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Year-round presence of Slaty Thrush (Turdus nigriceps nigriceps) in mountains of central Argentina

Year-round presence of Slaty Thrush (Turdus nigriceps nigriceps) in mountains of central Argentina Revista Brasileira de Ornitologia, 24(4), 329–334 ARTICLE December 2016 Year-round presence of Slaty Thr ush (Turdus nigriceps nigriceps) in mountains of central Argentina 1,3 2 David L. Vergara-Tabares and Tobías N. Rojas Instituto de Diversidad y Ecología Animal, CCT-Córdoba-CONICET. Rondeau 798, Córdoba (5000), Córdoba, Argentina. Instituto de Ecología Regional (UNT – CONICET). C.C. 34. Yerba Buena (4107), Tucumán, Argentina. Corresponding author: davidlautarov@gmail.com Received on 31 March 2016. Accepted on 22 December 2016. ABSTRACT: The migration patterns of passerine species in the Neotropical region present several gaps of knowledge. The migratory behavior of the Slaty Thrush ( Turdus nigriceps nigriceps) has been well characterized in their central and northern distribution along eastern slopes of the Andes from Argentina to Ecuador. The S laty Thrush was historically considered a migrant breeder in the southern extreme of their distribution. In the present study, we show new evidence of the resident status of this species in its southernmost distribution on western slopes of Sierras Grandes and Sierras de Comechingones in Córdoba Province, Argentina. There, the S laty Thrush has a year-round presence only at sites invaded by fleshy-fruited a lien plants. The main invasive plants form dense patches of vegetation and offer an abundant fruit supply that is highly consumed by this bird species during autumn–winter, when there are no native fruits available. We suggest that the Slaty Thrush was a migrant species in past decades, but the recent invasion by fleshy-fruited species could explain its actual year-round presence b y providing fruit in a period of the year of food shortage and new suitable habitats. KEY-WORDS: Chaco Serrano Woodland, Córdoba, nonbreeding season, plant invasion, western Sierras Grandes. INTRODUCTION on eastern slopes of the Andes from western Bolivia (Cochabamba and southern Beni) to northwestern Several species of the Turdidae family are distributed over Argentina (the southernmost distribution in La Rioja the different Argentinian ecosystems (Mazar-Barnett & and Córdoba Provinces). The bree ding season begins in November–December and ends in January–February, Pearman 2001), but the ecology of some of them is still poorly understood (Collar 2005). Slaty Thrush ( Turdus when nestlings leave the nests (Collar 2005). In austral nigriceps) is a medium size thrush (21.5 cm). Males are winter (June–September) populations at the southern end mostly dark gray above, blacker on the crown and have of the distribution migrate north following the Andean a white throat sharply streaked blackish; females are forests and reach eastern Peru. At the northern end of their distribution, T. nigriceps is resident and breeds basically brown where males are gray, though some gray shows on the sides and flanks (Ridgely & Tudor 2009). in montane woodlands and even in scrublands from According to Sibley & Monroe (1993), the Slaty Thrush southwestern Ecuador (mainly Loja) to northwestern have a controversial taxonomic status with two currently Peru (northern Cajamarca and Lambayeque; see Figure 1; recognized subspecies distributed alopatrically (Collar Ridgely & Greenfield 2001). In Argentina, T. ni griceps is a partial migrant in the southern Yungas of Tucumán, Jujuy 2005, Remsen-Jr. et al. 2015; it is considered as two full species for Ridgely & Tudor 2009). Both subspecies are and Salta Provinces (Rougès & Blake 2001, Capllonch et mainly frugivorous and occasionally consume arthropods al. 2008), and Collar (2005) suggests they may undertake and earthworms (Rougès & Blake 2001, Collar 2005). altitudinal movements. Details about the migratory Turdus nigriceps subalaris is an uncommon breeder behavior of this species in its southernmost distribution remains unclear (see Collar 2005 and Appendix I in in humid forests and woodlands in eastern Paraguay, southeastern Brazil and northeastern Argentina. In austral Capllonch et al. 2008). winter, this subspecies migrates to non-breeding areas in In Córdoba Province, the Slaty Thrush was northern to southern central Brazil (Ridgely & Tudor historically considered a scarce summer migrant (Nores et 2009, but see Vogel 2014). Turdus nigriceps nigriceps is a al. 1983, Yzurieta 1995) because of the absence of winter th records until the last decade of the 20 Century (M. Nores, fairly common breeder in montane forest and woodland Year-round presence of Slaty Thrush (Tur dus nigriceps nigriceps) in mountains of central Argentina David L. Vergara-Tabares and Tobías N. Rojas pers. comm. ). However, recent records during the non- atalantoides as well as L. lucidum and M. alba are native breeding period questioned the actual migratory status of from southeast Asia. Some of these species, including P. the subspecies in the southernmost area of its distribution angustifolia and P. atalantoides, occasionally form dense (Barri et al. 2015). In this area, the Slaty Thrush inhabits patches of vegetation and produce fruit during autumn– humid ravines of the Chaco Serrano woodlands (Yzurieta winter, when native fruit is scarce or absent (Vergara- 1995, Figure 1) from 900 to 1500 m a.s.l. (Luti et al. Tabares et al. 2016). The other three sites (Las Rabonas, 1979, Cabido et al. 1998). Currently, many areas of this Travesia and Luyaba; green areas in Figure 1) do not region suffer from anthropogenic alterations such as plant have fleshy-fruited invasive plants. In or der to control for invasions, urbanization, and periodic fires (Hoyos et al. aspects that may affect the presence of S laty Thrush, we 2010, Giorgis & Tecco 2014, Argañaraz et al. 2015). selected the six sites regarding its altitude (between 900 These alterations modify the environmental physiognomy and 1100 m a.s.l.) and similarity in plant community and food resource abundance and availability (Hoyos (mountain forests dominated by L. molleoides). As the et al. 2010, Tecco et al. 2013). Some invasive plants maximal distance between study sites (i.e. Las Rabonas such as Pyracantha spp., Ligustrum lucidum and Morus to Luyaba) is approximately 50 km, it is probable that alba produce fleshy fruits that are widely consumed and climatic conditions (precipitation or temperature) among dispersed by birds like Slaty Thrushes (Vergara-Tabares et all sites did not vary greatly. al. 2016). Fruit production by these plants may alter the temporal availability of this resource (Vergara-Tabares et al. 2016), because they produce fruits in periods of food scarcity (i.e. autumn-winter, Tecco et al. 2013). Thus, fleshy-fruited p lant invasions may be involved in a switch of Slaty Thrush behavior from migratory to resident. In the present study we (1) report the year-round presence of Slaty Thrush in its southernmost distribution in Chaco Serrano woodlands, and (2) discuss the potential effect of fleshy-fruited invasive plants on the residence status of the Slaty Thrush. METHODS Study area The study was carried out in six sites located on western slopes of Sierras Grandes and Sierras de Comechingones between 900 to 1300 m a.s.l., Córdoba Province, Argentina (Figure 1). The topography of each selected FIGURE 1. Distribution of Slaty Thrush ( Turdus nigriceps nigriceps) site is characterized by a ravine where runs a stream. and the southern portion of its distribution where we conducted All six sites present a plant assemblage corresponding fieldwork. In the upper frame, we show t he distribution of the western to the Chaco Serrano woodland (Luti et al. 1979). subspecies of Slaty Thrush ( sensu Ridgely & Tudor 2009); dark green Mean annual precipitation in the area is approximately in the northern part of the distribution shows the range of resident and breeder populations that inhabit southern Ecuador and northern 700–800 mm (concentrated in summer) and mean Peru; light green shows the areas where Slaty Thrush visits during the annual temperature is 17.5°C (data taken at the station austral winter; and dark green in the southern part of the distribution La Ventana; Acosta et al. 1992). The dominant wood indicates the breeding areas during austral spring-summer. In the right species are Lithraea molleoides, followed by Acacia caven, frame, we show our six study sites. Red areas indicate invaded sites by Celtis ehrenbergiana and Bouganvillea stipitata. Among fleshy fruited Pyracantha shrubs; from north to south: Las Calles, Los Hornillos, and San Javier. Green areas indicate sites that have not been dominant shrub plants are Heterothalamus alienus, and invaded by alien plants; from north to south: Las Rabonas; Travesía, species of the genera Flourensia sp. and Baccharis spp. and Luyaba. (Cabido et al. 1998). Three sites (Las Calles, San Javier, Sampling methods and Los Hornillos; red areas in Figure 1) are invaded by fleshy-fruited p lants. The most abundant invasive shru bs We performed visual and aural searches of Slaty Thrush correspond to fleshy-fruited Pyracantha angustifolia and P. atalantoides, and to a lesser extent Ligustrum lucidum, during April, July and September in 2014 and during Morus alba, and Olea europea. Both P. angustifolia and P. January, May, August, October and December 2015. Revista Brasileira de Ornitologia, 24(4), 2016 Year-round presence of Slaty Thrush (Tur dus nigriceps nigriceps) in mountains of central Argentina David L. Vergara-Tabares and Tobías N. Rojas In both years we looked for Slaty Thrush a long an we recorded the number of individuals of Slaty Thrush unstructured trail of three km along the ravine of each detected. During 2014, we sampled three sites (Los study site. These searches consisted of 4 h walks along Hornillos, San Javier and Luyaba, Table 1), and during the study sites during the morning or afternoon, and 2015 we sampled the remaining six sites mentioned. TABLE 1. Number of individuals of Slaty Thrush ( Turdus nigriceps nigriceps) captured using mist nets and number of individuals of this species recorded during unstructured trails in the southern end of their distribution during April, July, and September 2014. The study sites included t hose invaded by exotic fleshy fruited plants: Los Hornillos and San Javier, and a non-invaded site: Luyaba. April July September Habitat Locality Captures Trails Captures Trails Captures Trails Invaded Los Hornillos 3 7 4 11 3 10 San Javier 4 15 9 25 12 18 Non Invaded Luyaba2 1 0 0 0 0 We also used mist nets during between 20–29 April, before starting counts (Bibby et al. 1992). Slaty Thrush 10–19 July, and 20–29 September 2014 at three sites (Los individuals occurring within a 50-m fixed radius of each Hornillos, San Javier, and Luyaba; Table 1). Nets were point were recorded visually or aurally. Observations mounted in sites with more intense bird activity and were were made during 10 min at each point count and we separated by at least 50 m (i.e. near the streams and/or surveyed only under favorable weather conditions, within between patches of arboreal vegetation). Once captured, a 4-h period after sunrise. Point counts were conducted the birds were aged by looking at the bill and leg color between 6–11 January, 1–6 May, 1–6 August, 10–15 that appear with dark irregular spots when the individual October, and 26–31 December. is immature. Sex was determined based on plumage, as this species has sexual dichromatism. Birds were ringed Data analysis on their right leg with a color ring. In addition, feces produced by birds during the captures where collected To evaluate the effect of presence of Pyr acantha shrubs to identify plants consumed. We opened four 12-m nets and sampling period on Slaty Thrush a bundance we used from sunrise to 12:00 h and from 16:00 h to sunset during a two way GLM with interaction (Zuur et al. 2009). three successive days (approximately 108 h/net per site). We used the bird abundance obtained from surveys in During 2015, we performed a minimum of 20 trails conducted during 2015 as response variable and point counts (a total of 772 point counts) in each of the condition (with two levels: invaded and non-invaded) six sites to detect and count Slaty Thrushes (three among and the period (with five levels; Table 2) as factors. The these six sites where the same where we used mist nests six study sites were used as replicates, three invaded in the previous year; Figure 1 & Table 2). At each site, (Las Calles, Los Hornillos and San Javier) and three point counts were separated by at least 150 m to avoid non-invaded (Las Rabonas, Travesía and Luyaba). A double-counts between neighboring points. Point counts negative binomial error distribution was used to deal were established along the same unstructured trails where with overdispersion in abundance data. Analyses were we conducted the visual and aural surveys. At each point, performed using the software R (R Core Team 2014) and the researcher waited 5 min as a settling down period the package glmmADMB (Skaug et al. 2012). TABLE 2. Number of individuals of Slaty Thrush ( Turdus nigriceps nigriceps) registered throughout point counts and unstructured trails during January, May, August, October, and December 2015. In that year the study sites were Las Calles, Los Hornillos, and San Javier (invaded); and Las Rabonas, Travesía, and Luyaba (non-invaded). The number of point counts b y month and locality are indicated in parenthesis and the number outside the parenthesis indicates the total number of birds recorded in point counts. JanuaryMay August October December Count Count Count Count Count Trails Trails Trails Trails Trails Habitat Locality points points points points points Invaded Las Calles 0 (30) 1 0 (28) 1 0 (28) 2 0 (20) 0 1 (20) 3 Los Hornillos 2 (37) 12 3 (30) 18 2 (29) 15 2 (20) 5 5 (20) 9 San Javier 1 (30) 18 4 (29) 14 12 (30) 21 8 (22) 26 5 (29) 12 Non Invaded Las Rabonas 0 (29) 2 0 (20) 2 0 (25) 0 0 (20) 0 4 (21) 4 Travesia 0 (30) 0 0 (29) 0 0 (30) 0 0 (20) 0 0 (20) 0 Luyaba 0 (39) 0 0 (28) 0 0 (29) 0 1 (20) 0 0 (20) 1 Revista Brasileira de Ornitologia, 24(4), 2016 Year-round presence of Slaty Thrush (Tur dus nigriceps nigriceps) in mountains of central Argentina David L. Vergara-Tabares and Tobías N. Rojas RESULTS only obtained during the breeding season (November to February – Nores 1996, Capllonch et al. 2008, M. Slaty Thrush was registered during all sampling periods Nores, pers. comm.). If Slaty Thrush was a migrant that left southern areas in past decades, the current only in two of the sites invaded by non-native plants (Los Hornillos and San Javier) during 2014 and 2015 (Table resident behavior may be plausibly explained by recent 1 & 2). During April 2014 we captured and registered anthropogenic environmental changes, such as invasion thrushes at all study sites (i.e. Luyaba, Los Hornillos by fleshy-fruited exotic plants. Our results show t hat and San Javier). During July and September 2014, we Slaty Thrush was more abundant throughout the year in invaded vs. non-invaded areas, not only during the only captured and recorded thrushes at invaded sites (i.e. Los Hornillos and San Javier; Table 1). We captured fruiting period of invasive plants (Table 2), ruling out two individuals with immature plumage only in July the suggestion that the presence of the Slaty Thrush may at Los Hornillos, and two females in September in San be only related to invasive fleshy fruit during autumn– Javier. We collected feces from two individuals from Los winter. The pattern of presence observed suggests that plant invasion by Pyracantha species would have an Hornillos during July and three individuals from San Javier during September. In all of the feces we found seeds effect on resident behavior of Slaty Thrush, maybe due of L. molleoides and Pyracantha sp. to the generation of adequate micro or mesohabitats and The GLM analysis showe d that only the condition the availability of fruits during periods of fruit scarcity. (invaded or non-invaded) affected S laty Thrush Although the magnitude of plant invasion in our study sites is lesser than other regions in Chaco Serrano abundance, being the abundance higher at invaded sites ( = 34.04, P < 0.001), while the interaction between Woodland (e.g. Hoyos et al. 2010), the density, size and 1,27 condition and period, or period alone, did not affect bir d scattered distribution of patches of invasive plants may be abundance (Table 2 & Figure 2). sufficient for S laty Thrush requirements. There is evidence supporting the positive effects of fleshy fruited invasive plants on abundance of frugivorous birds (e.g. Gleditsch & Carlo 2011, Vergara-Tabares unpubl. data) and other researches have documented cases where individuals and populations respond rapidly to changing environmental conditions, leading to a modification in their migratory behavior (e.g. Berthold et al. 1992, Whittington et al. 1999). Slaty Thrush has been considered a partial migrant species, showing high seasonal fluctuations, and being more abundant during the breeding season in spring- January May August October December summer in the southern Yungas (Capllonch et al. 2008, Period Rougès & Blake 2001). In contrast, we obtained a similar FIGURE 2. Mean abundance of Slaty Thrush per site observed in number of records of the species throughout the year trails during 2015 in relation to sampling period, and particionated by invaded and non invaded condition. Green box indicates non invaded during 2014 and 2015, mainly at sites invaded by exotic sites and red box indicates sites invaded by Pyracantha shrubs. Boxes plants. At non-invaded sites, the presence of Slaty Thrush show standard error. was variable, occurring mainly during the breeding season, despite at a lower frequency than in invaded DISCUSSION areas. In addition, it is important to highlight that our study area was located at the southernmost end of the There is a gap in the current literature about the distribution of Slaty Thrush. This situation allows us to migratory status of Slaty Thrush in the southern areas discard the possibility that the Slaty Thrush found here of its distribution (Collar 2005). Our observations did not belong to a southern locality. indicate that Slaty Thrush has a year-round presence in From a general perspective regarding the distribution some sites characterized by invasive fleshy-fruit species of Slaty Thrush, previous evidence supports a resident (mainly Pyracantha shrubs) at the southern end of its status at the northern end of their distribution (Fjeldså distribution. Contrary to documented partial migratory & Krabbe 1990, Best et al. 1993, Rasmussen et al. 1996), behavior in northern Argentina (Capllonch et al. 2008), while other studies reveal a uniquely winter presence of the our data supports the recent consideration of Slaty species in the eastern Andes of central and southern Peru Thrush as a resident species in a reduced area of their (Schulenberg 1987, Walker 2001). Finally, Capllonch et southern distribution (Barri et al. 2015). Previous records al. (2008) analyzing twenty years of data, revealed the at Córdoba Province (during the 1980's and 90's) were migratory behavior of Slaty Thrush mainly in the Yungas Revista Brasileira de Ornitologia, 24(4), 2016 Slaty Thrush abundance (birds/site) Year-round presence of Slaty Thrush (Tur dus nigriceps nigriceps) in mountains of central Argentina David L. Vergara-Tabares and Tobías N. Rojas Fjeldså, J. & Krabbe, N. 1990. Birds of the high Andes.  A manual of northwestern Argentina, and Collar (2005) does not to the birds of the temperate zone of the Andes and Patagonia, rule out altitudinal movements of this species. Our data South America. Copenhagen & Svendborg: Zoological Museum, suggests that Slaty Thrush has a resident behavior in the University of Copenhagen & Apollo Books southern extreme of its distribution, clearly associated Giorgis, M. & Tecco, P. A. 2014. Árboles y arbustos invasores de la Provincia de Córdoba (Argentina): una contribución a la with sites invaded by fleshy fruited p lants. If Slaty Thrush sistematización de bases de datos globales. Boletín de la Sociedad was a migrant species in past decades, the recent invasion Argentina de Botánica, 49: 681–603. by fleshy fruited p lants and environmental changes Gleditsch, J. M. & Carlo, T. A. 2011. Fruit quantity of invasive caused by such invasion may explains the recent year- shrubs predicts the abundance of common native avian frugivores round presence of this species, through the creation of in central Pennsylvania. Diversity and Distributions, 17: 244–253. Hoyos, L. E.; Gavier-Pizarro, G. I.; Kuermmerle, T.;  Bucher, E. micro and/or mesohabitats and availability of fleshy fruits H.; Volker, C. R. & Tecco, P. A. 2010. Invasion of Glossy Privet during autumn–winter. (Ligustrum lucidum) and native forest loss in the Sierras Chicas of Cordoba, Argentina. Biological Invasions, 12: 3261–3275. Luti, R.; Solis, M.; Galera, F.; Müller-de-Ferreira, N.; Berzal, M.; ACKNOWLEDGEMENTS Nores, M.; Herrera, M. & Barrera, J. C. 1979. Vegetación, p. 297–368 In: Vasquez, J. B.; Lopez-Robles, A.; Sosa, D. F. & Saez, M. P. (eds.). Geografía física de la Provincia de Córdoba. Buenos Funding was provided by Association of Field Aires: Boldt. Ornithologists (Bergstrom Memorial Award to DLV-T). 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Year-round presence of Slaty Thrush (Turdus nigriceps nigriceps) in mountains of central Argentina

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Revista Brasileira de Ornitologia, 24(4), 329–334 ARTICLE December 2016 Year-round presence of Slaty Thr ush (Turdus nigriceps nigriceps) in mountains of central Argentina 1,3 2 David L. Vergara-Tabares and Tobías N. Rojas Instituto de Diversidad y Ecología Animal, CCT-Córdoba-CONICET. Rondeau 798, Córdoba (5000), Córdoba, Argentina. Instituto de Ecología Regional (UNT – CONICET). C.C. 34. Yerba Buena (4107), Tucumán, Argentina. Corresponding author: davidlautarov@gmail.com Received on 31 March 2016. Accepted on 22 December 2016. ABSTRACT: The migration patterns of passerine species in the Neotropical region present several gaps of knowledge. The migratory behavior of the Slaty Thrush ( Turdus nigriceps nigriceps) has been well characterized in their central and northern distribution along eastern slopes of the Andes from Argentina to Ecuador. The S laty Thrush was historically considered a migrant breeder in the southern extreme of their distribution. In the present study, we show new evidence of the resident status of this species in its southernmost distribution on western slopes of Sierras Grandes and Sierras de Comechingones in Córdoba Province, Argentina. There, the S laty Thrush has a year-round presence only at sites invaded by fleshy-fruited a lien plants. The main invasive plants form dense patches of vegetation and offer an abundant fruit supply that is highly consumed by this bird species during autumn–winter, when there are no native fruits available. We suggest that the Slaty Thrush was a migrant species in past decades, but the recent invasion by fleshy-fruited species could explain its actual year-round presence b y providing fruit in a period of the year of food shortage and new suitable habitats. KEY-WORDS: Chaco Serrano Woodland, Córdoba, nonbreeding season, plant invasion, western Sierras Grandes. INTRODUCTION on eastern slopes of the Andes from western Bolivia (Cochabamba and southern Beni) to northwestern Several species of the Turdidae family are distributed over Argentina (the southernmost distribution in La Rioja the different Argentinian ecosystems (Mazar-Barnett & and Córdoba Provinces). The bree ding season begins in November–December and ends in January–February, Pearman 2001), but the ecology of some of them is still poorly understood (Collar 2005). Slaty Thrush ( Turdus when nestlings leave the nests (Collar 2005). In austral nigriceps) is a medium size thrush (21.5 cm). Males are winter (June–September) populations at the southern end mostly dark gray above, blacker on the crown and have of the distribution migrate north following the Andean a white throat sharply streaked blackish; females are forests and reach eastern Peru. At the northern end of their distribution, T. nigriceps is resident and breeds basically brown where males are gray, though some gray shows on the sides and flanks (Ridgely & Tudor 2009). in montane woodlands and even in scrublands from According to Sibley & Monroe (1993), the Slaty Thrush southwestern Ecuador (mainly Loja) to northwestern have a controversial taxonomic status with two currently Peru (northern Cajamarca and Lambayeque; see Figure 1; recognized subspecies distributed alopatrically (Collar Ridgely & Greenfield 2001). In Argentina, T. ni griceps is a partial migrant in the southern Yungas of Tucumán, Jujuy 2005, Remsen-Jr. et al. 2015; it is considered as two full species for Ridgely & Tudor 2009). Both subspecies are and Salta Provinces (Rougès & Blake 2001, Capllonch et mainly frugivorous and occasionally consume arthropods al. 2008), and Collar (2005) suggests they may undertake and earthworms (Rougès & Blake 2001, Collar 2005). altitudinal movements. Details about the migratory Turdus nigriceps subalaris is an uncommon breeder behavior of this species in its southernmost distribution remains unclear (see Collar 2005 and Appendix I in in humid forests and woodlands in eastern Paraguay, southeastern Brazil and northeastern Argentina. In austral Capllonch et al. 2008). winter, this subspecies migrates to non-breeding areas in In Córdoba Province, the Slaty Thrush was northern to southern central Brazil (Ridgely & Tudor historically considered a scarce summer migrant (Nores et 2009, but see Vogel 2014). Turdus nigriceps nigriceps is a al. 1983, Yzurieta 1995) because of the absence of winter th records until the last decade of the 20 Century (M. Nores, fairly common breeder in montane forest and woodland Year-round presence of Slaty Thrush (Tur dus nigriceps nigriceps) in mountains of central Argentina David L. Vergara-Tabares and Tobías N. Rojas pers. comm. ). However, recent records during the non- atalantoides as well as L. lucidum and M. alba are native breeding period questioned the actual migratory status of from southeast Asia. Some of these species, including P. the subspecies in the southernmost area of its distribution angustifolia and P. atalantoides, occasionally form dense (Barri et al. 2015). In this area, the Slaty Thrush inhabits patches of vegetation and produce fruit during autumn– humid ravines of the Chaco Serrano woodlands (Yzurieta winter, when native fruit is scarce or absent (Vergara- 1995, Figure 1) from 900 to 1500 m a.s.l. (Luti et al. Tabares et al. 2016). The other three sites (Las Rabonas, 1979, Cabido et al. 1998). Currently, many areas of this Travesia and Luyaba; green areas in Figure 1) do not region suffer from anthropogenic alterations such as plant have fleshy-fruited invasive plants. In or der to control for invasions, urbanization, and periodic fires (Hoyos et al. aspects that may affect the presence of S laty Thrush, we 2010, Giorgis & Tecco 2014, Argañaraz et al. 2015). selected the six sites regarding its altitude (between 900 These alterations modify the environmental physiognomy and 1100 m a.s.l.) and similarity in plant community and food resource abundance and availability (Hoyos (mountain forests dominated by L. molleoides). As the et al. 2010, Tecco et al. 2013). Some invasive plants maximal distance between study sites (i.e. Las Rabonas such as Pyracantha spp., Ligustrum lucidum and Morus to Luyaba) is approximately 50 km, it is probable that alba produce fleshy fruits that are widely consumed and climatic conditions (precipitation or temperature) among dispersed by birds like Slaty Thrushes (Vergara-Tabares et all sites did not vary greatly. al. 2016). Fruit production by these plants may alter the temporal availability of this resource (Vergara-Tabares et al. 2016), because they produce fruits in periods of food scarcity (i.e. autumn-winter, Tecco et al. 2013). Thus, fleshy-fruited p lant invasions may be involved in a switch of Slaty Thrush behavior from migratory to resident. In the present study we (1) report the year-round presence of Slaty Thrush in its southernmost distribution in Chaco Serrano woodlands, and (2) discuss the potential effect of fleshy-fruited invasive plants on the residence status of the Slaty Thrush. METHODS Study area The study was carried out in six sites located on western slopes of Sierras Grandes and Sierras de Comechingones between 900 to 1300 m a.s.l., Córdoba Province, Argentina (Figure 1). The topography of each selected FIGURE 1. Distribution of Slaty Thrush ( Turdus nigriceps nigriceps) site is characterized by a ravine where runs a stream. and the southern portion of its distribution where we conducted All six sites present a plant assemblage corresponding fieldwork. In the upper frame, we show t he distribution of the western to the Chaco Serrano woodland (Luti et al. 1979). subspecies of Slaty Thrush ( sensu Ridgely & Tudor 2009); dark green Mean annual precipitation in the area is approximately in the northern part of the distribution shows the range of resident and breeder populations that inhabit southern Ecuador and northern 700–800 mm (concentrated in summer) and mean Peru; light green shows the areas where Slaty Thrush visits during the annual temperature is 17.5°C (data taken at the station austral winter; and dark green in the southern part of the distribution La Ventana; Acosta et al. 1992). The dominant wood indicates the breeding areas during austral spring-summer. In the right species are Lithraea molleoides, followed by Acacia caven, frame, we show our six study sites. Red areas indicate invaded sites by Celtis ehrenbergiana and Bouganvillea stipitata. Among fleshy fruited Pyracantha shrubs; from north to south: Las Calles, Los Hornillos, and San Javier. Green areas indicate sites that have not been dominant shrub plants are Heterothalamus alienus, and invaded by alien plants; from north to south: Las Rabonas; Travesía, species of the genera Flourensia sp. and Baccharis spp. and Luyaba. (Cabido et al. 1998). Three sites (Las Calles, San Javier, Sampling methods and Los Hornillos; red areas in Figure 1) are invaded by fleshy-fruited p lants. The most abundant invasive shru bs We performed visual and aural searches of Slaty Thrush correspond to fleshy-fruited Pyracantha angustifolia and P. atalantoides, and to a lesser extent Ligustrum lucidum, during April, July and September in 2014 and during Morus alba, and Olea europea. Both P. angustifolia and P. January, May, August, October and December 2015. Revista Brasileira de Ornitologia, 24(4), 2016 Year-round presence of Slaty Thrush (Tur dus nigriceps nigriceps) in mountains of central Argentina David L. Vergara-Tabares and Tobías N. Rojas In both years we looked for Slaty Thrush a long an we recorded the number of individuals of Slaty Thrush unstructured trail of three km along the ravine of each detected. During 2014, we sampled three sites (Los study site. These searches consisted of 4 h walks along Hornillos, San Javier and Luyaba, Table 1), and during the study sites during the morning or afternoon, and 2015 we sampled the remaining six sites mentioned. TABLE 1. Number of individuals of Slaty Thrush ( Turdus nigriceps nigriceps) captured using mist nets and number of individuals of this species recorded during unstructured trails in the southern end of their distribution during April, July, and September 2014. The study sites included t hose invaded by exotic fleshy fruited plants: Los Hornillos and San Javier, and a non-invaded site: Luyaba. April July September Habitat Locality Captures Trails Captures Trails Captures Trails Invaded Los Hornillos 3 7 4 11 3 10 San Javier 4 15 9 25 12 18 Non Invaded Luyaba2 1 0 0 0 0 We also used mist nets during between 20–29 April, before starting counts (Bibby et al. 1992). Slaty Thrush 10–19 July, and 20–29 September 2014 at three sites (Los individuals occurring within a 50-m fixed radius of each Hornillos, San Javier, and Luyaba; Table 1). Nets were point were recorded visually or aurally. Observations mounted in sites with more intense bird activity and were were made during 10 min at each point count and we separated by at least 50 m (i.e. near the streams and/or surveyed only under favorable weather conditions, within between patches of arboreal vegetation). Once captured, a 4-h period after sunrise. Point counts were conducted the birds were aged by looking at the bill and leg color between 6–11 January, 1–6 May, 1–6 August, 10–15 that appear with dark irregular spots when the individual October, and 26–31 December. is immature. Sex was determined based on plumage, as this species has sexual dichromatism. Birds were ringed Data analysis on their right leg with a color ring. In addition, feces produced by birds during the captures where collected To evaluate the effect of presence of Pyr acantha shrubs to identify plants consumed. We opened four 12-m nets and sampling period on Slaty Thrush a bundance we used from sunrise to 12:00 h and from 16:00 h to sunset during a two way GLM with interaction (Zuur et al. 2009). three successive days (approximately 108 h/net per site). We used the bird abundance obtained from surveys in During 2015, we performed a minimum of 20 trails conducted during 2015 as response variable and point counts (a total of 772 point counts) in each of the condition (with two levels: invaded and non-invaded) six sites to detect and count Slaty Thrushes (three among and the period (with five levels; Table 2) as factors. The these six sites where the same where we used mist nests six study sites were used as replicates, three invaded in the previous year; Figure 1 & Table 2). At each site, (Las Calles, Los Hornillos and San Javier) and three point counts were separated by at least 150 m to avoid non-invaded (Las Rabonas, Travesía and Luyaba). A double-counts between neighboring points. Point counts negative binomial error distribution was used to deal were established along the same unstructured trails where with overdispersion in abundance data. Analyses were we conducted the visual and aural surveys. At each point, performed using the software R (R Core Team 2014) and the researcher waited 5 min as a settling down period the package glmmADMB (Skaug et al. 2012). TABLE 2. Number of individuals of Slaty Thrush ( Turdus nigriceps nigriceps) registered throughout point counts and unstructured trails during January, May, August, October, and December 2015. In that year the study sites were Las Calles, Los Hornillos, and San Javier (invaded); and Las Rabonas, Travesía, and Luyaba (non-invaded). The number of point counts b y month and locality are indicated in parenthesis and the number outside the parenthesis indicates the total number of birds recorded in point counts. JanuaryMay August October December Count Count Count Count Count Trails Trails Trails Trails Trails Habitat Locality points points points points points Invaded Las Calles 0 (30) 1 0 (28) 1 0 (28) 2 0 (20) 0 1 (20) 3 Los Hornillos 2 (37) 12 3 (30) 18 2 (29) 15 2 (20) 5 5 (20) 9 San Javier 1 (30) 18 4 (29) 14 12 (30) 21 8 (22) 26 5 (29) 12 Non Invaded Las Rabonas 0 (29) 2 0 (20) 2 0 (25) 0 0 (20) 0 4 (21) 4 Travesia 0 (30) 0 0 (29) 0 0 (30) 0 0 (20) 0 0 (20) 0 Luyaba 0 (39) 0 0 (28) 0 0 (29) 0 1 (20) 0 0 (20) 1 Revista Brasileira de Ornitologia, 24(4), 2016 Year-round presence of Slaty Thrush (Tur dus nigriceps nigriceps) in mountains of central Argentina David L. Vergara-Tabares and Tobías N. Rojas RESULTS only obtained during the breeding season (November to February – Nores 1996, Capllonch et al. 2008, M. Slaty Thrush was registered during all sampling periods Nores, pers. comm.). If Slaty Thrush was a migrant that left southern areas in past decades, the current only in two of the sites invaded by non-native plants (Los Hornillos and San Javier) during 2014 and 2015 (Table resident behavior may be plausibly explained by recent 1 & 2). During April 2014 we captured and registered anthropogenic environmental changes, such as invasion thrushes at all study sites (i.e. Luyaba, Los Hornillos by fleshy-fruited exotic plants. Our results show t hat and San Javier). During July and September 2014, we Slaty Thrush was more abundant throughout the year in invaded vs. non-invaded areas, not only during the only captured and recorded thrushes at invaded sites (i.e. Los Hornillos and San Javier; Table 1). We captured fruiting period of invasive plants (Table 2), ruling out two individuals with immature plumage only in July the suggestion that the presence of the Slaty Thrush may at Los Hornillos, and two females in September in San be only related to invasive fleshy fruit during autumn– Javier. We collected feces from two individuals from Los winter. The pattern of presence observed suggests that plant invasion by Pyracantha species would have an Hornillos during July and three individuals from San Javier during September. In all of the feces we found seeds effect on resident behavior of Slaty Thrush, maybe due of L. molleoides and Pyracantha sp. to the generation of adequate micro or mesohabitats and The GLM analysis showe d that only the condition the availability of fruits during periods of fruit scarcity. (invaded or non-invaded) affected S laty Thrush Although the magnitude of plant invasion in our study sites is lesser than other regions in Chaco Serrano abundance, being the abundance higher at invaded sites ( = 34.04, P < 0.001), while the interaction between Woodland (e.g. Hoyos et al. 2010), the density, size and 1,27 condition and period, or period alone, did not affect bir d scattered distribution of patches of invasive plants may be abundance (Table 2 & Figure 2). sufficient for S laty Thrush requirements. There is evidence supporting the positive effects of fleshy fruited invasive plants on abundance of frugivorous birds (e.g. Gleditsch & Carlo 2011, Vergara-Tabares unpubl. data) and other researches have documented cases where individuals and populations respond rapidly to changing environmental conditions, leading to a modification in their migratory behavior (e.g. Berthold et al. 1992, Whittington et al. 1999). Slaty Thrush has been considered a partial migrant species, showing high seasonal fluctuations, and being more abundant during the breeding season in spring- January May August October December summer in the southern Yungas (Capllonch et al. 2008, Period Rougès & Blake 2001). In contrast, we obtained a similar FIGURE 2. Mean abundance of Slaty Thrush per site observed in number of records of the species throughout the year trails during 2015 in relation to sampling period, and particionated by invaded and non invaded condition. Green box indicates non invaded during 2014 and 2015, mainly at sites invaded by exotic sites and red box indicates sites invaded by Pyracantha shrubs. Boxes plants. At non-invaded sites, the presence of Slaty Thrush show standard error. was variable, occurring mainly during the breeding season, despite at a lower frequency than in invaded DISCUSSION areas. In addition, it is important to highlight that our study area was located at the southernmost end of the There is a gap in the current literature about the distribution of Slaty Thrush. This situation allows us to migratory status of Slaty Thrush in the southern areas discard the possibility that the Slaty Thrush found here of its distribution (Collar 2005). Our observations did not belong to a southern locality. indicate that Slaty Thrush has a year-round presence in From a general perspective regarding the distribution some sites characterized by invasive fleshy-fruit species of Slaty Thrush, previous evidence supports a resident (mainly Pyracantha shrubs) at the southern end of its status at the northern end of their distribution (Fjeldså distribution. Contrary to documented partial migratory & Krabbe 1990, Best et al. 1993, Rasmussen et al. 1996), behavior in northern Argentina (Capllonch et al. 2008), while other studies reveal a uniquely winter presence of the our data supports the recent consideration of Slaty species in the eastern Andes of central and southern Peru Thrush as a resident species in a reduced area of their (Schulenberg 1987, Walker 2001). Finally, Capllonch et southern distribution (Barri et al. 2015). Previous records al. (2008) analyzing twenty years of data, revealed the at Córdoba Province (during the 1980's and 90's) were migratory behavior of Slaty Thrush mainly in the Yungas Revista Brasileira de Ornitologia, 24(4), 2016 Slaty Thrush abundance (birds/site) Year-round presence of Slaty Thrush (Tur dus nigriceps nigriceps) in mountains of central Argentina David L. Vergara-Tabares and Tobías N. Rojas Fjeldså, J. & Krabbe, N. 1990. Birds of the high Andes.  A manual of northwestern Argentina, and Collar (2005) does not to the birds of the temperate zone of the Andes and Patagonia, rule out altitudinal movements of this species. Our data South America. Copenhagen & Svendborg: Zoological Museum, suggests that Slaty Thrush has a resident behavior in the University of Copenhagen & Apollo Books southern extreme of its distribution, clearly associated Giorgis, M. & Tecco, P. A. 2014. Árboles y arbustos invasores de la Provincia de Córdoba (Argentina): una contribución a la with sites invaded by fleshy fruited p lants. If Slaty Thrush sistematización de bases de datos globales. Boletín de la Sociedad was a migrant species in past decades, the recent invasion Argentina de Botánica, 49: 681–603. by fleshy fruited p lants and environmental changes Gleditsch, J. M. & Carlo, T. A. 2011. Fruit quantity of invasive caused by such invasion may explains the recent year- shrubs predicts the abundance of common native avian frugivores round presence of this species, through the creation of in central Pennsylvania. Diversity and Distributions, 17: 244–253. Hoyos, L. E.; Gavier-Pizarro, G. I.; Kuermmerle, T.;  Bucher, E. micro and/or mesohabitats and availability of fleshy fruits H.; Volker, C. R. & Tecco, P. A. 2010. Invasion of Glossy Privet during autumn–winter. (Ligustrum lucidum) and native forest loss in the Sierras Chicas of Cordoba, Argentina. Biological Invasions, 12: 3261–3275. Luti, R.; Solis, M.; Galera, F.; Müller-de-Ferreira, N.; Berzal, M.; ACKNOWLEDGEMENTS Nores, M.; Herrera, M. & Barrera, J. C. 1979. Vegetación, p. 297–368 In: Vasquez, J. B.; Lopez-Robles, A.; Sosa, D. F. & Saez, M. P. (eds.). Geografía física de la Provincia de Córdoba. Buenos Funding was provided by Association of Field Aires: Boldt. Ornithologists (Bergstrom Memorial Award to DLV-T). 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Journal

Ornithology Research – Springer Journals

Published: Dec 1, 2016

Keywords: Chaco Serrano Woodland; Córdoba; nonbreeding season; plant invasion; western Sierras Grandes

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