chamber containing the nest was entirely composed of soil, with fine roots emerging. There (Fig. 1) and consisted of a shallow cup made of fragments were many worn feathers from other bird species and of thin and pliable material, with some soil among them other nest materials lining the tunnel and loosely placed (Figs. 2A & B). Nest materials were mostly from plants, such as dry grass-like narrow leaves, inflorescences of at the ground of the cave below the tunnel entrance, Revista Brasileira de Ornitologia 27(2): 2019 Breeding biology of the Cipo Cinclodes Costa et al. Table 1. Attributes of the Cipo Cinclodes Cinclodes espinhacensis nests, eggs, nestling and fledglings found from 2009 to 2012 at Serra do Breu, Serra do Cipó, Brazil. Entrance type: tunnel on soil (T), rocky crevice or gallery (S); entrance opening: hidden (H), visible (V). Eggs 1–3 and all nestlings were from nest one; eggs 3–6 from nest 3 (egg 6 was rotten); eggs 7–8 and all fledglings from nest 4. Identification numbers of measured unities Nest Sites Entrance 1 2 3 4 5 6 n Mean SD Min Max Type/opening T/H T/V T/H T/V S/H S/H Height above ground (cm) 90.0 210.0 292.0 133.0 239.5 195.0 6 193.3 72.8 90.0 292.0 Distance to top (cm) - 34.0 40.0 28.0 - - 3 34.0 6.0 28.0 40.0 Opening width (cm) 16.0 18.0 5.0 13.0 44.0 - 5 19.2 14.7 5.0 44.0 Opening height (cm) 7.0 20.5 13.0 11.0 56.0 19.5 6 21.2 17.8 7.0 56.0 Length of the tunnel or 48.0 70.0 12.0 17.0 84.5 114.0 6 57.6 39.7 12.0 114.0 crevice (until nest; cm) Total length of the cavity 63.5 90.0 36.0 87.0 101.5 - 5 75.6 26.1 36.0 101.5 (including chamber; cm) Inclination (°) 43.0 20.0 55.0 - 45.0 - 4 40.8 14.8 20.0 55.0 Chamber with nest Width (cm) 19.0 - 21.0 - - - 2 20.0 1.4 19.0 21.0 Height (cm) 14.0 - 20.0 - - - 2 17.0 4.2 14.0 20.0 Nests 1 2 3 4 5 6 External diameter (cm) - - 15.0 24.0 - - 2 19.5 6.4 15.0 24.0 Internal diameter (cm) - - 10.0 12.0 - - 2 11.0 1.4 10.0 12.0 Depth (cm) - - 4.0 2.5 - - 2 3.3 1.1 2.5 4.0 Eggs 1 2 3 4 5 6 7 8 Width (mm) 21.6 21.5 21.6 21.1 20.9 - 20.5 19.4 7 20.9 0.8 19.4 21.6 Height (mm) 27.2 28.0 27.0 28.4 27.6 - 26.4 27.5 7 27.4 0.7 26.4 28.4 Mass (g) 6.1 5.9 6.0 6.0 5.6 5.3 5.2 5.1 8 5.7 0.4 5.1 6.1 Nestlings (0–1 day) 1 2 3 Body mass (g) 6.7 4.8 9.1 3 6.8 2.2 4.8 9.1 Body length (mm) 53.0 47.0 53.5 3 51.2 3.6 47.0 53.5 Tarsus length (mm) 11.4 10.5 12.0 3 11.3 0.8 10.5 12.0 Total culmen length (mm) 9.8 8.7 9.8 3 9.4 0.6 8.7 9.8 Bill width (mm) 12.0 9.7 12.1 3 11.3 1.4 9.7 12.1 Total head length (mm) 19.1 21.3 2 20.2 1.6 19.1 21.3 Fledglings (0 day) 1 2 Body mass (g) 51.2 52.2 2 51.7 0.7 51.2 52.2 Body length (mm) 150.0 165.0 2 157.5 10.6 150.0 165.0 apparently dropped from it. One of the birds attending paired birds was banded in 2009 (and disappeared in this nest was observed energetically shaking and mashing 2012), it is possible that at least one member of the pair a flight feather from other species with t he mandibles was the same at both breeding attempts. On 10 December before taking it to the nest. On 22 November 2009, three 2012, the marked bird was feeding a juvenile outside the nestlings were born (Fig. 2B) and on 16 December 2009, nest. After four years, on 04 January 2017, the nest was the nest was empty. not active, but the pile of nest materials below the tunnel Three years later, on 09 September 2012, this nest entrance was still there, where we found white eggshell was active again. Two birds were carrying narrow straws fragments. and gray mammal hairs to the nest, one non-marked and The nest two was discovered on 20 November 2009, another banded in July 2012. Given that just one of the apparently with eggs. It was inside a long tunnel – so deep Revista Brasileira de Ornitologia 27(2): 2019 Breeding biology of the Cipo Cinclodes Costa et al. Figure 1. Nest sites of the Cipo Cinclodes Cinclodes espinhacensis at Serra do Breu, southern Espinhaço Range, Brazil. For each nest two pictures show the overall (left) and close-up (right) location of the nest cavities (red arrows indicate entrances). Nest 1 (A & B), nest 2 (C & D), nest 3 (E & F), nest 4 (G & H), nest 5 (I & J), and nest 6 (K & L). Photo author: G.H.S. Freitas. Revista Brasileira de Ornitologia 27(2): 2019 Breeding biology of the Cipo Cinclodes Costa et al. Figure 2. Shallow cupped nests inside (A) and removed from the cavity (B), eggs (C), hatchlings (D), fledglings (E), and a dependent juvenile (F) of the Cipo Cinclodes Cinclodes espinhacensis at Serra do Breu, southern Espinhaço Range, Brazil. At (B), approximately 30 cm of a metric tape is apparent; at (C) and (D), part of a caliper with 1 mm graduation is apparent. Photo author: G.H.S. Freitas (A & C–F) and L.M. Costa (B). that the content was not accessible – at the border of a juveniles fledged w hen we approached the nest. Those rocky outcrop (Fig. 1C). The cross section of the tunnel were captured and collected (paratypes described in was triangular, with one rocky wall and the remaining Freitas et al. 2012; Fig. 2C). One was a male and the sides of soil with rootlets (Fig. 1D). The floor was lined other a female, both heavier than adults (c. 45 g). with feathers and thin dry grass-like leaves. Both adults The nest five was detected on 09 December 2012, were observed entering the tunnel. On 17 December with nestlings. Adults were seen taking food to the nest 2009, we witnessed an adult carrying food to the nest that and nestlings begging calls were heard. The nest was apparently contained at least one well-developed nestling. placed at the end of a long rocky gallery (Fig. 1J) that The nest three was found on 19 November 2009 opened inside a small cave located in the middle of a with three eggs, being one of them rotten. The nest was mountain slope (Fig. 1I). within a chamber of soil, after a tunnel with rock and soil The nest six was found on 13 December 2012, that opened inside a rocky crevice, c. 45 cm of the outside probably with eggs. The nest was unreachable inside (Figs. 1E & F). In the tunnel, we found feathers and thin a rocky crevice at the end of an extensive and narrow grass leaves near the nest. We observed one adult taking crevice between two large boulders (Figs. 1K & L). Two nest material into the nest cavity. On 16 December 2009, adults visited the nest, sometimes carrying nest material the nest was empty. in the beak. The nest four was first observed on 21 November 2009 with two eggs. It was located in a rocky outcrop bordering a stream (Fig. 1G). The entrance was a short, DISCUSSION not inclined, roughly triangular tunnel, with one rocky wall and the other sides were soil (Fig. 1H). There was a The Cipo Cinclodes is socially monogamous with biparental care during all nest stages. The bree ding small hole on the opposite side of the cavity containing the nest. Twenty-five days later, on 16 December, two season length was at least four to five months, from Revista Brasileira de Ornitologia 27(2): 2019 Breeding biology of the Cipo Cinclodes Costa et al. early September (nest building) to January (dependent Cipo Cinclodes following the standardized classification juveniles). The habitat used for nesting was rock schemes (Hansell 2000, Simon & Pacheco 2005) we outcrops, the typical environment of the campos rupestres found some difficulties. One of them was to classify landscape that occurs among grasslands, in slopes or the nests without typical tunnels preceding it as cavity/ bordering streams. Although Cipo Cinclodes uses all without-tunnel, because their entrances did not open habitat types available in our study area, including rocky directly to the exterior (like the Fig. 4A in Simon & outcrops, grasslands, and riparian areas, a recent habitat Pacheco 2005), but were always preceded by narrowing selection analyses revealed the importance of riparian rock entrances; so we kept it as cavity/with-tunnel. A areas for foraging (Freitas et al. 2019), while the present further doubt we have was about the elementary nest study evidenced the importance of the rocky outcrops to standard. Due to the imprecision of the terms, we think complete the Cipo Cinclodes life cycle. that the nests could be classified both as low cups and The breeding biology of the Cipo Cinclodes is overall as simple/platforms (sensu Simon & Pacheco 2005), or similar to that reported (observed or presumed) for its its equivalents cups and beds (sensu Hansell 2000). Cups congeners. There are at least minimal information about were suggested as the Cinclodes nest type by Simon & the breeding of all of the ~16 species recognized in the Pacheco (2005) and Zyskowski & Prum (1999). Those genus (Cawkell & Hamilton 1961, Sick 1973, Narosky last authors, in their nest-based phylogenetic analysis et al. 1983, Belton 1984, de la Peña 1987 & 2019, Graves of the Furnariidae, hypothesize that platforms and cups & Arango 1988, Bertolero & Zavalaga 2003, Greeney et are two ordered derived states of nests built in cavities, al. 2011, Salvador & Salvador 2012, Avalos & Gómez showing the putative importance in distinguishing 2014, Salvador 2015, Ojeda 2016, Vizcarra et al. 2018, between these nest types. We observed a thick platform Remsen-Jr. 2019). The Cipo Cinclodes' sister species, the with a prominent depression in the middle, which is Long-tailed Cinclodes, nests at end of tunnel excavated dissimilar to those nests of Olrog's Cinclodes (C. olrogi) in soil banks (some with rocks), frequently at roadcuts, or and Cordoba Cinclodes (C. comechingonus) as can be in roof beam within farm-house attics (Sick 1973, Belton seen on photographs in Salvador & Salvador (2012) that 1984). While for some species there are records of nest are distinctly cup-like and composed of less fragmented only in earthen banks (the Chestnut-winged Cinclodes C. material, mostly by broader straw-like grasses. albidiventris, the Cream-winged Cinclodes C. albiventris, Here, we provide the first detailed information on and the Stout-billed Cinclodes C. excelsior; Graves & many aspects of the breeding biology of Cipo Cinclodes. Arango 1988, Greeney et al. 2011, Salvador 2015), However, more information is required for a complete others seem to breed exclusively in natural rocky crevices understanding of the breeding ecology of Cipo Cinclodes, (the Royal Cinclodes C. aricomae, the Surf Cinclodes such as the duration of the nest stages, nestling and C. taczanowskii, and the White-bellied Cinclodes C. fledgling development, and reproductive success. We palliatus; Bertolero & Zavalaga 2003, Avalos & Gómez demonstrated that it agrees with those reported for other 2014, Vizcarra et al. 2018, Remsen-Jr. 2019). However, species of the genus, although some details differ from this differentiation can be due to a lack of adequate what is known for the closely related species, the Long- sampling, since for the remaining species of the genus tailed Cinclodes. The rock outcrop habitat of the campos there are records for both types of cavities, with some rupestres could be key to the breeding of Cipo Cinclodes, species nesting also in other kinds of burrows, such as tree as also documented for the other furnariid endemic to the holes (Cawkell & Hamilton 1961, Narosky et al. 1983, de campos rupestres, and sympatric at our study area, the Cipo la Peña 1987 & 2019, Salvador & Salvador 2012, Ojeda Canastero Asthenes luizae, despite their distinct nesting 2016). Cipo Cinclodes lies within that third group since habits (Costa et al. 2019). Investigating the availability the nests can be placed in natural holes among the rocks of suitable nesting sites for Cipo Cinclodes may elucidate or at the end of tunnels in an earthen substrate, although possible restrictions on their occupancy. Detailed studies the tunnels were always bordering a rock. Although we on the breeding biology of other Cinclodes are needed, did not observe the birds actively excavating tunnels as allowing to detect intra-generic and intra-specific others did for congeneric species (e.g., Sick 1973, Graves differentiation, and to better understand the evolution of & Arango 1988, Greeney et al. 2011), we suspect that the breeding strategies in Furnariidae. this occurred in some nests, since the burrows seemed to be recently made, with rootlets visible. ACKNOWLEDGEMENTS The nest ar chitecture of the Cipo Cinclodes was a shallow, flattened cup, composed of very fragmented and pliable material. The nests of the Long-tailed Cinclodes We thank the Fundação Grupo Boticário de Proteção à also differ by having some sticks within the soft cushion Natureza (0885_20102), CAPES, CNPq and FAPEMIG (Sick 1973). When classifying the nest shape and site of for the funding received; ICMBio and IBAMA/CEMAVE Revista Brasileira de Ornitologia 27(2): 2019 Breeding biology of the Cipo Cinclodes Costa et al. of the Stout-billed Cinclodes (Cinclodes excelsior), a high Andean for permits. We are grateful to all people that helped in furnariid. Condor 90: 251–253. fieldwork, especially to Claudiney L. Silva an d Roberto Greeney H.F., Martin P.R., Gelis R.A., Solano-Ugalde A., Bonier Cardoso (in memorian). We thank two anonymous F., Freeman B. & Miller E.T. 2011. Notes on the breeding of reviewers for suggestions that improved our manuscript. high-Andean birds in northern Ecuador. Bulletin of the British Ornithologists' Club 131: 24–31. Hahn I., Römer U. & Schlatter R.P. 2005. First description of nesting ecology of the endemic Grey-flanked Cinclodes Cinclodes oustaleti REFERENCES baeckstroemii from the Juan Fernández Islands, Chile. Acta Ornithologica 40: 165–169. 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Journal

Ornithology Research – Springer Journals

Published: Jun 1, 2019

Keywords: cavity nest; campos rupestres; egg; fledgling; Furnariidae; nest; nestling; reproduction

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