Range expansion and noteworthy records of Costa Rican birds (Aves)

We present new distribution information for 19 species of Costa Rican birds. Thirteen species show changes in altitudinal distribution, 9 are recorded at higher elevations such as Egretta rufescens (Gmelin, 1789), Heliomaster constantii (Delattre, 1843), Myiozetetes cayanensis (Linnaeus, 1766), and Lonchura malacca (Linnaeus, 1766), and 4 are recorded at lower elevations, Panterpe insignis Cabanis & Heine, 1860, Empidonax albigularis Sclater & Salvin, 1859, Sayornis nigricans (Swainson, 1827), and Dacnis venusta (Lawrence, 1862). We recorded 2 forest understory species, Geotrygon montana (Linnaeus, 1758), and Grallaria guatimalensis Prévost & Des Murs, 1842, inside the area of the county with the most urban development. Finally, Saltator grossus (Linnaeus, 1766), which was restricted to Caribbean forest, was recorded at the South Pacific rainforest for the first time.


Introduction
The avifauna of Costa Rica is comprised of 920 species, including extinct, accidental, regular migrants, and residents (Sandoval and Sánchez 2016).Since the publication of Stiles and Skutch (1989), the first field guide to the birds of Costa Rica and the first comprehensive compilation of bird species distribution in the country, the distribution of several bird species has changed (e.g.Sánchez et al. 1998, Sandoval et al. 2010, Biamonte et al. 2011).For example, notable records have been added of Caribbean species recorded on the Pacific slope (Alvarado-Quesada and Biamonte 2003, Sandoval andFernández-Ramírez 2012), Pacific rainforest species in the Central Valley and on the Caribbean slope (Sandoval and Ellis 2006, Barrantes and Biamonte 2004, Martínez et al. 2009), and dry-forest species recorded in Caribbean or Pacific rainforests (Sandoval andVargas 2007, Sandoval 2013).These changes in distribution are thought to be associated with landscape modifications and increasing of temperatures (Biamonte et al. 2011, Sandoval 2013) for some bird species, but due to other, unexplained reasons for others (Sandoval et al. 2010).Changes in distribution and range expansion appear to be an unstoppable phenomenon due to the constant changes in land use, temperature, and climate change (Crick 2004, Prieto-Torres et al. 2016).Herein, we provide new distribution information for 19 species of Costa Rican birds.

Methods
Our records are based on specimens or opportunistic observations, with supporting documentation, made between 1997 and 2016 from 15 localities in Costa Rica.Specimens were collected under permit (permit numbers 181-201-SINAC, SINAC-SF-611-SP-R-072-2014, and SINAC-SE-GASP-PI-R-059-2015) from the Ministerio del Ambiente y Energía de Costa Rica and the Sistema Nacional de Áreas de Conservación.All collected individuals were deposited in the Museo de Zología, Universidad de Costa Rica (MZUCR).Identifications were based on photographs and comparative specimen material at MZUCR or on published information and illustrations (Stiles andSkutch 1989, Garrigues andDean 2014).

Results
Cairina moschata (Linnaeus, 1758), Muscovy Duck.This species regularly breeds on both coasts below 500 m in Costa Rica, mainly in freshwater wetlands with and without open water (Stiles andSkutch 1989, Garrigues andDean 2014).In the rest of the country, it is common to observe feral individuals in artificial lagoons, mainly in parks at elevations up to 2000 m.Feral and wild individuals can be separated based on behavior, plumage differences, and body size.Feral individuals have unusual plumage (e.g.white body patches, crests, or curly tails) and are smaller.Wild individuals do not approach humans and are larger (pers.obs.).We observed 4 juveniles following two adult birds in Angostura Reservoir, Cartago province (09°52′00″ N, 083°39′00″ W; 569 m elev.), on 20 November 2014 (Fig. 1A).We observed a single individual foraging near a group of 50 Aythya affinis (Eyton, 1838), Lesser Scaup, in Cachí Reservoir, Cartago province (09°49′38″ N, 083°49′00″ W; 1000 m elev.), on 21 November 2015.These individuals lacked plumage characteristics that would suggest a feral origin (e.g.white plumage and a crest) and moved away when approached.Therefore, we are confident that these particular individuals were wild.These 2 observations represent the first breeding evidence and the highest elevational record in Costa Rica for non-feral individuals, respectively.(Gmelin, 1789), Reddish Egret.This species occurs mainly in brackish waters along both coasts of Costa Rica from November to April (Stiles andSkutch 1989, Garrigues andDean 2014).We observed an adult foraging in an ephemeral lagoon inside a cattle pasture at San Isidro de Coronado, San Jose province (09°58′59″ N, 084°00′19″ W; 1389 m elev.), from 23 December 2010-3 March 2011 (Fig. 1B).The dark morph of this egret may be confused with Egretta caerulea (Linnaeus, 1758), Little Blue Heron, due to a similar plumage color, but the bicolored beak with pinkish base and black tip is diagnostic of E. rufescens.This is the first inland and the highest elevational record documented for E. rufescens in Costa Rica.(Linnaeus, 1758), Yellow-crowned Night-heron.This species occurs along lowlands below 500 m on both coasts of Costa Rica (Stiles andSkutch 1989, Garrigues andDean 2014).On 18 October 2013 we observed 1 juvenile perched on the edge of an artificial pond at Hacienda Las Cóncavas, Cartago province (09°51′00″ N, 083°53′00″ W; 1350 m elev.).Juveniles may be confused with Nycticorax nycticorax Linnaeus, 1758, Black-crowned Night-heron, due to similarities in their plumage, but the entirely black beak occurs only in juvenile E. violacea (Fig. 1C).This is the highest elevational record in Costa Rica.(Temminck, 1822), Hookbilled Kite.This species occurs mainly near wetlands in lowlands and foothills below 1000 m on both coasts (Stiles andSkutch 1989, Garrigues andDean 2014).From February 1997-June 2016, we observed 75 individuals (3.75 observations/year) of both juveniles and adults flying and feeding on snails near Jardín Botánico Lankester (09°51′00″ N, 083°53′00″ W; 1350 m elev.) and at the Ujarras Valley area (09°49′38″ N, 083°49′00″ W; 1000 m elev.) (Fig. 1D).On 15 April 2011, we found a dead female (MZUCR 4201) on the ground within a planted forest of the non-native Cupressus lusitanica Mill. in Concepción, Heredia province (10°02′02″ N, 084°03′38″ W; 1500 m elev.).Another female was observed and photographed in Universidad Nacional main campus, Heredia province, on 21 March 2012 (09°59′56″ N, 084°06′38″ W; 1154 m elev.).Individuals of this kite are recognized by a hooked beak, pale iris, and yellowish to orange lore.No other diurnal raptor has these characteristics in the country.These observations represent the first confirmed records in the Central Valley, and the female found at Concepción is the highest elevational record for the species in Costa Rica.
Eupsittula canicularis (Linnaeus, 1758), Orangefronted Parakeet.This species occurs below 1000 m in the dry forest of Costa Rica (Stiles andSkutch 1989, Garrigues andDean 2014).On 16 December 2015, we observed 4 individuals eating guava, Psidium guajava L. in a private yard (Fig. 3B) at El Molino, Cartago province (09°51′32″ N, 083°55′38″ W; 1415 m elev.).This parakeet has an orange front and blue mid-crown (Fig. 3B), which distinguishes it from more common Psittacara finschi (Salvin, 1871), Crimson-fronted Parakeet, which has a red-fronted crown.This is the first record for the eastern Central Valley and the highest elevational record in Costa Rica.2016 (MZUCR 5081).This parrot has a brown hood with reddish auricular patch (Fig. 3C), which distinguishes it from other Costa Rican parrots.This is the first published record of this species in the Central Valley in Costa Rica.

Grallaria guatimalensis
Prévost & Des Murs, 1842, Scaled Antpitta.In Costa Rica, this species occurs in montane forests between 800 and 1600 m on both slopes of the Guanacaste, Tilaran, Volcánica Central, and Talamanca ranges (Stiles andSkutch 1989, Garrigues andDean 2014).One adult was observed on 11 May 2016 fighting against its reflection on a structure in a garden in the urban center of Barrio Dent, San José province (09°56′06″ N, 084°03′26″ W; 1200 m elev.) (Fig. 4A).The individual was collected (MZUCR5202).This antpitta is recognized and distinguished from other antpittas in Costa Rica by its scaled back and rufous breast and belly.This is the first record of this species within the most urbanized area of the Central Valley.

Empidonax albigularis
Sclater & Salvin, 1859, Whitethroated Flycatcher.This species occurs in Costa Rica at elevations between 500 and 1500 m along the western and southern flanks of Irazú Volcano, on the Caribbean slope of the Guanacaste, Tilarán and Central Volcanic mountain ranges; and in the intermontane valleys of the southern Pacific lowlands (Stiles andSkutch 1989, Garrigues andDean 2014).On 1 March 2015, we observed 1 individual perched on a clump of grass in a natural wetland at Medio Queso (11°01′48″ N, 084°41′15″ W; 35 m elev.) (Fig. 4B).We also collected 1 individual on 20 January 2016 at Coto 47, Puntarenas province, in grasslands (08°29′23″ N, 082°58′40″ W; 20 m elev.)(MZUCR 5111).This flycatcher is distinguished from other species of Empidonax by its white throat that contrasts with the brownish breast, yellow belly, and buff wing bars.These are the lowest records of this species in Costa Rica and the first from the northern Caribbean lowlands and the southern Pacific lowlands.(Swainson, 1827), Black Phoebe.This species occurs in Costa Rica at elevations between 500 and 2000 m and usually close to bodies of water such creeks, rivers, and lagoons (Stiles andSkutch 1989, Garrigues andDean 2014).On 3 October 2008, we observed 2 individuals and photographed a nest (Fig. 4C) under  the bridge of Río Corinto, Limon province (10°12′42″ N, 083°53′09″ W; 226 m elev.).Additionally, we observed on 21 March 2015 a single individual foraging at Río Sarapiquí, Reserva Tirimbina, Heredia province (10°23′45″ N, 084°08′03″ W; 193 m elev.).This species is recognized by its black body plumage contrasting with its white belly.These are the lowest records of this species in Costa Rica and the lowest record of breeding.

Sayornis nigricans
Myiozetetes cayanensis (Linnaeus, 1766), Rusty-margined Flycatcher.In Costa Rica this species occurs along the Golfo Dulce border, below 200 m, where it arrived from Panama in 2004 (Sandoval et al. 2010, Garrigues andDean 2014).We observed on 11 June 2016 a single individual perched on an exposed perch at the edge of a coffee plantation at Las Juntas de Coto Brus, Puntarenas province (08°51′01″ N, 082°56′25″ W; 880 m elev.) (Fig. 4D).This flycatcher is distinguished from M. similis (Spix, 1825), Social Flycatcher, by the rusty edges on the primary feathers of the wings and blackish cheeks.This is the first record outside of the Golfo Dulce region and the highest record in the country.
Saltator grossus Linnaeus, 1766, Slate-coloured Grosbeak.This species only occurs on the Caribbean slope of Costa Rica, at elevations up to 1200 m (Stiles andSkutch 1989, Garrigues andDean 2014).On 21 April 2016, we photographed an individual, which was foraging on fruits, at the edge of Quebrada Bonita, Carara National Park, Puntarenas province (09°46′30″ N, 084°36′18″ W; 42 m elev.) (Fig. 5B).This grosbeak has a plumbeous plumage, with a distinctive white throat and red beak.This is the first record of S. grossus on the Pacific side of Costa Rica.
Lonchura malacca (Linnaeus, 1766), Tricolored Munia.This species was observed in Costa Rica for the first time in May 1999 at La Guinea, Guanacaste province (Sandoval et al. 2010).From the first observation, L. malacca has expanded its range along the Pacific coast as far south as Palmar Sur, Puntarenas province (Sandoval et al. 2010).A group of 20-30 individuals was observed on 8 February 2015 at Barrio San José, Alajuela province (10°01′09″ N, 084°14′56″ W; 897 m elev.),where they were foraging in grasslands (Fig. 5C).One individual, a juvenile, was collected (MZUCR4991).This juvenile is distinguished from female seedeaters (e.g.Sporophila spp.), by its thick, black beak, rufous back and wings, which contrast with its clear, brown breast and belly.This is the first published record of L. malaccca from the Central Valley and the highest record in the country.

Discussion
The occurrence of some species outside of their regular Costa Rican distribution may be explained by similar habitat requirements.For example, the 4 species that are routinely found around wetlands-C. moschata, E. rufescens, N. violacea, and C. uncinatus-were all found in artificial wetlands in the country's interior.The elimination and reduction of natural wetlands near the coast are forcing these species to use other, often artificial water bodies, such as water reservoirs and small ornamental lakes, that are inland and at higher elevations, (Sánchez et al. 2014, Sandoval et al. 2016).Although this pattern has increased recently (Sandoval et al. 2010, 2016, Sandoval 2013), we still are unsure if birds are using these resources because they are suitable for their needs or simply because it is the only available habitat.More research is required to evaluate the long-term efficacy of these habitats to sustain viable bird populations.
Dry-forest obligate species (E.canicularis, A. abifrons, H. constantii, and A. rutila) and species that require open areas (G.swainsonii, M. cayanensis, and L. malacca) may be expanding due to more available habitat caused by increased urbanization and deforestation (Sandoval 2009, Biamonte et al. 2011).Additionally, widespread fragmentation of mesic forest eliminates potential dispersal barriers between once-isolated dry forests, which may facilitate the observed expansion of dry-forest and open-area species (Sandoval et al. 2010, Biamonte et al. 2011).Another cause for the movements of these species may be related to increased temperature, which allows for colonization at higher elevations (Colwell et al. 2008, Sekercioglu et al. 2008).Four species show movements to lower elevations (P.insignis, S. nigricans, E. albigularis, and Dacnis venusta).These species probably are undergoing elevational movements as has been reported for altitudinal migrants in the Neotropics that descend to lowland forest during the dry season (Loiselle andBlake 1991, Boyle 2010).However, the presence of these species in lowlands may be due to poor weather conditions in the highlands, which may cause individuals to move to the lowlands in search of food or to avoid the adverse weather (Avalos 2005, Boyle 2010, 2011).
Three species (G.montana, P. haematotis, and G. guatimalensis) show an unclear pattern of movement.Geotrygon montana and Grallaria guatimalensis are understory birds that have arrived to the downtown center of San José, the most urbanized area in Costa Rica.Probably G. montana has a natural propensity for vagrant movements, which allows it to colonize new places, but this leads some individuals to reach unusual places.The arrival of G. guatimalensis to a garden in the middle of the city is a mystery.We hypothesize that this species are using river vegetation to move between populations, and in this case, is possible to found at least 2 populations in a 10 km radius from our new record.Therefore, the individual that we found was probably moving between populations but became disorientated.Pyrilia haematotis, which are known to have altitudinal movements (Stiles and Skutch 1989), probably arrived in the Central Valley by these means.
(Black-cowled Oriole), Molothrus bonariensis(Gmelin, 1789) (Shiny Cowbird), and Tigrisoma fasciatum (Such, 1825) (Fasciated Tiger-Heron), which have colonized the Pacific rainforest (Alvarado-Quesada and Biamonte 2003, Sandoval et al. 2010, Sando-val and Fernández-Ramírez 2012).Until now, no reasons have been proposed for the movements of these species from the Caribbean to Pacific rainforests.These species are not recorded in habitats between the Caribbean and Pacific rainforests and appear to represent single movements of isolated individuals between habitats.Nevertheless, the similarity in habitat structure and weather conditions between Caribbean and Pacific rainforests may help the establishment of Caribbean species after colonization.