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Home , Allobates marchesianus, Alopoglossus angulatus, Alopoglossus atriventris, Ameerega hahneli, Anolis bombiceps, Arthrosaura reticulata

Herpetology Notes, volume 13: 753-767 (2020) (published online on 21 September 2020)

Herpetofauna of the Santa Cruz Reserve in the Peruvian

Matthew F. Metcalf1,*, Alexander Marsh1, Emerson Torres Pacaya2, Devon Graham2, and Charles W. Gunnels IV1

Abstract. The Amazon is the largest rainforest on the planet and is known for its despite growing deforestation from agricultural development, urbanisation, wildfires, and unregulated mining. It is increasingly important to better understand regionalised biodiversity through fauna inventories because of these anthropogenic pressures. We conducted this study between May 2019 and August 2019 to identify herpetofauna biodiversity at the Santa Cruz Forest Reserve in Loreto, . During the study period, we recorded and via visual encounter surveys and opportunistic encounters. We further supplemented these sightings by secondary data compiled from previous observations. In total, we recorded 200 of herpetofauna at this reserve: 15 families of comprising 106 species, and 21 families of reptiles comprising 94 species. The visual encounter surveys adequately sampled the diversity of amphibians that would have been expected given this protocol and the timeframe of the study. In contrast, this procedure did not sample reptiles as well in terms of both species richness and diversity; more species would be expected given additional sampling. The combined approach of this study, however, provided a robust inventory of the Santa Cruz Forest Reserve, which can be used to support future on-site studies and management plans throughout the region.

Keywords. Amphibians, Reptiles, Amazon, Peru, Inventory, Reserve

Introduction cattle ranching (Veiga et al., 2002) are major ecological concerns. These industries require large swaths of The Amazon Basin is one of the most complex and disturbed landscapes, which negatively affects wildlife biodiverse regions on the planet (Kauffmann-Zeh, 1999; populations and, therefore, the existence of species and Myers et al., 2000). The extent of this biodiversity is so whole communities that live in the basin (Barlow et pronounced that new species across different taxonomic al., 2016). For example, oil palm plantations fragment groups are discovered each year within the basin (e.g., , which support less diverse communities of ferns: Cárdenas et al., 2016; insects: Perry et al., 2016; wildlife and contribute to polluted waterways (Vijay et fish: Oberdorff et al., 2019). Much of this biodiversity is al., 2016). To mitigate these effects, conservation areas imperiled, however, because of anthropogenic activities such as national and ecological stations must (Barlow et al., 2016). Deforestation and degradation as a result of increased mining and oil drilling be established and maintained throughout the Amazon (Finer et al., 2008; Espejo et al., 2018), agricultural because of the extensive endemism that occurs across practices (Glinskis and Gutiérrez-Vélez, 2019), and different areas of the basin (da Silva et al., 2005; Peres, 2005; Freitas et al., 2017). In order to best conserve this rich biodiversity through the further establishment of conservation priorities, we must first understand community compositions within the different regions that make up the Amazon Basin. Amphibians and reptiles make up a significant 1 Department of Biological Sciences, Florida Gulf Coast proportion of tetrapods in the Amazon and are, University, 10501 FGCU Blvd S., Fort Myers, Florida therefore, of significant conservation interest, although 33965, USA. 2 Project Amazonas, 701 E. Commercial Blvd, #200, Fort their presence can be obscured by their small size and/or Lauderdale, Florida 33334, USA. cryptic behavioural patterns. Data on the biogeography, * Corresponding author. E-mail: [email protected] conservation status, and general life history of many 754 Matthew F. Metcalf et al.

Amazonian herpetofauna are severely lacking, despite 2019). In addition, the Peruvian Amazon is expected to the fact that amphibians and reptiles are key indicators have among the world’s most diverse species richness of of environmental disruptions (Stuart et al., 2004). amphibian and reptile communities (Vasconcelos et al., For example, these taxa have highlighted the effect 2012; Roll et al., 2017). This is also a rapidly developing of globally infectious diseases such as chytrid fungus area. For example, the human population in the province (Skerratt et al., 2007; Russell et al., 2019) and the of Loreto has grown by 28.6% from 1993 to 2017 and direct biodiversity loss in (Scheele et al., 2019), the urban core of Iquitos, an otherwise isolated city in as well as the indirect biodiversity collapse in tropical the eastern Peruvian Amazon, has grown by 26.4% from (Zipkin et al., 2020). As industrialisation and 2000 to 2015 (INEI, 2020). To add to a growing list of agricultural activities advance throughout the Amazon, herpetofaunal inventories throughout Loreto (see Table reductions and complete losses of amphibian and 1), this study describes the composition of herpetofauna reptile populations are expected (Nobre et al., 2016). in the Santa Cruz Forest Reserve in Loreto, Peru. These Consequently, biodiversity inventories are crucial valuable insights into amphibian and reptile community to evaluate conservation status of herpetofauna structures will provide baseline data for future studies, as communities (Oliveira et al., 2017; Shaney et al., 2017), well as detail the ecological and geographic importance identify regional endemism and new species (da Silva of the Santa Cruz Forest Reserve. et al., 2005; Treurnicht et al., 2017; de Oliveira et al., 2020), and develop proactive conservation management Materials and Methods strategies that mitigate the most destructive effects of Study site.—The Santa Cruz Forest Reserve deforestation (Groves et al., 2002; Guralnick et al., (-3.5214ºS, -73.1803ºW; 115.82 m a.s.l.) is owned 2018). Herpetofauna surveys in the Amazon Basin are and operated by Project Amazonas, which purchased critical to create community baseline structures to assist the first parcel in 2008 (Fig. 1). Additional plots of future research and identify conservation management primary and secondary forest and agricultural lands priorities (Fonseca et al., 2019). were gradually incorporated to create 232 hectares The Peruvian Amazon is one of the most biologically of contiguous protected area. The reserve is located diverse regions within Amazonia (Rodríguez and approximately 22 km northeast of the city of Iquitos. Knell, 2004; Finer et al., 2008). Peru has among the Bordering the reserve is an agricultural property used for highest number of newly discovered amphibian species cattle ranching and yuca (cassava) and plantain farming. globally (Catenazzi and Bustamante, 2007; Wake and There are also three adjacent community reserves which Vredenburg, 2008; Lehr et al., 2017; Santa-Cruz et al., increase the forest continuity outside of the Santa Cruz

Table 1. Herpetofauna observed in selected rapid biological inventories from nearby regions within Loreto, Peru, including observationsTable 1. Herpetofauna from the Santa observed Cruz in Forest selected Reserve. rapid biological inventories from nearby regions within Loreto, Peru, including observations from the Santa Cruz Forest Reserve.

LOCATION Ns An Ca Gy Ch Cr Lz Am Sn SOURCE Ampiyacu, Apayacu, Yaguas, 104 62 1 1 3 3 19 - 15 Rodríguez and Knell (2004) Medio Putumayo Sierra del Divisor 109 67 1 – 2 1 17 – 21 Barbosa de Souza and Rivera (2006) Mastés 109 74 – – 2 2 18 – 13 Gordo et al. (2006) Nanay-Mazán-Arabela 93 53 1 – 2 2 23 – 12 Catenazzi and Bustamante (2007) Cuyabeno-Güeppí 107 59 – – 3 3 22 1 19 Yánez-Muñoz and Venegas (2008) Maijuna 108 63 1 2 1 1 22 – 18 von May and Venegas (2010) Yaguas-Cotuhé 128 73 1 1 4 3 21 – 25 von May and Mueses-Cisneros (2011) Ere-Campuya-Algodón 128 68 – – 4 2 22 1 31 Venegas and Gagliardi-Urrautia (2013) Medio Putumayo-Algodón 142 89 1 – 4 3 20 – 25 Chávez and Mueses-Cisneros (2016) Santa Cruz Forest Reserve 200 102 1 3 3 2 34 1 54 This study

Abbreviations: Ns – number of species; An – Anuran; Ca – Caudata; Gy – Gymnophiona; Ch – Chelonian; Cr – Crocodylian; Lz – ; Am – Amphisbaenian; Sn – . Herpetofauna of the Santa Cruz Forest Reserve in the Peruvian Amazon Basin 755

Forest Reserve boundaries. Much of the reserve is Sampling.—Sampling of herpetofauna occurred primary forest (~60%) and the rest is secondary forest, between May 2019 and August 2019 using visual which is being actively restored through the planting of encounter surveys (VES) along nine different 250- native primary forest vegetation. meter transects throughout the reserve. We conducted VES similarly to methods used by Doan (2003), which did not include time constraints. Observers walked at a reasonable pace but used as much time as necessary to sufficiently sample each transect. VES transects served to sample amphibians and reptiles found on the ground and within the lower canopy. We then conducted transects during multiple time periods to best capture herpetofauna across varying activity patterns. We aggregated diurnal surveys into four time slots: 06:00 – 08:00 h, 08:00 – 10:00 h, 10:00 – 12:00 h, and 12:00 – 14:00 h. Similarly, we conducted nocturnal surveys across four time slots: 18:00 – 20:00 h, 20:00 – 22:00 h, 22:00 – 24:00 h, and 24:00 – 02:00 h. We conducted transects across habitat types found at the reserve and adjacent pasture lands with three replicate sampling transects for each habitat type (primary forest, secondary forest, and pasture lands), resulting in nine unique transects. Over the entire research period, we sampled each transect once per diurnal and nocturnal time slot so that every replicate transect was sampled across all four diurnal and all four nocturnal time slots. Our data include species collected by opportunistic encounters (OE) during the timeframe of this study in 2019. This sampling type represents any species found during the overall stay at Santa Cruz (May to August 2019) but outside of the organised transects. For example, we captured one Drymarchon corais while hiking an unused trail. We recorded this observation as OE because researchers captured the snake outside of a designated VES transect but within the boundaries of the Santa Cruz Forest Reserve during the timeframe of this study. Regardless of sampling method, we attempted to capture all encountered and then photograph the individual to confirm species identification. We safely released all specimens at or near the point of capture. In order to supplement our data, we included secondary data (SD) contributed by Project Amazonas. Secondary data included the observation of herpetofauna species - whether they were visual, through photographs, or voucher specimens - accumulated and vetted by Project Amazonas staff and/or other researchers since acquiring the property in 2008. Figure 1. Top map shows the position of Santa Cruz Forest Reserve relative to Iquitos and surrounding communities Data analysis.—We ran statistical analyses in R (R along the Amazon River Basin in Peru. Bottom map shows the Core Team, 2017) using the vegan package (Oksanen et borders of the Santa Cruz Forest Reserve (outlined in white) al., 2007) to create a species accumulation curve of all with adjacent agricultural pasture (outlined in yellow). amphibians and reptiles found during visual encounter 756 Matthew F. Metcalf et al. surveys. We also extrapolated species richness and diversity for animals sampled during the VES because observed species frequently underestimates real species richness (Hughes et al., 2001). We measured species richness and diversity indices in terms of HILL numbers (Hill, 1973), which provides multiple benefits in context of this study (Chao et al., 2014). HILL numbers show expected doubling property when combining independent species assemblages. In addition, they are defined in terms of expected numbers of species, providing a clear and biologically relevant unit for evaluation and comparison (Chao et al., 2014). We extrapolated estimates of species richness and diversity for the first three HILL numbers based on separate evaluations of all collected amphibian and reptiles using the iNEXT package (Hsieh et al., 2016). We used this approach to estimate species richness, the Shannon diversity index, and the Simpson diversity index, which were represented by q = 0, q = 1, q = 2 respectively.

Results We surveyed herpetofauna throughout the Santa Cruz Forest Reserve from May to August 2019. Over this period, we conducted 72 VES transects, totalling 170.3 person-hours of sampling effort. Nocturnal surveys required more time (x̄ = 65.89 min per 250-m transect) than diurnal surveys (x̄ = 32.69 min per 250-m transect). We recorded additional species opportunistically during the study timeline and from previous records collected by researchers and staff at Santa Crus Forest Reserve since 2008. We found 102 herpetofauna species during the duration of this study. Of the 571 amphibians we sampled across the 72 VES transects, all were anurans except for one caudata (Bolitoglossa altamazonica). By comparison, we observed only 110 reptiles during the same VES transects. All of these reptiles were , except for five snake species. During the VES, we found Bothrops atrox, scurrulus, and cenchoa on one occasion each, and Micrurus surinamensis and compressus on two occasions each. Amphibians found during VES and OE observations accounted for 53% of species (54 species) across 11 families (Fig. 2, Table 2) and reptiles made up 47% of Figure 2. Sample of amphibians found at the Santa Cruz species (48 species) within 17 families (Fig. 3, Table Forest Reserve. (A) dapsilis, (B) Vitreorana 3). For amphibians, we observed 41.5% of species ritae, (C) ventrimaculata, (D) exclusively during VES transects and 24.5% exclusively triangulum, (E) Boana punctata, (F) Osteocephalus mutabor, during opportunistic encounters. Overall, we found (G) Lithodytes lineatus, (H) Chiasmocleis bassleri, (I) 75.5% of amphibian species during VES transects and Phyllomedusa bicolor, (J) Pipa snethlageae. Photos by 56.6% in opportunistic encounters. Reptiles, however, Alexander Marsh. Herpetofauna of the Santa Cruz Forest Reserve in the Peruvian Amazon Basin 757

trended differently. We recorded only one species (Chironius scurrulus; 2%) exclusively in VES transects. During opportunistic encounters, we observed 51% of the reptile species exclusively. Overall, we documented 45% of reptiles across both methods. Secondary data from previous observations added 52 species of amphibians to the Santa Cruz Forest Reserve’s list, which includes one new order (Gymnophiona) and four new families. Secondary data also added 46 reptile species to the list which includes one new order (Amphisbaenia) and three new families. The VES and OE data from this study added 16 new species of amphibians and nine new species of reptiles that had not been recorded in the Santa Cruz Forest Reserve previously. The upward trajectory of the species accumulation curve suggests that the herpetofauna community that could be found during the 72 VES transects was more diverse than the 102 observed species (Fig. 4A). This trend in the species accumulation curve seemed to be a result of reptile sampling. The 72 transects appeared to be deficient in identifying the species richness of reptiles that would be found with VES transects (Fig. 4B). The 110 individually observed reptiles represented 24 species. However, the iNEXT extrapolation of species richness (q = 0) suggests that an additional 13 species would be found (37.4 species ± 26.87–86.34 95% CI) after sampling at least 700 animals. In contrast, visual encounter surveys appeared to be a stronger measure for recording the species richness and diversity of amphibians (Fig. 4B). The iNEXT extrapolation curves suggest that amphibian diversity would approach its asymptote only after the number of collected animals doubled from the 571 amphibians across the 42 species that we found during VES transects. However, this extra sampling would be expected to discover only two additional amphibian species (44.4 species ± 42.46– 55.09 95% CI). Observed measures of amphibian and reptile diversity (Shannon index, q = 1 and Simpson index, q = 2) were closer to the expected asymptotes based on the number of collected animals.

Discussion

Figure 3. Sample of reptiles found at the Santa Cruz Forest Of the 200 species observed at the Santa Cruz Forest Reserve. (A) Paleosuchus trigonatus, (B) Anolis transversalis, Reserve, seven species are listed by the IUCN Red List (C) Copeoglossum nigropunctatum, (D) Plica plica, (E) as either data deficient or vulnerable. Five amphibians Epicrates cenchria, (F) Atractus snethlageae, (G) Siphlophis are listed as data deficient ( conspicuus, compressus, (H) Micrurus suranimensis, (I) Lachesis muta, delius, Ranitomeya amazonica, Ranitomeya (J) Podocnemis unifilis. Photos by Alexander Marsh. variabilis, and Vitreorana ritae) and two reptiles (turtles) listed as vulnerable (Chelonoidis denticulata and 758 Matthew F. Metcalf et al.

Podocnemis unifilis). However, the true conservation status of many of these species remains unclear as most are either unstudied or very poorly studied. In addition, taxonomic determinations remain an ever-evolving and prevalent issue for many Amazonian amphibians and reptiles. As cryptic species continue to be recognised (e.g., Elmer and Cannatella, 2008; Sturaro et al., 2017), it is expected the species richness in this biological hotspot will increase. The VES was the most rigorous methodology used in this study, although this method sampled only those animals that would make use of the ground and/or forest understory. Other microhabitats, such as the mid- and upper-canopy and aquatic environments, could not be sampled with this procedure, which explains why we encountered fewer species with VES than with the opportunistic encounters and secondary data. Given the sampling pressure utilised in this study, VES transects were extremely successful in sampling the amphibian community. However, the reptile community curves suggest more species would be observed with additional sampling. The ability of the VES to sample a relatively complete amphibian community likely reflects that frogs were much more numerous than the entire class of reptiles. The addition of opportunistic encounters and secondary data produced a more robust collection of species found in the reserve, yet these procedures lack Figure 4. Species diversity for amphibians and reptiles found methodological rigor due to varying factors, such as during visual encounter surveys conducted in the Santa Cruz observer expertise and variable sampling intensities. We Forest Reserve. (A) Species accumulation curve (± 95% CI) encourage continued floral and faunal inventories in this for all herpetofauna observed during the consecutive visual area, especially when supplemented by additional and encounter survey transects. (B) Sample interpolation (solid complimentary sampling methods. For example, studies lines) and extrapolation (dashed lines) curves (± 95% CI) have shown micro-environmental characteristics may based on the number of sampled amphibians and reptiles, respectively. Three measures of diversity are illustrated in the influence niche distributions in groups (Menin et al., panels: 0 = Species richness, 1 = Shannon index of biodiversity, 2007) such as Pristimantis (López-Rojas et al., 2015). and 2 = Simpson index of biodiversity. Future studies are planned to incorporate these new methods into identifying a more complete herpetofauna community at this location. As predicted for the Peruvian Amazon (Vasconcelos et habitat corridor between sites. We did, however, al., 2012; Roll et al., 2017), the Santa Cruz Forest Reserve observe very few snakes during VES transects, which showed a high degree of herpetological biodiversity despite its small size. Several rapid biological may be a result of their secretive habits and movement inventories have recently documented herpetofauna patterns in addition to transects being conducted over a communities throughout the Loreto region surrounding short timeframe. Further research should reveal a more the Santa Cruz Forest Reserve (Table 1). This study’s concrete understanding of snake assemblages in this approach detected a comparably high species richness area. in reference to these inventories, despite our study Tropical forests remain at the forefront of biodiversity involving only one location, a significantly smaller study conservation concerns due to increasing anthropogenic area, and lacking multiple capture methods. The Santa threats (de Solar et al., 2016). The rainforests in the Cruz Forest Reserve is centrally located between many western Amazon, and the Peruvian Amazon Basin of these rapid inventories and may serve as an important in particular, represent one of the largest remaining Herpetofauna of the Santa Cruz Forest Reserve in the Peruvian Amazon Basin 759

Table 2. Amphibians recorded at the Santa Cruz Forest Reserve in Loreto, Peru. Record Types: VES = Visual Encounter Survey; OE = Opportunistic Encounter; SD = Secondary Data. IUCN Red List rankings: DD = Data Deficient, LC = Least Concern, NL = Not Listed, VU = Vulnerable. * indicates species only found in adjacent pasture land surveys. Table 2.

SPECIES VES OE SD IUCN ANURA Allobates conspicuus (Morales, 2002) X X X DD Allobates femoralis (Boulenger, 1884) X X X LC Allobates marchesianus (Melin, 1941) X LC Bufonidae Rhaebo glaberrimus (Günther, 1869) X LC Rhaebo guttatus (Schneider, 1799) X LC Rhinella dapsilis (Myers and Carvalho, 1945) X X X LC Rhinella margaritifera (Laurenti, 1768) X X X LC Rhinella marina (Linnaeus, 1758) X X X LC Centrolenidae Vitreorana ritae (Lutz, 1952)* X DD Ceratophryidae Ceratophrys cornuta (Linnaeus, 1758) X LC Niceforonia nigrovittata (Andersson, 1945) X LC Noblella myrmecoides (Lynch, 1976) X LC quixensis Jiménez de la Espada, 1872 X X X LC Pristimantis academicus Lehr et al., 2010 X NL Pristimantis acuminatus (Schreve, 1935) X LC Pristimantis altamazonicus (Barbour and Dunn, 1921) X X LC Pristimantis carvalhoi (Lutz, 1952) X X LC Pristimantis conspicillatus (Günther, 1858) X LC Pristimantis croceoinguinis (Lynch, 1968) X X X LC Pristimantis delius (Duellman and Mendelson, 1995) X DD Pristimantis diadematus (Jiménez de la Espada, 1872) X LC Pristimantis lanthanites (Lynch, 1975) X LC Pristimantis malkini (Lynch, 1980) X LC Pristimantis martiae (Lynch, 1974) X X X LC Pristimantis ockendeni (Boulenger, 1912) X X X LC Pristimantis orcus (Lehr et al. 2009) X LC Pristimantis padiali (Moravec et al., 2010) X LC Pristimantis peruvianus (Melin, 1941) X LC Pristimantis variabilis (Lynch, 1968) X X LC Pristimantis ventrimarmoratus (Boulenger, 1912) X LC Strabomantis sulcatus (Cope, 1874) X X LC Dendrobatidae hahneli (Boulenger, 1884) X X X LC Ameerega trivittata (Spix, 1824) X LC

760 Matthew F. Metcalf et al.

Table 2. Continued. Table 2.

SPECIES VES OE SD IUCN ANURA Ranitomeya amazonica (Schulte, 1999) X DD AromobatidaeRanitomeya ventrimaculata (Shreve, 1935) X X LC RanitomeyaAllobates conspicuus variabilis (Morales, (Zimmermann 2002) and Zimmermann, 1988) X X X DD Hemiphractidae Allobates femoralis (Boulenger, 1884) X X X LC HemiphractusAllobates marchesianus helioi (Sheil (Melin, and Mendelson, 1941) 2001) X X LC BufonidaeHemiphractus proboscideus (Jiménez de la Espada, 1870) X LC Rhaebo glaberrimus (Günther, 1869) X LC BoanaRhaebo boans guttatus (Linnaeus, (Schneider, 1758) 1799) X X LC BoanaRhinella calcarata dapsilis (Troschel(Myers and in Carvalho,Schomburgk, 1945) 1848) X X X LC BoanaRhinella cinerascens margaritifera (Spix, (Laurenti, 1824) 1768) X X X LC BoanaRhinella fasciata marina (Günther, (Linnaeus, 1859) 1758) X X X LC CentrolenidaeBoana geographicus (Spix, 1824) X LC BoanaVitreorana lanciformis ritae (Lutz, (Cope, 1952)* 1871) X X X DDLC CeratophryidaeBoana microderma (Pyburn, 1977) X LC BoanaCeratophrys nympha cornuta (Faivovich (Linnaeus, et al. 2006)1758) X X LC CraugastoridaeBoana punctata (Schneider, 1799) X X LC DendropsophusNiceforonia nigrovittata brevifrons (Andersson, (Duellman 1945) and Crump, 1974) X X LC DendropsophusNoblella myrmecoides koechlini (Lynch, (Duellman 1976) and Trueb, 1989) X LC DendropsophusOreobates quixensis leucophyllatus Jiménez de (Beireis, la Espada, 1783) 1872 X X X LC DendropsophusPristimantis academicus marmoratus Lehr (Laurenti, et al., 2010 1768) X NLLC DendropsophusPristimantis acuminatus minutus (Peters,(Schreve, 1872) 1935) X X LC DendropsophusPristimantis altamazonicus miyatai (Vigle (Barbour and Goberdhan-Vigle, and Dunn, 1921) 1990)* X X LC DendropsophusPristimantis carvalhoi parviceps (Lutz, (Boulenger, 1952) 1882) X X LC DendropsophusPristimantis conspicillatus rhodopeplus (Günther, (Günther, 1858) 1858) X X LC DendropsophusPristimantis croceoinguinis rossalleni (Goin, (Lynch, 1959) 1968) X X X LC DendropsophusPristimantis delius sarayacuensis (Duellman and(Shreve, Mendelson, 1935) 1995) X X DDLC DendropsophusPristimantis diadematus triangulum (Jiménez (Günther, de la 1869)* Espada, 1872) X X X LC NyctimantisPristimantis rugicepslanthanites (Boulenger, (Lynch, 1975) 1882) X LC OsteocephalusPristimantis malkini buckleyi (Lynch, (Boulenger, 1980) 1882) X X LC OsteocephalusPristimantis martiae cabrerai (Lynch, (Cochran 1974) and Goin, 1970) X X X LC OsteocephalusPristimantis ockendeni deridens (Boulenger, (Jungfer et al.,1912) 2000) X X X LC OsteocephalusPristimantis orcus leprieurii (Lehr et(Duméril al. 2009) and Bibron, 1841) X X LC OsteocephalusPristimantis padiali mutabor (Moravec (Jungfer et al.,and 2010)Hödl, 2002) X X LC OsteocephalusPristimantis peruvianus planiceps (Melin, (Cope, 1941)1874) X X X LC OsteocephalusPristimantis variabilis taurinus (Lynch, Steindachner, 1968) 1862 X X X LC OsteocephalusPristimantis ventrimarmoratus yasuni (Ron and (Boulenger, Pramuk, 1999) 1912) X LC ScarthylaStrabomantis goinorum sulcatus (Bokermann, (Cope, 1874) 1962) X X LC DendrobatidaeScinax cruentommus (Duellman, 1972) X LC ScinaxAmeerega funereus hahneli (Cope, (Boulenger, 1874) 1884) X X X LC ScinaxAmeerega garbei trivittata (Miranda-Ribeiro, (Spix, 1824) 1926) X LC ruber (Laurenti, 1768) X LC dorisae (Goin, 1957) X LC

Herpetofauna of the Santa Cruz Forest Reserve in the Peruvian Amazon Basin 761

Table 2. Continued. Table 2.

SPECIES VES OE SD IUCN ANURA Trachycephalus coriaceus (Peters, 1867) X LC AromobatidaeTrachycephalus cunauaru (Gordo et al., 2013) X NL TrachycephalusAllobates conspicuus resinifictrix (Morales, (Goeldi, 2002) 1907) X X X DDLC TrachycephalusAllobates femoralis typhonius (Boulenger, (Linnaeus, 1884) 1758) X X X LC Allobates marchesianus (Melin, 1941) X LC BufonidaeAdenomera andreae (Müller, 1923) X X X LC AdenomeraRhaebo glaberrimus hylaedactyla (Günther, (Cope, 1869) 1868) X X X LC EngystomopsRhaebo guttatus petersi (Schneider, (Jiménez 1799) de la Espada, 1872) X LC HydrolaetareRhinella dapsilis schmidti (Myers (Cochran and Carvalho, and Goin, 1945) 1959)* X X X LC LeptodactylusRhinella margaritifera bolivianus (Laurenti, (Boulenger, 1768) 1898) X X X LC LeptodactylusRhinella marina diedrus (Linnaeus, (Heyer, 1758) 1994) X X X LC CentrolenidaeLeptodactylus discodactylus (Boulenger, 1884) X LC LeptodactylusVitreorana ritae leptodactyloides (Lutz, 1952)* (Andersson, 1945) X X DDLC CeratophryidaeLeptodactylus pentadactylus (Laurenti, 1768) X X LC LeptodactylusCeratophrys cornuta rhodonotus (Linnaeus, (Günther, 1758) 1869) X LC CraugastoridaeLeptodactylus stenodema (Jiménez de la Espada, 1875) X LC LeptodactylusNiceforonia nigrovittata wagneri (Peters, (Andersson, 1862) 1945) X X X LC LithodytesNoblella myrmecoides lineatus (Schneider, (Lynch, 1976)1799) X X X LC PseudopaludicolaOreobates quixensis ceratophyes Jiménez de (Rivero la Espada, and 1872Serna, 1985) X X X LC Pristimantis academicus Lehr et al., 2010 X NL ChiasmocleisPristimantis acuminatus bassleri (Dunn, (Schreve, 1949) 1935) X X X LC ChiasmocleisPristimantis altamazonicus tridactyla (Duellman (Barbour and and Mendelson, Dunn, 1921) 1995) X X X LC CtenophrynePristimantis carvalhoigeayi (Mocquard, (Lutz, 1952) 1904) X X LC HamptophrynePristimantis conspicillatus boliviana (Parker, (Günther, 1927) 1858) X X LC SynapturanusPristimantis croceoinguinis rabus (Pyburn, (Lynch, 1977) 1968) X X X LC Phyllomedusidae Pristimantis delius (Duellman and Mendelson, 1995) X DD CruziohylaPristimantis craspedopus diadematus (Funkhouser,(Jiménez de la 1957) Espada, 1872) X LC PhyllomedusaPristimantis lanthanites bicolor (Boddaert, (Lynch, 1975) 1772) X X LC PhyllomedusaPristimantis malkini tarsius (Lynch, (Cope, 1980)1868) X X X LC PhyllomedusaPristimantis martiae vaillantii (Lynch, (Cope, 1974) 1868) X X X LC Pipidae Pristimantis ockendeni (Boulenger, 1912) X X X LC PipaPristimantis pipa (Linnaeus, orcus (Lehr 1758) et al. 2009) X X X LC PipaPristimantis snethlageae padiali (Müller, (Moravec 1914) et al., 2010) X X LC CAUDATA Pristimantis peruvianus (Melin, 1941) X LC Plethodontidae Pristimantis variabilis (Lynch, 1968) X X LC BolitoglossaPristimantis ventrimarmoratusaltamazonica (Cope, (Boulenger, 1874) 1912) X X LC GYMNOPHIONA Strabomantis sulcatus (Cope, 1874) X X LC CaeciliidaeDendrobatidae SiphonopsAmeerega hahneliannulatus (Boulenger, (Mikan, 1822) 1884) X X X LC MicrocaeciliaAmeerega trivittata albiceps (Spix, (Boulenger, 1824) 1882) X LC Typhlonectidae Typhlonectes compressicauda (Duméril and Bibron, 1841) X LC 762 Matthew F. Metcalf et al.

Table 3. Reptiles recorded at the Santa Cruz Forest Reserve in Loreto, Peru. Record Types: VES = Visual Encounter Survey; OE = Opportunistic Encounter; SD = Secondary Data. IUCN Red List rankings: DD = Data Deficient, LC = Least Concern, NL = Not Listed, VU = Vulnerable. * indicates species only found in adjacent pasture land surveys. Table 2. Table 3.

SPECIES VESVES OE SD SD IUCN IUCN AMPHISBAENIAANURA Amphisbaenidae Aromobatidae AmphisbaenaAllobates conspicuus alba (Linnaeus, (Morales, 1758) 2002) X X XX LCDD CROCODYLIA Allobates femoralis (Boulenger, 1884) X X X LC Alligatoridae Allobates marchesianus (Melin, 1941) X LC BufonidaeCaiman crocodilus (Linnaeus, 1758) X LC PaleosuchusRhaebo glaberrimus trigonatus (Günther, Schneider, 1869) 1801 X X LCLC : Rhaebo guttatus SAURA (Schneider, 1799) X LC Alopoglossidae Rhinella dapsilis (Myers and Carvalho, 1945) X X X LC AlopoglossusRhinella margaritifera angulatus (Laurenti, (Linnaeus, 1768) 1758) XX X X LC LC AlopoglossusRhinella marina atriventris (Linnaeus, (Duellman, 1758) 1973) XX X XX LCLC CentrolenidaeAlopoglossus buckleyi (O’Shaughnessy, 1881) X X X LC PtychoglossusVitreorana ritae brevifrontalis (Lutz, 1952)* (Boulenger, 1912) X X LCDD DactyloidaeCeratophryidae AnolisCeratophrys bombiceps cornuta Cope, (Linnaeus, 1875 1758) X X XX NLLC CraugastoridaeAnolis fuscoauratus D’Orbigny, 1837 X X X NL AnolisNiceforonia ortonii nigrovittata Cope, 1868 (Andersson, 1945) X X XX NLLC AnolisNoblella punctatus myrmecoides Daudin, (Lynch, 1802 1976) X X LC LC AnolisOreobates trachyderma quixensis Cope,Jiménez 1876 de la Espada, 1872 XX X XX NLLC AnolisPristimantis transversalis academicus Duméril, Lehr 1851et al., 2010 X X X X NL NL Gekkonidae Pristimantis acuminatus (Schreve, 1935) X LC HemidactylusPristimantis altamazonicus mabouia Moreau (Barbour de Jonnés, and Dunn, 1818 1921) X X X NL LC Pristimantis carvalhoi (Lutz, 1952) X X LC ArthrosauraPristimantis conspicillatusreticulata (O’Shaughnessy, (Günther, 1858) 1881) X X X X LC LC CercosauraPristimantis arguluscroceoinguinis (Peters, (Lynch,1862) 1968) XX X XX LCLC CercosauraPristimantis ocellatadelius (Duellman (Wagler, 1830)and Mendelson, 1995) X X LC DD CercosauraPristimantis oshaughnessyidiadematus (Jiménez (Boulenger, de la Espada,1885) 1872) X X X NLLC IphisaPristimantis elegans lanthanites Gray, 1851 (Lynch, 1975) X X LC LC LoxopholisPristimantis parietalis malkini (Lynch, (Cope, 1886)1980) XX LCLC PotamitesPristimantis ecpleopus martiae (Cope,(Lynch, 1875) 1974) X X X X LC LC Pristimantis ockendeni (Boulenger, 1912) X X X LC EnyalioidesPristimantis laticepsorcus (Lehr (Guichenot, et al. 2009) 1855) XX X X LC LC EnyalioidesPristimantis microlepispadiali (Moravec (O’Shaughnessy, et al., 2010) 1881) XX LCLC Mabuyidae Pristimantis peruvianus (Melin, 1941) X LC CopeoglossumPristimantis variabilis nigropunctatum (Lynch, 1968)(Spix, 1825) XX X XX LCLC Phyllodactylidae Pristimantis ventrimarmoratus (Boulenger, 1912) X LC ThecadactylusStrabomantis sulcatus solimoensis (Cope, (Bergmann 1874) and Russell, 2007) X XX LCLC PolychrotidaeDendrobatidae PolychrusAmeerega marmoratushahneli (Boulenger, (Linnaeus, 1884) 1758) X X XX LCLC Sphaerodactylidae Ameerega trivittata (Spix, 1824) X LC Gonatodes concinnatus (O’Shaughnessy, 1881) X X X LC

Herpetofauna of the Santa Cruz Forest Reserve in the Peruvian Amazon Basin 763

Table 3. Continued. Table 2.

SPECIESSPECIES VESVES OE OE SD SD IUCN IUCN ANURA Gonatodes humeralis (Guichenot, 1855) X X X LC AromobatidaePseudogonatodes guianensis Parker, 1935 X X X LC TeiidaeAllobates conspicuus (Morales, 2002) X X X DD AllobatesAmeiva ameiva femoralis (Linnaeus, (Boulenger, 1758) 1884) X X X X LC LC AllobatesKentropyx marchesianus altamazonica (Melin,Cope, 1876 1941) X X LCLC BufonidaeKentropyx pelviceps Cope, 1868 X X X LC RhaeboTupinambis glaberrimus teguixin (Günther,(Linnaeus, 1869) 1758) X X LC TropiduridaeRhaebo guttatus (Schneider, 1799) X LC RhinellaPlica plica dapsilis (Linnaeus, (Myers 1758) and Carvalho, 1945) X X XX NLLC RhinellaPlica umbra margaritifera (Linnaeus, (Laurenti, 1758) 1768) X X X X LC LC RhinellaStenocercus marina fimbriatus (Linnaeus, (Avila-Pires, 1758) 1995) XX X X LCLC Centrolenidae Uracentron flaviceps (Guichenot, 1855) X LC SQUAMATA: Vitreorana SERPENTES ritae (Lutz, 1952)* X DD CeratophryidaeBoidae CeratophrysBoa constrictor cornuta Linnaeus, (Linnaeus, 1758 1758) XX LCLC Craugastoridae Corallus caninus (Linnaeus, 1758) X LC NiceforoniaCorallus hortulanus nigrovittata (Linnaeus, (Andersson, 1758) 1945) X XX LCLC NoblellaEpicrates myrmecoides cenchria (Linnaeus, (Lynch, 1758) 1976) X X X NL LC OreobatesEunectes murinus quixensis (Linnaeus, Jiménez 1758)de la Espada, 1872 X X XX NLLC ColubridaePristimantis academicus Lehr et al., 2010 X NL PristimantisChironius carinatus acuminatus (Linnaeus, (Schreve, 1758) 1935) X XX NLLC PristimantisChironius exoletus altamazonicus (Linnaeus, (Barbour 1758) and Dunn, 1921) X X X LC LC PristimantisChironius fuscus carvalhoi (Linnaeus, (Lutz, 1758) 1952) X XX LCLC PristimantisChironius multiventris conspicillatus (Schmidt (Günther, and Walker,1858) 1943) X X LC LC PristimantisChironius scurrulus croceoinguinis (Wagler, (Lynch, 1824) 1968) XX X X LCLC PristimantisDendrophidion delius dendrophis (Duellman (Schlegel, and Mendelson, 1837) 1995) X X LC DD PristimantisDrymarchon diadematuscorais (Boie, (Jiménez 1827) de la Espada, 1872) X XX LCLC PristimantisDrymoluber lanthanitesdichrous (Peters, (Lynch, 1863) 1975) X X X LC LC PristimantisLeptophis ahaetulla malkini (Linnaeus,(Lynch, 1980) 1758) XX LCLC PristimantisMastigodryas martiae boddaerti (Lynch, (Sentzen, 1974) 1796) X X X X LC LC PristimantisOxybelis fulgidus ockendeni (Daudin, (Boulenger, 1803) 1912) X X XX LCLC PristimantisPhrynonax poecilonotus orcus (Lehr (Günther,et al. 2009) 1858) X X LC LC PristimantisSpilotes pullatus padiali (Linnaeus, (Moravec 1758) et al., 2010) X XX LCLC PristimantisSpilotes sulphureus peruvianus (Wagler, (Melin, 1824) 1941) X X LC LC DipsadidaePristimantis variabilis (Lynch, 1968) X X LC PristimantisAtractus collaris ventrimarmoratus (Peracca, 1897) (Boulenger, 1912) X X LC LC StrabomantisAtractus major sulcatus (Boulenger (Cope, ,1894) 1874) X XX LCLC Dendrobatidae Atractus snethlageae (da Cunha and do Nascimento, 1983) X LC AmeeregaClelia celia hahneli (Daudin, (Boulenger, 1803) 1884) X X XX LCLC AmeeregaDipsas catesbyi trivittata (Sentzen, (Spix, 1796)1824) X X X LC LC indica (Laurenti, 1768) X LC Dipsas pavonina (Schlegel, 1837) X LC

764 Matthew F. Metcalf et al.

Table 3. Continued. Table 2.

SPECIESSPECIES VESVES OE OE SD SD IUCN IUCN ANURA Drepanoides anomalus (Jan, 1863) X LC AromobatidaeErythrolamprus reginae (Linnaeus, 1758) X X LC AllobatesErythrolamprus conspicuus typhlus (Morales, (Linnaeus, 2002) 1758) X X XX LCDD AllobatesHelicops angulatusfemoralis (Linnaeus,(Boulenger, 1758) 1884) X X X X LC LC AllobatesHelicops polylepismarchesianus (Günther, (Melin, 1861) 1941) X X LCLC BufonidaeHydrops martii (Wagler, 1824) X LC RhaeboImantodes glaberrimus cenchoa (Linnaeus, (Günther, 1758)1869) X X X LCLC RhaeboImantodes guttatus lentiferus (Schneider, (Cope, 1894)1799) X X LC LC RhinellaOxyrhopus dapsilis formosus (Myers (Wied-Neuwied, and Carvalho, 1820) 1945) X X XX NLLC RhinellaOxyrhopus margaritifera melanogenys (Laurenti, (Tschudi, 1768) 1845) X X X NL LC RhinellaOxyrhopus marina petolarius (Linnaeus, (Linnaeus, 1758) 1758) X X XX LCLC Centrolenidae vanidicus (Lynch, 2009) X LC VitreoranaPhilodryas ritaeargentea (Lutz, (Daudin, 1952)* 1803) X X LCDD Ceratophryidae Pseudoboa coronata (Schneider, 1801) X X LC CeratophrysSiphlophis cervinus cornuta (Laurenti, (Linnaeus, 1768) 1758) XX LCLC Craugastoridae Siphlophis compressus (Daudin, 1803) X X X LC NiceforoniaTaeniophallus nigrovittata brevirostris (Andersson, (Peters, 1863) 1945) X X LCLC NoblellaXenodon myrmecoidesrabdocephalus (Lynch, (Wied-Neuwied, 1976) 1824) X X LC LC ElapidaeOreobates quixensis Jiménez de la Espada, 1872 X X X LC PristimantisMicrurus hemprichii academicus (Jan, Lehr 1858) et al., 2010 X X LC NL PristimantisMicrurus filiformis acuminatus (Günther, (Schreve, 1859) 1935) X X LCLC PristimantisMicrurus langsdorfii altamazonicus (Wagler, (Barbour 1824) and Dunn, 1921) X X X LC LC PristimantisMicrurus lemniscatus carvalhoi (Linnaeus, (Lutz, 1952) 1758) X XX LCLC PristimantisMicrurus spixii conspicillatus (Wagler, 1824) (Günther, 1858) X X LC LC PristimantisMicrurus surinamensis croceoinguinis (Cuvier, (Lynch, 1817) 1968) XX X XX LCLC ViperidaePristimantis delius (Duellman and Mendelson, 1995) X DD PristimantisBothrops atrox diadematus (Linnaeus, (Jiménez 1758) de la Espada, 1872) X X XX NLLC PristimantisBothrops bilineatus lanthanites (Wied-Neuwied, (Lynch, 1975) 1821) X X NL LC PristimantisBothrops taeniatus malkini (Wagler, (Lynch, 1824)1980) XX LCLC PristimantisLachesis muta martiae (Linnaeus, (Lynch, 1766) 1974) X X X X NL LC TESTUDINES Pristimantis ockendeni (Boulenger, 1912) X X X LC ChelidaePristimantis orcus (Lehr et al. 2009) X LC PristimantisPlatemys platycephala padiali (Moravec (Schneider, et al., 1792) 2010) X XX NLLC PodocnemididaePristimantis peruvianus (Melin, 1941) X LC PristimantisPodocnemis variabilisunifilis (Troschel, (Lynch, 1848)1968) X X XX VULC TestudinidaePristimantis ventrimarmoratus (Boulenger, 1912) X LC StrabomantisChelonoidis denticulata sulcatus (Cope, (Linnaeus, 1874) 1766) X XX VULC Dendrobatidae Ameerega hahneli (Boulenger, 1884) X X X LC Ameerega trivittata (Spix, 1824) X LC wilderness areas, and boasts ample species richness there is growing scientific and social demand to

(Rabosky et al., 2019). While habitat loss and mitigate negative effects on biodiversity and ecosystem fragmentation continue to occur throughout Amazonia, services (Haila, 2002). In particular, preserved lands Herpetofauna of the Santa Cruz Forest Reserve in the Peruvian Amazon Basin 765 and primary forests are increasingly important for (2016): Exploring conservation discourses in the Galapagos protecting biodiversity throughout the tropics (Gibson Islands: A case study of the Galapagos giant tortoises. Ambio et al., 2011). Protected reserves, sustainable use areas, 45: 706–724. Cárdenas, G.G., Tuomisto, H., Lehtonen, S. (2016): Newly and indigenous lands serve as essential biodiversity discovered diversity in the tropical fern Metaxya based on sanctuaries and economic mixed-use areas (Miranda et morphology and molecular phylogenetic analyses. Kew Bulletin al., 2016; Karin et al., 2018; Kauano et al., 2020), yet 71: 5. https://doi.org/10.1007/s12225-016-9618-9. may not be sufficient for species that fill a unique and Catenazzi, A., Bustamante, M. (2007): Anfibios y reptiles/ narrow niche (e.g. freshwater turtles; Fagundes et al., Amphibians and reptiles, p. 62–67, 130–134, and 206–213, in 2016). Vriesendorp et al. 2007. RI–18 Perú: Nanay-Mazán-Arabela. Conservation is trans-disciplinary and is, therefore, Rapid Biological Inventories Report 18. The Field Museum, Chicago. influenced by social and geo-political dynamics Chamberlain, E.C., Rutherford, M.B., Gibeau, M.L. (2012): Human (Chamberlain et al., 2012; Benitez-Capistros et al., perspectives and conservation of grizzly bears in Banff National 2016). As the Santa Cruz Forest Reserve has grown Park, Canada. Conservation Biology 26: 420–431. since its recent inception, Project Amazonas has Chao, A., Gotelli, N.J., Hsieh, T.C., Sander, E.L., Ma, K.H., Colwell, proactively maintained positive interactions with local R.K., Ellison, A.M. (2014): Rarefaction and extrapolation with communities through education, healthcare, research, Hill numbers: a framework for sampling and estimation in species diversity studies. Ecological Monographs 84: 45–67. and conservation. This multidisciplinary approach is Chávez, G., Mueses-Cisneros, J.J. (2016): Anfibios y reptiles/ of particular importance as the region continues to Amphibians and reptiles, p. 119–131, 300–311, and 456–465, develop and human communities expand from urban in Pitman et al. 2016. RI–28 Perú: Medio Putumayo-Algodón. centres into forested areas. The high species richness Rapid Biological Inventories Report 28. The Field Museum, found at the Santa Cruz Forest Reserve highlights this Chicago. successful approach and affirms the reserve’s vital role da Silva, J.M.C., Rylands, A.B., Da Fonseca, G.A. (2005): The fate as a protected conservation unit in close proximity to of the Amazonian areas of endemism. Conservation Biology 19: 689–694. Iquitos. Research such as this can now be used to inform de Oliveira, E.A., da Silva, L.A., Silva, E.A.P., Buimarães, K.L.A., conservation and wildlife management practices within Penhacek, M., Martínez, Rodrigues, L.R.R., Santana, D.J., the reserve and the surrounding areas. Hernández-Ruz, E.J. (2020). Four new species of Pristimantis Jiménez de la Espada, 1870 (Anura: Craugastoridae) in the Acknowledgments. Research was conducted under FGCU eastern Amazon. PLoS ONE 15: e0229971. IACUC #1819-05. This project would not have been possible de Solar, R.R.C., Barlow, J., Andersen, A.N., Schoereder, J.H., without the financial and overall support from the offices of Berenguer, E., Ferreira, J.N., Gardner, T.A. (2016): Biodiversity FGCUScholars (Undergraduate Research) and the FGCU Honors consequences of land-use change and forest disturbance in the College. We are extremely grateful to Project Amazonas for their Amazon: A multi-scale assessment using ant communities. hospitality and to everyone involved with the fantastic crew at Biological Conservation 197: 98–107. the Santa Cruz Forest Reserve. We also want to thank the FGCU Doan, T.M. (2003): Which methods are most effective for surveying Behavior Research Group for their discussions and edits rain forest herpetofauna? Journal of 37: 72–81. to this and other manuscripts as well as Prairie Gunnels for Elmer, K.R., Cannatella, D.C. (2008): Three new species of assistance in the field. 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Accepted by Fabrício Oda