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Habitat Use and Activity of Bothrops Bilineatus Smaragdinus Hoge, 1966 in the Western Brazilian Amazon (Serpentes: Viperidae)

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Habitat Use and Activity of Bothrops Bilineatus Smaragdinus Hoge, 1966 in the Western Brazilian Amazon (Serpentes: Viperidae) Herpetology Notes, volume 14: 567-580 (2021) (published online on 21 March 2021) Habitat use and activity of Bothrops bilineatus smaragdinus Hoge, 1966 in the western Brazilian Amazon (Serpentes: Viperidae) Wirven Lima da Fonseca1, Radraque Rodrigues Correa1, Andesson de Souza Oliveira1, Igor Soares de Oliveira2, and Paulo Sérgio Bernarde1,* Abstract. We present information on the habitat use and activity of the pitviper Bothrops bilineatus smaragdinus in floodplain forests of the western Brazilian Amazon. During a one-year period (April 2018–March 2019) we performed 816 h of time- limited visual searches and recorded 35 individuals, with a further two recorded through occasional encounters, for a total of 37 snakes. Pitvipers were encountered at a frequency of one snake every 23 h (0.04 snakes/h). At night, snakes displayed sit- and-wait hunting activity in 84.9% of recorded cases, while movement was observed in only 15.1%. Adult specimens mainly positioned themselves on branches during hunting, whereas juveniles utilized leaves. Occurrence of snakes was significantly correlated with the frequency of three frog species (Osteocephalus leprieuri, O. taurinus, Scinax ruber), which are part of these vipers’ diet, and it was inversely correlated to rainfall and trail flooding. Bothrops b. smaragdinus was most frequently encountered during the dry season, at the lowest recorded relative humidity, and less frequently during the rainy season. The low encounter frequency may be associated with increased tree canopy humidity and vertical amphibian migration of the Osteocephalus species, which occur at lower heights during the dry season. Keywords. Arboreality, pitviper, sit-and-wait strategy, activity patterns, ecology Introduction factors, including spatial and temporal temperature and humidity distributions, all vary significantly from the Although arboreal amphibians and reptiles form a soil to the upper canopy layer (Madigosky and Vatnick, very diverse component of the tropical environment 2000; Madigosky, 2004; Shaw, 2004). As it concerns and present some remarkable ecological interactions arboreal snakes, environmental features like foliage with other species (e.g., Duellman, 1978; Shaw, 2004; structure, microclimate, and prey type and availability, Dial and Roughgarden, 2004; Wilson et al., 2007), those as well as snake body size, weight, and shape, may that inhabit tropical rainforest canopies are among the determine the perch and forage heights that these least studied vertebrates (e.g., Kays and Allison, 2001; snakes are able to reach and explore (Lillywhite and Guayasmin et al., 2006). In the Amazon, arboreal and Henderson, 1993). sub-arboreal snakes account for 19–35% of community Information on the natural history of snakes is species composition (e.g., Duellman, 1978; Martins and paramount to uncovering their evolutionary biology and Oliveira, 1998; Bernarde and Abe, 2006). Within this ecology (Greene, 1997). However, vast forested areas three-dimensional environment, biotic factors, including have experienced rapid deterioration in the last several plant structure, epiphytic plant availability, and decades, especially in the Amazon, which makes obtaining predator-prey and host-parasite dynamics, and abiotic ecology and biodiversity knowledge a priority for future management and conservation actions (Martins and Oliveira, 1998). Arboreal snakes are sensitive to changes in habitat and are more likely to be severely affected by 1 Laboratório de Herpetologia, Centro Multidisciplinar, Campus deforestation, due to their adaptations and specializations Floresta, Universidade Federal do Acre, Cruzeiro do Sul, Acre 69980-000, Brazil. to their specific habitat (Lillywhite and Henderson, 1993). 2 Laboratório de Etnociências, Ecologia e Conservação, Centro Furthermore, assessments of habitat use and activity of de Educação e Letras, Campus Floresta, Universidade Federal venomous arboreal snakes may also contribute to the do Acre, Cruzeiro do Sul, Acre 69980-000, Brazil. understanding of the circumstances in which snakebite * Corresponding author. E-mail: [email protected] occurs, providing valuable data for prevention guidelines © 2021 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0. (Sazima, 1988; Oliveira and Martins, 2001). 568 Wirven Lima da Fonseca et al. Pitvipers of the genus Bothrops Wagler, 1824 occur characterized as an “Open Alluvial Forest with Palm from Mexico to Argentina (Campbell and Lamar, 2004) Trees” (Acre, 2010) that is partially flooded seasonally and currently comprise 45 species (Uetz et al., 2020). due to its proximity to the Moa River. The LMRF canopy These snakes inhabit several types of habitats, ranging presents an average height of approximately 20 m, with from open areas to dense forest and including habitat a few emerging tree species that can reach heights up disturbed by human activities (Campbell and Lamar, to 35 m. The canopy is dense, primarily composed of 2004). Available studies on the ecology of these snakes the tree genera Brosimum (Moraceae), Enterolobium are generally focused on their activity and habitat (Fabaceae), and Virola (Myristicaceae) (Turci et al., use (e.g., Sazima, 1988; Oliveira and Martins, 2001; 2009). Large trees present tabular roots (“sapopembas”) Nogueira et al., 2003; Wasko and Sasa, 2012; Leão et as an adaptation to the unstable LMRF soil and seasonal al., 2014), and mostly cover terrestrial species, with floods (Turci et al., 2009). The understory displays relatively few studies of arboreal ones (e.g., Turci et a high abundance of grasses (Poaceae) and spiny al., 2009; Andrade et al., 2010; Marques et al., 2012). palms (Astrocaryum, Arecaceae), and relatively few Additional studies on the ecology of arboreal pitvipers herbaceous species, such as heliconias (Heliconiaceae), are therefore not only desirable but essential to fulfil a arrowroot (Marantaceae), and wild gingers (Costaceae). notorious knowledge gap concerning these animals. The diversity of spiny palms is relatively low, and only Bothrops bilineatus (Wied-Neuwied, 1821) is considered a few species, including Euterpe precatoria, Iriartella a complex of species comprising four clades (Dal Vechio et stenocarpa, and Bactris sp., have been recorded in the al., 2018). The taxon for which we report our observations area (Turci et al., 2009). herein corresponds to the “Western Amazonia” clade Data collection. Fieldwork was conducted by four (Dal Vechio et al., 2018), corresponding to the subspecies researchers during a one-year period, between April B. b. smaragdinus Hoge, 1966. This arboreal snake 2018 and March 2019. Three permanent trails were presents nocturnal habits and feeds on amphibians, small systematically inspected, one of length 800 m and mammals, lizards, bats, and other snakes (Dixon and two of 600-m length each (Fig. 1). The time-limited Soini, 1986; Martins et al., 2002; Campbell and Lamar, visual search method (TLVS; Campbell and Christman, 2004; Turci et al., 2009; Fonseca et al., 2019a; Venegas 1982) was applied, which consists of slowly walking et al., 2019). Although B. b. smaragdinus is generally along a transect while searching for snakes visually considered uncommon in the wild (Bernarde et al., exposed in the environment. This method allows for 2011a), some reports of locations where it may be one of documentation of activity and habitat use patterns in the the most frequent animals found during visual searches field. A single person can search both sides of a trail, in the natural environment are available (Silva et al., but two people can optimize the method by searching 2020). There is evidence that this species may be the one side each. When this method is carefully performed, second-ranked venomous snake concerning snakebites in two individuals can search approximately 400 m of a some regions (e.g., Letícia, Amazonas, Colombia; Shell, trail in about 3 h. In this study, around 68 TLVS person- Pastaza, Ecuador; Cruzeiro do Sul, Acre, Brazil; Haad, hours were undertaken each month, totalling 816 1980/81; Smalligan et al., 2004; Mota-da-Silva et al., TLVS person-hours, as follows: 3 h on Trail 1 (400 m 2019). Due to the high vulnerability of arboreal snakes for each pair of researchers) and 4 h on Trails 2 and 3 to habitat devastation and their medical interest, we here (two researchers simultaneously on each track). Field present novel information on the habitat use and activity sampling was performed between 18:00–22:30 h. All patterns of B. b. smaragdinus in a floodplain forest located B. b. smaragdinus individuals recorded on Trails 2 and 3 in the western Brazilian Amazon. were collected as voucher specimens (License SISBIO 12178), while individuals encountered on Trail 1 were Material and Methods only observed and not collected. The following data were recorded for each collected specimen: total length Study area. This study took place in the Lower Moa (TL), sex, and gut contents. Voucher specimens have River Forest (LMRF) in Cruzeiro do Sul Municipality, been deposited at the Universidade Federal do Acre, Acre State, Brazil (7.3738°S, 72.4728°W; Fig. 1), a Campus Floresta Herpetological Collection (UFACF site in the western Amazon. This region presents a hot 4299–4317). Seven daytime visits were made in an and humid tropical climate with an average annual attempt to record the activity of specimens observed temperature of 24°C (Ribeiro, 1977), with the driest during previous nights. months occurring from May–October. The LMRF is Habitat Use and Activity of Bothrops
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