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 bilineatus smaragdinus 569

Figure 1. Location of the study area (red circle) and tracks sampled in the Lower Moa River Forest, Cruzeiro do Sul Municipality, Acre State, Brazil. In the inset at lower left, Acre State is identified by the black colour. In the inset at upper right, trail colours include blue (Trail 1), red (Trail 2), and yellow (Trail 3).

During fieldwork, individuals were observed for 5 Collection of environmental variables. Frogs min in order to record their activity patterns according considered potential prey for B. b. smaragdinus as to the following protocol: (1) encounter time; (2) perch well as others seen in the vegetation during TLVS substrate; (3) height above ground (measured with a were counted and identified (Bernarde et al., 2013). common tape measure or laser distance measurer); (4) Temperature and relative humidity data were recorded activity (hunting, moving, or resting), as inferred from at the beginning and the end of daily fieldwork using the individual’s posture (see Oliveira and Martins, 2001; an Akrom Kr811 thermo-hygrometer (Akrom Produtos Turci et al., 2009); and (5) direction of an individual’s Eletrônicos, São Leopoldo, Brazil) positioned 1.5 m head in relation to the tree trunk when an individual aboveground, and the data were then averaged for was hunting on branches. When encountered again, subsequent analyses. Rainfall data were obtained from individual snakes could be recognized by their natural a meteorological station located 3.5 km from the study colour patterns on the head, body, and tail, associated area (Inmet, 2019). A common measuring tape or laser with individual size, through the use of pictures taken in measurer (for very high heights) were used to define the the field with a Nikon Coolpix P900 camera. This was height of the substrate on which the snakes were found, facilitated by several snakes that remained stationary, in the diameter of tree trunks at breast height (DBH) was the same trees or branches, or close to the same spot where calculated from their circumference as obtained with they were previously observed (at a distance of up to 30 a measuring tape, and the diameters of branches were m). Bothrops b. smaragdinus individuals encountered measured with callipers when possible. The flooding more than once during the same month were not counted rate of each trail was obtained by considering the multiple times for the seasonality analyses. Individuals percentage of flooded linear trail distance (i.e., if 100 m with a total body length of ≤ 30 cm were considered of a 400-m trail were flooded, this percentage would be juveniles, as this length corresponds to the approximate given as 25%), and the average flood values per month size of neonates (25.5–27 cm; Grego et al., 2012). were used. 570 Wirven Lima da Fonseca et al.

Data analysis. The Spearman correlation test was used (below 90%) were observed during the dry season, to evaluate the relationship between B. b. smaragdinus between June and October (Table 1). All trails presented occurrences and predictor variables (prey, rainfall, high flood levels (40–100%) as lake levels increased temperature, relative humidity, flooding), as primary in the LMRF, which occurred in the rainy season from data were not normally distributed. This correlation test December–March (Table 1). statistically determines the strength of a relationship Activity.­ Bothrops b. smaragdinus were mostly between paired data. Results were considered significant observed performing hunting activities at night (n = 63, at P < 0.05. 82.9%; Fig. 2A–C, E, G, H), followed by locomotion activity (n = 13, 17.1%; Fig. 2D). Individuals performing Results ambush hunting exhibited a caudal luring strategy on 44 occasions (Fig. 2C). During daytime encounters (n = 17), Encounters. A total of 35 B. b. smaragdinus individuals individuals were most often observed resting (n = 14; was recorded on the three investigated trails during our Fig. 2F), and only three individuals hunted in the early surveys (ca. one individual per 23 h of searching, or morning (Table 2). 0.04 snake/h; Fig. 2; Table 1; Appendices I, II). Eighteen Correlation between biotic and abiotic factors. individuals were collected as voucher specimens on The occurrence of B. b. smaragdinus was positively Trails 2 and 3 (11 males with TL 499–668 mm and mean correlated with the frequency of three amphibian prey TL = 588 mm; seven females with TL 316–758 mm and species (Osteocephalus leprieurii, O. taurinus, Scinax mean TL = 578 mm). The stomach of one specimen ruber; R = 0.707; P = 0.01; n = 12). Conversely, the contained a treefrog, Scinax ruber (Hylidae), and another occurrence of B. b. smaragdinus was inversely correlated a lizard, Gonatodes humeralis (Sphaerodactylidae). with rainfall (R = –0.6430; P = 0.02; n = 12) and flooding Bothrops b. smaragdinus was the most abundant snake (R = –0.9325; P < 0.0001; n = 12). No correlations recorded during the surveys, corresponding to 27% of were observed between B. b. smaragdinus occurrence total snake species found (n = 130 individuals of 21 and relative humidity (R = –0.4588; P = 0.1336; I = species). On Trail 1, 17 B. b. smaragdinus were observed 12), temperature (R = 0.2699; P = 0.39; n = 12) and on 58 occasions, including both encounters and repeated the frequency of all amphibian species detected on the encounters. In addition, one juvenile was occasionally vegetation (R = –0.3364; P = 0.28; n = 12). recorded on Trail 1 after completing a TLVS on Trail Substrate use. In general, B. b. smaragdinus was 2, and another was collected off the trails. A total of 37 observed between 0.3 m and 18.0 m in height (mean = individuals were recorded, and most presented a brown 6.4 m; n = 63 observations) when hunting on trees with (59.5%) tail tip, while the rest (40.5%) exhibited a white diameters varying between 1.9 cm to 45.1 cm (mean = tail tip, independent of sex or age (Fig. 2A, B). 12.2 cm; n = 49) (Appendix I). Most individuals were Seasonality. Forty-one of the encounters (75.9%) found up to 5 m in height (n = 39, 51%; Fig. 3A). occurred during the dry season, with no individuals Individuals > 30 cm in total length were observed encountered during rainy season from December–March coiled up on branches during hunting activities (n = 56 (Table 1). Three juveniles (approximately 250 mm in total observations; Fig. 2A–C, E), and only a single individual length) were observed in November, at the beginning of was found 0.3 m above the ground, as it was hunting on the rainy season. On the other hand, frogs were present a fallen palm leaf. Juveniles < 30 cm in length (n = 4) on the vegetation during all months, exhibiting a slightly were observed on leaves (n = 6 observations, including higher abundance in the rainy season, when 53.8% of all two repeated observations; Fig. 2G, H). Diameters of observed frogs were encountered (Table 1; Appendix II). branches used for hunting ranged from 5.2–12.3 mm Osteocephalus leprieurii and O. taurinus were the (mean = 8.4 mm; n = 28). Resting activity was recorded most abundant anuran species detected throughout 14 times, and the individuals usually remained on the year, corresponding to 50% of all amphibians recorded same substrate used for hunting during the previous night on the vegetation (Appendix II). Furthermore, these (heights from 1.8–11.4 m; mean = 4.8 m; n = 9; Fig. 3B). species were the most frequent during the dry season Based on 57 observations, we calculated snake residence (64.4% of encounters). The third most abundant time on the same substrate (branch and tree). In most amphibian was the toad Rhinella margaritifera (35% cases (17), the snake remained on the same substrate of encounters), which was seen more frequently during only during the night of the first encounter, followed the rainy season (70% of all records for this species; by two days (9) and three days (6). In two occasions, Appendix II). The lowest relative air humidity levels Habitat Use and Activity of Bothrops bilineatus smaragdinus 571

Figure 2. Shown are several Bothrops bilineatus smaragdinus specimens encountered during our surveys. Adults may exhibit white (A) or brown (B) tail tips. Individuals performing different activities include (C) the use of caudal luring to hunt, (D) locomotion, (E) and sit-and-wait hunting with a tongue flick. (F) The same individual in (E) is shown resting during the day in the same tree. (G) and (H) are juveniles (< 30 cm in total length) hunting on leaves. Photos taken by Wirven Lima da Fonseca (A–D, H) and Paulo Sérgio Bernarde (E–G). 572 Wirven Lima da Fonseca et al.

Table 1. Bothrops bilineatus smaragdinus encounters on trails during the Time Limited Visual Searches in the Lower Moa River Forest, Cruzeiro do Sul Municipality, Acre State, Brazil, and the biotic and abiotic variables relevant to the present study. Reported variables include encounters with the snake (Encounters); the general presence of frogs on the vegetation (Frogs); the presence of the Osteocephalus leprieurii, O. taurinus, and Scinax ruber, the three frog species recorded as prey of B. b. smaragdinus (Prey); the average temperature at night (Temperature, °C); the average relative humidity at night (Humidity, %); total monthly rainfall (Rainfall, mm); and the linear percentage of trails flooded (Flood, %). Months are indicated by capital letters, beginning in April 2018 and ending in March 2019. Repeated encounters with the same individual during the same month were not taken into account, only in different months.

2018 2019 Variable A M J J A S O N D J F M Encounters 9 1 5 9 9 12 5 4 0 0 0 0 Frogs 48 56 56 46 62 54 97 104 58 119 34 69 Prey 40 26 33 29 50 46 58 52 20 26 13 16 Temperature 24.8 25.1 25.5 26 25 25.4 26.8 26.2 25.7 23.8 23.5 24.4 Humidity 97.5 92.6 86.3 88 86 87.8 85.4 92.8 92.8 90.9 93.6 91.9 Rainfall 243.2 166 23.6 37.4 69.6 33.4 233.4 397.8 191.2 358.6 412.8 389.4 Flood 0 20 0 0 0 0 20 20 40 80 100 60

up to 15 and 17 days residence times were documented the diet of B. b. smaragdinus in this study (with prey (Fig. 3B). Individuals moving on the vegetation were including only two frogs and one lizard), we confirmed observed between 1.4 and 19.9 m in height (mean = 5.7 that adults of this snake species prey on ectothermic m; n = 13; Appendix I). animals (e.g., Martins et al., 2002) and also often use caudal luring as a strategy (Fonseca et al., 2019a). Discussion Moreover, the specific prey found in the stomachs of three specimens (Osteocephalus taurinus, Scinax ruber, Bothrops b. smaragdinus was the most frequently Gonatodes humeralis) represents only arboreal habits encountered snake species during our surveys in the (Dixon and Soini, 1986; Miranda et al., 2015). LMRF (Silva et al., 2020). The encounter rate for the Although males (11 individuals) were more frequently species (0.04 snakes per hour) was higher than that encountered than females (8), the overall number recorded for B. atrox, which was 0.02 in the same study of specimens collected is insufficient to adequately area and 0.02 in the Adolfo Ducke Forest Reserve, in discuss sex ratios. In general, males displayed a larger Manaus (Oliveira and Martins, 2001; Turci et al., 2009). average size (588 mm) than females (578), but the The high abundance of B. b. smaragdinus in this locality largest specimen was a female of length 758 mm, while is intriguing since this species had not previously been the largest male was 668 mm in length. At this same recorded in species survey studies developed in terra locality, Turci et al. (2009) recorded a similar pattern, firme areas (e.g., Avila-Pires et al., 2009; Bernarde et al., of a 780 mm female and a 670 mm male specimen. 2011b; Fonseca et al., 2019b). This may indicate that B. However, in Bothrops species, females tend to be larger b. smaragdinus may be less frequent or more difficult to than males (Almeida-Santos and Salomão, 2002; Silva detect by visual searches in other vegetation structures. et al., 2017; Bisneto and Kaefer, 2019). Thus, the pattern Both male and female juvenile and adult B. b. we detected may be due to insufficient sampling. smaragdinus in this population exhibited tail tips Unlike the general seasonality occurrence pattern with a colour different from the rest of the body. Tail observed for Amazonian snake species registered by tips can be white or brown, regardless of age and sex TLVS, where abundance is higher during the rainy season (Fonseca et al., 2019a). Tail tip colour retention in adult (Martins and Oliveira, 1998; Oliveira and Martins, 2001; Bothrops species indicates that these individuals may Bernarde and Abe, 2006), B. b. smaragdinus was more feed on ectothermic prey and use their tail as a decoy frequently encountered in the dry season (74.5% of the and lure prey as a hunting strategy (Martins et al., 2002). records), when relative humidity was lowest. On the Although we obtained relatively little information on other hand, frogs (potential prey) were registered on the Habitat Use and Activity of Bothrops bilineatus smaragdinus 573

Table 2. Daytime Bothrops bilineatus smaragdinus observations on Trail 1. All observations were made in 2018. No. of Humidity Temperature Date Time of Day Activity Individuals (%) (°C) 27 April 09:00–9:30 h 3 Hunting 90.3 23.1 15 June 09:40 h 1 Sleeping 90.7 23.9 7 July 14:40–15:45 h 6 Sleeping 74.2 27.7 20 July 09:05 h 1 Sleeping 88.6 22.8 18 September 14:20–15:15 h 4 Sleeping 56.5 33.1 17 October 17:35 h 1 Sleeping 82.0 29.0 8 November 17:20 h 1 Sleeping 89.7 25.8 vegetation during the entire year at the study area, peaking that the assessed B. b. smaragdinus population migrates during the dry season, although with lower uniformity vertically and seasonally throughout the year, perhaps in and diversity compared to the rainy season (Miranda et correlation with the availability of Osteocephalus prey. al., 2015). In addition, amphibian species belonging to the Regardless of the abundance of frogs in the lower forest genus Osteocephalus, recorded as the stomach content of strata (i.e., < 2 m in height above ground), the third most B. b. smaragdinus (Dixon and Soini, 1986), were more abundant species was Rhinella margaritifera, which abundant during the dry season, and the B. b. smaragdinus presents diurnal activity on litter and uses the vegetation as frequency was correlated with Osteocephalus encounters a resting spot, remaining still (Miranda et al., 2015). Thus, throughout the year. The two frog species belonging to this amphibian is not expected to be part (or an important this genus were most frequently observed at heights in the trees above 3.5 m and up to 12 m (Miranda et al., 2015), and they are known to be common canopy inhabitants Figure 3. (A) Range of documented heights at which (Doan, 2004; Guayasamin et al., 2006). Bothrops bilineatus smaragdinus were observed during The increased encounter rate with these amphibians nocturnal hunting activity (n = 63). (B) Residence time of B. during the driest months is likely due to decreased b. smaragdinus in the same location during consecutive days canopy humidity during this period in tropical (n = 56). forests (Freiberg, 1997; Madigosky and Vatnick, 2000; Madigosky, 2004). As a consequence of the dry conditions higher in the canopy, these species descend to lower strata and become detectable during visual searches (Doan, 2004). Low humidity is also an important factor that can influence the activity of some snake species (Lillywhite and Henderson, 1993; Daltry et al., 1998; Moore and Gillingham, 2006; Subach et al., 2009). In the present study, this relationship seems to be indirect, through prey availability (here: Osteocephalus treefrogs), since no correlation between B. b. smaragdinus frequency and humidity levels was observed. Frogs and squamate reptiles represent two canopy ecology extremes, as the former are generally intolerant of desiccation while the latter are tolerant (Shaw, 2004). In addition, snake prey location and distribution are significant factors in the evolution of snake habitat selection (Reinert, 1993). Thus, spatial and temporal prey availability may be determinant for the occurrence of certain snake species (e.g., Chandler and Tolson, 1990; Lillywhite and Henderson, 1993; Bernarde et al., 2000; Madsen et al., 2006). It is likely 574 Wirven Lima da Fonseca et al. portion) of the B. b. smaragdinus diet, since these snakes rodent. All observations of this species in the LMRF preferably hunt more active prey (Turci et al., 2009; indicate strict arboreality while hunting (Turci et al., Fonseca et al., 2019a; Venegas et al., 2019). Most frogs in 2009; Fonseca et al., 2019a), and it may hunt near the study area that use vegetation occur at heights < 2.1 m ground level only rarely or opportunistically. Although (Miranda et al., 2015), whereas B. b. smaragdinus usually competition and predation may have an effect on this B. hunts in higher strata. This reinforces the hypothesis of b. smaragdinus population, prey availability and habitat lower prey availability during the rainy season. However, structure are considered to be among the most important other factors, such as competition or predation, should factors that influence seasonal snake movements (e.g., also be considered as potential determinants for B. b. Reinert, 1993; Gregory et al., 2001; Heard et al., 2004; smaragdinus habitat selection. Hirai, 2004). During the rainy season, with the resulting Another hypothesis may explain the low frequency higher humidity, large areas of this forest become of B. b. smaragdinus in lower strata during the rainy flooded, and Osteocephalus encounters probably season, which is the snakes’ attempt to minimize decrease due to vertical migration towards upper strata competition vertically. Another viperid, B. atrox, is also (e.g., Doan, 2004; Guayasamin et al., 2006). Thus, the present in this forest, and it is the second-most abundant most plausible hypothesis is that B. b. smaragdinus is snake species (Silva et al., 2020). This generalist snake more active in the upper strata during the rainy season may be a potential B. b. smaragdinus competitor, since compared to the dry season, which reduces the potential it is mostly active during the rainy season (Oliveira for detection by active search methods from the ground. and Martins, 2001; Turci et al., 2009), feeds on prey As reported by Turci et al. (2009) and Fonseca et al. in common with B. b. smaragdinus (frogs including (2019a), B. b. smaragdinus is preferably a nocturnal Osteocephalus, small lizards, small mammals), and snake that applies an ambush strategy to hunt and often hunts on the vegetation at heights of up to 1.5 m uses caudal luring to decoy prey. The use of their tail (Martins and Oliveira, 1998; Bisneto and Kaefer, 2019). as bait is paramount for snakes that feed on active prey Furthermore, B. atrox is also ophiophagous, including (Fonseca et al., 2019a). For Osteocephalus, which is cannibalism (Martins and Oliveira, 1998; Bernarde and a nocturnal treefrog group that commonly jumps onto Abe, 2010; Rodrigues et al., 2016; Bisneto and Kaefer, several types of substrate (trunks, branches, leaves, 2019), and it is abundant during the rainy season in this palm leaves, vines, bushes) at different heights (Miranda forest (Turci et al., 2009). Thus, it may also represent a et al., 2015), this tactic may be efficient in the three- potential B. b. smaragdinus predator. Compared to B. dimensional environment where B. b. smaragdinus b. smaragdinus, B. atrox reaches a larger size (over 1.5 generally occurs (Fonseca et al., 2019a). However, these m; Martins and Oliveira, 1998; Oliveira and Martins, snakes were observed active up to nearly 20 m in height 2001). In addition, B. atrox juveniles were observed at above ground level, higher than previously recorded a height of 1.5 m, and two adults were seen during this (2 m: Duellman, 1978; 7 m: Turci et al., 2009; 18 m: study hunting at heights of 2.5 and 4.2 m during the rainy Fonseca et al., 2019a). In the Neotropics, most arboreal season, which reinforces the potential predator status of snake species are active below 5 m in height, and mostly B. atrox on B. b. smaragdinus. Despite the record of a near ground level (e.g., Lillywhite and Henderson, pitviper (Porthidium lansbergii) as a prey of B. asper 1993; Martins and Oliveira, 1998). Our observations are (Roldan et al., 2011), a species belonging to the B. atrox among the highest records for Amazonian snake species, species group, no records of B. atrox preying on other and they are the highest recorded for B. b. smaragdinus. viperid species are available, suggesting that further Bothrops b. smaragdinus used the same substrate to studies are required in this regard. Prey availability rest during the day and remained in the same place for may determine the mobility range of arboreal snakes, up to 17 days. Its cryptic colouring (green) and its low and competition and/or other factors may lead to dietary mobility probably contribute to avoiding or minimizing changes or to optional terrestrially of strictly arboreal predation pressure, especially by visually-oriented species (Lillywhite and Henderson, 1993). diurnal predators, such as birds of prey, which are among One adult B. b. smaragdinus specimen was observed the main Neotropical forest predators (Lillywhite and hunting at only 0.3 m from the ground during the Henderson, 1993; Martins et al., 2008). Furthermore, rainy season. Turci et al. (2009) also observed an adult the use of vegetation for hunting and resting may female in the same situation in the rainy season and, contribute to reduce the risk of predation by terrestrial when assessing the snake’s stomach content, found a predators (e.g., Martins, 1993). Habitat Use and Activity of Bothrops bilineatus smaragdinus 575

Juveniles and adults of the same species can use References substrate in different ways (e.g., Reinert, 1993; Oliveira Acre (2010): Guia para o Uso da Terra Acreana com Sabedoria: and Martins, 2001; Shine et al., 2002; Wilson et al., Resumo Educativo do Zoneamento Ecológico-Econômico do 2007), which may be associated with morphology Acre: Fase II (Escala 1:250.000). Rio Branco, Brazil, Secretaria (body size or colour), prey availability, and predation. de Estado de Meio Ambiente do Acre. We recorded four juveniles (TL < 30 cm) hunting Almeida-Santos, S.M., Salomão, M.G. (2002): Reproduction in by ambush on tree leaves. On the other hand, large neotropical pitvipers, with emphasis on species of the genus Bothrops. In: Biology of the Vipers, p. 445–462. Schuett, amphibians (e.g., Osteocephalus) were not observed G.W., Hoggren, M., Douglas, M.E., Greene, H.W., Eds., Eagle on small leaves (Miranda et al., 2015), which cannot Mountain, Utah, USA, Eagle Mountain Publishing. support their weight. However, juvenile Osteocephalus, Andrade, D.V., Marques, O.A.V., Gavira, R.S.B., Barbo, F.E., small hylids, and Pristimantis species were observed Zacariotti, R.L., Sazima, I. (2010): Tail luring by the golden on smaller leaves (Miranda et al., 2015), and these lancehead (Bothrops insularis), an island endemic snake from represent suitable prey for B. b. smaragdinus juveniles. south-eastern Brazil. South American Journal of Herpetology 5: Adult B. b. smaragdinus were mostly recorded hunting 175–180. Avila-Pires, T.C.S., Vitt, L.J., Sartorius, S.S., Zani, P.A. (2009): on tree branches, but not on leaves (Turci et al., 2009; Squamata (Reptilia) from four sites in southern Amazonia, with Fonseca et al., 2019a; this study). This probably reflects a biogeographic analysis of Amazonian lizards. Boletim do individual body size and weight, which prevents larger Museu Paraense Emílio Goeldi, Ciências Naturais 4: 99–118. individuals access to certain microhabitats, which Bernarde, P.S., Abe, A.S. (2006): A snake community at Espigão therefore become inaccessible to adults (e.g., Plummer, do Oeste, Rondônia, southwestern Amazon, Brazil. South 1981; Henderson, 1993; Shine et al., 2002). American Journal of Herpetology 1: 102–113. Bernarde, P.S., Abe, A.S. (2010): Hábitos alimentares de serpentes em Espigão do Oeste, Rondônia, Brasil. Biota Neotropica 10: Conclusions 167–173. Although B. atrox is usually the most abundant viperid Bernarde, P.S., Kokubum, M.N.C., Marques, O.A.V. (2000): in Amazon forests, B. b. smaragdinus may be the most Atividade e uso de habitat em Thamnodynastes strigatus frequent snake species in certain environments (such as (Günther, 1858), no sul do Brasil (Serpentes, Colubridae). Boletim do Museu Nacional do Rio de Janeiro 428: 1–8. floodplain forest) during visual night searches. Bothrops Bernarde, P.S., Costa, H.C., Machado, R.A., São Pedro, V.A. b. smaragdinus generally hunts by ambushing its prey in (2011a): Bothriopsis bilineata bilineata (Wied, 1821) the forest canopy up to nearly 20 m above ground, and (Serpentes: Viperidae): new records in the states of Amazonas, it uses caudal luring as its main behavioural strategy to Mato Grosso and Rondônia, northern Brazil. Check List 7: attract prey. In a reflection of body size and the availability 343–347. of suitably-sized prey, adult B. b. smaragdinus preferably Bernarde, P.S., Machado, R.A., Turci, L.C.B. (2011b): Herpetofauna use branches to hunt, whereas juveniles prefer leaves. da área do Igarapé Esperança na Reserva Extrativista Riozinho da Liberdade, Acre – Brasil. Biota Neotropica 11: 117–144. Bothrops b. smaragdinus was more frequently Bernarde, P.S., Albuquerque, S., Miranda, D.B., Turci, L.C.B. observed during the driest period, when canopy humidity (2013): Herpetofauna da floresta do baixo rio Moa em Cruzeiro is reduced and potential frog prey (including treefrogs of do Sul, Acre – Brasil. Biota Neotropica 13: 220–244. the genus Osteocephalus) migrates vertically towards Bisneto, P.F., Kaefer, I.L. (2019): Reproductive and feeding the lower stratum. Conversely, during the rainy season biology of the common lancehead Bothrops atrox (Serpentes, when flooding in the study area increased local relative Viperidae) from central and southwestern Brazilian Amazonia. humidity, B. b. smaragdinus activity may shift to the Acta Amazonica 49: 105–113. Campbell, H.W., Christman, S.P. (1982): Field techniques upper forest strata, where prey availability is higher, and for herpetofaunal community analysis. In: Herpetological which makes the detection of these snakes more difficult Communities: a Symposium of the Society for the Study of during visual night searches. Amphibians and Reptiles and the Herpetologist’s League, p. 193–200. Scott, N.J., Jr., Ed., Washington, D.C., USA, United Acknowledgements. The authors would like to thank the States Fish and Wildlife Service. Coordination of Superior Level Staff Improvement (CAPES) – Campbell, J.A., Lamar, W.W. (2004): The Venomous Reptiles Financial Code 001, the Brazilian National Council for Scientific of the Western Hemisphere. Ithaca, New York, USA, Cornell and the Technological Development (CNPq) for financial support University Press. (PIBIC/UFAC), to authors RRC and ASO, and the Instituto Chico Chandler, C.R., Tolson, P.J. (1990): Habitat use by a boid snake, Mendes de Conservação da Biodiversidade (ICMBio) for the Epicrates monensis, and its anoline prey, Anolis cristatellus. license permit (SISBIO/12.178). Journal of Herpetology 24: 151–157. 576 Wirven Lima da Fonseca et al.

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(2004): Physical transport, heterogeneity, Natural history of Bothrops itapetiningae Boulenger, 1907 and interactions involving canopy anoles. In: Forest Canopies, (Serpentes: Viperidae: Crotalinae), an endemic species of the p. 270–296. Lowman, M.D. Rinker, H.B., Eds., New York, Brazilian Cerrado. Journal of Herpetology 48: 324–331. USA, Elsevier. Lillywhite, H.B., Henderson, R.W. (1993): Behavioral and Dixon, J.R., Soini, P. (1986): The Reptiles of the Upper Amazon functional ecology of arboreal snakes. In: Snakes: Ecology and Basin, Iquitos Region, Peru, Second Edition. Milwaukee, Behavior, p. 1–48. Seigel, R.A., Collins, J.T., Eds., New York, Wisconsin, USA, Milwaukee Public Museum. USA, McGraw-Hill. Doan, T.M. (2004): Extreme weather events and the vertical Madigosky, S.R. (2004): Tropical microclimate considerations. In: microhabitat of rain forest anurans. Journal of Herpetology 38: Forest Canopies, p. 24–48. Lowman, M.D., Rinker, H.B. Eds., 422–425. New York, USA, Elsevier. Duellman, W.E. (1978): The biology of an equatorial herpetofauna Madigosky, S.R., Vatnick, I. (2000): Microclimatic characteristics in Amazonian Ecuador. Miscellaneous Publications, Museum of of a primary tropical Amazonian rain forest, ACEER, Iquitos, Natural History, University of Kansas 65: 1–352. Peru. Selbyana 21: 165–172. Fonseca, W.L. da, Correa, R.R., Oliveira, A.S., Bernarde, P.S. Madsen, T., Ujvari, B., Shine, R., Olsson, M. (2006): Rain, rats and (2019a): Caudal luring in the neotropical two-striped forest pythons: climate-driven populations dynamics of predators and pitviper Bothrops bilineatus smaragdinus Hoge, 1966 in the prey in tropical Australia. Austral Ecology 31: 30–37. Western Amazon. Herpetology Notes 12: 365–374. Marques, O.A.V., Martins, M., Develey, P.F., Macarrão, A., Sazima, Fonseca, W.L. da, Silva, J.D., Abegg, A.D., Rosa, C.M., Bernarde, I. (2012): The golden lancehead Bothrops insularis (Serpentes: P.S. 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(2006): A new species of frog of the Miranda, D.B., Albuquerque, S., Turci, L.C.B., Bernarde, P.S. Eleutherodactylus lacrimosus assemblage (Leptodactylidae) (2015): Richness, breeding environments and calling activity from the western Amazon Basin, with comments on the utility of of the anurofauna of the lower Moa river forest, state of Acre, canopy surveys in lowland rainforest. Herpetologica 62: 191–202. Brazil. Zoologia 32: 93–108. Haad, J.S. (1980/81): Accidentes humanos por las serpientes de los Moore, J.A., Gillingham, J.C. (2006): Spatial ecology and multi- gêneros Bothrops y Lachesis. Memórias do Instituto Butantan scale habitat selection by a threatened rattlesnake: the Eastern 44/45: 403–423. Massasauga (Sistrurus catenatus catenatus). Copeia 2006: Heard, G.W., Black, D., Robertson, P. (2004): Habitat use by the 742–751. inland carpet python (Morelia spilota metcalfei: Pythonidae): Mota-da-Silva, A., Sachett, J., Monteiro, W.M., Bernarde, P.S. seasonal relationships with habitat structure and prey distribution (2019): Extractivism of palm tree fruits: a risky activity because of in a rural landscape. Austral Ecology 29: 446–460. snakebites in the state of Acre, Western Brazilian Amazon. Revista Henderson, R.W. (1993): Foraging and diet in West Indian Corallus da Sociedade Brasileira de Medicina Tropical 52: e20180195. enhydris (Serpentes: Boidae). Journal of Herpetology 27: 24–28. Nogueira, C., Sawaya, R.J., Martins, M. (2003): Ecology of the Hirai, T. (2004): Dietary shifts of frog eating snakes in response pitviper, Bothrops moojeni, in the Brazilian Cerrado. Journal of to seasonal changes in prey availability. Journal of Herpetology Herpetology 37: 653–659. Habitat Use and Activity of Bothrops bilineatus smaragdinus 577

Oliveira, M.E., Martins, M. (2001): When and where to find a Wilson, D., Heinsohn, R., Endler, J.A. (2007): The adaptative pitviper: activity patterns and habitat use of the lancehead, significance of ontogenetic colour change in a tropical python. Bothrops atrox, in central Amazonia, Brazil. Herpetological Biology Letters 3: 40–43. Natural History 8: 101–110. Plummer, M.V. (1981): Habitat utilization, diet and movements of a temperate arboreal snake (Opheodrys aestivus). Journal of Herpetology 15: 425–432. Reinert, H.K. (1993): Habitat selection in snakes. In: Snakes: Ecology and Behavior, p. 201–240. Seigel, R.A., Collins, J.T., Eds., New York, USA, McGraw-Hill. Ribeiro, A.G. (1977): O clima do Estado do Acre. Boletim Geográfico 35: 112–141. Rodrigues, G.M., Maschio, G.F., Prudente, A.L. (2016): Snake assemblages of Marajó Island, Pará State, Brazil. Zoologia 33: 1–13. Roldan, J.S., Lucero, M.F. (2011): A prey item not previously recorded for Bothrops asper: a case of ophiophagy involving two sympatric pit viper species. Herpetotropicos 5: 107–109. Sazima, I. (1988): Um estudo da biologia comportamental da jararaca, Bothrops jararaca, com uso de marcas naturais. Memórias do Instituto Butantan 50: 83–99. Shaw, D.C. (2004): Vertical organization of canopy biota. In: Forest Canopies, p. 73–101. Lowman, M.D., Rinker, H.B., Eds., New York, USA, Elsevier. Shine, R., Sun, L., Kearney, M., Fitzgerald, M. (2002): Why do juvenile Chinese pit-vipers (Gloydius shedaoensis) select arboreal ambush sites? Ethology 108: 897–910. Silva, F.M., Oliveira, L.S., Nascimento, L.R.S., Machado, F.A., Prudente, A.L.C. (2017): Sexual dimorphism and ontogenetic changes of Amazonian pit vipers (Bothrops atrox). Zoologischer Anzeiger 271: 15–24. Silva, J.L., Fonseca, W.L., Mota-da-Silva, A., Amaral, G.L.G., Ortega, G.P., Oliveira, A.S., et al. (2020): Venomous snakes and people in a floodplain forest in the Western Brazilian Amazon: potential risks for snakebites. Toxicon 187: 232–244. Smalligan, R., Cole, J., Brito, N., Laing, G.D., Mertz, B.L., Manock, S., et al. (2004): Crotaline snake bite in the Ecuadorian Amazon: randomised double blind comparative trial of three South American polyspecific antivenoms. British Medical Journal 329: 1129–1133. Subach, A., Scharf, I., Ovadia, O. (2009): Foraging behavior and predation success of the sand viper (Cerastes vipera). Canadian Journal of Zoology 87: 520–528. Turci, L.C.B., Albuquerque, S., Bernarde, P.S., Miranda, D.B. (2009): Uso do hábitat, atividade e comportamento de Bothriopsis bilineatus e de Bothrops atrox (Serpentes: Viperidae) na floresta do Rio Moa, Acre, Brasil. Biota Neotropica 9: 197–206. Uetz, P., Freed, P., Hošek, J. (2020): The Reptile Database. Available at: http://www.reptile-database.org. Accessed on 29 April 2020. Venegas, P.J., Chávez-Arribasplata, J.C., Almora, E., Grilli, P., Duran, V. (2019): New observations on diet of the South American two-striped forest-pitviper Bothrops bilineatus smaragdinus (Hoge, 1966). Cuadernos de Herpetologia 33: 29–31. Wasko, D.K., Sasa, M. (2012): Food resources influence spatial ecology, habitat selection, and foraging behavior in an ambush- hunting snake (Viperidae: Bothrops asper): an experimental study. Zoology 115: 179–187. 578 Wirven Lima da Fonseca et al.

Appendix I. Vegetation use by Bothrops bilineatus smaragdinus recorded during nocturnal limited visual searches in the Lower Moa River Forest, Cruzeiro do Sul Municipality, Acre State, Brazil in 2018. The use of a palm leaf, as opposed to a large leaf of a regular tree, is indicated by the substrate term “Palm.” Instances of caudal luring are indicated by an asterisk (*). Tree trunk size is indicated as diameter at breast height (DBH).

Branch Time Height DBH Individual Date Trail Substrate Diameter Activity (h) (m) (cm) (mm) I 4 April 19:50 1.4 2 Branch 1.9 6.2 Moving II 4 April 20:18 10.0 2 Branch 7.9 7.1 Hunting III 4 April 21:45 8.6 2 Branch 7.5 10.6 Hunting* IV 19 April 21:32 4.5 3 Branch 5.5 9.5 Hunting* V 19 April 22:02 8.5 3 Branch 12 7.1 Hunting VI 25 April 18:15 1.3 1 Branch 2.9 8.4 Hunting* VI 26 April 18:15 1.3 1 Branch 2.9 8.4 Hunting VII 26 April 18:50 2.5 1 Branch 5.5 9.1 Moving VIII 26 April 19:20 0.3 1 Palm - 8.2 Hunting* IX 26 April 21:23 6.7 1 Branch 5.6 9.2 Hunting* X 18 May 19:10 10.6 1 Branch 7.4 8.9 Hunting* XI 14 June 18:00 3.3 1 Palm 4.2 12.0 Moving XII 14 June 18:00 18.0 1 Branch 39.4 - Hunting* XIII 14 June 18:15 4.8 1 Leaf 17.6 7.4 Hunting* VII 14 June 19:00 6.8 1 Branch 10.8 6.9 Hunting* XIV 28 June 20:24 0.8 2 Branch 2.3 7.0 Hunting* XV 1 July 19:50 5.7 2 Branch 11.3 5.2 Hunting* XIII 4 July 18:20 2.0 1 Branch 7.1 7.8 Moving VII 4 July 19:00 2.3 1 Branch 8.9 9.9 Hunting* XVI 4 July 20:45 7.0 1 Branch 15.4 - Moving XVII 4 July 20:50 6.7 1 Branch 13.6 8.8 Hunting* XVIII 4 July 20:46 2.6 1 Branch 11.1 9.7 Hunting VII 5 July 18:40 2.3 1 Branch 8.9 9.9 Hunting* XVI 5 July 20:30 6.5 1 Branch 11.6 - Moving XVIII 5 July 20:45 2.6 1 Branch 11.1 9.7 Hunting IX 5 July 20:50 11.4 1 Branch 17.1 - Hunting* XVII 5 July 20:50 6.7 1 Branch 13.6 8.8 Hunting* XIX 6 July 18:31 7.3 1 Branch 31.7 - Hunting* VII 6 July 18:50 2.3 1 Branch 8.9 9.9 Hunting* XVI 6 July 20:30 8.9 1 Branch 11.5 - Hunting* XVII 6 July 20:50 6.7 1 Branch 13.6 8.8 Hunting* XVIII 6 July 20:45 2.6 1 Branch 11.1 9.7 Hunting* IX 6 July 20:53 11.4 1 Branch 17.1 - Hunting* XX 8 July 19:26 6.7 2 Branch 6.8 - Hunting* XIII 22 August 18:15 5.9 1 Leaf 10.3 - Hunting* XIX 22 August 18:40 7.3 1 Branch 14.2 - Hunting* XVIII 22 August 20:40 8.3 1 Branch 16.3 - Hunting*

Habitat Use and Activity of Bothrops bilineatus smaragdinus 579

Appendix I. cont.

Branch Time Height DBH Individual Date Trail Substrate Diameter Activity (h) (m) (cm) (mm) XXI 24 August 20:15 4.2 2 Branch 5.5 7.8 Hunting XXII 24 August 21:23 3.2 2 Branch 5.8 6.9 Hunting XXIII 24 August 21:40 3.9 2 Branch 7.7 11.2 Moving XIII 27 August 18:15 5.9 1 Leaf 10.3 - Hunting* XIX 27 August 18:30 13.5 1 Branch 45.1 - Hunting XVIII 27 August 20:40 8.3 1 Branch 16.3 - Hunting XIX 28 August 18:32 9.3 1 Branch 23.2 - Hunting* XXIV 28 August 20:02 3.5 1 Branch 2.3 6.8 Moving XVIII 28 August 20:30 8.3 1 Branch 16.3 - Hunting XXV 29 August 18:15 7.5 3 Branch 6.7 - Hunting XXVI 29 August 21:43 10.5 2 Branch 13.2 - Hunting XI 12 September 18:10 1.4 1 Branch 9.4 8.7 Moving XXIV 12 September 19:31 1.7 1 Branch 3.1 9.6 Hunting XVI 12 September 20:35 1.8 1 Branch 9.3 10.4 Hunting* XVII 12 September 20:55 3.4 1 Branch 10.9 12.1 Hunting* XI 17 September 18:08 13.3 1 Branch 42 - Hunting* XXVII 17 September 18:40 4.0 1 Branch 11.2 8.1 Moving XXVIII 17 September 19:09 2.4 1 Branch 7.7 6.7 Moving XXIV 17 September 19:45 4.8 1 Branch 4.4 - Hunting XVI 17 September 20:30 1.8 1 Branch 9.3 10.4 Hunting XVII 17 September 20:50 4.2 1 Branch 9.9 12.3 Hunting XIX 20 September 19:07 5.9 1 Branch 12.3 - Hunting XVI 20 September 20:30 1.8 1 Branch 9.3 10.4 Hunting IX 20 September 20:55 4.8 1 Branch 9.2 - Hunting XXIX 24 September 20:28 5.5 2 Branch 12.3 - Hunting XXX 24 September 20:45 8.2 2 Branch 15.5 - Hunting* XXXI 24 September 21:05 2.5 3 Branch 11.4 5.2 Hunting XXXII 25 September 20:24 2.4 2 Branch 5.4 6.2 Hunting XI 1 October 18:15 14.1 1 Branch 8.4 - Hunting XIII 1 October 18:20 4.5 1 Leaf 14.5 - Hunting XIX 1 October 18:30 1.6 1 Branch 4.3 7.6 Hunting* XI 9 October 18:15 12.4 1 Branch 23.5 - Moving XI 15 October 18:15 14.2 1 Branch 14.8 - Hunting* XIX 15 October 18:35 12.4 1 Branch 16.8 - Hunting XVI 15 October 18:35 1.8 1 Branch 12.6 12.2 Hunting* XXXIII 17 October 21:30 3.5 2 Branch 6.8 6.7 Hunting* XII 2 November 18:10 19.9 1 Branch 31.1 - Moving XXXIV 6 November 18:30 2.3 1 Leaf 3.7 6.2 Hunting* XXXV 12 November 21:00 3.3 1 Leaf 4.3 6.4 Hunting*

580 Wirven Lima da Fonseca et al.

Appendix II. Numbers of frogs observed along trails in the Lower Moa River Forest, Brazil, during our surveys from April 2018–March 2019.

2018 2019 Taxon Total A M J J A S O N D J F M

Bufonidae Rhinella margaritifera 2 24 12 12 6 3 29 44 29 72 16 35 284

Craugastoridae Pristimantis fenestratus 1 1 Pristimantis ockendeni 1 1 Pristimantis reichlei 1 1 1 1 1 1 6 Pristimantis sp. 1 1 2

Hylidae Boana calcarata 2 2 8 2 14 Boana cinerascens 1 2 1 1 3 8 Boana fasciata 1 3 1 1 2 8 Boana geographica 3 3 8 2 16 Boana lanciformis 1 1 Boana punctata 1 1 Dendropsophus brevifrons 2 2 Dendropsophus marmoratus 1 1 Dendropsophus parviceps 2 8 10 Dendropsophus sp. 2 1 3 5 11 Osteocephalus leprieurii 38 17 18 13 27 33 34 20 8 10 6 10 234 Osteocephalus taurinus 2 9 14 16 23 13 22 32 12 16 5 6 170 Scinax ruber 1 2 2 5 Sphaenorhynchus dorisae 1 1 Trachycephalus typhonius 1 1

Phyllomedusidae Cruziohyla craspedopus 1 1 Phyllomedusa bicolor 4 5 6 2 1 3 1 2 24 Phyllomedusa vaillantii 1 1 Total 48 56 56 46 62 54 97 104 58 119 34 69 803

Accepted by Mirco Solé