Annotated checklist of the birds ( Aves ) of Cerro Hoya National Park , Azuero Peninsula , Panamá

1 Smithsonian Tropical Research Institute, Apartado Postal 0843-03092, Panamá, Republic of Panama 2 Rainforest Trust, 25 Horner Street, Warrenton, VA 20186, USA 3 University of Washington, Department of Biology and Burke Museum of Natural History and Culture, Seattle, WA 98195-1800, USA 4 Universidad de Panamá, Escuela de Biología, Departamento de Zoología, Panamá, Republic of Panama 5 Apartado Postal 0823-02757, Panamá, Republic of Panama * Corresponding author. E-mail: millerma@si.edu Check List 11(2): 1585, February 2015 doi: http://dx.doi.org/10.15560/11.2.1585 ISSN 1809-127X © 2015 Check List and Authors


INTRODUCTION
The Azuero Peninsula, the largest north-south peninsula in Central America, is an 8,000 km 2 landmass that juts southward from the western Panamanian mainland.Considered the cultural and agricultural cradle of Panama, here-as in most of the Pacific forests of Central America-deforestation began with Spanish colonization in the 16th century (Murphy and Lugo 1995), and increased sharply in the early 20th century (Heckadon-Moreno 2009).By the middle of the 20th century, roughly half of the lowlands of the Azuero Peninsula had been deforested, largely converted to cattle pasture (Wright and Samaniego 2008;Heckadon-Moreno 2009).Although, in its native state, the Azuero Peninsula should be nearly entirely forested (Wright and Samaniego 2008), today less than 15% is covered in mature forest, with perhaps another 20% covered in secondary forest.Of the remaining Azuero mature forest, most can be found in Cerro Hoya National Park and La Tronosa Forest Reserve (07.3°N, 080.6°W) found just to the east of Cerro Hoya National Park.
Cerro Hoya National Park (~ 07.4-07.2°N, 080.9-080.6°W; Figure 1) includes a mountainous region isolated from Panama's Central Cordillera by 150 km of extremely hot, seasonally dry, and deforested lowlands.Within Panama, these highlands have a geology that is unique to the Azuero and adjacent Soná Peninsulas, as they originated as oceanic volcanoes during the Early and Middle Eocene (56-41 Mya, Buch et al. 2011), and subsequently shifted northward into their current position.The southern Azuero region that includes the present day Cerro Hoya mountain range has been an emergent feature of the proto-isthmus and subsequent Isthmus of Panama since at least the late Eocene (> 38 Mya; Herrera et al. 2012).During glacial periods in the Pleistocene the temperature in the lowlands of Panama may have been as much as 5°C lower than at present, and some species of plants now confined to high montane areas occurred at much lower elevations (Piperno et al. 1990).The majority of montane flora and fauna found in the Cerro Hoya region probably dispersed from the Talamancan or Central Cordilleran highlands across lowland regions during such periods of lower temperatures.
The montane forests of Cerro Hoya remain one of the most poorly studied highland regions in all of Middle America.In 1925, R. Benson made a minor collection of birds in the central Azuero region, at Montuoso (~ 07.7° N, 080.9°W), north of Cerro Hoya National Park.However, the first major scientific expedition to the area was undertaken by Aldrich and Bole in 1932, who collected

MATERIALS AND METHODS
In February 1996, a team from the Philadelphia Academy of Natural Sciences (including GRA and RSR) made what is believed to be the first contemporary scientific collection focused on the highlands of Cerro Hoya.This expedition began on the coast at Cobachón (07.23°N, 080.64°W, this location and all subsequent named locations are mapped in Figure 2).(Note that on some maps of this region, e.g., Army Map Service 4037-I, "Horcones," several rivers are mislabeled.The town of Cobachón is shown to be at the mouth of the river labeled "Quebrada Punta Blanca" on this map.A smaller river about 4.5 km to the west is labeled "Río Cobachón".Because of these map errors, the location of Cobachón is incorrectly stated in Siegel and Olsen [2008]).The expedition ascended on horseback to a base camp at 650 m above sea level (a.s.l.) at Cascajilloso (07.28°N, 080.72°W), birds and mammals (Aldrich and Boyle 1937) in the lowlands northwest of Cerro Hoya National Park but did not explore the montane regions in the area.C.W. Myers provides the first detailed scientific description of the biota of the montane region surrounding Cerro Hoya (Myers 1962), crediting mammalogist C.O. Handley with providing him a hand-drawn map to the area.Based on his account, Myers managed to work above 1,200 m, but like Handley was unable to summit, and goes so far as to claim that the only known instance of a successful summit of the highest of the three peaks of Cerro Hoya was obtained by one of Aldrich and Bole's guides.
Interest in the avifauna of Cerro Hoya was rekindled at the end of the 20th century with the description of the Azuero Parakeet (Pyrrhura picta eisenmanni Delgado, 1985) by Delgado (1985)-who first suggested that the Cerro Hoya area was ornithologically the most poorly known region of Panama-and subsequently with the listing of Cerro Hoya National Park as an Important Bird Area for Panama (Angehr 2003).Here we provide an annotated checklist of the birds of the lowlands and where the team worked for three days.On 20 February, GRA ascended to a nearby peak at 1,380 m a.s.l. on foot.Trip dates: 16-22 February 1996.
In 2004 a team from the Marjorie Barrick Museum and STRI (including MJM and JK) visited the lowlands just inside the park boundary near Restingue (07.24°N, 080.90°W), southern Veraguas.The goal of this trip was to collect representative lowland bird species as part of a more comprehensive survey of the birds of Panama, rather than to create a comprehensive survey of the avian diversity in Cerro Hoya, and therefore we only report those bird species collected as museum vouchers during that trip.Records from this trip are included here because they represent important records for the southern dry forest lowlands of the park area.The 2011 trip represents the only attempted ornithological expedition to the Cerro Hoya highlands during the rainy season.During this trip, more time was spent getting into and out of the basecamp than working at the site, which testifies to the difficulty of highland access on Cerro Hoya.This expedition departed on foot from El Cortezo (07.43°N, 080.63°W) and made base camp in an area known as La Bajía (07.34°N, 080.66°W).Trip dates: 24-28 June 2011.
A STRIBC team (including MJM and DBR) returned in April 2013 to collect additional specimens and to sample more highland taxa.This trip began on foot from La Provincia (07.38°N, 080.67°W) and established a base camp at 450 m a.s.l. in an area known locally as Pavo (07.33°N, 080.70°W), above the Río Pavo.During this expedition, mistnets were deployed primarily at the forested edge of the highest pasture above Pavo (750 m a.s.l.), although daily shotgun collecting trips occurred between 950 and 1,375 m a.s.l.Trip dates: 3-7 April 2013.

RESULTS
We recorded a total of 225 confirmed bird species, with one additional hummingbird taxon (Selasphorus sp.) questionable.This includes nine species on the Red List of globally threatened bird species (IUCN 2013), including one Endangered, four Vulnerable, and four Near-Threatened species (Table 1).We recorded only 27 Nearctic-Neotropical migratory species, and only 10 species that could be considered primarily montane species (Angehr 2006).Based on the range maps in Angehr and Dean (2010), four species in our checklist were previously unknown from the Azuero Peninsula and represent range extensions of approximately 150 km.Below we provide details on 16 species of special interest.

Accounts of Species of Interest
Great Curassow (Crax rubra Linnaeus, 1758).At least one female was photographed by remote camera traps installed by J. Fort and colleagues to measure large mammal populations on Cerro Hoya.Two photographic instances occurred (8 and 10 March 2012), both showing a female curassow above Pavo at 785 m a.s.l. at 07.32° N, 080.70°W. Additionally, a female crown comb from a hunted curassow, killed by the owner, was on display at our field shelter in Pavo in 2013.Great Curassow are considered globally Vulnerable (IUCN 2013) and although were likely once widespread in Panama, are now only regularly observed in Darien National Park in extreme eastern Panama.
Brown-backed Dove (Leptotila battyi [Rothschild, 1901]).Although endemic to both the southern Azuero Peninsula and Coiba Island, where it is much more common, it is virtually unknown from continental Panama, except for Cerro Hoya National Park, where it is apparently rare.
Azuero (Painted) Parakeet (Pyrrhura picta eisen manni Delgado, 1985).Although this species is treated by the AOU (1998, 2013) as a subspecies, many authorities consider it as a species (e.g., Angehr 2003; Angehr and     STRIBC 4609,4610,4615,4616,4617,4618,4619,4620,4621,4622 Arremonops conirostris (Bonaparte, 1850)  Dean 2010); molecular systematics of the Pyrrhura complex have failed to fully resolve species limits (Ribas et al. 2006).Although geographically range-restricted, this species is surprisingly conspicuous in mid-elevations throughout the area.In addition to habitat loss, a specimen of a probable escaped cage bird from Panama City (STRIBC 0165) suggests that this species is probably also threatened by collection for the local pet trade.Great Green Macaw (Ara ambiguus Bechstein, 1811).In 1996, this species was seen daily flying overhead in small flocks (up to eight individuals) in the Río Cobachón valley, but not in either the coast areas nor higher above (i.e., > 500 m a.s.l.).RSR and D. Agro returned returned to the Cobachón area and were shown by locals a macaw nest in a Cuipo growing on a steep ridge.The nest was a natural hollow ca.20 m above ground level and they heard young vocalizing in the nest.They learned later that the nest was removed by poachers.This species is considered globally Endangered (IUCN 2013) and persists only in isolated populations in remote areas of Panama.
Violet Sabrewing (Campylopterus hemileucurus mel litus Bangs, 1902).This species breeds only in montane areas (although it descends to the lowlands outside of the breeding season) and thus the Cerro Hoya population is likely isolated by 150 km from the nearest conspecific population in the Central Cordillera.We observed no phenotypic differences in our voucher specimens.
Mountain-gem sp.nov.(Lampornis sp.nov.)In 1996, GRA observed a Lampornis hummingbird that he attributed to L. calolaemus homogenes (Purple-throated Mountain-gem) found in the western central cordillera of Panama.The 1996 expedition failed to collect a specimen.In 2011, OGL and fellow expedition members collected two males that provided phenotypic, and ultimately genetic evidence, of the distinctiveness of the Cerro Hoya form (Figure 3).In 2013, six additional specimens were obtained, all males showing the distinctive rufous belly and non-iridescent crown traits that separate the Cerro Hoya taxon from L. calolaemus homogenes.A full species description is under review.Lampornis hummingbirds are tolerant of mixed forest and open habitat, and while the global population of this species is likely small given the available montane habitat in the Azuero Peninsula, the population is likely stable, having last been connected to populations in other montane areas in Panama when lowland temperatures were cooler during the Pleistocene (Piperno et al. 1990).In fact, the loss of montane habitats due to global climate change likely represents the greatest conservation threat to this newly discovered species (e.g., Pounds et al. 1999;Şekercioğlu et al. 2012).
Glow-throated Hummingbird (Selasphorus ardens Salvin, 1870).The potential occurrence of a hummingbird of the genus Selasphorus in the Cerro Hoya region was first reported by F. Delgado, who claimed to have collected an immature male in 1994 (Collar et al. 1994;Stattersfield et al. 1998;Angehr 2003).Unfortunately, this specimen has not been available for scientific study, and is apparently lost (Delgado pers. comm. to GRA).In 1996, D. Agro reported a glimpse of a possible Selas phorus ardens, at 850 masl in oak forest.In early 2011, L. Martínez took a photograph (Figure 4) of a possible Selasphorus hummingbird at approximately 1,000 m a.s.l.near La Bajía (photograph coordinates: 07.33° N, 080.66°W).However, certain phenotypic characters of this photographed hummingbird are more similar to Calliphlox bryantae Lawrence 1867.The 2011 and 2013 expeditions were done mainly to confirm the existence of Selasphorus in the Cerro Hoya highlands.Yet, despite intensive efforts in 2011 and 2013, no individual was observed or collected.Thus, while there is circumstantial evidence that some species of small hummingbird in the "bee" clade (e.g., McGuire et al. 2007) occurs on Cerro Hoya, whether they represent Calliphlox bryantae, Selasphorus ardens, or (considering the considerable disjunction in range from these two species) even an  undescribed hummingbird species remains to be determined.Notably, species in the bee hummingbird clade, such as Selasphorus and Calliphlox prefer open montane habitats, yet MJM observed closed forest canopy at 1,375 m a.s.l.above Pavo, near the summit.This may indicate that little suitable habitat for species of "bee" clade hummingbirds occurs on Cerro Hoya.Unless a specimen is collected and deposited in a formal natural history collection, we recommend removing Selasphorus from the list of species occurring in Cerro Hoya.
Yellow-bellied Sapsucker (Sphyrapicus varius [Linneus, 1766]).A non-breeding migrant from North America, this species was previously known only from the western Caribbean lowlands and occasionally the western highlands of Panama.Our record represents the first record of this species from not only the Azuero Peninsula, but all the Pacific slope of Panama.
Smoky-brown Woodpecker (Veniliornis fumigatus [d'Orbigny, 1840]).Only found during the 1996 expedition, when it was rare, being seen and heard at 650 m a.s.l.This represents a range extension for this species, which was previously unknown from the Azuero Peninsula.It would be a priority to collect specimens of this species, as it is a montane endemic that deserves further scrutiny given that the closest conspecific population is in the central cordillera.
Mountain Elaenia (Elaenia frantzii frantzii [Lawrence, 1865]).A lone individual was collected during the 1996 expedition.Previously, this species was unknown from the Azuero Peninsula, with the nearest conspecific population occurring in the central cordillera.
Three-wattled Bellbird (Procnias tricarunculatus [Verreaux & Verreaux, 1853]).Considered globally Vulnerable (IUCN 2013), Three-wattled Bellbirds were heard consistently throughout the day above 950 m a.s.l. by the 2013 team.This species is known to have microgeographic variation in vocalizations.To our ear, the call type sounded different from that heard in the Talamanca highlands.More detailed studies should be undertaken to compare this population's vocal characteristics to that of the Talamanca highlands and the population on the upper reaches of Isla Coiba that have also been recently discovered to vocalize and are probably nesting (GRA pers.obs.).More detailed work on the population structure of Three-wattled Bellbirds is warranted, and should include the population of Cerro Hoya.
Orange-billed Nightingale-Thrush (Catharu s aur anti irostris griseiceps Salvin, 1866).Although this montane taxon is isolated by 150 km from conspecifics in the central cordillera of Panama, our lone male specimen is indistinguishable from a series of specimens from Chiriquí and Veraguas.
Tropical Parula (Setophaga pitiayumi speciosa [Ridgway, 1902]).Based on the range map in Angehr and Dean (2010) as well as the species description in Wetmore et al. (1984), this species is unknown from the Azuero Peninsula.Our lone specimen appears assignable to the S. p. speciosa, subspecies previously known from the Talamanca highlands, rather than S. p. cirrha Wetmore 1957, endemic to Isla Coiba, which is perhaps surprising, given the geographic proximity of Coiba and the number of lowland bird taxa shared between Isla Coiba and Cerro Hoya such as Leptotila battyi.
Undescribed wood-warbler taxon (Basileuterus taxon novum).A single specimen of a distinctive form of Basileuterus of the B. melanogenysignota species complex was collected during the 2013 expedition at 1,300 m a.s.l. in closed lower montane forest; several other individuals were observed.The specimen is phenotypically more similar to B. ignotus Nelson, 1912 in plumage than to the geographically closer taxa of western Panama (B. m. eximius Nelson, 1912 andB. m. bensoni Griscom, 1927).A genetic study of relationships in this group is pending.
White-winged Tanager (Piranga leucoptera Trudeau, 1839).A single male was collected during the 1996 expedition.Prior to this collection, this montane-obligate species was unknown from the Azuero Peninsula, with the closest conspecific population occurring in the central cordillera roughly 150 km to the north.Other males were observed during the 2009 and 2013 expeditions.
White-naped Brush-Finch (Azuero) (Atlapetes albinucha azuerensis Aldrich & Boyle, 1937).A single specimen of this poorly known and distinctive subspecies was collected in 2013.First described by Aldrich and Boyle (1937), a sole specimen was collected on Cerro Hoya in 1962 by C.O. Handley's team (Wetmore et al. 1984).As far as we know, this taxon has not been collected since.

DISCUSSION
Our species list for Cerro Hoya represents the most comprehensive species list for any site in the Azuero Peninsula and also the Pacific lowlands of Panama.Because of its topographic and habitat diversity, and because it contains the largest remaining areas of moist lowland and montane forests, Cerro Hoya National Park has the highest bird species richness of any area in the Azuero Peninsula.For example, Lasky and Keitt (2007) recorded only 71 species of birds from a survey of five dry forest fragments scattered throughout the Azuero Peninsula, although this survey, like our survey of Cerro Hoya, is likely incomplete.The presence of several species of large-bodied birds such as Crax rubra and Ara ambiguus provide further evidence that the avian community of Cerro Hoya is relatively intact and complete and has considerable conservation value.
While our list is based on the results of five expeditions, the relatively low numbers of migratory passerines, birds of prey, and nocturnal birds was lower than reasonably expected for a complete Panamanian site checklist (Angehr et al. 2006).Because our final expedition recovered several montane species that were unrecorded in prior expeditions, we believe that additional montane species remain to be discovered on Cerro Hoya.We urge continued ornithological activity in the region, especially at its highest elevations.
Nonetheless, based on the overall composition of our species list, it is likely that overall avian species richness is substantially lower than our estimates for many Panamanian National Parks, typically 300 to 500 species (e.g., Karr 1990;Angehr et al. 2006).Some of this is due to the general trend of lower bird species richness in more seasonal, drier lowlands of the Pacific Panama relative to the wetter, less seasonal Caribbean forests (Karr 1976;Ridgely and Gwynne 1989).Furthermore, while our sampling of montane species may be incomplete, it is clear than overall species richness of highland species in Cerro Hoya is substantially lower than that of the central cordillera, which can be explained by both the common biogeographical phenomenon of decreasing species richness towards the tips of peninsulas (Simpson 1964) along with the island biogeographic phenomenon of montane forest sky island habitats (islands of montane forest habitat isolated by inhospitable lowland habitats; e.g., Warshall 1995).
While sky-island biogeography leads to lower overall species richness, it can result in elevated levels of endemism in montane taxa (Warshall 1995).Of the ten confirmed montane-obligate bird species on Cerro Hoya, four are endemic taxa at either the species or subspecies level.Such a high proportion of endemic fauna highlights the evolutionary distinctiveness of the Cerro Hoya avifauna, which provides an extremely strong argument for increased conservation attention in the region.

ACKNOWLEDGEMENTS
We like to thank the members of the various expedition teams who accompanied us on difficult trips to this inaccessible region-1996 expedition: F. Delgado, D. Engleman, L. Engleman, D. Agro, M. Allen, T. Pedersen, D. Wechsler, S. Conine, and our guide Daniel Saenz (the amazing ornithological experience of this group results in the depth of records we were able to present in this paper); 2004 expedition: G. Spellman, J. DaCosta, P. Guitton-Mayerma; 2011 expedition: A. Santos Murgas, J.A. Ramírez; 2013 expedition: J. L. Garzón.In 2009, Dr. C. Garibaldi and the PROBIO project of the University of Panama provided logistical support to J. Arauz, allowing for his trip.Additionally, we'd like to thank the 2013 guides, M. Ureña and A. Moreno, who provided exceptional muscle, stamina, and knowledge of Cerro Hoya; we would not have been able to mount that expedition without their support.Finally, ornithological knowledge rests on the foundation of scientifically collected and curated specimens, and we thank Panama's Adminstración de Medio Ambiente (ANAM) and its 1996 predecessor, INRENARE (Instituto Nacional de Recursos Naturales Renovables) for its support of scientific ornithological collecting in Panama.Finally, we would like to acknowledge the logistical support of E. von Gal, R. Metzel, and G. Durán of the Azuero Earth Project, which is at the vanguard of efforts to conserve the flora and fauna of the forests of Cerro Hoya National Park.

LITERATURE CITED
Miller et al. | Birds of Cerro Hoya National Park, Panamá highlands of the region based on the results of five ornitho logical expeditions to the region between 1996 and 2013.

Figure 1 .
Figure 1.Map showing location of Cerro Hoya National Park and Azuero Peninsula relative to the central cordillera of western Panama.Darkened areas represent those montane areas above 950 m a.s.l.Only 77 km 2 of such habitat occur in Cerro Hoya National Park.With the exception of a few scattered montane patches just to the north, the Cerro Hoya highlands are separated by at least 150 km from the more extensive central and Talamanca highland ridge of Costa Rica and western Panama.
Trip dates: 6-8 March 2004.In 2009, ECC, a professional birding guide in Panama, spent one month observing birds in Cerro Hoya National Park, accompanied by J.P. Ríos.They entered the area by boat from Cambutal into Cobachón, making a base camp in the Cobachón valley at approximately 300 m a.s.l.Towards the end of the expedition, they climbed above an estimated 750 m a.s.l. to observe montane taxa.As well as the 2004 expedition, this expedition provides important records of the lowland avifauna in the southern region of the park.Trip dates: 1-31 July 2009.

Figure 2 .
Figure 2. Map showing specific locations visited during the five expeditions described in the text.

Figure 4 .
Figure 4. Photograph of unknown hummingbird near La Bajía taken in 2011.Photo courtesy of Laurencio Martínez.
Miller et al. | Birds of Cerro Hoya National Park, Panamá

Table 1 .
Checklist of bird species, IUCN status, and collection/observation details from five ornithological expeditions to Cerro Hoya National Park.
Continued Miller et al. | Birds of Cerro Hoya National Park, Panamá
Continued Miller et al. | Birds of Cerro Hoya National Park, Panamá
1 i.e., found only above 750 m a.s.l. 2 range extensions include taxa not previously recorded for southern Veraguas or Los Santos provinces.Miller et al. | Birds of Cerro Hoya National Park, Panamá