88urn:lsid:arphahub.com:pub:84CAD438-4D58-581C-86A1-48EF43C3EC79Neotropical Biology and ConservationNBC2236-3777Pensoft Publishers10.3897/neotropical.14.e3957239572Research ArticleColubridaeBiodiversity & ConservationNatural HistoryZoology & Animal BiologyRediscovery of the enigmatic forest racer snake, Dendrophidionboshelli Dunn, 1944 (Serpentes, Colubridae): actions for the conservation of a critically endangered speciesRedescoberta da enigmática cobra florestal Dendrophidion boshelli Dunn, 1944 (Serpentes, Colubridae): ações para a conservação de uma espécie criticamente ameaçadaRojas-MoralesJulian Andrésjulian.herpetologia@gmail.com1Marín-MartínezMateo2Zuluaga-IsazaJuan Camilohttps://orcid.org/0000-0001-7679-13962Corporación Universitaria Santa Rosa de Cabal (UNISARC), Santa Rosa de Cabal, Risaralda, ColombiaCorporación Universitaria Santa Rosa de CabalManizalesColombiaGrupo de Ecología y Diversidad de Anfibios y Reptiles, Universidad de Caldas, Manizales, ColombiaUniversidad de CaldasManizalesColombia
20193012201914457758996985E89-79A0-5EF3-8CE0-C7916FAA55713008201930112019Julian Andrés Rojas-Morales, Mateo Marín-Martínez, Juan Camilo Zuluaga-IsazaThis is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Dendrophidionboshelli is a poorly known and endemic snake species from the Middle Magdalena river valley in Colombia. It was described in 1944 based on a single specimen from the municipality of Caparrapí, department of Cundinamarca. Since the original description, only three additional specimens have been established. As part of the results of a herpetological monitoring in the Miel I Hydroelectric project, department of Caldas-Colombia, three additional specimens of D.boshelli were found in 2014–2015. The specimens represent the second known population of the species. We presented morphological data and pholidosis; description of the coloration in life, and a description of the habitat. Recently, D.boshelli was included as a Critically Endangered (CR) species in the Red Book of Reptiles of Colombia, and the IUCN Redlist. For this reason, to promote the local conservation of this and other endemic and threatened species in the Miel I area, we suggested some actions at the local level, such as establishing a conservation area with legal status in the Middle Manso River basin, which is a tributary of the Miel I Hydroelectric project.
Dendrophidionboshelli é uma espécie de cobra endêmica e pouco conhecida do meio do vale do rio Magdalena, na Colômbia. Esta serpente foi descrita em 1944 com base em um único espécime do município de Caparrapí, departamento de Cundinamarca. Desde a sua descrição, apenas três indivíduos adicionais são conhecidos. Recentemente, como parte dos resultados de um monitoramento herpetológico no projeto hidrelétrico Miel I, próximo à localidade-tipo, foram encontrados três exemplares adicionais de D.boshelli. Os exemplares representam a segunda população conhecida da espécie. Dados morfológicos, a descrição de sua coloração na vida e uma descrição do habitat são apresentados. Recentemente, D.boshelli foi incluída no Livro Vermelho dos Répteis da Colômbia na categoria Perigo Crítico (CR), e também para a Lista Vermelha da IUCN. Por ese motivo, para promover a conservação local desta e de outras espécies endémicas e ameaçadas na área do projeto Miel I, sugerimos algumas ações no nível local, como estabelecer uma área de conservação com status legal no rio Manso, que é tributario do projeto hidreléctrico Miel I.
Colombiaendemic and threatened specieshabitat preservationMagdalena River valleysnakesColômbiaespécies ameaçadaspreservação de hábitatserpentesvale do rio MagdalenaIntroduction
Compared to other vertebrates, snakes are still relatively unknown in many aspects of natural history, and consequently in their status of conservation (Greene 1997; Cundall and Greene 2000; Campbell and Lamar 2004; de Fraga et al. 2013). Some tropical ecosystems, such as rainforests, can support a high snake's diversity with some species reaching high local abundances (Martins and Oliveira 1998; Guimarães et al. 2014; Lynch 2015); however, an important proportion of species of the tropical snake’s assemblages are considered rare species because they are barely observed and therefore poorly represented in scientific collections and literature (Lynch et al. 2016).
Snakes of the genus Dendrophidion Fitzinger, currently comprise 15 Neotropical species (Uetz et al. 2019). They are diurnal semi-arboreal colubrids with a body slightly compressed, dorsal scales keeled, head clearly differentiated from the neck, eyes prominent with rounded pupils, and with a very long tail (30–50% of the total length; Lieb 1988; Stafford 2003; Freire et al. 2010; Cadle, 2012a, b; Cadle and Savage 2014). This genus is distributed from southern Mexico to Bolivia (Lieb 1988; Freire et al. 2010; Natera et al. 2015). Dendrophidionboshelli Dunn, 1944, is a forest racer snake only known by three individuals collected at the type locality in the middle Magdalena River valley, Colombia (Dunn 1944; Caicedo-Portilla and Lynch 2015). The intra-generic relationships of D.boshelli are poorly understood, given that it is categorized as incertae sedis in the genus by Lieb (1988). Similarly, there is insufficient information about its natural history. It is suspected that, like other species of the genus, D.boshelli is a stream-dwelling species that feeds on anurans (Cadle 2012b; Caicedo-Portilla and Lynch 2015). Since it is only known from the type locality, and a nearby heavily intervened area in Colombia, D.boshelli was recently categorized as Critically Endangered (CR) in the IUCN Redlist (Caicedo et al. 2017), and included in the Red Book of reptiles of Colombia (Caicedo-Portilla and Lynch 2015).
Here, we present the discovery of a new population of this species, expanding the knowledge by providing new morphological data and a distribution and habitat update. Also, we present the first photographs in life of the species. We also propose a series of steps to promote the protection of the habitat for this and other vertebrate endangered species, in the Middle Manso River basin, department of Caldas, Colombia.
Methodology
During 2014–2015, more than 400 effective sampling hours were invested in monitoring the diversity and distribution of the herpetofauna in the Manso River, which supplies the Miel I Hydroelectric Power Plant, at the east of the department of Caldas (Figs 1, 2). During fieldwork, we registered three specimens assignable to the snake D.boshelli. The identification was made after reviewing the specimens and comparing them with the holotype (Instituto de Ciencias Naturales, ICN-10117) and the original description (Dunn, 1944). All three specimens were collected under the research permit granted by the pertinent environmental authority (Corporación Autónoma Regional de Caldas - Corpocaldas), and housed in the herpetological collection of the Natural History Museum at the Centro de Museos of the Universidad de Caldas (MHN-UCa) (Table 1). Snout vent length (SVL) and Tail length (TL) were registered with a ruler to the nearest mm. Temperature and humidity were registered with an Extech thermo-hygrometer. Ventral and sub-caudal counts follow Dowling (1951). Sex was determined on the basis of presence/absence of hemipenis verified through a ventral incision at the base of the tail.
Map of the known distribution of Dendrophidionboshelli. (1) Type locality, Volcanes village, municipality of Caparrapí, department of Cundinamarca. (2) El Valiente village, municipality of Caparrapí, department of Cundinamarca. (3) New record, Manso River transfer, La Sonrisa village, municipality of Samaná, department of Caldas, Colombia.
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Morphometric characters and scale counts of Dendrophidionboshelli specimens from Manso River, municipality of Samaná, department of Caldas, Colombia. Characters impossible to be precisely recorded due corporal damage are marked with an asterisk (*).
Character
ICN 10117 (Holotype, ♀)
MHN-UCa 239 ♂
MHN-UCa 263 ♂
MHN-UCa 271 ♂
SVL (mm)
253
419
480
531
TL (mm)
56 *
*
340
369
TC/SVL
–
–
0.72
0.69
Dorsals
15-15-15
15-15-15
15-15-15
15-15-15
Ventrals
135
136
136
141
Subcaudals
37 *
133
134
128
Preoculars
1-1
1-1
1-1
1-1
Post-oculars
2-2
2-2
2-2
2-2
Temporals
2+2
2+2
2+2
2+2
Supralabials
8/9 (4–6)
9/9 (4–6)
8 (3–5)/9 (4–6)
9/9 (4–6)
Infralabials
10/ 9 (1–6)
9/ 9 (1–6)
9/ 9 (1–6)
9/9 (1–6)
Preventrals
3
3
3
3
Gulars
3
4
4
3
Cloacal plate
Undivided
Divided
Divided
Divided
Dorsocaudal reduction
–
*
8>6, 14–15
8>6, 20–21
Habitat of the new located population. Records come from the adjacent area to the entry point of the Manso River transfer (5.608767N; -74.955333W, WGS84, 650 m), La Sonrisa village, “Corregimiento Berlín”, municipality of Samaná, department of Caldas, Colombia. This area is 55 km north-west from the type locality (Fig. 1). Upstream vegetation of the Manso River transfer belongs to a mature forest in good conditions, currently interrupted by trails in its interior, as well as livestock and agricultural crops (e.g. Avocado and coffee, Perseaamericana and Coffeaarabica, respectively), towards the hilltops of the mountains (Fig. 2). Such activities necessarily involve the intervention of the forest and, as a consequence, there is extraction and selective use of wood. The forest has a continuous canopy by and large, with five strata in its vertical structure and trees of up to 30 m. A rich and well-formed understory is present. This forest is characterized mainly by the abundance and dominance of palms (Geonoma, Oenocarpus and Welfia; Arecaceae), in addition to a high abundance of riparian vegetation belonging to the genera Asplundia, Cyclanthus, Dicranopygium (Cyclanthaceae), and Costus (Costaceae). Humidity varies between 54−88% and temperatures between 23−29 °C, in addition to a precipitation between 3500−4000 mm per year (Díaz-Ayala and Zuluaga-Isaza 2015). Interior conditions include vegetation species of advanced state of succession, such as Pleurothyrium sp. (Lauraceae), Virolasebifera (Myristicaceae), Welfiaregia (Arecaceae), Compsoneuramutisii (Myristicaceae), Geonoma sp. (Arecaceae), among others. This area belong to the Pre-montane Tropical Forest life zone (bp-PM) sensuHoldridge (1982), or to the Middle Magdalena Tropical-humid Zonobiome (Rodríguez et al. 2006).
Habitat of Dendrophidionboshelli in the Manso River basin, La Sonrisa village, municipality of Samaná, department of Caldas, Colombia. (A) Panoramic view of the general habitat (B) Interior of the forest (C) Manso River at the point of transfer (D) Recent burning -September 2019- to expand agricultural areas (E) Recent intervention -open road- inside the primary forest. Photographs: Julián Andrés Rojas and Mateo Marín.
https://binary.pensoft.net/fig/368145Results
The first snake (MHN-UCa 0239; SVL 419 mm, tail broken) was registered on 18 May 2014 at 11:35 h, road killed 150 m above the Manso River transfer site. The second individual (MHN-UCa 0263; SVL 480 mm, TL 340 mm; Fig. 3) was registered on 2 December 2014 at 09:20 h, resting on a hollow at 1.7 m high in a wall of rock on the edge of the Manso River. The third individual (MHN-UCa 0271; SVL 531 mm, TL 369 mm) was found on 4 April 2015 at 20:00 h (28.7 °C, 82% relative humidity), perched on a bush branch 1.47 m above the ground and >100 m away from the river. The three specimens are adult males and present a similar coloration, consisting of a light green back on the anterior part of the body -including the head-, being yellowish towards the edge of the ventral scales; the back turns reddish with brown tones later from the first 1/6 of the total length until the tip of the tail (Fig. 3). On their backs all the specimens present 79–84 black stripes crossed transversely, of less than a scale wide and reaching up to the fourth row of dorsal scales. These crossed black stripes have at their ends and in the spaces between scales, a bright yellowish green spot. The belly is uniformly yellow from the second pre-ventral scale to the tip of the tail, but has a more vivid tone towards anterior part of the venter (Fig. 4). Lateral edges of the ventral scales present a black spot, forming almost a continuous line in the anterior part of the body because the spots cover almost the entire edge of the scales (Fig. 3). The head is olive green dorsally, turning brown in the scales that border the orbit. Supra and infra-labial scales are white, with light orange spots concentrated on the edge, which is only observable at close range; a black line borders the upper part of all the supra-labial scales, being more conspicuous posteriorly (Fig. 3). Dendrophidionboshelli is found in sympatry with congenerics D.percarinatum and D.bivitattum in the Manso River.
Adult male of Dendrophidionboshelli from the Manso River, La Sonrisa village, municipality of Samaná, department of Caldas, Colombia (MHN-UCa 0263; SVL 480 mm, TL 340 mm). Photographs: Julián Andrés Rojas.
Photographs showing ventral coloration in newly euthanized individuals of Dendrophidionboshelli, (A) MHN-UCa 0263; (B) MHN-UCa 0271. Photographs: Julián Andrés Rojas.
https://binary.pensoft.net/fig/368147
Threats to the conservation of Dendrophidionboshelli. Currently, although it is difficult to determine how affected this species may be in the Manso River area, due to the lack of sufficient population data − only three individuals for more than 400 h of survey − different anthropogenic factors may be recognized as a threat to the species in the near future. The expansion of grazing land for cattle breeding is the main factor leading to deforestation in the Manso River habitat. In addition, near this area Uranium exploitation is planned, for which the forests bordering the river could be intervened by the construction of more roads and the movement of people and heavy machinery (Fig. 2E). This interference in this habitat directly affects the associated biodiversity, which include different vertebrate endemic and threatened species (Fig. 5), some of which are monitored with a functional connectivity approach at the landscape scale, supported by ISAGE S.A. In addition, one of the registered individuals of D.boshelli was road killed on the road that leads to the point of the river transfer. As this is a diurnal and terrestrial snake’s species, it may be more susceptible to vehicular run-over than other snakes, as has been observed in other Neotropical forests (i. e. Hartmann et al. 2011; Maschio et al. 2016).
Endemic and threatened vertebrate species from the Manso River transfer point, municipality of Samaná, department of Caldas, Colombia. (A) Rulyranasusatamai, (B) Sachatamiapunctulata, (C) Bolitoglossalozanoi, (D) Anolislimon, (E) Anolissulcifrons, (F) Capitohypoleucus, (G) Rhamphastosvitellinus, (H) Aotusgriseimembra, (I) Choloepushoffmanni, (J) Leoparduspardalis. Photographs: Raúl Gil (F, G), Julián Andrés Rojas (A, B, C, D, E, H, I, J).
https://binary.pensoft.net/fig/368148Discussion
In recent years, some species of snakes have been rediscovered in Colombia (i.e. Atractuswagleri, Passos & Arredondo, 2009; Trilepidajoshuai, Rojas-Morales & González-Durán, 2011; Coniophanesandressensis, Caicedo-Portilla, 2014; Imantodesphantasma, Medina-Rangel et al., 2018; Vanegas-Guerrero et al., 2019), which should promote the need for field studies to monitor populations of these little-known species. The recording of species after several decades since the last known description is a relatively common case for snakes. Some species are difficult to find because they occupy hidden microhabitats, live in inaccessible places or have low densities, among other factors (Henderson et al. 1988; Greene 1997; Curcio et al. 2002; Sawaya et al. 2008; Medina-Rangel et al. 2018). In addition, many localities are only sampled a few times with long intervals between field surveys.
Caicedo-Portilla and Lynch (2015) suggested that D.boshelli may be affected by the decrease in amphibians, as has been suggested for other species in the genus Dendrophidion (Cadle 2012b). Rio Manso has registered the greatest diversity of amphibians compared to other sites in the area of the Miel I Hydroelectric project (Díaz-Ayala and Zuluaga-Isaza 2015). This could corroborate what was proposed by Caicedo-Portilla and Lynch (2015), indicating a possible relationship between the presence of D.boshelli and a diverse amphibians assemblage. It should be noted that in the Manso River we also recorded other species of snakes that inhabit well preserved habitats (e.g. Oxyrhopusoccipitalis, Scaphiodontophisannulatus) (Rojas-Morales et al. 2018). Currently, the information about the distribution of D.boshelli is still inconclusive, and it is possible that this species has a wider distribution along the Middle Magdalena River, encompassing the lowland and pre-montane humid forests of the Eastern and Central Cordilleras in Colombia. Their presence is estimated likely in areas such as primary forests of the Serranía of the Quinchas (department of Boyacá), the Samaná and Claro rivers canyons (departments of Antioquia and Caldas), and as far to the north to reach Serranía of San Lucas.
Compared to other more charismatic animals, such as birds and mammals, snakes have received little scientific attention to develop conservation programs and strategies (Mullin and Seigel 2009). There is a strong argument from a scientific perspective that, in practice, the critical issue generally boils down to the preservation of habitat. If the habitat is retained, the snake -or other- population will generally persist; whereas if the habitat is lost, so is the population of interest (Seigel and Mullin 2009). Thus, we strongly advocate for the legal protection of the representative habitat of D.boshelli in the Manso River, as the essential core of any broad conservation initiative.
Conclusions
Although there are good habitat conditions in the area of the detected population, there is no legal conservation target figure that guarantees its permanence over time, and therefore it is susceptible to human intervention (e.g. conversion of the ecosystem for the establishment of crops and roads), as observed during years 2018–2019 (Fig. 2D, E). Approximately 4 km to the north of the Manso River, exists the “Distrito de Manejo Integrado Laguna de San Diego”, which is a non-restricted conservation area for recreational and touristic purposes. For this reason, to mitigate the possible negative impacts in the short term, we suggest the following conservation actions at the local level:
Establishing a conservation area with vested legal status for the Middle Manso River basin, with the justification of preserving endemic and threatened biodiversity, as well as the water resource for hydroelectric generation. We propose the figure of “Protective Forest Reserve” in the terms of Decree Law 2811 of 1974, National Code of Renewable Natural Resources and Protection of the Environment, Art. 204., which defines protective forest area as: “the zone that must be conserved permanently with natural or artificial forests, to protect these same resources or other renewable natural resources. In the protective forest area, the protective effect must prevail and only the secondary fruit of the forest will be allowed to be obtained”. We propose the delimitation and protection of 756 ha around the transfer point of the Manso River, covering the forest and headwaters of streams and creeks that drain to the river (Fig. 6).
Restoring structural connectivity between the forest fragments of the Manso river basin with the National Natural Park Selva de Florencia and DMI Laguna de San Diego to facilitate the flow of fauna and flora through this area.
Promoting the establishment of visual signals to announce the presence of threatened wildlife in the vicinity of the area of Miel I Hydroelectric project. This seems to be an action to reduce vertebrate mortality from road kill. Road kill mortality has not been evaluated locally and deserves specific research.
Developing a Dendrophidionboshelli focused monitoring plan, in order to know local density and ecological traits for local conservation strategies. This is necessary to know how this species is influenced locally in relation to environmental changes and habitat availability.
We call attention to the non-mining exploitation around the Manso River by the U308 Corp, in the “Corregimiento Berlín”.
Proposed conservation area for the habitat of the Middle Manso River basin, municipality of Samaná, department of Caldas, Colombia. Map edition was based on a Landsat 8 image of August, 2018.
To ISAGEN S.A E.S.P. and Universidad de Caldas for their economic and logistical support. To the local guides (Jaime, Jorge and Toño) who accompanied us during fieldwork. The senior author is deeply indebted to Martha Calderón (ICN) for allowing the review of specimens under her care, including the holotype of the species. We thank our field partners in Rio Manso, Juan David Corrales, Abel Rojas, Raúl Gil and Andrés Murillo, for all their biological information and photographs. Thanks to the Autonomous Regional Corporation of Caldas (Corpocaldas) for granting the research and collection permit (Resolution 164 of May 12, 2014). To Julián Salazar and Héctor Ramírez Cháves for the workspace in the Museo de Historia Natural of the Universidad de Caldas. To Vanesa Serna for her help with the SIG work in Figure 6. We are deeply indebted to Save The Snakes for their financial support to an education program regarding snakes. Special thanks to Héctor Ramírez Cháves, Luis Felipe Esqueda, Juan Salvador Mendoza, and two anonymous referees, for their comments and suggestions on the manuscript.
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