INTRODUCTION

threatened

In contrast to the mainland, the geographic isolation of islands promotes a suite of ecological conditions that may result in speciation, thus endemism (Kier et al., 2009; Fordham and Brook, 2010), and/or behavioral and morphological adaptations. Moreover, islands warrant attention for bird conservation because they are home for about one fifth of the worldwide avifauna, of which nearly 40% are threatened (Johnson

and Stattersfield, 1990; Biber, 2002; Trevino et al., 2007). The large number (>1500) of islands surrounding the Panamanian Isthmus, on both the Atlantic and Pacific coasts, are interesting because they were isolated from the mainland only recently (12,000–20,000 years) (Olson, 1997). However, most avian surveys in Panama have been restricted to the mainland.

In Panama, the islands of Coiba National Park (CNP) are particularly important because they contain some of the last remaining lowland humid forests in the southwest Pacific of Panama (Milton and Mittermeier, 1977). This park is a 270,125-ha archipelago composed by 9 larger islands and more than 100 islets. The largest islands of the park, Coiba and Jicarón, are separated by 6-7 km and have been isolated from each other presumably for as long as the archipelago has been from the mainland. The floristic composition of both islands is nearly 50% different from the mainland (Ibáñez, 2011), and is distributed among various habitat types, that are critical for the resident birds in the park, as well as for migratory bird species that use these islands as stopover points and, potentially, wintering areas.

Previous bird surveys in CNP have been conducted mainly on Coiba (Wetmore 1957, 1965, 1968, 1972; Wetmore et al., 1984; Ibáñez and Cabot 1997), leaving the bird communities of the rest of the islands unstudied. Understanding the bird community assemblages in the islands of the Coiban archipelago is critical, for example, to identify evolutionary significant units (ESUs) of interest and enforce conservation efforts (Crandall et al., 2000). Here, we provide the first annotated checklist of birds for Jicarón and Jicarita, using the results of 8 expeditions between 2004 and 2019. We compare the composition of the avifauna between the two largest islands, Coiba and Jicarón, and describe some species of interest for conservation.

METHODS

1. Study site

CNP is characterized by a humid tropical monsoonic forest, a rainfall of up to 3,403 mm yr-1, an average temperature of 26.4ᵒ C, and a marked

seasonality, where the dry season extends from mid-December to mid-April (Cardiel et al. 1997; Glynn & Wellington, 1983). The islands in this park were used as a prison colony between 1919 and 2004, and was declared a protected area in 1991. In 2005, the park was declared by UNESCO as a World Heritage Site and it is currently managed by MiAmbiente (the Panamanian Ministry of Environment) and the Coiba Committee, with representatives of different sectors. We conducted bird surveys in two islands of the Coiban archipelago (Fig. 1): Jicarón (1,868 ha), the second largest island in the park, and Jicarita (136 ha), which is the southernmost point of the Republic of Panama (Ibáñez, 2011). Respectively, their highest elevation is 392 and 122 m above sea level. Both islands are surrounded by rocky coast and have a very steep terrain, limiting access to a few landing sites. Further, Jicarita island has a continuous rocky cliff on its southernmost part. The habitats surveyed included coast, forest edge and interior, up to 1 km into the forest, including coastal vegetation, dry, secondary, and mature forest (Ibáñez, 2011).

Fig. 1
Map showing the islands of Jicarón and Jicarita in Coiba National Park, in relation to the Republic of Panama (top left). Map was created using aGIS4 in QGIS 2.18.14

2. Data collection

O. J. conducted a first bird surveys between 31 December, 2003 and 5 January, 2004 on the islands of Jicarón and Jicarita. G.R.A. obtained bird observations on both islands between 15 and 17 February, 2015. P.L.C.-C. and C.M.M-M. conducted surveys as part of a different project, with trips dates as follow: 23–31 July, 2017; 19–22 December, 2017; 3–7 January, 2018; 24–30 March, 2018; 12–13 April, 2019; and July 26–28, 2019. We made eight fieldtrips to Jicarón and three to Jicarita. Expeditions were conducted under research permit No. SE/APH-1-15 and SC/A-23-17 and corresponding renewals, approved by MiAmbiente.

We conducted bird observations in Jicarón via strip transects along the coast of the island, observation points (i.e., 7°17'26.4"N, 81°48'15.6"W; 7°16'59.6"N, 81°46'16.6"W; and 7°13'41.8"N, 81°48'10.7"W) and opportunistic sightings. Some birds were observed, opportunistically, while going around the islands by boat and some were also photographed using camera traps (Reconyx PC900 Hyperfire – Reconyx, Inc, WI, USA) used for a different project. On Jicarita, birds were observed on “observation points” (i.e., 7°13'13.6"N, 81°48'08.1"W) and an aquatic transect along the southernmost part of the island. Bird identifications were based on Angehr and Dean (2010), and the AOS Checklist (Chesser et al. 2019) for scientific and English names. Furthermore, to depict whether we have observed the complete species richness on Jicaron, we did a species richness accumulation curve using R package Vegan (Oksanen et al. 2019).

RESULTS

Overall, we recorded 115 species of birds on Jicarón (115) and Jicarita (53), from 39 and 22 families, respectively. The Jicarita list is a subset of that of Jicaron, with no species recorded from the former that was not also recorded from the latter. Our results include 23 new records for the CNP checklist. The most numerous family was Tyrannidae with 17 species, followed by Parulidae and Scolopacidae with 9 and 8 species, respectively. Further, we added 10 migratory bird species to the CNP checklist, making a total of 29 migratory bird species. The number of

species shared between Coiba and Jicarón was 87.

Based on the Red List (IUCN 2019), two species on Jicaron and Jicarita are considered Near Threatened and one Vulnerable (Table 1). Further, our records expand the distributional range of the Bronzed Cowbird (Molothrus aeneus), Southern Lapwing (Vanellus chilensis), and Black-crowned Night-Heron (Nycticorax nycticorax).

Table 1.

List of the avifauna community at two islands of Coiba National Park (Jicarón and Jicarita). IUCN Status: LC – Least Concern (left as blank spaces); NT – Near Threatened; and VU – Vulnerable. The number of species per family are provided in brackets

Continue Table 1.

Continue Table 1.

Continue Table 1.

Continue Table 1.

Continue Table 1.

Continue Table 1.

Continue Table 1.

Continue Table 1.

Continue Table 1.

Notes on some species of special interest. Black-crowned Night-Heron (Nycticorax nycticorax Linnaeus, 1758): during the trip in December, 2017, we observed a single adult individual flying near our camping area. This is the first record of this species in CNP and reports of this species are uncommon in the region (see Angehr and Dean, 2010).

Bronzed cowbird (Molothrus aeneus Wagler, 1829): this species is considered to be common on the eastward Pacific slopes of Panama. Individual were observed in Jicarón Island, representing a distribution expansion of this species.

Grey-headed (Brown-backed) Dove (Leptotila plumbeiceps battyi): this form (together with the subspecies malae of the Azuero Peninsula) is considered a full species by most references (e.g. Wetmore 1968; Monroe and Sibley 1993; Baptista et al., 1997; Gibbs et al., 2001; Dickinson 2003; Birdlife International, 2019) other than AOS (Chesser et al., 2019). It was common on Jicaron and also encountered on Jicarita. It is otherwise restricted to Coiba, Cébaco, and the Azuero Peninsula (Wetmore, 1968) and Rancheria (G.R.A. pers. obsn). It is considered Vulnerable by BirdLife International (2019).

Mealy Parrot (Amazona farinosa Boddaert, 1783): this species is considered Near Threatened. On Jicarón Island, we observed a small group (< 12 individuals) of Mealy Parrots foraging in the forest canopy and vocalizing. Sightings occurred on the expedition of July, 2017 in mature forest at about 1 km from the coast.

Scarlet macaw (Ara macao Linnaeus, 1758): we observed individuals of Scarlet Macaw in the island of Jicarón, during the visit in March, 2018. Individuals were observed in Punta Ursula, the southern tip of Jicarón Island (7°13'41.8"N, 81°48'10.7"W), foraging seeds of the tropical almond (Terminalia catappa). Considering this species was not observed in any other field trip, we presumed these individuals fly from Coiba Island when this valuable resource is available (Fig. 2).

Fig. 2
Scarlet Macaw (Ara macao). Photo credit: Christian Ziegler

Wandering Tattler (Tringa incana Gmelin, 1789): this small shorebird is a rare transient, with few sightings in Panama, most records being from the Frijoles islets off the north coast of Coiba (i.e. eBird: checklist S27159064 by Groenendijk, 2016). We observed a single individual along the rocky shore in the northwest section of Jicaron.

Western Kingbird (Tyrannus verticalis Say, 1823): we recorded a single individual of this vagrant species on December 20, 2017. The individual was on coastal vegetation (Fig. 3) near Punta Ursula. In general, this species is rarely documented in Panama and our observation represents the southernmost record for this species, replacing its previous report of the locality El Chorogo, in the Province of Chiriqui (eBird: checklist S21016561 by Montanez, 1999).

Fig. 3
Western Kingbird (Tyrannus verticalis). Photo credit: PLC

Yellow-crowned Night-Heron (Nyctanassa violacea Linnaeus, 1758): the only record of this species was taken by a camera trap in Punta Ursula of Jicarón Island. The photographed individual was an immature (Fig. 4) and represents the southernmost record for this species in Panama. This species was first recorded by first Wetmore (1957) in Coiba Island and recent reports are uncommon.

Fig. 4
Yellow-crowned Night-Heron (Nyctanassa violacea). Photo credit: CMMM

Yellow-headed Caracara (Milvago chimachima Vieillot, 1816): this species was first recorded on Coiba in 1993 and since 2001 has become common throughout the island (G.R.A. pers. obsn.). In the past 30 years, the species has undergone a remarkable range extension throughout Panama (Fig. 5)

Fig. 5
Yellow-headed Caracara (Milvago chimachima). Photo credit: Christian Ziegler

DISCUSSION

This study represents the first annotated checklist of birds for Jicarón and Jicarita. We documented 115 species of birds from 39 families in Jicarón and 53 species from 22 families in Jicarita. We recorded 23 bird species that have not been observed on Coiba or other islands of the archipelago, representing new records for CNP (Ibáñez and Cabot 1997). Hence, our results enlarge the reported avifauna of CNP to 191 species, from 45 families. Our findings indicate that 10.4% of the Panamanian avifauna has been recorded on Jicarón and Jicarita, including 11 of the 20 endemic subspecies of Coiba, plus 29 migratory species (67 for CNP), 4 transient, 2 vagrant and 1 breeding migratory (Angehr and Dean, 2010).

The largest numbers of species recorded corresponded to the family Tyrannidae with 17 species, followed by Parulidae and Scolopacidae with eight species each. Among our observations, the most commonly

observed species on Jicarón were Grey-headed (Brown-backed Dove) (Leptotila plumbeiceps battyi), Rufous-tailed Hummingbird (Amazilia tzacatl), and Bananaquit (Coereba flaveola).

We did not record Coiba Spinetail (Cranioleuca dissita) on either island. This species is thus presumably restricted to Coiba and Ranchería alone. Likewise, we did not record the Coiba endemic subspecies of Scaly-breasted Hummingbird (Phaeochroa curvierii saturatior), Southern Beardless-Tyrannulet (Camptostoma obsoletum orphnum), Sepia-capped Flycatcher (Leptopogon amaurocephalus idius), Scrub Greenlet (Hylophilus flavipes xuthus), Rufous-browed Peppershrike (Cyclarhis gujanensis coibae), Tropical Parula (Parula pitiayumi cirrha), Streaked Saltator (Saltator albicollis scotinus), Yellow-faced Grassquit (Tiaris olivacea raviola), or Thick-billed Seed-Finch (Oryzoborus angolensis fractor).

We only recorded four nocturnal species, including Rufous Nightjar (Antrostomus rufus), Yellow-Crowned Night-Heron (Nyctanassa violacea), Black-Crowned Night-Heron (Nycticorax nycticorax), and the Tropical Screech-Owl (Megascops choliba). However, we only recorded nocturnal species from at or near our camping site, or that were photographed by camera traps, which function continuously throughout the day and night. Although our camera trapping effort is significant (~5000 trap-nights), camera traps were mounted on trees at 50 cm above the ground and would not record most arboreal species. Thus, there are potentially more nocturnal bird species Jicarón Island.

Including our checklist, there are currently 67 migratory birds known for the park, of which 16 species are warblers (Angehr and Dean, 2010), indicating that 37% of the migratory warblers recorded for Panama use Coiba National Park during their migration, and 20% use Jicarón. These records suggest that the Coiban archipelago may play a role as a stopover point for migratory bird species. In contrast with the mainland in Panama (Fischer and Vasseur, 2002), the islands of Coiba National Park provide stopover points with reduced anthropogenic effects, since there are no human settlements other than the Ministry of Environment visitors center and the Police station on Coiba Island and the

Smithsonian field station on Ranchería Island.

With regard to seabirds, we noted a colony of >200 individuals of Brown Boobies nesting in rocky cliffs at the southernmost point of the island (Fig. 6). This represents the largest colony of Brown Boobies in the archipelago. Angehr et al. (2004) reported a colony of 120 Brown Boobies and 80 Brown Pelicans nesting at this site, as well as a nesting colony of 28 Brown Boobies on Uva Island in the Contreras Islands in the northern part of CNP.

Fig. 6
Brown Boobies (Sula leucogaster). Photo credit: Christian Ziegler

While our list includes 53 species of birds for Jicarita, this may not represent the complete checklist as we made only short visits to the island in three occasions. Our checklist is the result of eight short expeditions; however, there are a number of sites on these islands, particularly Jicarón, that we have not visited due to logistic and access constraints. Therefore, the avifauna on both islands may be larger than our results suggest, particularly for Jicarón. For instance, using R package Vegan (Oksanen et al. 2019), we produced a species richness accumulation curve only for Jicarón (Fig. 7), but the curve does not reach an asymptote, indicating that our surveys did not fully sample the avifauna of these islands.

Fig. 7
Species richness accumulation curve for Jicarón Island, based on field observations

Our data indicate that species richness similarity between Jicarón and Coiba is about 45%, although the latter is 27 times larger. Thus, the islands of CNP, along other mainland sites (i.e. Bahia Honda and Cerro Hoya), offer an opportunity for studying population dynamics, migration patterns, and behavioral adaptations (Wright and Steadman, 2012) between the islands of CNP and the mainland. The annotated checklist we present here for Jicarón and Jicarita contribute to the baseline information of bird community composition in CNP. We hope our records contribute to an improvement of management policies and, conservation awareness for CNP, and encourage more bird community monitoring on the islands of CNP, as well as other important protected areas in the mainland of the Pacific of Panama such as the sky-island of Cerro Hoya and of Bahia Honda (Buitrago-Rosas et al. 2019; Jimenez and Aparicio, 2005).

Acknowledgements

We thank Omar Lopez, Valerie McMillan, and especially Christian Ziegler for logistic support during the 2015 Coiba Bioblitz, as well as

all sponsors of this expedition. Logistic support was also provided by Smithsonian Tropical Research Institute. We would like to acknowledge Meg Crofoot and Brendan Barrett for enabling us to participate in expeditions in 2017 and 2019 that were part of a different project, which was made possible thanks to a Coss Award for International Field Research awarded to Brendan Barrett and CMMM and a L.S.B. Leakey Foundation grant awarded to Brendan Barrett. Support was also provided to CMMM by a Packard Foundation Fellowship (2016-65130) awarded to Meg Crofoot. CMMM is funded by SENACYT, scholarship program number BIDP-2017-2018. We are grateful to Brendan Barrett, Zarluis M. Mijango, and Evelyn del Rosario for company in the field, and especially to our boat driver Eliecer Vega for transporting us wherever it is needed in CNP. OJ is supported by the National Science Foundation Graduate Research Fellowship under grant no. DGE-1247192.

References

Panama. Agroforestry systems, 54(2), pp.103-113. Fordham, D. A. & Brook, B. W., 2010. Why tropical islands endemics are acutely susceptible to global change. Biodiversity and conservation, 19(2), pp. 329-342.

Angehr, G. R., & Dean, R. (2010). The birds of Panama: a field guide. A Zona Tropical Publication from Comstock Publishing Associates, Cornell University Press.

Biber, E., 2002. Patterns of endemic extinctions among island bird species. Ecography. 25(6), pp.661-676.

BirdLife International (2018) IUCN Red List for birds. Downloaded from http://www.birdlife.org on 28/07/2018.

Buitrago-Rosas, D., Medina, J. L., Castillo-Caballero, P. L., Ortega, J., Garzón, J. L. & Falk, J. J., 2019. Highland avian surveys in Cerro Hoya National Park (Azuero, Panamá) reveal new range extensions, including a rare hummingbird (Selasphorus sp.). Ornitología Neotropical, 30, pp.89-97.

Cardiel, J. M., Castroviejo, S. & Velayos, M., 1997. El Parque Nacional Coiba: El medio físico. In: Castroviejo, S. (Ed.), Flora y Fauna del Parque Nacional de Coiba (Panama). Serviprint Press, Madrid, pp. 11–30.

Crandall, K. A., Bininda-Emonds, O. R., Mace, G. M. & Wayne, R. K., 2000. Considering evolutionary processes in conservation biology. Trends in ecology & evolution, 15(7), pp.290-295.

Chesser, R. T., K. J. Burns, C. Cicero, J. L. Dunn, A. W. Kratter, I. J Lovette, P. C. Rasmussen, J.V. Remsen, J. D. Rising, D. F. Stotz & K. Winker (2016) Fiftyseventh Supplement to the American Ornithologists' Union: Checklist of North American Birds. The Auk 133: 544–560.

Fischer, A. & Vasseur, L., 2002. Smallholder perceptions of agroforestry projects in Panama. Agroforestry systems, 54(2), pp.103-113.

Glynn, P. W., Wellington, G. M., Glynn, O. & Wells, J. W., 1983. Corals and coral reefs of the Galapagos Islands. University of California Press, California.

Groenendijk, K., 2016. eBird checklist: http://ebird.org/ebird/view/checklist?subID=S27159064. eBird, Ithaca, New York, USA. Available at http://www.ebird.org [Accessed 22 March 2020].

Ibáñez, A., 2011. Guía botánica del Parque nacional Coiba. International Cooperative Biodiversity Groups: Instituto Smithsonian de Investigaciones Tropicals: Secretaría Nacional de C.

Ibáñez, C., & Cabot, J., (1997). Las aves del Parque Nacional de Coiba (Panamá). In:Castroviejo, Santiago (Eds.). Flora y Fauna del Parque Nacional de Coiba (Panamá). pp. 457-467.

Jimenez B., & Aparicio (2005), K. Birds of Bahia Honda (Veraguas, Panama). In:Castroviejo, S., & Ibáñez, A. (Eds.). Estudios sobre la biodiversidad de la región de Bahía Honda (Veraguas, Panamá) (Vol. 20). Editorial CSIC-CSIC Press.

Johnson, T. H. & Stattersfield, A. J., 1990. A global review of island endemic birds. Ibis, 132(2), pp.167-180.

Kier, G., Kreft, H., Lee, T. M., Jetz, W., Ibisch, P. L., Nowicki, C., Mutke, J. & Barthlott, W., 2009. A global assessment of endemism and species richness across island and mainland regions. Proceedings of the National Academy of Sciences, 106(23), pp.9322-9327.

Méndez-Carvajal, P. G. (2012). Population study of Coiba howler monkeys (Alouatta coibensis coibensis) and Coiba capuchin monkeys (Cebus capucinus imitator), Coiba Island National Park, Republic of Panama. Journal of primatology., 1(2), 104.

Miller, M. J., Angehr, G. R., Ridgely, R. S., Klicka, J., Ch, O. G. L., Arauz, J., Campos, C. E. & Buitrago-Rosas, D. (2015). Annotated checklist of the birds (Aves) of Cerro Hoya National Park, Azuero Peninsula, Panamá. Check List, 11(2), 1585.

Milton, K., & Mittermeier, R. A. (1977). A brief survey of the primates of Coiba Island, Panama. Primates, 18(4), 931-936.

Montanez, D., 1999. eBird checklist: http://ebird.org/ebird/view/checklist?subID=S21016561. eBird, Ithaca, New York, USA. Available at http://www.ebird.org [Accessed 22 March 2020].

Oksanen, J., Blanchet, F. G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P. R., O’Hara, R. B., Simpson, G. L., Solymos, P. & Stevens, M. H. H., 2018. vegan: Community Ecology Package. R package version 2.5-2. 2018.

Olson, S. L., 1997. Avian biogeography in the islands of the Pacific Coast of western Panama. The Era of Allan R. Phillips: A Festschrift.

Reyes, D., Alcalá, R. E., Arias, D., & Osorio-Beristain, M. (2009). Genetic structuring at a fine scale in the Russet-crowned Motmot (Momotus mexicanus) in a tropical dry forest in central Mexico. Western North American Naturalist, 69(2), 171-174.

Sanderson, J. G., & Trolle, M. (2005). Monitoring elusive mammals: unattended cameras reveal secrets of some of the world's wildest places. American Scientist, 93(2), 148-155.

Thornton, D. H., Branch, L. C., & Sunquist, M. E. (2012). Response of large galliforms and tinamous (Cracidae, Phasianidae, Tinamidae) to habitat loss and fragmentation in northern Guatemala. Oryx, 46(4), 567-576.

Trevino, H. S., Skibiel, A. L., Karels, T. J. & Dobson, F. S., 2007. Threats to avifauna on oceanic islands. Conservation Biology, 21(1), pp.125-132.

Weckel, M., Giuliano, W., & Silver, S. (2006). Jaguar (Panthera onca) feeding ecology: distribution of predator and prey through time and space. Journal of Zoology, 270(1), 25-30.

Wetmore, A., 1957. The birds of isla Coiba, Panamá. Smithsonian Miscellaneous Collections.

Wetmore, A., 1965. The birds of the Republic of Panama. Part 1: Tinamidae (Tinamous) to Rynchopidae (Skimmers). Smithsonian Miscellaneous Collections, Volume 150. Smithsonian Institution Press, Washington, D. C., USA.

Wetmore, A., 1968. The birds of the Republic of Panama. Part 2: Columbidae (Pigeons) to Picidae (Woodpeckers). Smithsonian Miscellaneous Collections, Volume 150. Smithsonian Institution Press, Washington, D. C., USA.

Wetmore, A., 1972. The birds of the Republic of Panama. Part 3. Passeriformes: Dendrocolaptidae (Woodcreepers) to Oxyruncidae (Sharpbills). Smithsonian Miscellaneous Collections, Volume 150.

Wetmore, A., Pasquier, R. F., & Olson, S. L. 1984. The Birds of the Republic of Panama. Part 4. Hirundinadae (Swallows) to Fringillidae (Finches). Smithsonian Institution: Washington D. C.

Wright, N. A. & Steadman, D. W., 2012. Insular avian adaptations on two Neotropical continental islands. Journal of biogeography, 39(10), pp.1891-1899.

Fordham, D. A. & Brook, B. W., 2010. Why tropical islands endemics are acutely susceptible to global change. Biodiversity and conservation, 19(2), pp. 329-342.

Sanderson, J. G., & Trolle, M. (2005). Monitoring elusive mammals: unattended cameras reveal secrets of some of the world's wildest places. American Scientist, 93(2), 148-155.