The Shiny Cowbird, Molothrus bonariensis (Gmelin, 1789) (Aves: Icteridae), at 2,800 m asl in Quito, Ecuador

Abstract Background The Shiny Cowbird, Molothrus bonariensis Gmelin, 1789, is a brood parasite of hundreds of small-bodied birds that is native to South American lowlands. Within the last 100 years this species has been expanding its range throughout the Caribbean, towards North America, but has rarely been seen above 2,000 m asl. New information Here, we present records of Shiny Cowbirds in Quito, a city located 2,800 m above sea level that harbors a bird community typical of the Andean valleys. We found two juvenile individuals parasitizing two different pairs of Rufous-collared Sparrow (Zonotrichia capensis Müller, 1776). This report constitutes an altitudinal range expansion of reproductive populations of ca. 500m, which may have beenprompted by anthropogenic disturbance.


Introduction
The Shiny Cowbird, Molothrus bonariensis Gmelin, 1789, is a brood parasite of hundreds of small-bodied birds, and the Rufous-collared Sparrow, Zonotrichia capensis Muller, 1776 is one of its main hosts (Mason 1986, Lowther 2013. It is native to South American lowlands (Bird Life International and NatureServe 2012), but within the last 100 years has been expanding its distribution throughout the Caribbean, towards North America (Post et al. 1993) with some isolated records from Costa Rica and Mexico (Kluza 1998, Sandoval et al. 2010 (Fig. 1). The species occupies lowlands and it has rarely been seen above 2,000 m asl (Hilty andBrown 1986, Lowther 2011); however, there are notorious records in Bolivia and Peru above 3,000 m asl (Miller 1917, Fjeldsa and Krabbe 1990, Jaramillo and Burke 1999, Balderrama 2006, Schulenberg et al. 2007. Particularly in Ecuador, it has been mostly recorded between 900 and 1,000 m asl, but also regularly higher to ca. 1,400 to 1,600 m asl Greenfield 2001, Ridgely and. There have been isolated records in the highlands (as high as 2,700 m asl) but there are no reports of these birds breeding at such altitudes. There also are records in the Pichincha province (up to 2,700 m asl) (Fjeldsa andKrabbe 1990, Ridgely andGreenfield 2001), and vocal recordings available from the southern city of Loja (2,100 m asl) and from lake San Pablo in the north of the country (2,700 m asl) in the sound library Xeno-Canto (www.xenocanto.org) (Fig. 2). In the year 2000 the Shiny Cowbird was first spotted in the inter Andean valley of Cumbayá, at 2,300 m asl, 7 km to the east of Quito, Ecuador (Carrion 2001, Carrion pers. obs.). These birds are now regular inhabitants of that area and may be observed there year round, sometimes in groups of more than 50 individuals (Carrion pers. obs.).
Here, we present records of juvenile Shiny Cowbirds at 2,800m asl in Quito-Ecuador's capital city located in the inter Andean valley, with a population of over 1.6 million people. The bird community of the city is typical of the inter Andean valleys (   Distribution of the Shiny Cowbird in Ecuador, modified from . Areas in blue represent areas below 2000 m asl where the shiny cowbird has been previously reported , black dots represent isolated, higher altitude records (up to 2700 m asl) Greenfield 2006, Xeno-canto Foundation 2012), and the red dot marks the city of Quito, where we report the presence of the Shiny Cowbird.

Materials and methods
In the campus of the Pontificia Universidad Católica del Ecuador (PUCE), Quito, Ecuador (0°12'40"S, 78°29'28"W), we observed two juveniles of M. bonariensis interacting with Zonotrichia capensis Müller, 1776, between 11 April and 15 May 2015. One of the juveniles of M. bonariensis was larger and more developed than the other, and each was associated with a different Z. capensis pair. We observed the juveniles of M. bonariensis displaying food begging behaviors to adult Z. capensis (which included chasing the sparrows on the ground), and vocalizing intensely on bushes and tree branches. The adults of Z. capensis were observed feeding the Shiny Cowbirds on several occasions (Fig. 3a, b) but they were not observed feeding fledglings of their own species.

Diagnosis
The observed individuals of Shiny Cowbird matched the morphological and behavioral characterstics of the species (Fig. 3a, b, c). The most remarkable characteristic was the dull grayish coloration on the dorsum, but paler on the venter and throat, and the greyish white eyebrows (Hilty andBrown 1986, Restall et al. 2006 (Fig. 3a, b) that matches that of the subspecies M. b. occidentalis, and not that of M. b. aequatorialis-which is darkeras would be expected for the location of Quito in the north of the country. Nevertheless, juvenile coloration might not match that of adults and more studies should be conducted for subspecific assignment perhaps using an integrative taxonomic approach combining molecular, morphological and biogeographic information.

Discussion
In recent years the Shiny Cowbird has colonized the Caribbean and the east coast of the United States (Fig. 1). Particularly in Ecuador, this species seemed to be restricted to below ca. 2,000m asl (Hilty and Brown 1986, Ridgely and Greenfield 2001, Restall et al. 2006, Lowther 2011, with isolated higher altitude records (Fjeldsa and Krabbe 1990, Greenfield 2001, Xeno-canto Foundation 2012) (Fig. 2), and had never before been reported in the high-altitude city of Quito. Surely, this inability to colonize the city was puzzling since it has a very long history of habitat alteration, and one of the Shiny Cowbird's most common hosts, Z. capensis, does well in high elevations and is abundant in Quito (Carrion 2001, Ridgely and Greenfield 2001). Even though there is strong evidence suggesting habitat fragmentation is the main driver of M. bonariensis range expansions (Arendt and Vargas Mora 1984, Post et al. 1993, Hansen et al. 2005 we believe that in this case, climate change might be playing an important role as well. Recent climate warming may have relaxed climatic conditions allowing this species to expand towards higher elevations. There is, in fact, evidence of temperature increases in the Ecuadorian Andes (e.g., Vuille et al. 2008), which may be related to range expansions such as the one presented in this contribution. Climate induced distributional shifts have been fairly well documented especially in species with high dispersal ability like birds, insects and marine invertebrates (Parmesan 2006). Several authors have reported range expansions of species towards higher altitudes (Paulson 2001, Parmesan 2006, Moritz et al. 2008, Chen et al. 2009, Chen et al. 2011. Along the Andes there are several examples of upslope expansion of distributions of plants and birds (Weng et al. 2007, Feeley et al. 2010, Forero-Medina et al. 2011, Morueta-Holme et al. 2015. Also, according to recent evidence, tropical species respond more strongly than temperate ones to warming temperatures, with range shifts that match local temperature increase more closely than in temperate-zone montane species (Freeman and Freeman 2014).
Avian brood parasites, including cuckoos and cowbirds, often reduce the reproductive success of their hosts (Tuero et al. 2007). Costs associated with such parasitism promote the evolution of host antiparasitic defenses -such as responding aggressively towards cowbirds to prevent them from gaining access to the nest, burying or ejecting parasite eggs, or abandoning parasitized nests -and create a coevolutionary arms race between hosts and parasites (Astie and Reboreda 2005). Nevertheless, a number of hosts, even commonly parasitized hosts like the Rufous-collared sparrow, have not evolved antiparasite defenses, despite the associated fitness costs, due probably to morphological or ecological constraints (Carro and Fernández 2013). In addition, in the case of invasive parasites, native hosts may be naïve to the parasite and lack defenses or appropriate mechanisms to counteract its negative effects (Taraschewski 2006, Fassbinder-Orth et al. 2013. The level of threat posed by invasive Cowbirds on native bird communities apparently depends on the local species present (i.e., whether they lack defenses against brood parasitism), and is closely related to other human disturbances, mainly habitat fragmentation (Rothstein andPeer 2005, Peer et al. 2013. In the specific case of the Shiny Cowbird, several studies have found negative effects of this parasite, especially for already endangered and/or endemic bird species (Post 2011, Price et al. 2011, Domínguez et al. 2014). In fact, there is evidence that suggests that Shiny Cowbird parasitism, coupled with habitat loss, almost drove the Pale-headed Brush-Finch, Atlapetes pallidiceps Sharpe, 1900, a critically endangered endemic to south-central Ecuador, to extinction (Oppel et al. 2004. Therefore, the Shiny Cowbird range expansion presented in this study may be of concern, especially for native, endemic, or endangered species that may be parasitized by this species. More studies are urgently needed to assess the threat posed by this invasive species to native avian fauna in the high Andes in order to guide management or control measures for this invasive brood parasite.