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Hybridization between Yellow-billed Cardinal Paroaria capitata and Red-crested Cardinal P. coronata in southern Argentina

Hybridization between Yellow-billed Cardinal Paroaria capitata and Red-crested Cardinal P.... Revista Brasileira de Ornitologia 27(2): 129–131. SHORT-COMMUNIC ARTICLE ATION June 2019 Hybridization between Yellow-billed Cardinal Paroaria capitata and Red-crested Cardinal P. coronata in southern Argentina 1,4 2 3 Luciano N. Segura , Federico A. De Maio & Mauricio Failla Sección Ornitología, Museo de La Plata, Universidad Nacional de La Plata-Conicet, La Plata, Buenos Aires, Argentina. Centro de Investigaciones y Transferencia, Universidad Nacional de Río Negro, Viedma, Río Negro, Argentina. Proyecto Patagonia Noreste, Balneario El Cóndor, Río Negro, Argentina. Corresponding author: luchosegura79@gmail.com Received on 26 February 2019. Accepted on 28 June 2019. ABSTRACT: The genus Paroaria is a group of conspicuous songbirds widely distributed in South America that has been studied recently to delimit its species and establish their phylogenetic relationships. Although hybridization has been reported between the most phylogenetically related species of the genus, we here present a case of hybridization between the Yellow-billed Cardinal (P. capitata) and Red-crested Cardinal (P. coronata) for the first time, two phylogenetically unrelated members of the group. This data contributes to the knowledge of this avian group whose systematics is still under debate. KEY-WORDS: breeding biology, hybrids, interbreed, Neotropical birds, Patagonia Species delimitation has been a crucial topic in the natural Yellow-billed and Red-crested Cardinal (a riverine and history of birds, both for systematic and ecological an open-forest cardinal respectively, two phylogenetically studies (de Queiroz 2007). Systematic studies on the distant species in Paroaria). genus Paroaria, a group of conspicuous songbirds widely This study was conducted at Viedma, Río Negro distributed in South America (Jaramillo 2011), indicate province, northeastern Patagonia, Argentina (40 48'S; that it comprises six to eight species splitted into two 63 01'W; Fig. 1). The study area is representative of the ecological groups: the riparian species (P. gularis, P. baeri, “Monte” ecoregion (Brown et al. 2006), with large areas P. xinguensis, P. capitata, P. cervicalis and P. nigrogenis) and of native xerophytic vegetation altered by extensive and the open-forest species (P. coronata and P. dominicana) low-density cattle grazing. This region is characterized b y (Dávalos & Porzecanski 2009). Estimated divergence warm summers (maximum temperature of 42.3 C) and times range from 3.7 to 5.0 mya for the split between cold winters (minimum temperature of -13.5 C), with the open-forest vs. riparian clades, which has led them to most precipitations occurring between November and show at present both morphological (Jaramillo 2011) and March. The National Meteorological Survey of Argentina genetic (Dávalos & Porzecanski 2009, Areta et al. 2017) from 1987–2017 reports mean annual rainfall as 257 mm differences. During the last decades, it has been reported and mean annual temperature as 15°C. At the local scale, some natural hybridization between species of this genus, the nesting territory was located on the southern margin for example between P . baeri and P. gularis (Jaramillo 2011, of the Negro River, in a wetland dominated by the exotic Lopes & Gonzaga 2013, Areta et al. 2017), two non-sister Salix viminalis (Salicaceae). The area was surveyed every species but still phylogenetically close “riverines” (Dávalos 5–8 days, since the first evidence of hybridization, with & Porzecanski 2009). However, in captivity conditions, the help of binoculars and photographic cameras. hybridization has also been reported among less related In March 2016 (end of 2015–2016 breeding season) Paroaria species (P. dominicana and P. nigrogenis, two we located an interspecific pair moving together in the genetically distant species; McCarthy 2006) and even nesting area (Fig. 2A). We inspected the surroundings with species of other genera and even families (P. coronata shrubs and forests to locate the nest (see details in Segura with Sicalis flaveola, Gubernatrix cristata, Cardinalis et al. 2015), but we could not find it. On 18 April, we saw cardinalis, Chrysomus ruficapillus and Molothrus both parents with a fledgling for the first time (Fig. 2B bonariensis; McCarthy 2006). In this contribution, we & C) and delivering food to it. We observed the family present the first recor d of natural hybridization between group until the beginning of June, and since then, we Hybridization between Yellow-billed Cardinal and Red-crested Cardinal Segura et al. detected only adults throughout the winter, until spring began. The size and p lumage of our hybrid juvenile (Fig. 2D) strikingly resembled that of P. capitata juveniles (Fig. 2E), although the bill color and tarsus were gray, like P. coronata. In the last decades, individuals of both species have been reported in atypical southern localities in relation to the original distribution (Fig. 1). For example, on web platforms such as EcoRegistros (2018) or eBird (2018), the records of both species in the Negro River (northern Patagonia) and cities in southern Buenos Aires province (central-eastern Argentina) are increasingly frequent. A possible explanation is that both species are traditionally captured and sold in illegal trade in a large fraction of their distribution area (UNEP-WCMC 2009), and the release of individuals from captivity in areas near urban centers would explain this atypical distribution. The sympatry area between both species is extensive (Fig. 1) and the contact is not recent (Dávalos & Porzecanski 2009, Areta et al. 2017). However, no hybrids have been reported within this area. On the one hand, this lack of previous reports could be simply due to an artifact of poor sampling, but considering that both species are conspicuous and relatively common in their respective habitats, it is unlikely that this could be the reason. However, there may be some behavioural or ecological Figure 1. Distribution area of the Yellow-billed Cardinal barriers within their sympatry area (Randler 2006) that Paroaria capitata (blue shaded) and Red-crested Cardinal P. coronata (green shaded) in South America (A); Jaramillo 2011). keep them from hybridizing in a natural way. Although Area surveyed in this study (B). our birds paired and reproduced in natural conditions, we Figure 2. Mixed breeding pair composed by a Yellow-billed Cardinal, Paroaria capitata, and a Red-crested Cardinal, P. coronata (A). Red-crested Cardinal feeding the hybrid fledging (B). Familiar group moving together on the ground (C). The hybrid fledging (D). A pure Yellow-billed fledging (E). P hoto authors: Graciela Balda (A, B, D), Eugenio Sicardi (D), Giselle Mangini (E). Revista Brasileira de Ornitologia 27(2): 2019 Hybridization between Yellow-billed Cardinal and Red-crested Cardinal Segura et al. do not ignore the particular situation regarding the lack REFERENCES of conspecifics in an unusual austral distribution area for Areta J.I, Dornas T., Kirwan G.M., Araújo-Silva L.E. & Aleixo A. both species, which could have favored the interspecific 2017. Mixing the waters: a linear hybrid zone between two hybridization (see Baker 1996). riverine Neotropical cardinals (Paroaria baeri and P. gularis). Emu It has been discussed that genetic differences between 117: 40–50. the related P. capitata and P. cervicalis (and even P. gularis) Baker M.C.  1996.  Female buntings from hybridizing populations prefer conspecific males. Wi lson Bulletin 108: 771–775. are so small that cases of hybridization are expected Brown A.D., Martínez-Ortíz U., Acervi M. & Corcuera J. 2006. (Dávalos & Porzecanski 2009), but P. capitata and P. Situación ambiental Argentina 2005. Buenos Aires: Fundación coronata are more divergent (Dávalos & Porzecanski Vida Silvestre Argentina. 2009, Areta et al. 2017). In this sense, phylogenetic Dávalos L.M. & Porzecanski A.L. 2009. Accounting for molecular results within Paroaria indicate that the mitochondrial stochasticity in systematic revisions: species limits and phylogeny of Paroaria. Molecular Phylogenetics and Evolution 53: 234–248. gene tree contained a deep split between open-forest (P. de Queiroz K. 2007. Species concepts and species delimitation. dominicana and P. coronata) and riparian species (all other Systematic Biology 56: 879–886. Paroaria). Our results show that, despite this genetic eBird. 2018. eBird: an online database of bird distribution and split, they still maintain the ability of interbreeding as an abundance. http://www.ebird.org (Access on 26 December 2018). EcoRegistros. 2018. Cardenilla (Paroaria capitata) and Cardenal ancestral condition (see Podos & Nowicki 2004). Común (Paroaria coronata). http://www.ecoregistros.org (Access Even though we cannot infer if the hybrid offspring on 26 December 2018). has post-zygotic barriers to freely interbreed with the Jaramillo A. 2011. Genus Paroaria, p. 642– 644. In: del Hoyo J., Elliott parental species, the fact that two genetically distant A. & Christie D.A. (eds.). Handbook of the birds of the world, v. 16 Paroaria may naturally hybridize, as first reported (tanagers to New World blackbirds). Barcelona: Lynx Editions. Lopes L.E. & Gonzaga L.P. 2013. Taxonomy, natural history, and here, may be an additional evidence that tropical bird conservation of Paroaria baeri (Aves: Thraupidae). Tropical species, and Paroaria species in particular, may hold the Zoology 26: 87–103. potential to mate and interbreed for a very long time after McCarthy E.M. 2006. Handbook of avian hybrids of the world. Oxford: speciation (Weir & Price 2011, Areta et al. 2017). The Oxford University Press. Podos J. & Nowicki S. 2004. Beaks, adaptation, and vocal evolution genus Paroaria, therefore, may represent an interesting in Darwin's Finches. BioScience 54: 501–510. system to further research on the role of hybridization on Randler C. 2006. Behavioural and ecological correlates of natural the evolution and speciation of birds. hybridization in birds. Ibis 148: 459–467. Segura L.N., Mahler B., Berkunsky I. & Reboreda J.C. 2015. Nesting biology of the Red-crested Cardinal (Paroaria coronata) in south temperate forests of central Argentina. Wilson Journal of ACKNOWLEDGEMENTS Ornithology 127: 249–258. UNEP-WCMC. 2018. UNEP-WCMC Species Database: CITES-listed We thank Martín Méndez, Graciela Balda and Eugenio species. http://www.unep-wcmc.org (Access on 28 December 2018). Sicardi for help in data collection, and Facundo X. Weir J.T. & Price T.D. 2011. Limits to speciation inferred from times to secondary sympatry and ages of hybridizing species along a Palacio and an anonymous reviewer for helpful comments latitudinal gradient. American Naturalist 177: 462–469. on a previous version of this manuscript. L.N.S. is a CONICET Research Fellow. Associate Editor: Fábio R. Amaral. Revista Brasileira de Ornitologia 27(2): 2019 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Ornithology Research Springer Journals

Hybridization between Yellow-billed Cardinal Paroaria capitata and Red-crested Cardinal P. coronata in southern Argentina

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Abstract

Revista Brasileira de Ornitologia 27(2): 129–131. SHORT-COMMUNIC ARTICLE ATION June 2019 Hybridization between Yellow-billed Cardinal Paroaria capitata and Red-crested Cardinal P. coronata in southern Argentina 1,4 2 3 Luciano N. Segura , Federico A. De Maio & Mauricio Failla Sección Ornitología, Museo de La Plata, Universidad Nacional de La Plata-Conicet, La Plata, Buenos Aires, Argentina. Centro de Investigaciones y Transferencia, Universidad Nacional de Río Negro, Viedma, Río Negro, Argentina. Proyecto Patagonia Noreste, Balneario El Cóndor, Río Negro, Argentina. Corresponding author: luchosegura79@gmail.com Received on 26 February 2019. Accepted on 28 June 2019. ABSTRACT: The genus Paroaria is a group of conspicuous songbirds widely distributed in South America that has been studied recently to delimit its species and establish their phylogenetic relationships. Although hybridization has been reported between the most phylogenetically related species of the genus, we here present a case of hybridization between the Yellow-billed Cardinal (P. capitata) and Red-crested Cardinal (P. coronata) for the first time, two phylogenetically unrelated members of the group. This data contributes to the knowledge of this avian group whose systematics is still under debate. KEY-WORDS: breeding biology, hybrids, interbreed, Neotropical birds, Patagonia Species delimitation has been a crucial topic in the natural Yellow-billed and Red-crested Cardinal (a riverine and history of birds, both for systematic and ecological an open-forest cardinal respectively, two phylogenetically studies (de Queiroz 2007). Systematic studies on the distant species in Paroaria). genus Paroaria, a group of conspicuous songbirds widely This study was conducted at Viedma, Río Negro distributed in South America (Jaramillo 2011), indicate province, northeastern Patagonia, Argentina (40 48'S; that it comprises six to eight species splitted into two 63 01'W; Fig. 1). The study area is representative of the ecological groups: the riparian species (P. gularis, P. baeri, “Monte” ecoregion (Brown et al. 2006), with large areas P. xinguensis, P. capitata, P. cervicalis and P. nigrogenis) and of native xerophytic vegetation altered by extensive and the open-forest species (P. coronata and P. dominicana) low-density cattle grazing. This region is characterized b y (Dávalos & Porzecanski 2009). Estimated divergence warm summers (maximum temperature of 42.3 C) and times range from 3.7 to 5.0 mya for the split between cold winters (minimum temperature of -13.5 C), with the open-forest vs. riparian clades, which has led them to most precipitations occurring between November and show at present both morphological (Jaramillo 2011) and March. The National Meteorological Survey of Argentina genetic (Dávalos & Porzecanski 2009, Areta et al. 2017) from 1987–2017 reports mean annual rainfall as 257 mm differences. During the last decades, it has been reported and mean annual temperature as 15°C. At the local scale, some natural hybridization between species of this genus, the nesting territory was located on the southern margin for example between P . baeri and P. gularis (Jaramillo 2011, of the Negro River, in a wetland dominated by the exotic Lopes & Gonzaga 2013, Areta et al. 2017), two non-sister Salix viminalis (Salicaceae). The area was surveyed every species but still phylogenetically close “riverines” (Dávalos 5–8 days, since the first evidence of hybridization, with & Porzecanski 2009). However, in captivity conditions, the help of binoculars and photographic cameras. hybridization has also been reported among less related In March 2016 (end of 2015–2016 breeding season) Paroaria species (P. dominicana and P. nigrogenis, two we located an interspecific pair moving together in the genetically distant species; McCarthy 2006) and even nesting area (Fig. 2A). We inspected the surroundings with species of other genera and even families (P. coronata shrubs and forests to locate the nest (see details in Segura with Sicalis flaveola, Gubernatrix cristata, Cardinalis et al. 2015), but we could not find it. On 18 April, we saw cardinalis, Chrysomus ruficapillus and Molothrus both parents with a fledgling for the first time (Fig. 2B bonariensis; McCarthy 2006). In this contribution, we & C) and delivering food to it. We observed the family present the first recor d of natural hybridization between group until the beginning of June, and since then, we Hybridization between Yellow-billed Cardinal and Red-crested Cardinal Segura et al. detected only adults throughout the winter, until spring began. The size and p lumage of our hybrid juvenile (Fig. 2D) strikingly resembled that of P. capitata juveniles (Fig. 2E), although the bill color and tarsus were gray, like P. coronata. In the last decades, individuals of both species have been reported in atypical southern localities in relation to the original distribution (Fig. 1). For example, on web platforms such as EcoRegistros (2018) or eBird (2018), the records of both species in the Negro River (northern Patagonia) and cities in southern Buenos Aires province (central-eastern Argentina) are increasingly frequent. A possible explanation is that both species are traditionally captured and sold in illegal trade in a large fraction of their distribution area (UNEP-WCMC 2009), and the release of individuals from captivity in areas near urban centers would explain this atypical distribution. The sympatry area between both species is extensive (Fig. 1) and the contact is not recent (Dávalos & Porzecanski 2009, Areta et al. 2017). However, no hybrids have been reported within this area. On the one hand, this lack of previous reports could be simply due to an artifact of poor sampling, but considering that both species are conspicuous and relatively common in their respective habitats, it is unlikely that this could be the reason. However, there may be some behavioural or ecological Figure 1. Distribution area of the Yellow-billed Cardinal barriers within their sympatry area (Randler 2006) that Paroaria capitata (blue shaded) and Red-crested Cardinal P. coronata (green shaded) in South America (A); Jaramillo 2011). keep them from hybridizing in a natural way. Although Area surveyed in this study (B). our birds paired and reproduced in natural conditions, we Figure 2. Mixed breeding pair composed by a Yellow-billed Cardinal, Paroaria capitata, and a Red-crested Cardinal, P. coronata (A). Red-crested Cardinal feeding the hybrid fledging (B). Familiar group moving together on the ground (C). The hybrid fledging (D). A pure Yellow-billed fledging (E). P hoto authors: Graciela Balda (A, B, D), Eugenio Sicardi (D), Giselle Mangini (E). Revista Brasileira de Ornitologia 27(2): 2019 Hybridization between Yellow-billed Cardinal and Red-crested Cardinal Segura et al. do not ignore the particular situation regarding the lack REFERENCES of conspecifics in an unusual austral distribution area for Areta J.I, Dornas T., Kirwan G.M., Araújo-Silva L.E. & Aleixo A. both species, which could have favored the interspecific 2017. Mixing the waters: a linear hybrid zone between two hybridization (see Baker 1996). riverine Neotropical cardinals (Paroaria baeri and P. gularis). Emu It has been discussed that genetic differences between 117: 40–50. the related P. capitata and P. cervicalis (and even P. gularis) Baker M.C.  1996.  Female buntings from hybridizing populations prefer conspecific males. Wi lson Bulletin 108: 771–775. are so small that cases of hybridization are expected Brown A.D., Martínez-Ortíz U., Acervi M. & Corcuera J. 2006. (Dávalos & Porzecanski 2009), but P. capitata and P. Situación ambiental Argentina 2005. Buenos Aires: Fundación coronata are more divergent (Dávalos & Porzecanski Vida Silvestre Argentina. 2009, Areta et al. 2017). In this sense, phylogenetic Dávalos L.M. & Porzecanski A.L. 2009. Accounting for molecular results within Paroaria indicate that the mitochondrial stochasticity in systematic revisions: species limits and phylogeny of Paroaria. Molecular Phylogenetics and Evolution 53: 234–248. gene tree contained a deep split between open-forest (P. de Queiroz K. 2007. Species concepts and species delimitation. dominicana and P. coronata) and riparian species (all other Systematic Biology 56: 879–886. Paroaria). Our results show that, despite this genetic eBird. 2018. eBird: an online database of bird distribution and split, they still maintain the ability of interbreeding as an abundance. http://www.ebird.org (Access on 26 December 2018). EcoRegistros. 2018. Cardenilla (Paroaria capitata) and Cardenal ancestral condition (see Podos & Nowicki 2004). Común (Paroaria coronata). http://www.ecoregistros.org (Access Even though we cannot infer if the hybrid offspring on 26 December 2018). has post-zygotic barriers to freely interbreed with the Jaramillo A. 2011. Genus Paroaria, p. 642– 644. In: del Hoyo J., Elliott parental species, the fact that two genetically distant A. & Christie D.A. (eds.). Handbook of the birds of the world, v. 16 Paroaria may naturally hybridize, as first reported (tanagers to New World blackbirds). Barcelona: Lynx Editions. Lopes L.E. & Gonzaga L.P. 2013. Taxonomy, natural history, and here, may be an additional evidence that tropical bird conservation of Paroaria baeri (Aves: Thraupidae). Tropical species, and Paroaria species in particular, may hold the Zoology 26: 87–103. potential to mate and interbreed for a very long time after McCarthy E.M. 2006. Handbook of avian hybrids of the world. Oxford: speciation (Weir & Price 2011, Areta et al. 2017). The Oxford University Press. Podos J. & Nowicki S. 2004. Beaks, adaptation, and vocal evolution genus Paroaria, therefore, may represent an interesting in Darwin's Finches. BioScience 54: 501–510. system to further research on the role of hybridization on Randler C. 2006. Behavioural and ecological correlates of natural the evolution and speciation of birds. hybridization in birds. Ibis 148: 459–467. Segura L.N., Mahler B., Berkunsky I. & Reboreda J.C. 2015. Nesting biology of the Red-crested Cardinal (Paroaria coronata) in south temperate forests of central Argentina. Wilson Journal of ACKNOWLEDGEMENTS Ornithology 127: 249–258. UNEP-WCMC. 2018. UNEP-WCMC Species Database: CITES-listed We thank Martín Méndez, Graciela Balda and Eugenio species. http://www.unep-wcmc.org (Access on 28 December 2018). Sicardi for help in data collection, and Facundo X. Weir J.T. & Price T.D. 2011. Limits to speciation inferred from times to secondary sympatry and ages of hybridizing species along a Palacio and an anonymous reviewer for helpful comments latitudinal gradient. American Naturalist 177: 462–469. on a previous version of this manuscript. L.N.S. is a CONICET Research Fellow. Associate Editor: Fábio R. Amaral. Revista Brasileira de Ornitologia 27(2): 2019

Journal

Ornithology Research – Springer Journals

Published: Jun 1, 2019

Keywords: breeding biology; hybrids; interbreed; Neotropical birds; Patagonia

References

  • Mixing the waters: a linear hybrid zone between two riverine Neotropical cardinals (Paroaria baeri and P. gularis)
    Areta, JI; Dornas, T; Kirwan, GM; Araújo-Silva, LE; Aleixo, A
  • Female buntings from hybridizing populations prefer conspecific males
    Baker, MC
  • Accounting for molecular stochasticity in systematic revisions: species limits and phylogeny of Paroaria
    Dávalos, LM; Porzecanski, AL
  • Species concepts and species delimitation
    de Queiroz, K
  • Genus Paroaria
    Jaramillo, A; del Hoyo, J; Elliott, A; Christie, DA
  • Taxonomy, natural history, and conservation of Paroaria baeri (Aves: Thraupidae)
    Lopes, LE; Gonzaga, LP
  • Beaks, adaptation, and vocal evolution in Darwin’s Finches
    Podos, J; Nowicki, S
  • Behavioural and ecological correlates of natural hybridization in birds
    Randler, C
  • Nesting biology of the Red-crested Cardinal (Paroaria coronata) in south temperate forests of central Argentina
    Segura, LN; Mahler, B; Berkunsky, I; Reboreda, JC
  • Limits to speciation inferred from times to secondary sympatry and ages of hybridizing species along a latitudinal gradient
    Weir, JT; Price, TD