BIOTROPICA 34(1): 101117

2002

Microgeographic Variation in Species Composition of the Herpetofaunal Communities of Tambopata Region, Peru1
Tiffany M. Doan 2 Department of Biology, University of Texas at Arlington, Box 19498, Arlington, Texas 76019, U.S.A. and Wilfredo Arizabal Arriaga 3 Museo de Historia Natural, Universidad Nacional de San Antonio Abad de Cusco, Urb. Los Angeles E-1, Cusco, Peru

ABSTRACT
Neotropical herpetofaunas have been studied at selected Central and South American sites, but intra-regional analyses in the Neotropics have not been possible due to lack of long-term data. A particular problem in interpreting herpetofaunal communities is the large geographic distances between the known localities. Such sampling does not take into account the patchiness of the habitat and this prevents analysis of regional diversity. In this study, ve Neotropical herpetofaunal communities within a small geographic area (1600 km2) were examined to determine if species composition varies microgeographically. We sampled sites within the Tambopata Province, southeastern Peru. The ve sites were surveyed intensively during a two-year period. The herpetofauna of the Tambopata region includes 210 species and, because of extensive sampling, has the highest overall herpetofaunal richness of any known region. Sites were compared using the coefcient of biogeographic resemblance (CBR). The CBRs were similar among all sites but the differences were determined primarily by their positions with respect to the two main rivers of the region and not directly correlated to distance among sites. Sites were also examined by partitioning their species into six microhabitat classes. Sites were found to differ in their proportions of reptiles and amphibians in each microhabitat class. The results of our study were compared to former investigations of various sites within the Tambopata region and elsewhere. This study identied more species than past investigations in all cases. Species composition was shown to vary at a microgeographic level. Based on our ndings, we recommend that future studies examine multiple sites within each region to fully comprehend the herpetofaunal communities that exist in complex rain forest habitats.

RESUMEN
Las herpetofaunas neotropicales se han estudiado en algunos lugares de Centro y Sud America, pero analises intra regionales no han sido posibles por falta de datos a largo plazo. Un problema de analisis de las comunidades de herpe tofauna es la gran distancia geograca entre los localidades estudiadas. Este tipo de censos no toman en cuenta la heterogenidad del habitat y no permite el examen de la diversidad regional. En el presente estudio se examinaron cinco comunidades neotropicales de herpetofauna dentro de un ambito geograco pequeno (1600 km2), para determinar si la composicion de especies vara microgeogracamente. La investigacion fue realizada en la Provincia de Tambopata, al sureste del Peru. Las cinco localidades se censaron intensivamente durante un perodo de dos anos. La herpetofauna de la region consiste de 210 especies, y como resultado de muestreos extensivos, presenta la mayor riqueza que cualquier region conocida del mundo. Las localidades se compararon con el coeciente de semejanza biogeograca. Los coecientes fueron similares entre todos los localidades, pero las diferencias fueron producto de la posicion con respecto a los dos ros principales de la region y no estuvieron correlacionados con la distancia. Tambien se clasicaron de acuerdo al tipo de microhabitat que utilizon los especies estudiadas. Las localidades dieren en proporcion de reptiles y anbios en los seis de microhabitats denidos. Los resultados de nuestro estudio se compararon con investigaciones previos, en Tambopata y otras regiones. En todos los casos, nuestro estudio identico mas especies que las investigaciones previas. La composicion de especies vara a nivel microgeograco, por lo que recomendamos que en lo sucesivo se examinen varias localidades dentro de cada region para as abarcar totalmente las comunidades de herpetofauna que ocurren en selvas intrincadas. Key words: Amazon; Anura; community ecology; herpetofauna; lowland tropical rain forest; Peru; regional diversity; Reptilia; species composition; Tambopata.

IN THE PAST THREE DECADES, MAJOR ADVANCES have been made in the description and analysis of Neotropical herpetofauna (Duellman 1990, 1999;
1 Received 26 February 2001; revision accepted 6 November 2001. 2 E-mail: tiffperu@yahoo.com 3 E-mail: wilari@yahoo.com

Caldwell 1996). Herpetofaunal communities at several lowland locations have been surveyed in moderate detail: La Selva Biological Station, Costa Rica (Guyer 1990, 1994; Donnelly 1994); Barro Colorado Island, Panama (Rand & Myers 1990); Santa Cecilia, Ecuador (Duellman 1978); Iquitos region, Peru (Dixon & Soini 1986, Rodrguez & Duellman 1994); Manu National Park, Peru (Ro-

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TABLE 1. Survey dates at each of the ve Tambopata sites. Site Tambopata Research Center 8/189/4/1997 11/2912/15/1997 2/92/26/1998 7/318/17/1998 10/2911/17/1998

EcoAmazona Dates 1/222/7/1997 5/256/8/1997 10/710/23/1997 3/164/1/1998 5/266/12/1998 9/59/21/1998

Cusco Amazonico 2/72/27/1997 4/185/3/1997 9/59/21/1997 1/222/7/1998 6/126/26/1998 8/199/5/1998

Explorers Inn 3/174/3/1997 7/137/31/1997 10/2511/11/1997 4/185/8/1998 10/610/29/1998

Sachavacayoc Centre 2/283/17/1997 6/126/29/1997 11/1111/29/1997 5/85/25/1998 7/137/31/1998

drguez & Cadle 1990, Morales & McDiarmid 1997); Guama Ecological Research Station, Brazil (Crump 1971); and rain forest near Manaus, Brazil (Zimmerman & Rodrigues 1990). Many of these herpetofaunal communities were chronicled in Gentry (1990) and analyzed by Duellman (1990). The only treatises covering the entire Amazonian region were Lynch (1979) concerning amphibians and Dixon (1979) concerning reptiles. Despite these investigations, present knowledge of Amazonian and Central American rain forest herpetofaunal communities remains incomplete (Caldwell 1996, Campbell 1999, Duellman 1999). Large geographic distances exist between the Neotropical sites that have been studied in detail (Duellman 1988, da Silva & Sites 1995, Duellman & Mendelson 1995). This fact is problematic because these rain forests are not homogeneous throughout their distribution (Gentry 1988, Tuomisto et al. 1995). There are tremendous gaps in herpetofaunal investigation from the great expanses of habitat between these sites, and local and regional effects on the herpetofauna have not been studied at all. Accordingly, studies of multiple sites within a small geographic region would be advantageous in directly examining the effects of microgeographic factors on amphibian and reptile faunas. Tambopata Province of the Madre de Dios Department, Peru, lies at the southwestern edge of the Amazon basin near the Andean foothills and encompasses ca 36,268 km2 covered primarily by lowland tropical/subtropical moist forest (Gentry & Leon 1997). Tambopata has a distinct six month dry season and receives ca 2000 mm of rain annually (Erwin 1984, Gentry & Leon 1997). Tambopata has been recognized as a region of high diversity and holds world record numbers of birds, tabanid ies, tiger beetles, damselies and dragonies, and butteries (Stewart 1988). Several re-

search sites within Tambopata are adjacent to two main rivers: Ro Madre de Dios and its tributary, the Ro Tambopata. Localities in Tambopata have received varying amounts of herpetological attention. Duellman and Salas (1991) and Duellman (1987, 1995) surveyed Cusco Amazonico and McDiarmid and Cocroft (pers. comm.) inventoried Explorers Inn. Two other sites, Sachavacayoc Centre and Tambopata Research Center, were the subjects of small rapid assessment studies that produced preliminary species lists (Rodrguez & Em mons 1994, Salas 1995, Sehgemeble 1997). We intensively surveyed ve localities within Tambopata for 23 months (19971998). The surveyed area stretches ca 114 km (air line) and encompasses slightly less than 1600 km2. Abundance data were generated for 76 anuran species and 50 reptile species, 16 of which have over 250 capture records. With such an extensive data set, much may be revealed about the communities of these ve geographically proximate sites. Our goal was to examine patterns within and among the herpetofaunal communities of Tambopata to understand nescale variation in herpetofaunas in a well-studied rain forest region. Additionally, by assessing local heterogeneity, combined data on the herpetofauna of these sites provide a more complete notion of the herpetofauna in this region.

MATERIALS AND METHODS

The eld study, known as Proyecto Tambopata (PT; Doan & Arizabal 2000a), was conducted from January 1997 to November 1998. Five sites were visited on a continuously rotating schedule of 18 days per site for a minimum of ve visits per site throughout the two-year period (Table 1). During the rst visit at each site, four quadrat parcels and two visual encounter survey (VES) parcels were installed. Quadrat parcels measured 80 70 m and

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contained 56 quadrats each; 1 ha VES parcels contained 24 straight-line transects in each. During each site visit, one half of the 224 quadrats was randomly sampled, 84 during the night and 28 during the day. Also during each site visit, each of the 48 transects was sampled twice, once during the day and once at night. An identical number of parcels was installed at each site and identical sampling of those parcels was conducted during each visit. For a complete methodological description, see Doan and Arizabal (2000a). Voucher specimens of some species from various localities were deposited at the Museo de Historia Natural, Universidad Nacional de San Antonio Abad de Cusco (UNSAAC). The ve sampled sites are near the capital of the Department of Madre de Dios, Puerto Maldonado, which lies at 212 m elevation within the Tambopata Province. A portion of the Tambopata Province lies within the over 1,000,000 ha Parque Nacional Bahuaja Sonene. As of September 2000, with expansion of the national park and creation of the Reserva Nacional Tambopata (RNT), four sites lie in the buffer zone outside of the reserve, and one site, Tambopata Research Center, lies within the RNT. At the time of the study, all ve sites were within the former Zona Reservada Tambopata Candamo. Two sites lie along Ro Madre de Dios downriver from Puerto Maldonado, whereas the other three are upriver from the town, on Ro Tambopata. See Figure 1 for a map of all sites. SITES. Information about each of the ve sites is listed in Table 2. Each site has a different management history and a different complement of forest types. Forest types of the Tambopata region were rst categorized by Erwin (1984) and then dened and described in greater detail by Phillips (1993, 1994) based on oristic and soil characteristics. For the purposes of this study, we follow the classication of Phillips (1993). To conduct the required studies during the Proyecto Tambopata investigation (Doan & Arizabal 2000a), we chose one forest type at each site to construct all parcels to minimize within-site variation. Although we preferred older and higher terra rme (Types G and H) and old oodplain (Type F) forest types, these selections were not possible at all sites (Table 2). In addition to the forest types classied by Phillips (1993), isolated stands of bamboo (Guadua weberbaueri and G. angustifolia) can be found within more poorly drained and/or disturbed areas of some aforementioned forest types, adding to the habitat diversity of some sites (EI, SC, and TRC).

DATA ANALYSIS. We analyzed two types of data that were gathered during our surveys. The rst type, termed community data, included all species captured, whether quadrat, VES, or opportunistic capture. Relative abundance was not considered for community data because accurate records of individuals were not kept for specimens captured in an opportunistic fashion. The second data type, termed abundance data, included only those species and individuals captured during VES or quadrat sampling, allowing analysis of relative abundance among sites. We cannot assume that the abundance data we collected reect actual abundance because sampling in complex habitats, especially tropical rain forests, is almost certainly biased because of differing observability and ease of capture of different species (Pearman et al. 1995); however, because of the standard, rigorous sampling during each visit at each site, any bias that did exist in our surveys was constant throughout the study period, allowing us to be condent of our analyses of relative abundances among sites. Two metrics, the Shannon-Wiener diversity index (the most popular and reliable diversity index; Ludwig & Reynolds 1988, Hayek 1994) and the coefcient of biogeographic resemblance (Duellman 1990), were used to examine diversity and similarity among sites. All other statistical tests (ANOVA, Pearson correlation, and Spearmans coefcient of rank correlation) were performed using Statistica for Windows 4.5 (StatSoft 1993).

RESULTS AND DISCUSSION

TAMBOPATA SPECIES COMPOSITION. After the intensive survey of Proyecto Tambopata, revised species lists were compiled for each site and for the Tambopata region as a whole. Seven species were recorded for the rst time in the province (Doan & Arizabal 2000b), including one species that was also new for Peruthe colubrid snake Ninia hudsoni. A total of 210 amphibian and reptile species have now been recorded for Tambopata, distinguishing this region as having the most diverse herpetofauna known in the world and exceeding the 185 species in the upper Ro Aguarico region of Ecuador (Duellman 1978). Tambopata contains 29.3 percent of the reptile species known to occur in Peru and 30.1 percent of the amphibian species (Carrillo de Espinoza & Icochea 1995, Morales 1995). See Appendix 1 for a complete checklist of species recorded at the sites. Even though the project consisted of identical intensive sampling for the entire two years, some

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FIGURE 1. Map of Departamento de Madre de Dios. The shaded area is the Tambopata Province, which includes the Reserva Nacional Tambopata (RNT) and a portion of the Parque Nacional Bahuaja Sonene (PNBS). EA EcoAmazona; CA Cusco Amazonico; EI Explorers Inn; SC Sachavacayoc Centre; and TRC Tambopata Research Center.

species were recorded for the rst time within the nal months. Figure 2a shows species accumulation curves of reptiles and amphibians over time. Figure 2b details capture of novel species by study month. Although the increase of the curves diminished with time, the curves still have positive slopes and it is likely that additional species remained to be found (especially more elusive reptiles such as snakes), justifying the importance of long-term studies in discovering faunal elements that exist at low densities or exhibit secretive lifestyles. Herpetofaunal richness (i.e., number of species)

at each site is listed in Table 3. Diversity (i.e., number of species incorporated with relative number of individuals per species) of sampled parcels, calculated using the Shannon-Wiener diversity index, is also listed in Table 3. The highest amphibian diversity was found at TRC, whereas CA had the highest reptile diversity (Table 3). In addition to examining the diversity of the entire Tambopata herpetofauna, community differences between sites, determined using the CBR, are listed for each site pair in Table 4. For comparison purposes, CBRs were also computed between each Tambo-

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TABLE 2. Information about each of the ve Tambopata sites included in the study. All forest types are based on the Phillips (1993) classication. A Permanently Flooded Swamp Forest; B Seasonally Flooded Swamp Forest; C Lower Floodplain Forest; D Middle Floodplain Forest; E Upper Floodplain Forest; F Old Floodplain Forest; G Terra Firme Clay Forest; and H Terra Firme Sandy-Clay Forest. B/F, B/G, and F/G are transition types among the regular forest types.

none Duellman 1987, Duellman & Salas 1991, Duellman 1995 McDiarmid & Cocroft, pers. comm. Cocroft & Hambler 1989

Past herpetological studies

Study forest type

F/G bamboob

F/G bamboob F, G,

Rodriguez 1994a, Salas 1995 Not recognized as a transition type by Phillips (1993). Characterized for the rst time by Doan and Arizabal (2000a). Indicates that signicant stands of bamboo occur within the forest types.
b a

B/Fa

F, B/F F, G,

H F, G,

Forest types

Salas 1997

A, B, C, D, E, A, B, C, D, E, H, B/G, F/G A, B, C, D, E, B/G, F/G A, B, C, D, E, B/G, F/G

FIGURE 2. (a) Species accumulation curve for reptiles and amphibians of Tambopata over the two-year sampling period. (b) Number of new species captured by month of the study.

A, B

pata site and two sites within the Parque Nacional Manu, also within the Department of Madre de Dios (Table 4). Estacion Biologica Cocha Cashu and Pakitza Park Guard Station are ca 290 km to the westnorthwest of Puerto Maldonado and have similar habitat types to Tambopata (Fig. 1). These two sites are the geographically closest sites to Tambopata where herpetofauna has been previously surveyed (Rodrguez & Cadle 1990, Morales & McDiarmid 1997). Despite the similarity of the overall herpetofaunal composition at Tambopata (as exhibited by similar CBRs), some interesting cases occurred when species were apparently absent from some sites but were abundant at others. One notable example is the absence of the often-conspicuous frog Edalorhina perezi from the Ro Tambopata sites. Squamate diversity also differed markedly between the Ro Tambopata and Ro Madre de Dios sites. Although species richness was similar, diversity of squamates was quite different because of the high abundance of lizards and snakes at EA and CA. Gonatodes humeralis, Pseudogonatodes guianensis, and Prionodactylus eigenmanni were observed several times each day at EA and CA; Ptychoglossus

Coordinates River, distance, and direction from Puerto Maldonado Site (abbreviation)

EcoAmazona (EA) Cusco Amazonico (CA) Explorers Inn (EI) Sachavacayoc Centre (SC) Tambopata Research Center (TRC)

Madre de Dios 35.2 km ENE Madre de Dios 15 km ENE Tambopata 30 km SSW Tambopata 35 km SSW Tambopata 86.5 km SSW

12 68 12 69 12 69 12 69 13 69

31 55 32 03 50 17 51 21 08 37

44 58 28 36 18 45 10 57 53 02

S W S W S W S W S W

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TABLE 3. Species richness and diversity of amphibians and reptiles at Tambopata by site. Species richness is based on all species known to occur at the site, recorded by us or previous authors. Diversity is based on only those individuals and species captured during quadrat or visual encounter survey sampling. The number in parentheses represents the sampling richness. Species richness Site EcoAmazona Cusco Amazonico Explorers Inn Sachavacayoc Centre Tambopata Research Center Amphibians Reptiles 53 58 77 55 78 56 89 85 50 61 Total 109 147 162 105 139 Amphibians 2.422 2.303 2.111 2.275 2.729 (47) (42) (42) (45) (52) Diversity Reptiles 2.153 2.369 2.162 1.787 2.326 (34) (32) (19) (30) (28) Overall 2.798 2.666 2.250 2.448 2.924 (81) (74) (61) (75) (80)

brevifrontalis and Prionodactylus argulus were captured less frequently but still on a regular basis at those two sites. Ptychoglossus has never been recorded at any of the Ro Tambopata sites. The only lizard species captured regularly at EI, SC, and TRC was Anolis fuscoauratus. Additionally, comparisons between the Tambopata sites and the Manu sites showed remarkably similar anuran communities, whereas the reptile communities differed more strongly. All species of Tambopata can be classied according to microhabitat use. Categories used in this study were semifossorial (or leaf litter), terrestrial, small shrubs, large tree trunks, canopy, and aquatic. The two latter microhabitat categories were not actively studied in this investigation but limited captures of anurans were made in these types. Categories used here pertain to the microhabitat type that the species utilized most often, although it may have been captured in other types occasionally. The percentage of amphibian species in each microhabitat category did not differ signicantly among sites (ANOVA: P 0.05). Percentages for each microhabitat type at each site are detailed in Figure 3. Microhabitat distributions of reptile species were highly correlated between EA and CA (Pearson r 0.973); SC and TRC were also quite similar (r 0.969); however, for all other pairs of communities, signicant differences existed. EcoAmazona and CA both had high, roughly equal numbers of leaf litter and shrub species. At SC and TRC, shrub dwellers made up the largest portion of species, followed by terrestrial reptiles. Explorers Inn was unique in having terrestrial reptiles as its highest percentage. When abundances of individuals in each microhabitat class were considered instead of numbers of species, the resulting comparative prole was somewhat different (Fig. 3b, d). Correlations of abundances were high among sites for amphibians

and sites did not differ signicantly (ANOVA: P 0.05), which was similar to the species richness results, but the distribution of percentages in each type category was different. At all sites, amphibian abundance was highest in leaf litter, whereas richness was higher in either shrub or leaf litter microhabitats, depending on site. The correlation between amphibian microhabitat category distribution, expressed as richness and abundance data, was relatively low (r 0.736). For reptile abundances per microhabitat, sites differed signicantly (as they did when richness data were used). Similar to the results based on richness data, EA and CA showed a high correlation (r 0.976), as did SC and TRC (r 0.989). EcoAmazona and CA had approximately equal percentages of individuals in leaf litter and shrub microhabitats, but the other sites showed differing patterns. At both SC and TRC, shrub dwelling was the dominant type and EI had approximately equal terrestrial and shrub microhabitat percentages. When comparing reptile richness and abundance microhabitat data, differences were much smaller than they were with the amphibian data; a correlation between the two reptile data sets was high at r 0.929. The largest difference among the reptile data sets is that, although leaf litter, terrestrial, and shrub microhabitats were all important at each site in the species richness data, only one or two types dominated per site in the abundance data. Scott (1976) found that species richness of leaf litter herpetofauna in Central America and Southeast Asia was inversely correlated with density of individuals. We tested this by correlating relative abundance (which was substituted for density in this study because sampling parcels at all sites were identical in number and size) and richness by site of amphibians and reptiles. For leaf litter amphibians, a Spearmans correlation of r 0.894 re-

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TABLE 4. Coefcient of biogeographic resemblance (CBR) for anurans, reptiles, and total herpetofauna of Tambopata between pairs of sites. The number in italics on the diagonal is the number of species at that site. Above the diagonal are number of species in common. Below the diagonal are CBRs. Comparisons with Estacion Biologica Cocha Cashu and Pakitza list the number of species in common on the right and the CBRs on the left for each faunal group. EA EcoAmazona; CA Cusco Amazonico; EI Explorers Inn; SC Sachavacayoc Centre; and TRC Tambopata Research Center. Anurans EA EA CA EI SC TRC 53 0.800 0.708 0.782 0.692 EA EA CA EI SC TRC 56 0.771 0.703 0.789 0.720 EA EA CA EI SC TRC CA 50 58 0.748 0.727 0.736 CA 59 89 0.777 0.681 0.592 CA EI 51 58 77 0.729 0.785 Reptiles EI 52 68 85 0.691 0.762 Total EI SC TRC 91 88 103 109 109 105 92 126 0.807 147 120 98 0.764 162 0.705 92 0.710 105 0.702 0.786 0.754 139 0.769 0.705 0.700 Cocha Cashu Anurans-67 EA CA EI SC TRC 45 48 52 42 52 0.726 0.711 0.675 0.700 0.727 Reptiles-53 37 44 39 34 36 0.638 0.615 0.565 0.654 0.626 Pakitza Anurans-67 EA CA EI SC TRC 39 48 53 41 53 0.650 0.768 0.736 0.672 0.741 Reptiles-60 36 46 49 31 41 0.621 0.617 0.676 0.564 0.678 All-128 75 94 102 72 95 0.633 0.684 0.703 0.618 0.712 All-122 82 92 91 76 89 0.678 0.657 0.619 0.673 0.679 FIGURE 3. Microhabitat usage percentages. (a) Amphibian microhabitat usage by number of different species. (b) Reptile microhabitat usage by number of different species. (c) Amphibian microhabitat usage by individuals. (d) Reptile microhabitat usage by individuals. Microhabitat categories: spots leaf litter; wide diagonal stripes terrestrial; grey shrubs; thin diagonal stripes arboreal; white canopy; and horizontal stripes aquatic. Sites: EA EcoAmazona; CA Cusco Amazonico; EI Explorers Inn; SC Sachavacayoc Centre; and TRC Tambopata Research Center. SC 45 48 47 50 0.761 TRC 45 52 56 43 61 SC 43 44 51 55 0.760 TRC 46 53 64 49 76

sulted, conrming the results of Scott (1976). For reptiles, however, the opposite was true with r 0.894. To examine this richness/density phenomenon further, we correlated richness and abundance

of amphibians and reptiles across all microhabitat categories. For amphibians there was no correlation (r 0.564), but reptiles were strongly correlated (r 1.000). Based on our results, it appears that anurans are not limited by space when many microhabitats are available. Presumably, the positive

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correlation of richness and abundance of reptiles was caused by overwhelming numbers of reptiles at EA and CA, regardless of microhabitat type. Many of the dissimilarities seen in the microhabitat use categories may be due to differences in forest types among sites. Although many studies have assumed lowland tropical rain forest to be a homogeneous habitat, in fact, the variety of forest types within the habitat present particular challenges to the species in each type because of differences in water availability, soil composition, and vegetation cover (Tuomisto et al. 1995, Caldwell 1996). Swamp forest present in the sampling parcels at EA likely explains the high numbers of hylid frogs captured during sampling at that site. Indeed, 19 percent of all amphibians captured at EA were hylids as opposed to 6.8 to 13.2 percent at the other four sites. For most hylids, water is essential for larval development (Duellman 1978) and they were often found calling from ooded areas at night. The second most abundant frog at EA, Hamptophryne boliviana, is also dependent on standing water in temporary pools for reproduction (Duellman 1978). In contrast, other common anurans such as Eleutherodactylus spp. are not tied to water because they exhibit direct development of terrestrial ova (Rodrguez & Duellman 1994). Old oodplain/seasonally ooded swamp forest transition at CA presents an interesting complex of resources to the herpetofauna of CA. As with EA, Adenomera andreae and H. boliviana were the most common species at CA, but unlike EA, hylids were not particularly abundant in our study parcels. Indeed, only 6.8 percent of amphibian individuals were hylids, the lowest percentage for all sites. The relatively open ground cover of old oodplain forest made ideal habitat for two species of Leptodactylus (L. leptodactyloides and L. didymus) that were generally uncommon at all other sites. At EI, we sampled a forest type unique to the Tambopata sites, Type H, terra rme sandy-clay forest. This forest type was found to support a relatively poor herpetofauna. Only 2430 amphibians and 77 reptiles were captured during sampling, which was only 85 percent of the amphibian individuals found at CA, the second poorest site, and only 44 percent of the abundance found at SC. Explorers Inn had less than half the number of reptile individuals found at any other site. Both SC and TRC had Type F/G transition with a large amount of bamboo in the study parcels. Herpetofaunal communities at the two sites, however, differed markedly. Sachavacayoc Centre was dominated by A. andreae and Eleutherodactylus

toftae, with also a large number of Scinax spp. Tambopata Research Center had a more even representation of species with none emerging as truly dominant. Differences between the two sites may be attributed to the higher elevation of TRC. As noted by other authors, elevation particularly affects the richness and abundance of the genus Eleutherodactylus (Rodrguez 1994a). Additionally, TRC has areas dominated by bamboo forest (Foster 1994, Kratter 1997) that make it possible to encounter bamboo inhabitants such as Dendrobates biolat and Bothriopsis bilineata, which range from the bamboo forest into the nearby F/G transition forest. COMPARISONS WITH FORMER STUDIES. As stated above, only four of the sites we sampled had been subject to past species inventories. At all sites, our sampling added a number of species that had not been recorded previously. Appendix 1, in addition to listing the species captured at each site, indicates whether the species was previously recorded or discovered at a site for the rst time during PT. As would be expected, sites with the most intensive former sampling, CA and EI, had the lowest number of additional species records. We added 5 species of anurans, 4 lizards, and 4 snakes to the CA list for a total of 147 herpetofaunal species. Added to the list of EI species were 6 anuran, 3 lizard, 1 amphisbaenian, and 3 snake species for a total of 162 species. Sachavacayoc Centre and TRC had much greater increases in species richness because of limited former sampling at those sites. Thirtyeight anuran species, 1 turtle species, 7 lizard species, and 20 snake species, including 3 Micrurus species and Lachesis muta, augmented the SC list to 105 species. At TRC, 20 anuran species, 1 caecilian, 2 lizard species, and 15 snake species were added to the list for a total of 139 species. Interestingly, EA, the only site not to have been biologically investigated previously, has a currently known total of 109 species, even higher than SC, which had been subject to former investigations. Duellman and Salas (1991) published an annotated checklist of CA in which they discussed the species inventory, noting that certain species probably occurred at CA that had not been recorded. Based on more sampling, we may now evaluate their comments. They stated that three anuran species known to occur at Lago Sandoval (a lake slightly upriver and on the opposite bank from CA) should be found at CA. Of the three, Hyla geographica was found by us at CA. Duellman and Salas (1991) additionally stated that Micrurus spixii and B. bilineata should occur there. We captured

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M. spixii but not Bothriopsis. Because CA completely lacks bamboo, the preferred microhabitat of Bothriopsis (pers. obs.), we do not think that Bothriopsis occurs at CA. Duellman and Salas (1991) also compared CA with EI, Cocha Cashu, and Pakitza. They stated that it seemed likely that Bolitoglossa altamazonica, Agalychnis craspedopus, Phyllonastes myrmecoides, Ophryoessoides aculeatus, and Enyalioides palpebralis reach their southern limits at Parque Nacional Manu (which contains Cocha Cashu and Pakitza; Fig.1). Based on current data, each of those species is now known to range south to Tambopata. Bolitoglossa occurs at TRC; Agalychnis occurs at EI and TRC; Phyllonastes occurs at EI, SC, TRC, and Tambopata Jungle Lodge; Stenocercus (O.) aculeatus (see Avila-Pires [1995] for current taxonomy) occurs at EI and Bahuaja Inn; and E. palpebralis occurs at all ve PT sites. Rodrguez (1994a) also commented on the Tambopata herpetofauna, concentrating on EI and TRC. She noted that TRC has a higher richness of Eleutherodactylus than EI, an observation conrmed by our study. We recorded 12 species of Eleutherodactylus at TRC but only 7 at EA, 9 at CA, 7 at EI, and 7 at SC. When examining the abundance of Eleutherodactylus, the same pattern was apparent: at EA, 5.0 percent of the total number of individuals were Eleutherodactylus; at CA, 7.0 percent; at EI, 18.3 percent; and at SC, 18.1 percent; whereas at TRC, 38.0 percent of the total individuals captured during sampling were Eleutherodactylus. Additionally, Eleutherodactylus diversity was more even (0.588) at TRC than at other sites (0.1750.510). At the four other sites, one species (E. toftae at CA and SC; E. peruvianus at EA and EI) dominated; but at TRC, while E. toftae was most abundant, over 100 individuals of E. peruvianus and E. skydmainos were recorded, also with high numbers of E. altamazonicus and E. cruralis. We agree with Rodrguez (1994a) that the likely reason for the greater diversity and abundance of Eleutherodactylus at TRC is its higher elevation and proximity to the Andean foothills. Rodrguez (1994a) also poposed possible expla nations for the absence of Colostethus trilineatus (formerly listed as C. marchesianus) at TRC, claiming that an unknown microhabitat factor precluded its existence at TRC; however, we did capture this species at TRC, but at relatively low numbers. Rodrguez (1994a) also commented on the lack of small Hyla at TRC. On the contrary, we found many small species of Hyla, including H. koechlini, H. leali, H. punctata, and H. rhodopepla, previously

unrecorded at this site. Much of the disparity in sampling between Rodrguez (1994a) and Proyecto Tambopata may be attributed to differences in sampling period. As Rodrguez (1994a) pointed out, all the Conservation International sampling took place during a single dry season, the period during which observable anuran richness and abundance is low in southeastern Peru. When Rodrguez (1994b) discussed the rain forest sites from the CI expedition (EI, TRC, and Cerros del Tavara) plus CA and two Ro Manu sites, Pakitza and Cocha Cashu, she found apparent physiographic boundaries for some species. She suggested that Ro Madre de Dios is a barrier to dispersal for both E. perezi and Scarthyla goinorum (formerly listed as S. ostinodactyla; De la Riva 2000). Supporting this notion, during two years of continuous sampling we never encountered E. perezi at any of the Ro Tambopata sites. On the other hand, we did capture S. goinorum, often in high numbers, at all sites included in our study. Again, it appears that the short-term dry season rapid assessment was not able to record a representative sample of the herpetofauna at Tambopata. CONCLUSIONS. As an intensive study of such a large herpetofauna, this investigation has highlighted many patterns present in rain forest amphibian and reptile communities. Small-scale geographic differences appear to be important in shaping amphibian and reptile communities, as expressed by diversity and richness (Table 3), microhabitat types (Fig. 3), and differences in herpetofaunal composition in various forest types among sites. Herpetofaunal community structure is not dependent on only one or a small set of factors; many effects comprise the patterns demonstrated in this study. Data collected in this study suggest that the characteristics of a regional herpetofauna are not fully exposed when only one or few localities within a region are sampled. Unlike past studies that examined herpetofaunal communities, the current investigation examined ve communities in a small geographic area that have nearly identical climates. Therefore, it was possible to exclude the effects of large-scale habitat heterogeneity and evolutionary history of the organisms to view present-day microgeographic patterns of diversity and abundance. It is clear that herpetofaunal rain forest communities are not homogeneous entities, even on a ne scale such as that in this study. Large differences exist among local communities that appear to be caused by small-scale geographic features such as local hydrography, topography, soil types, and re-

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sulting forest types. In this study, we examined some of these differences to elucidate patterns caused by those factors. In doing so, we contribute a more representative sample and portray a more realistic heterogeneous view of the regional herpetofaunal diversity than has been previously reported. Although we provide total numbers of species per site, some error is involved in this because of unequal former sampling of sites. For analysis of richness, we used both species that we observed during PT plus those recorded by past researchers. Because EI and CA had been sampled extensively, those two sites had the highest overall richness and the other three sites were lower. Species lists for EI and CA are probably nearly complete. We feel condent that with additional sampling at the three other sites, their richness gures will increase to comparable levels. Additionally, as we state that Tambopata has the most diverse herpetofauna in the world, we must be aware that its status as such is likely only temporary. As demonstrated by the Tambopata species accumulation curves (Fig. 2), even more species remain to be discovered at these sites, demonstrating that short-term ecological studies of tropical herpetofauna probably do not capture the true picture of the herpetofaunal diversity. When other regions become more intensively studied, their known richness may increase to comparable levels.

Based on the results of our study, we suggest that future sampling of tropical herpetofaunas include multiple localities for each region studied in order to examine microgeographic patterns of relative abundance, species composition, and regional herpetofaunal diversity. Rapid assessment studies would benet by examining the species accumulation curves presented in this study (Fig. 2) and elsewhere. In this way, they may be able to gauge what proportion of the community they have actually sampled and estimate the proportion of species yet to be recorded. Such a practice would avoid the often-incomplete diversity sampling associated with rapid assessments. Overall, we suggest that future investigations should be of a long-term nature to determine the dynamics of the patterns that arose in this investigation in order to conduct valid population and community analyses.

ACKNOWLEDGMENTS
We thank Huw Lloyd, James I. Watling, Chris Kirkby, Aleyda Curo Miranda, Jose A. Ochoa Camara, and all of our many assistants for their help and support in the eld. We also thank Jacqueline Ramrez and Victor Velasquez Zea for assistance in obtaining permits. Todd A. Castoe, Jonathan A. Campbell, Walter Schargel, James I. Watling, Eric N. Smith, Ron Bonnet, Laurie J. Vitt, William E. Duellman, and Maureen A. Donnelly helped improve the manuscript. Marvalee Wake aided in caecilian identication. Funding was provided by the Percy Sladen Memorial Fund, the Tambopata Reserve Society (UK), the Grand Circle Foundation, the Lindeth Charitable Trust, the Albert Reckitt Trust, and the Anglo-Peruvian Society.

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APPENDIX 1. List of hepetofaunal species of Tambopata. An X signies that the species had been recorded by a previous investigation. PT signies the species was captured during Proyecto Tambopata. EA EcoAmazona; CA Cusco Amazonico; EI Explorers Inn; SC Sachavacayoc Centre; and TRC Tambopata Research Center. Taxon Anura Bufonidae Bufo glaberrimus B. marinus B. poeppigi B. typhonius complex Dendrophryniscus minutus Centrolenidae Centrolenella sp. Dendrobatidae Colostethus trilineatus Dendrobates biolat Epipedobates femoralis E. hahneli E. trivitattus Hylidae Agalychnis craspedopus Hemiphractus scutatus Hyla acreana H. allenorum H. boans H. brevifrons H. calcarata H. fasciata H. geographica H. granosa H. koechlini H. lanciformis H. leali H. leucophyllata H. marmorata H. minuta H. parviceps H. punctata H. rhodopepla H. riveroi H. rossalleni H. sarayacuensis H. schubarti H. trianguluma Osteocephalus leprieuri Osteocephalus sp. (pearsoni)b O. taurinus Phrynohyas coriacea P. venulosa Phyllomedusa atelopoides P. bicolor P. camba P. palliata P. tarsius P. tomopterna P. vaillanti Scarthyla goinorum Scinax chiquitana S. cruentomma S. garbei S. icterica S. pedromedinai S. rubra EA CA EI SC TRC

PT PT PT

X XPT XPT

XPT XPT X XPT XPT X

X XPT XPT XPT

XPT XPT X XPT PT

PT PT PT

XPT XPT XPT

XPT XPT XPT X XPT X

PT PT XPT

PT XPT XPT XPT XPT PT PT

PT PT PT PT PT PT PT PT

XPT XPT X X XPT PT XPT XPT X XPT X X XPT X X X

X X X XPT XPT XPT XPT XPT X XPT XPT X XPT XPT XPT XPT XPT PT XPT XPT XPT XPT XPT XPT XPT XPT PT XPT XPT X X PT XPT XPT XPT XPT

XPT XPT X PT PT PT PT PT PT PT PT XPT PT PT PT PT PT PT PT PT PT PT PT PT XPT

XPT XPT XPT X XPT PT X PT XPT XPT PT PT PT X XPT XPT XPT XPT XPT X X PT PT XPT PT PT XPT X X XPT

PT PT PT PT PT PT

XPT X XPT XPT X X XPT

PT PT PT PT PT PT PT PT

XPT X XPT X PT XPT XPT XPT XPT

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APPENDIX 1. Continued. Taxon Sphaenorhychus lacteus Leptodactylidae Adenomera andreaehylaedactylac Ceratophrys cornuta Edalorhina perezi Eleutherodactylus altamazonicus E. carvalhoi E. croceoinguinis E. cruralis E. diadematus E. fenestratus E. imitatrix E. lacrimosus E. martiae E. mendax E. ockendeni E. peruvianus E. skydmainos E. toftae E. ventrimarmoratus Ischnocnema quixensis Leptodactylus bolivianus L. didymusd L. fuscus L. knudseni L. leptodactyloidese L. pentadactylus L. petersiie L. rhodomystax L. rhodonotus Lithodytes lineatus Phyllonastes myrmecoides Physalaemus petersi Vanzolinius discodactylus Microhylidae Altigius alios Chiasmocleis bassleri C. ventrimaculata Ctenophryne geayi Elachistocleis bicolor Hamptophryne boliviana Pipidae Pipa pipa Pseudidae Pseudis paradoxa Ranidae Rana palmipes Caudata Plethodontidae Bolitoglossa altamazonica Gymnophiona Caeciliadae Caecilia sp. Siphonops annulatusf Testudinata Chelidae Phrynops geoffrianus P. gibbus Platemys platycephala EA PT PT PT PT PT PT PT PT PT PT PT PT PT PT PT PT PT PT PT PT PT PT PT PT PT XPT XPT XPT PT X XPT X XPT XPT XPT X XPT X XPT XPT XPT XPT XPT X X X XPT PT XPT XPT X XPT X PT PT PT XPT XPT PT PT PT XPT XPT XPT XPT XPT XPT X X XPT XPT XPT XPT X XPT PT XPT PT XPT PT XPT PT PT PT PT PT PT XPT PT PT X XPT XPT XPT XPT XPT XPT PT XPT X XPT XPT XPT PT XPT XPT XPT XPT CA XPT XPT XPT XPT XPT PT XPT XPT X EI XPT XPT XPT XPT X XPT XPT X XPT XPT PT PT PT PT XPT XPT XPT X XPT XPT X PT SC TRC

PT

X X

X X XPT

X X X

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APPENDIX 1. Continued. Taxon Kinosternidae Kinosternon scorpioides Pelomedusidae Podocnemis unilis Testudinidae Geochelone denticulata Crocodilia Alligatoridae Caiman crocodilius Melanosuchus niger Paleosuchus palpebrosus P. trigonatus SquamataSauria Gekkonidae Gonatodes hasemani G. humeralis Pseudogonatodes guianensis Thecadactylus rapicauda Gymnophthalmidae Alopoglossus angulatus Bachia dorbignyii B. trisanale Cercosaura ocellata Iphisa elegans Prionodactylus argulus P. eigenmanni Ptychoglossus brevifrontalis Hoplocercidae Enyalioides laticeps E. palpebralis Polychrotidae Anolis fuscoauratus A. nitens scypheusa A. ortonii A. punctatus Polychrus liogasterg Scincidae Mabuya nigropunctatag Teiidae Ameiva ameiva Dracaena guianensis Kentropyx altamazonica K. pelviceps Tupinambis teguixin Tropiduridae Stenocercus aculeatusg S. roseiventris Tropidurus plicag T. umbra ochrocollarisg Uracentron azureum U. aviceps SquamataAmphisbaenia Amphisbaenidae Amphisbaena albaf A. fuliginosaa SquamataSerpentes Aniliidae Anilius scytale EA CA X PT PT PT X XPT X X X PT XPT XPT XPT X X XPT X XPT XPT XPT XPT XPT XPT X X XPT PT X PT XPT XPT PT X XPT XPT XPT XPT XPT XPT X X XPT X PT X X X X XPT XPT X X XPT XPT XPT PT X PT PT XPT XPT XPT XPT EI SC TRC

PT PT PT PT PT PT PT PT PT PT PT PT PT PT PT PT PT PT PT PT

XPT X

XPT X X XPT XPT XPT PT PT XPT XPT XPT X X XPT X XPT XPT XPT XPT X XPT PT X X

XPT XPT PT PT XPT XPT XPT XPT XPT PT PT XPT PT

XPT XPT PT XPT XPT XPT X XPT XPT X XPT X

PT PT

X PT

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APPENDIX 1. Continued. Taxon Boidae Boa constrictor Corallus caninus C. hortulanus Epicrates cenchria Eunectes murinus Colubridae Atractus badiusa A. elaps A. ammigerus A. major Chironius carinatus C. exoletus C. fuscus C. multiventris C. scurrulus Clelia clelia Dendrophidion dendrophis Dipsas catesbyi D. indica D. variegata Drepanoides anomalus Drymarchon corais corais Drymobius rhombifer Drymoluber dichrous Enuilus sclateri Erythrolamprus aesculapii Helicops angulatus H. leopardinus H. polylepis Imantodes cenchoa I. lentiferus Leptodeira annulata Leptophis ahaetulla Liophis cobella L. reginae L. typhlus Ninia hudsonia Oxybelis aeneus O. fulgidus Oxyrhopus formosus O. melanogenys O. petola Philodryas viridissimus Pseudoboa coronata Pseudoeryx plicatilis Pseustes poecilonotus P. sulphureus Rhinobothryum lentiginosuma Siphlophis cervinus Spilotes pullatus Taeniophallus occipitalis Tantilla melanocephala Tripanurgos compressus Xenodon rhabdocephalus X. severus Xenopholis scalaris Xenoxybelis argenteusa X. boulengeri Elapidae Micrurus annellatus EA CA XPT PT PT PT PT PT PT PT PT PT PT PT PT PT PT PT PT PT PT PT PT XPT XPT X PT X X XPT X XPT X X XPT XPT XPT XPT XPT X XPT XPT XPT X XPT X XPT X X XPT X X PT PT PT XPT X XPT X XPT X X PT XPT X X X XPT PT X X X XPT XPT X XPT X XPT X X X X X X X X PT PT PT PT PT PT PT PT EI X XPT XPT XPT X PT X XPT X XPT XPT X PT X X XPT X X XPT X XPT X XPT X XPT X XPT XPT X PT PT PT PT PT PT SC TRC X X X XPT PT PT PT PT PT PT XPT XPT XPT PT X XPT XPT XPT XPT XPT X PT XPT XPT XPT PT PT PT PT

PT XPT X PT PT

PT

PT PT PT

PT

Herpetofauna of Tambopata, Peru

117

APPENDIX 1. Continued. Taxon M. lemniscatus helleri M. spixii obscurus M. surinamensis Leptotyphlopidae Leptotyphlops diaplocius Typhloplidae Typhlops reticulatus Viperidae Bothrops atrox Bothriopsis bilineata smaragdina Lachesis muta
a Range extension b Indentity of this c Identity of these

EA PT PT

CA XPT PT X X X X

EI PT X XPT

SC PT PT

TRC PT XPT PT

PT

XPT

XPT X XPT

XPT PT

XPT XPT XPT

reported in Doan and Arizabal (2000b). species is questionable and it may represent an undescribed species. two species is questionable and we could not distinguish them in the eld. We chose to consider them as one species until further work is completed (Angulo, pers. comm.). d We follow Heyer et al. (1996) in the taxonomy of this species. e We follow Heyer (1994) in the taxonomy of this species. f Only captured within the town of Puerto Maldonado. g We follow Avila-Pires (1995) for the taxonomy of this species.