RECENT HERPETOLOGICAL RECORDS OF SELDOM-OBSERVED SPECIES FROM THE CORDILLERA DE TALAMANCA, COSTA RICA

Jelmer Groen1, Laura Tiemann2, Bobby Bok3, Sander Schagen4 & Wouter Beukema5* 1Ecologisch Adviesbureau FaunaX, Tijnjedijk 89, 8936AC Leeuwarden, the Netherlands. 2Department of Neurology, Technische Universität München, 81675 Munich, Germany. 3St. Michael College, Leeghwaterweg 7, 1509BS Zaandam, the Netherlands. 4De Apollo, Oudaen 6, 1081BZ Amsterdam, the Netherlands. 5Reptile, Amphibian & Fish Conservation Netherlands (RAVON), Toernooiveld 1, 6525ED Nijmegen, the Netherlands. *Correspondence: w.beukema@ravon.nl

Costa Rica is home to a diverse herpetofauna, currently boasting 215 species of amphibians and 268 species of reptiles (Zumbado-Ulate et al., 2019, www.reptile-database.reptarium. cz/). Particularly in recent decades, the country's herpetofauna has been subject to considerable research attention (Sasa et al., 2010;Zumbado-Ulate et al., 2019). Part of this attention is related to extensive amphibian declines that have been observed during the past decades all over the country as well as in the rest of Central America (e.g., Whitfield et al., 2016). These declines likely resulted as a consequence of multiple anthropogenic, environmental, and pathogen-related threats and their mutual interactions (Lips et al., 2005;Pounds et al., 2006). Namely, these include habitat destruction, pollution and fragmentation, climate change, introduction of invasive species, and emerging diseases. One particularly widespread and detrimental cause of amphibian declines is the presence of the fungal pathogen Batrachochytrium dendrobatidis (Bd). Epizootics linked to Bd peaked during the 1980s and 1990s (e.g., Whitfield et al., 2016). Currently, Bd occurs widely throughout the country in an endemic state that continues to pose risk to amphibians (Zumbado-Ulate et al., 2019, 2022. However, various dramatically-declined species have recently shown signs of recovery, while previously 'lost' amphibian taxa are being rediscovered (Abarca et al., 2010;González-Maya et al., 2013;Chaves et al., 2014;Jimenez & Alvarado 2017;Zumbado-Ulate et al., 2019, 2022. While some of these findings may indeed reflect shifts in disease dynamics, it is important to consider that these records may also represent observations of rarely recorded species, and are now only being recorded due to an increase in survey efforts, including expeditions to previously unexplored areas (e.g., Boza-Oviedo et al., 2012;Salazar-Zuniga et al., 2019). One of the least-explored areas in Costa Rica is the Cordillera de Talamanca. A result of the tectonic uplift, this mountain range extends from southwest of the capital San José to beyond the Panamanian border (Marshall, 2007), rises up to an elevation of 3819 m asl, and is covered by the largest remaining natural forest in Central America. Due to the longstanding isolation of ancestral populations in this region, the Cordillera de Talamanca is the area in Costa Rica with the highest degree of endemism (Sasa et al., 2010).
Three informal herpetological surveys into the Cordillera de Talamanca as part of an ecotouristic visit to Costa Rica were conducted during July-August 2021 (Fig. 1). Visual records of reptiles and amphibians were gathered at three visited areas, comprising of the Valle del Silencio ( Fig. 2A), the headwaters of the Río Lori (Cerro Arbolado, Fig. 2B, C) in Parque Internacional La Amistad, and the highlands of the Parque Nacional Tapantí -Macizo de la Muerte (Fig. 2D) (Fig. 3A). The individual was identified as a member of the B. bramei -B. gomezi species group based on moderately webbed hands and feet, truncate toe tips with welldeveloped subterminal pads, brownish-red dorsal colour which becomes lighter posteriorly along the trunk, and grey-black venter and flanks with light cream flecks (Wake et al., 2007). Photo voucher UTADC 9766 (University of Texas at Arlington Collection of Vertebrates Digital Collection, as B. cf. gomezi); ID verified by Eduardo Boza-Oviedo and Jonathan Campbell. This is the second record for the B. bramei -B. gomezi species group from Provincia de Limón, extending the distribution 21 km west in a straight line from the closest known locality for B. bramei at Cerro Dudu, and 25 km northwest in a straight line from the closest known locality for B. gomezi on the continental divide at Cerro Kasir (Boza-Oviedo et al., 2012). Bolitoglossa bramei and B. gomezi cannot be distinguished from each other based on colour pattern alone (Wake et al., 2007). Recent phylogenetic work revealed that two lineages of this group occur seemingly intermittently in the area visited by us (i.e. along the Cordillera de Talamanca between Ujarrás and the Panamanian border); one of these corresponds to B. bramei, while the other was attributed to B. gomezi, even though the authors acknowledge that the latter ID is tentative given that genetic material from the type locality of B. gomezi near San Vito is not available (Boza-Oviedo et al., 2012). Whether the second lineage indeed comprises B. gomezi, or represents an undescribed lineage from the same species group, remains unclear. Syntopic species included Bolitoglossa splendida Boza-Oviedo, Rovito, Chaves, García-Rodríguez, Artavia, Bolaños & Wake, 2012 (see also below), Craugastor aenigmaticus Parra-Olea, 2018, andPristimantis caryophyllaceus (Barbour, 1928).  Wake et al., 1973) which might represent a previously unnoticed diagnostic character for this species. Two consecutive night surveys resulted in records of four individuals of this species, of which two were found ~1.50 m high up on moss covered tree branches, one was climbing ~2.50 m high in vegetation, and one was walking on the forest floor. One of the recorded individuals (an adult male), recognizable by its colour pattern, had been photographed before during an excursion led by a local nature guide in November 2020 (Spizaetus Tours, pers. com.). The salamander was recorded ~70 m from where it was initially found    (Fig. 5A). Identified as B. sooyorum based on long and slender limbs, moderately-webbed (3/4) hands and feet, distinctly-flattened rounded digits that extend beyond the webbing, and its dark lavender brown dorsal, limb, and feet colour, interspersed by profuse, minute, yellow cream flecks (Vial, 1963). Photo voucher UTADC 9777 (University of Texas at Arlington Collection of Vertebrates Digital Collection); ID verified by Jonathan Campbell and Twan Leenders. Our observation comprised a single individual that was recorded sitting exposed in a large arboreal bromeliad at a height of ~1.60 m during light rain, in the direct vicinity of the type locality. To the best of our knowledge, B. sooyorum has not been formally recorded for decades (no records available via www.gbif.org after 1994) . However, salamanders characterized by a similar colour pattern as the individual observed by us have in recent years been increasingly recorded in the vicinity of the B. sooyorum type locality, often by citizen scientists. These salamanders are generally identified as Bolitoglossa cerroensis (Taylor, 1952) (see e.g., www.inaturalist.org, n = 7 observations since 2010). Yet, B. cerroensis was described as having a cream-coloured dorsum with brown stippling and longitudinal streaking, a dark upper tail, dark upper eyelids, and ventral cream mottling. This  description as well as the drawings of B. cerroensis in Taylor (1952), strikingly differ from salamanders observed in the vicinity of the B. sooyorum type locality. Instead, the salamanders from this area strongly match with the description of B. sooyorum by Vial (1963). Thus, we attribute the individual observed by us to that species. Moreover, we tentatively suggest that the observations made by citizen scientists might have been incorrectly assigned to B. cerroensis, while they actually constitute observations of B. sooyorum. Recent phylogenetic work confirms that B. sooyorum and B. cerroensis constitute separate evolutionary lineages, as opposed to being part of a single, morphologically variable species (e.g., Batista et al., 2014;Kubicki and Arias, 2016). A clear need hence exists for further research into salamander systematics along the Macizo de la Muerte, in order to shed light on the occurrence and relationships of its various salamander species (García-París et al., 2000). Syntopic species included Isthmohyla picadoi (Dunn, 1937).   at Arlington Collection of Vertebrates Digital Collection); ID verified by Jonathan Campbell and Twan Leenders. This is the second record (and second individual) of B. splendida, roughly 1,050 m east in a straight line from the type locality, but north of the Río Lori. Like the holotype, the individual was female and   5B). Six individuals were found crawling on mossy road banks. Identified as B. tica based on a combination of the following characteristics: particularly well-defined head, long and slender tail, reddish-brown dorsal colouration with a darker tail, and whitish flecks on the lower flanks and venter (García-París et al., 2008;Leenders, 2016). Not all individuals displayed whitish flecks. Photo voucher UTADC 9779-9781 (University of Texas at Arlington Collection of Vertebrates Digital Collection); ID verified by Jon Campbell and Twan Leenders. Our records extend the highly restricted distribution of this species about 6.3 km south in a straight line from the closest known locality near Tres de Junio along the Carretera Interamericana, and increases the elevation limit for B. tica from 2500 m to 2765 m (García-París et al., 2008). Syntopic species included Bolitoglossa pesrubra (Taylor, 1952) and I. picadoi.

Bolitoglossa compacta
Isthmohyla pictipes (Cope, 1875). Provincia de Limón; Cantón de Talamanca; Distrito Telire; Valle del Silencio, which is part of Parque Internacional de la Amistad, near a cabin along a trail leading to the Rio Terbí (9.1119 N, -82.9614 W, 2,466 m a.s.l.), recorded on 2 August 2021 around 20:00 h (Fig. 4A). Identified as I. pictipes based on colour pattern, comprising a bright-green dorsum, and a whitish band with dark mottling separating the dorsum and venter, the latter being brightly yellow coloured. Photo voucher UTADC 9795 (University of Texas at Arlington Collection of Vertebrates Digital Collection); ID verified by Jonathan Campbell and Twan Leenders. This rare hylid is listed as Critically Endangered on The IUCN Red List of Threatened species as a result of drastic declines attributed to B. dendrobatidis (IUCN SSC Amphibian Specialist Group, 2020). A single metamorph was found on a leaf at ~1.20 m above the surface. The individual showed impaired locomotion activity reminiscent of B. dendrobatidis infection. Syntopic species included B. compacta, C. podiciferus, and D. ventrimaculatus. Chaves-Acuña et al. (2020) recently reviewed the (historical) distribution, paucity of recent records, and status of I. pictipes. Its distributional range stretches from the northern slopes of the Cordillera Central in Costa Rica found in the evening on the upper side of a Heliconia sp. leaf, at a height of ~1.50 m above the surface. Like the holotype, the newly recorded individual was missing its tail. The individual displayed a notable difference between day time and night time colouration not described in the original description (Boza-through the highlands of the Cordillera de Talamanca, where the type locality is located ("between Cerro Pat and the headwaters of the Río Lari, elev. 1,520-2,135 m", Arias & Chaves, 2014) and reaches its southernmost limit in La Amistad International Park bordering Panama (Bolaños et al., 2008). While between the years of 1957 and 1979 more than 200 observational records were submitted to public collections, the last record was documented in the mid 90ies (Chaves-Acuña et al., 2020, Appendices 1, 2). Although it is true that most of the species' range has not been exhaustively surveyed by herpetologists (Bolaños, 2009;García-Rodríguez et al., 2012;IUCN 2020), several recent surveys have been conducted in highland areas close to sites of historical and potential occurrence for I. pictipes (Abarca, 2012;Acosta-Chaves et al., 2015;Hertz et al., 2012), which have not led to any new observations. However, in their recent publication, Chaves-Acuña et al. (2020) report findings of adults and larvae of I. pictipes in the Cerro de la Muerte region, roughly two decades after it was last registered. Thus, the observation presented here constitutes, to the best of our knowledge, the first sighting in several decades from the eastern Costa Rican Cordillera de Talamanca, located roughly 93 km southeast in a straight line from the nearest site of recent rediscovery. The rediscovery of I. pictipes at several sites in the Cordillera de Talamanca, together with recently reported records of I. angustilineata (Taylor, 1952) (Nishida 2006) and I. rivularis (Taylor, 1952) (Olsen & Cossel, 2014;Jiménez et al., 2019), could "indicate a trend towards reappearance in stream-breeding congeners that have remained undetected for several years or even decades in Costa Rica" (Chaves-Acuña et al., 2020). The near simultaneous rediscovery of I. pictipes (including adults, metamorphs and tadpoles) at several sites from which they had previously disappeared is a significant result for the conservation of I. pictipes.
Bothriechis nigroviridis Peters, 1859. Provincia de Limón; Cantón de Talamanca; Distrito Telire; Parque Internacional de la Amistad, on two different locations on and along a trail (9.1145 N, 82.9622 W and 9.1237 N, 82.9613 W, 2,469 m and 2,431 m a.s.l.), recorded on August 2, 2021 around 11:00 h and 14:00 h (Fig. 4D). Identified as B. nigroviridis based on its unmistakable colour pattern, and on distribution (Doan et al., 2016). Photo voucher UTADC 9782-9783 (University of Texas at Arlington Collection of Vertebrates Digital Collection); ID verified by Jonathan Campbell. Two female individuals were encountered during a day hike, basking on ground level on and along the trail. Our records fall within the known distribution and elevation range, but are noteworthy because they confirm that at the highest elevations, where night temperatures drop significantly, B. nigroviridis appears to be chiefly diurnal and ground-dwelling, rather than arboreal and nocturnal (e.g., Leenders, 2019). Syntopic species included Mesaspis monticola (Cope, 1878).

CONCLUDING REMARKS
In summary, the noteworthy records reported here include the rediscovery of Isthmohyla pictipes in the eastern section of the Costa Rican Cordillera de Talamanca, the second record of Bolitoglossa splendida, and the geographical and elevational range extension for B. tica and B. bramei / B. gomezi. We comment on the morphology and ecology of Bolitoglossa compacta, and the ecology of Bothriechis nigroviridis. Finally, we discuss the status of Bolitoglossa sooyorum and B. bramei / B. gomezi, emphazising the need for further research into salamander systematics along the slopes of the Macizo de la Muerte and the eastern section of the Costa Rican Cordillera de Talamanca. Ultimately, the objective of publishing anecdotal records, like the ones presented here, is to eventually aid in assessing the species´ conservation status as well as to inform future conservation efforts and further focused research.