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Volume 10 2004 No. 1
ECOTROPICA 10: 1–14, 2004 © Society for Tropical Ecology
MEASURING AND MONITORING AMPHIBIAN DIVERSITY IN TROPICAL FORESTS. I. AN EVALUATION OF METHODS WITH RECOMMENDATIONS FOR STANDARDIZATION
Mark-Oliver Rödel 1,2 & Raffael Ernst 2
University of Mainz, Institute of Zoology, Department of Ecology, Saarstrasse 21, D-55099 Mainz, Germany 2 Theodor-Boveri-Institute, Biocenter of the University, Department of Animal Ecology and Tropical Biology (Zoology III), Am Hubland, D-97074 Würzburg, Germany
Abstract : The need for standardization of field methods within and across studies has been recognized by the majority of ecologists throughout the world. However, comparable studies based on a standardized protocol are still scarce. We provide a guideline for effectively sampling and monitoring tropical forest amphibians and give recommendations for standardization. Based on a four-year study on amphibians in Taï National Park, Côte d’Ivoire, we evaluate commonly used techniques, and offer a catalogue of efficient techniques, along with suggestions for improvement of particular methods, with regard to study objectives and specific amphibian guilds. For simple short-term surveys we recommend visual and acoustic encounter surveys, accompanied by opportunistic trapping. The transect design introduced here proved to be most adequate for representative sampling and appeared to be appropriate for most studies that involve multivariate data. It is especially useful for long-term studies. Transects furthermore provide an effective method of investigating at least leaf litter frogs, not only at their breeding sites but also throughout the whole range of habitats used by them, thus generating a much more complete picture of an amphibian community than is possible with other methods. Accepted 4 February 2004. Key words : Tropical amphibian monitoring, standardization, method evaluation, Taï National Park, West Africa.
In theory there is no disagreement about the necessity to standardize ecological field methods and data acquisition in order to guarantee comparability between different studies, as well as to enhance the power of predictions resulting therefrom. The need for standardization of techniques across and within studies has continuously been emphasized by several authors (e.g., Heyer et al. 1994, Adis et al. 1998). Those who are involved in community ecological field research know well that this is a crucial factor when it comes to generalizing results in order to make them
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accessible to those who urgently need scientific guidelines to back up their practical efforts. This becomes especially important when looking at phenomena such as the well known world-wide amphibian decline, which seems to have affected even populations in pristine habitats and continues to affect or even wipe out whole populations with terrifying rapidity (Houlahan et al. 2000, Kiesecker et al. 2001, Pounds 2001). In these cases synergistic efforts are urgently needed, calling for unified methods and data output (Alford & Richards 1999, Parris 1999, DAPTF 2002). However, in reality there still is a lack of studies that can be compared without reservations, especially studies that were conducted in different parts of the world, although precisely this kind of comparison is 1
All evaluations and recommendations are based on a study of tropical amphibian assemblages conducted over four years (1999–2002) in Taï National Park. More detailed descriptions of TNP are provided by Rompaey (1993). such as standard plot sampling (Allmon 1991. b. Poynton 1999). 6°47’-7°25’W). Every subunit was marked with numbered colored flag-tape. We avoided extensive cutting and thus manipulation of important habitat features. Lawson 1986. Whereas quadrat sampling can be used to determine the species present in a homogenous area. Parts of the habitats on the park’s periphery were subject to more or less intense logging and cultivation until 1998 (P. Parren & de Graaf 1995. also for para-ecologists. data: Taï Monkey Project). four in secondary forest). Precipitation is distributed across two more or less distinct periods. The mean annual temperature is about 25° C (Rompaey 1993). It can be characterized as humid tropic seasonal (Riezebos et al. as well as their relative abundances and densities. The second. The starting coordinate for each transect always marked the southeast corner to ensure identical geographic orientation between sampling units. Our study sites are either pristine forest areas or have not been logged or cultivated since 1978. Richards 1996). Africa: Howell 2002) reflect this need. and unpubl.3 km. The maximum distance between transects was 6. 5°50’N. The intention of this paper is thus to provide a guideline to choosing effective and comparable methods for the monitoring of tropical forest amphibian assemblages in general. 2001) were a priori excluded from testing. TNP is the largest remaining protected area of rain forest in West Africa. and iv) has a low environmental impact. The minimum distance between adjacent transects was 200 m. We aim to present a methodology that i) provides quantitative and qualitative data useful for rapid surveys as well as long-term monitoring programs. Given the lack of time for the development of effective conservation programs. that ii) is easy to handle. Each had a north-south extension of 200 m and an east-west extension of 100 m. TNP is part of the Upper Guinea forest block. transect sampling can provide similar data across habitat or dis- MATERIAL AND METHODS Study site The study was conducted in Taï National Park (TNP). The first. The rectangular transect design is a combination of two widely used standard techniques. Floristically the TNP belongs to the Guinean-Congo-Region (Guillaumet 1967. The core dry season lasts from November until February/March. Doan 2003) or total removal plots (Barbault & Trefaut Rodrigues 1978. PACPNT 2000). that stretches west of the Dahomey Gap from Ghana into Sierra Leone and Guinea (Schiøtz 1967. standardization of methods that yield broad-scale comparative data is now needed more than ever. Thus widely used techniques. 2001. consists of a series of small squares (quadrats) that are laid out at randomly selected sites within a habitat then thoroughly searched for amphibians. 1994. Riezebos et al. known as transect sampling. Côte d’Ivoire. The major rainy season stretches from September to October. Selection of sites and design of sampling units We chose sites within existing macrohabitats (primary/ secondary forest) to establish a total of ten rectangular transects (six in primary forest.RÖDEL & ERNST essential for academic and practical purposes alike. A number of recently published regional field monitoring manuals for amphibian surveys (Latin America: Lips et al. as they may result in severe disturbance to the system under investigation. Formenty pers. 1979a. Transect paths were kept open so that walking at a constant speed was possible at all times. Transects were arranged in pairs. map “Projet OMS Forêt de Taï”). We report on our experiences with already existing methods and with methods that we thought needed modifications to enhance their effectiveness and to enable the use of new statistical analysis methods. on the basis of our experience in the field as well as with consecutive data analyses. situated in western Côte d’Ivoire (5°08’6°07’N. Daily tempe2 . proved to be most effective for forest amphibians. Vonesh 2001. comm. thus ensuring that all habitat types of a certain area within the very inhomogeneous forest were covered. Rodda et al. Our study site was located 23 km southeast of the small town of Taï and comprised about 30 km2 of primary and secondary rain forest around the Station de Recherche en Ecologie de Taï (SRET. A minor rainy season lasts from March/April to July. uses linear transects instead of squares. ratures vary between 20 and 33° C. known as quadrat sampling (plot design). We thereby evaluated several methods that are already commonly used and present a set of techniques that. 7°20’W). Mean annual precipitation in the study area was 1806 mm during 1988–2002 (± 297mm. (1994) and PACPNT (2000). iii) is efficient concerning time and money. followed by a short dry season in July/August. For data acquisition the complete transect length of 600 m was subdivided in 25 m subunits (24 subunits/transect).
for comparison of local with regional species pools).5 2 2. secondary forests. thereby recording all amphibians within a distance of 100 cm from either side of the path. and to investigate correlations of species assemblages with environmental variables.AMPHIBIAN MONITORING IN TROPICAL FORESTS turbance gradients (Jaeger 1994. Sampling methods and sampling effort Habitat characterization. surface and depth. We assumed that the number of plants with small dbh is greater in degraded. the vegetation of all 25 m segments within a distance of about 100 cm left and right of the transect was recorded by counting the number of plants belonging to a certain category (diameter at breast height. Specimens heard but not seen within this distance were not searched for and not included in the SVTS data sets (see below). thus providing data that are useful to test for sex. In addition to species identity we recorded sex and snout-vent-length (SVL) of every individual. Categories of habitat variables measured on transects. Standardized visual transect sampling (SVTS). Repeated controls of identical transects on consecutive days were avoided to ensure independence of samples. In addition.. lower tree stratum: 3–10 m.5 3 3. every aquatic habitat (lentic and lotic) located at a maximum distance of 25 m from either side of the transect was recorded with respect to type. For a discussion of the advantages of rectangular sample units over quadratic or circular ones see Krebs (1989) and McCune & Grace (2002). divided into seven categories corresponding to particular densities. definition category 1 1.5 m. A simplified method originally developed by Braun-Blanquet (1964) for determination of vegetation coverage in vegetation analyses was used to estimate the percentage of leaf litter coverage. Usually four to six transects per day were sampled during daytime.5 m).or downscaling data without neglecting local habitat diversity (e.30–0. both in time and space. Pearman 1997). Sampling was interrupted for the duration of the recording in order not to overestimate locations in which animals had previously been captured. Transects were intensively patrolled at a constant speed (0. To assess habitat preferences of particular species (e. Sampling was performed independent of prevailing weather conditions. In order to quantify the availability of potential aquatic breeding sites. bush and shrub stratum: 0.or age-specific differences in habitat use. Definitions of habitat variables are summarized in Table 1. To avoid duplicate recordings.5–1. dbh = diameter of plants at breast height. substrate moisture was determined in four categories during every transect walk. whereas primary for- ests show increasing numbers of plants of larger dbh (Chatelain et al. we characterized all habitats using several variables that were recorded at two defined points within each 25 m subunit (beginning and midpoint). captured frogs were marked by TABLE 1. Additionally. Jaeger & Inger 1994). rectangular ones provide the possibility of easily up.g. Compared to linear transects. vegetation density was measured in four strata (see text). A maximum of four transects was patrolled at night. Edaphic parameters were registered as general substrate types according to Lieberoth (1982).5 4 5 6 7 vegetation density absent transition gaps predominating transition closed areas predominating transition closed substrate types forest soil arenaceous forest soil loamy soil arenaceous soil sabulose soil muddy soil swampy soil dbh [cm] 0–5 6–10 11–20 21–50 > 50 leaf cover (%) 0–20 21–40 41–60 61–80 81–100 3 .g. As far as possible all individuals were captured.. to assign them to particular guilds).35 m/s). understory: < 0. dbh). These parameters included vegetation density in four strata (canopy: > 20 m. 1996.
Anurans that are strong jumpers (e. The resulting data are expressed in numbers of individuals of a certain species found in an area per unit time. this behavior can be exploited for acoustic monitoring. may be underestimated when exclusively using visual techniques. Calls from greater distances cannot be unambiguously identified and the chance of duplicate recordings in neighboring segments increases.g. In the transect corners. We used these methods continuously in all habitats of the study area including the transect areas.g. Audio strip transects represent a commonly used method for acoustic monitoring (Zimmerman 1994). other than sex and species. 12 and 20). Coding schemes used for individual recognition were not applied. Furthermore. this technique allows the detecting of cryptic species that. habitat analyses can be based on data obtained from the general habitat characterization for single transects or segments. Removal of additional toes may decrease the recapture rate of marked individuals by more than 6 –18 % for each additional toe removed after the first (Parris & McCarthy 2001). As opposed to visual sampling. At capturing sites a thorough description of the microhabitat was recorded.5 4 hours of transect sampling. For practical reasons “man-hours” can be used. VES can only provide information on the presence or absence of a species in an area but are inadequate for determining abundances. keeping the transect routine identical for both techniques. Trapping with pitfall or funnel traps along drift fences. For both SVTS and SATS. This technique has been formalized as the time-constrained technique of Campbell & Christman (1982). beginning with segment 1: segment 1. Henle et al. An area or habitat is searched systematically for individuals in a defined time period. data can be expressed in numbers of individuals per time and surface units. Visual (VES) and acoustic (AES) encounter surveys. Thus. Individuals below nine mm SVL were not marked due to their small size. species composition. only calls coming from the right-hand side in the first segments were registered (i. which can be adjusted to the complexity of the habitats being sampled. In concordance with these authors the methods were only used as a qualitative or semi-quantitative tool within the scope of our studies.. According to Corn & Bury (1990). It can be used to determine the species richness of an area and the species composition of a local assemblage.. 1994.. VES and AES thus could be used to evaluate if the randomly chosen transects represented the regional species pool. following the characterization routine used for general habitat description. 8. Drift fences consisted of durable green plastic gauze.and AES-effort was kept comparable to the time spent on SVTS and SATS surveys throughout the entire study period.5 m to either side of the transect was defined. 1997). Standardized acoustic transect sampling (SATS). Due to the simplicity of the method. and to estimate relative abundances of species within an assemblage (Crump & Scott 1994). Bufo species).5 m high and stapled vertically onto wooden stakes. Likewise microhabitat description was not always possible. VES and AES are frequently used for rapid assessments and the evaluation of larger areas.RÖDEL & ERNST toe clipping (Donnelly et al. 0. This device is useful to determine species richness of epigaeic organisms (Corn 1994). Total VES. Pitfall traps with drift fences were installed in two of the primary forest transects from March to April 1999. Throughout transect walks a combination of visual and acoustic techniques was applied at all times. and as the time-constrained searches of Corn & Bury (1990). Counts can be used to estimate relative abundance of calling males. The width of the acoustic transect depends on the ability to detect each species’ advertisement call. Capture success may vary greatly between species (Corn & Bury 1990. In those cases. thus creating 25 m x 25 m acoustic sampling plots. as well as breeding habitat use and breeding phenology of species (Zimmerman 1994). Recaptures were excluded from the analyses.e. Dodd 1991). Since in the majority of frog species males use species-specific calls to advertise their position to potential mates and rivals (Wells 1977). This corresponds to 765 transect walks. Ptychadena species) are more difficult to trap than terrestrial species that lack these abilities (e. For that reason a maximum recording distance of 12. and additionally in only one of these transects from January 2001 to September 2002. during SATS it was often impossible to determine individual parameters. From February 1999 to December 2000 we compiled 382. individual marking should be restricted to studies in which individual recognition is indispensable. An array of fences and traps consisted of a central trap (buckets: . despite their potential abundance. and also for evaluating if species that are rarely found on a transect belong to a particular local species pool or represent single migrating specimens that have habitat preferences not covered by the transects.
In addition. Each segment was tightened around a plastic bucket with an opening angle of 45°. Branch & Rödel 2003). The data from pitfall and funnel traps can be expressed as number of individuals per trap-day. TC = species recorded during transect walks (SVTS and SATS combined). Additionally. we applied that method during a herpetological survey of the Haute Dodo and Cavally forests. 5 Ta ïF . FIG. unpubl.AMPHIBIAN MONITORING IN TROPICAL FORESTS 275 mm deep. Funnel traps summed to a total of 384 trap-days. results were analyzed for leaf litter. which are situated south and west of TNP respectively (Rödel & Branch 2002. 1. fossorial and aquatic species independent of families. They were checked at least every morning. In the course of this study. 285 mm top diameter. Hillers et al. Data from each sampling method were compared with each other and to a list of species records that we gathered through January 1999 to September 2002 for the forest parts of the SRET region (Appendix 1). Number of species per family recorded using different sampling methods. AES/VES = visual and acoustic encounter surveys (only species that have been recorded in forest habitats around SRET station). SVTS = species recorded during visual transect walks. arboreal. funnel traps (see Branch & Rödel 2003) were installed in a primary forest transect from 18 to 27 September 2002. Pitfall trapping time summed to a total of approximately 4000 trap-days. and in a forest fragment (Paulé-Oula 2) outside TNP from 30 August to 12 September 2002 (A. Numbers above bars represent total number of species recorded with the respective method. The ends of each segment were flanked with additional plastic buckets. using a particular sampling method. one on either side. Trap = pitfall and funnel traps. Duct tape was used to reduce the diameter of the buckets and construct funnel-like openings in order to impede escaping from traps. data). Traps were checked at least on a daily basis. SATS = species recorded during acoustic transect walks. 220 mm bottom diameter) and two triangular fence segments (total length 16 m). as sampling success and efficiency may vary with regard to the particular biology of a species. Sampling success is referred to as number of species within families recorded. TaïF = all species recorded with all methods in forest habitats around SRET station..
fusciventris. P. nienokouensis.. bibroni. P. see Appendix 1). Ptychadena pumilio. Hoplobatrachus occipitalis. annulatus) were exclusively recorded during transect walks.) were recorded exclusively outside forest habitats (e. H.g. Appendix 1). Rödel & Ernst 2000. 56 amphibian species are known to occur in TNP (Schiøtz 1967. During transect sampling (SVTS. Taking all methods into account. Effectiveness in detecting species within given families differed significantly between methods (Friedman test. two species were each listed in two guilds (compare Appendix). 1. Failure to detect particular species in this region was most probably due to their general scarcity (e.g. TC. B. thus making overall sampling success very high (Tab. rather than actual sampling method insufficiency. N = 10. Perret 1988. RESULTS In total. χ2 = 19.7 %) of nine families.g. Sampling efficiency in families containing higher numbers of genera and/or species was only marginally lower. .0 % of TaïF) in eight families. 2002. sp. 1. compare Appendix 1). SATS. regularis. Number of species per amphibian guild recorded using different sampling methods. Seven species (Bufo maculatus.. Phrynobatrachus calcaratus. H. Phlyctimantis boulengeri ). Two fossorial species were exclusively detected either with VES and pitfall traps (Hemisus sp. p = 0. VES/AES revealed 39 forest species (90. Sampling success and data quality varied between different methods.002. P.RÖDEL & ERNST FIG. 2)..3 % of TNP species). Hyperolius guttulatus). Rödel et al.199.2 %) were recorded with pitfall and funnel trapping. Using all methods we recorded 50 species in the region of the SRET (89. For abbreviations see Fig. 2. tested for TaïF. Ten species (23. Four arboreal frogs were exclusively recorded with these methods (Hyperolius picturatus. df = 5. SVTS. and P. AES/VES. Trap). mascareniensis. SATS) we recorded a total of 15007 individual amphibians belonging to 37 species (86. Numbers above bars represent total number of species recorded with the respective method. Phrynobatrachus fraterculus. 43 species were recorded in forest habitats within the study region (Fig. Bufo superciliaris) or simply absence in the area under investigation (e. 2. Rödel 2000. 1. and between different amphibian families or guilds (Figs. Families containing only 6 a few species in the TNP area showed the highest recording rates. clearing around SRET) and thus ignored in the analysis.) or pitfalls only (Geotrypetes seraphini). 2003. Three leaf litter species (Amnirana occidentalis.
AMPHIBIAN MONITORING IN TROPICAL FORESTS TABLE 2.0 100. A distance of 1 m (visual) and 12.7 0. With the exception of Acanthixalus sonjae. but that concerned mostly single specimens.5 m (acoustic) proved to work equally well in all habitats investigated.0 80.0 SVTS 0.0 100.47 specimens per trap-day in contrast to 0.0 100. Family / guild Caecilidae Pipidae Bufonidae Hemisotidae Ranidae Petropedetidae Astylosternidae Arthroleptidae Hyperoliidae Rhacophoridae leaf litter arboreal fossorial aquatic TaïF 1 1 2 1 5 11 1 3 17 1 22 18 2 3 TC 0.0 Trap 100.0 100.0 66. df = 4.0 100.7 % of recorded arboreal species). tested for TaïF. Schaich & Hamerle post hoc multiple comparisons revealed no significant differences between methods at α = 0. Most specimens were captured with funnel traps (0. VES/AES.0 0.0 100.0 100.7 0.0 AES/VES 0.0 100.0 76.0 100.4 0. VES and AES revealed highest species numbers.03 specimens per trap-day in pitfall traps).0 72.7 100. neither between given family or guild.2 66.0 64. In contrast.0 100.0 100.7 100. nocturnal leaf litter frogs (arthloeptids.5 100.0 100..05.0 100. this was most probably due to the small overall sample size and high heterogeneity of species numbers in families and guilds (Bortz et al.4 100.0 0. Quantification of these data.0 0. In Haute Dodo and Cavally forests we captured 38 % of the recorded amphibian species (16 of 42) with a combination of pitfall and funnel traps.294.8 0. For other abbreviations see text and Fig. when being a part of the transect line itself.8 0.0 0.0 100. Most arboreal frogs could be recorded with SVTS.0 50.0 100. All other species were recorded with VES/AES (Rödel & Branch 2002.0 100.0 100.0 76. SVTS.) vegetation density.0 100.8 100.067. asytlosternids) were best recorded with SATS. all were recorded using other methods as well.0 40.0 100. TC.0 100. 1990). Diurnal ground-dwelling frogs were best recorded quantitatively using SVTS.3 We could not detect a statistical difference in sampling efficiency between different amphibian guilds using the methods employed (Friedman test. χ2 = 10. However.8 0.g.0 36. Reference is the number of species that were recorded using all methods in forested habitats around the SRET station (TaïF).0 86.0 0.0 SATS 0. Branch & Rödel 2003).0 100. unpubl. As in TNP. As aquatic sites were only taken into account. data). Percentage of species within an amphibian family or guild that were recorded using a particular method.0 100. We only captured a few leaf litter frogs.0 77. Trapping success was highest in leaf litter frogs (56.0 50.0 100.0 100. other than based on time units.0 68.0 81. which is mute. The traps proved to be inadequate in qualitative and quantitative sampling since even small species such as Phrynobatrachus villiersi (SVL: 10–15 mm) managed to escape regularly (several direct observations). In TNP funnel traps were ineffective. 1.0 0. the fossorial Geotrypetes seraphini was recorded with pitfall traps only. presence and abundance of purely aquatic species and tadpoles of all species were underestimated with all methods used here. 7 .0 100.0 100. Trap).0 31. N = 4. but very low in arboreal species (6. quantitative data for all arboreal species were best assembled with SATS. in a primary forest transect with none in the forest fragment (Hillers et al. was difficult as detectability of species varied considerably with (e.0 0.0 100. Likewise.0 33.0 77.5 % of recorded leaf litter frogs). transect walks made it possible to search for amphibians in a very comparative way.5 100. p = 0. SATS. No additional species were detected with funnel traps.0 0.
a combination of SVTS and SATS. Although the combination of AES and VES provided an adequate approximation to real conditions (see also Doan 2003). However. or Phrynobatrachus alticola. ii: specific aims. However. Simple presence/absence data of aquatic species and stages can best be gathered by direct observation (surfacing individuals) and with dip-netting. Rödel et al. VES and AES yielded highest species numbers. We found no additional species and only very few specimens by funnel trapping. According to Pearman et al. In this study this has been done by determining relative species richness with reference to families or guilds. The methods VES and AES in combination with pitfall traps with drift fences were useful in sampling additional. When including relative abundance measurements these methods were insufficient. iii: efficiency. pitfall traps and drift fences . Methods of collecting quantitative data for aquatic amphibians and for tadpole assemblages have been described by Shaffer et al. Cardioglossa leucomystax. determined by using a particular sampling method. SVTS was generally the best method for detecting diurnal leaf litter frogs. species not encountered during transect sampling.g. (1997) and Rödel (1998a). in order to sample particularly secretive leaf litter species. Some taxa. Semlitsch et al. such as the very abundant Arthroleptis sp. as an adequate measure. Thus even time-based quantification of these data is questionable. e. The percentage of species within supraspecific taxonomic units. Pitfall trapping was only useful in detecting fossorial species that were not encountered during transect walks. which are mute (Drewes 1984.. such as species of the genus Acanthixalus. Although widely used and recommended. Olson et al. Therefore transect sampling can be considered to be the method of choice when sampling leaf litter anurans. They suggest using relative species richness within taxonomic entities. whereas visual sampling appeared to be superior to acoustic sampling. Standard plot sampling and total removal plots were not tested. 1996). The combined transect sampling methods provided a close approximation to the real presence and abundance of species. but is certainly just as well suited for the investigation of tropical anuran assemblages in general. these methods do not seem to sample a given fauna adequately well (Allmon 1991.. genera or families. especially arboreal and fossorial. and will likewise hold true for other arboreal anurans throughout the tropics. In general SATS was very efficient in detecting nocturnal leaf litter frogs and treefrogs but less successful in detecting diurnal leaf litter frogs. We found it impossible to quantify VES and AES other than in relation to time. Doan 2003).g. We found it more realistic to apply a (clearly subjective) measure for habitat complexity on which to base collection effort during VES/AES.RÖDEL & ERNST DISCUSSION Choice of methods should reflect the best compromise between i: practicability. were nearly as successful in detecting species. spending more time in complex. inaccessible areas than in areas that are easy to monitor. Schiøtz 1999. such as species groups. such as the Hylidae. Compiling data on presence and abundance of aquatic species and tadpoles was outside the scope of this study and these species and stages were inadequately sampled with all methods used here. Whereas transect walks provide the possibility of monitoring amphibians in a very comparative way. (1994). 2003). but appear not to be appropriate when standardized quantitative sampling is required. This was also true for most of the arboreal species belonging to the families Hyperoliidae and Rhacophoridae.2. Rödel & Ernst 2003). data acquisition varies considerably depending on habitat type in VES and even AES. Migrating pipid frogs can also be easily recorded with pitfall and funnel traps. especially in long-term field studies within temperate regions (e. as well as SVTS alone. and iv: environmental impact. In addition.1. The differences in efficiency of visual versus acoustic sampling varied between taxa. and failed to detect aquatic and fossorial species. Arthroleptis sp. (1995) a simple comparison of species numbers may not be sufficient to evaluate the efficiency of different sampling methods. can then be compared to the real conditions in an area or habitat. VES and AES are useful tools for the compilation of species inventory lists. Bury & Corn 1987. Vonesh 2001. Nonetheless. as they impose a severe disturbance on the system under investigation and thus were not suitable to our goals. this only holds true if species numbers alone are considered. acoustic sampling appeared to be indispensable since these species were more readily detected by their calls than 8 by sight. The advantage of transect sampling was especially obvious when focusing on leaf litter species. Rödel 2003. during rapid assessment surveys (for recent West African examples see Rödel & Branch 2002. The methods tested within this study proved to perform with varying degrees of efficiency. could be detected exclusively using visual sampling methods.
If the investigation is interrupted for some time. the fossorial Hemisus perreti and the aquatic Silurana epitropicalis. Traps have to be checked at least daily. traps have to be uninstalled or closed and reopened when starting again. if not on amphibians then on other organisms. SVTS and SATS provided data on species and habitats und thus may reveal changes in composition and species abundance. (2004) had high trapping success with pitfalls in Gabon when considering numbers of individuals. However only two species. e. Parris 1999. Thus data should be gathered throughout a whole season to obtain a thorough knowledge of the local fauna. Doan 2003). as trapping success per trap per time unit. Data can be used for comparisons between habitats. However. Rodda et al. none of them uniquely found by this method. VES and AES are less time consuming.) that leopard (Panthera pardus) tracks TABLE 3. Transects will have an environmental impact. be quantified in relation to time. It is advisable to perform them randomly independent of prevailing weather conditions. With the exceptions of aquatic and fossorial species they pro- vided data that cover the whole community very well. In our experience. this method cannot be recommended for standardized sampling of tropical anurans. Theoretically it might well be that trapping will result in dislocating at least some species from the area where traps have been established.g.. The impact of traps and drift fences was difficult to judge. however. Burger et al. When considering the relatively high costs and time investment due to the high level of maintenance required (Parris 1999). Donnelly et al. However trapping success depends very much on choice of site.6 % of all individuals captured with this method. the frequency of sampling can be reduced when general phenological traits of the species recorded have been clarified.AMPHIBIAN MONITORING IN TROPICAL FORESTS proved to be the least effective method. A comparison of trapping data with data other than those of the observer in question seems to be difficult. (2001) report on similar experiences using this method in a herpetological survey in Guyana. 2001. experience of investigator and prevailing weather conditions (see Branch & Rödel 2003). We observed (e. Transect walks are time intensive. seasons and years.g. QS/TR = quadrat sampling/total removal sampling (data from Allmon 1991. Effectiveness of methodology in regard to type of data required. Costs with regard to time spent for data acquisition was highest in trapping and in transect walks. accounted for 72. SVTS and SATS have been proven to be the only methods that provided quantitative data on forest amphibians with regard to space and time. generalization of data with regard to phenology or abundances is less possible. amphibian guild and environmental impact. in theory. Vonesh 2001. 1. They collected only six species (out of a total of 132 species of amphibians and reptiles being recorded). for other abbreviations see text and Fig. as well as environmental changes. Data from both trapping methods can. VES and AES had probably the lowest environmental impact. TC leaf litter frogs arboreal frogs fossorial amphibians aquatic frogs qualitative data quantitative data environmental impact costs (time) costs (material) utility (ecology) utility (conservation) +++ ++ – +++ +++ +++ low high low very high very high SVTS +++ ++ – +++ +++ ++ low high low high high SATS ++ ++ – – +++ ++ low high low high high AES/VES +++ +++ + +++ + + very low low very low low high Trap + – +++ + + – medium very high low very low low QS/TR +++ – – – +++ +++ very high high low very low low 9 . one should test the efficiency at a particular site in advance before installing these traps on a broad scale. in consecutive field seasons.
Canopy fogging of an overstory tree – recommendations for standardization. Barbault.. 1990. & M. Part II: Trapping results and reptiles. Department of the Interior.. Linsenmair. R. Gbamlin. Ouoro provided invaluable help during fieldwork.): Measuring and monitoring biological diversity.. Gabon: Species turnover along an elevational gradient. and the “Taï Monkey Project” provided logistic support.. Lips et al. However. Boehnke. Ecol. Berlin a.R. The presented transect design proved to be adequate for representative sampling and appeared to be appropriate for most studies involving multivariate structure data.. 5: 37–53.P. & K. Brazil.W.D. (eds. For simple short-term surveys we recommend VES and AES.Y. R.R. Spichiger. Foster. Christman. and C. and B. The access permit to TNP was issued by the “Ministère de la Construction et de l’Environnement. & R. 20: 64–77. Floren.. Trefaut Rodrigues. 1997. 1987.C. Chatelain. 193–200 in Scott.A. Alford. 2004. REFERENCES Adis.. Braun-Blanquet. T. Branch.M. W. & S. P. Branch. Acad. 1964. M. McDiarmid.): Herpetological communities. & M. 1998. Springer Verlag.A. 1991. Central Amazon. 01 LC0017). Campbell. & K. Ecol.. 3. Observations sur la reproduction et la dynamique des populations de quelques anoures tropicaux I. 939 pp.1964. Gautier. Channing. (ed. Pflanzensoziologie. Straight-line drift fences and pitfall traps. Calif. Trop. Salamandra 39: 91–110. Allmon. & M. & A. P. Pp. 2 ed. Ecol. J. Observations sur la reproduction et la dynamique des populations de quelques anoures tropicaux IV. W. N. J. G.A.W.. J. Phrynobatrachus accraensis. Hammond.. noire. 865 pp. Sci... Observations sur la reproduction et la dynamique des populations de quelques anoures tropicaux III. Barbault. Hofer. in the worst case. TROPENBOS . Glos. Syst..-O. 10 . 1996. Wildlife Research Report 13. 1994. Burger. Springer Verlag. Standard methods for amphibians. Olson et al. A. Trefaut Rodrigues. Bortz. Ptychadena maccarthyensis et Ptychadena oxyrhynchus.-A. possibly accompanied by opportunistic trapping.S. 1979b.” G.Côte d’Ivoire helped with transportation. Furthermore transects provide an effective method of investigating leaf litter frogs in particular. Various administrative services and lodging facilities in TNP were provided by the “Centre de Recherche en Ecologie” and the “Projet Autonome pour la Conservation du Parc National de Taï. Verteilungsfreie Methoden der Biostatistik.B. U. Arthroleptis poecilonotus. All this support is gratefully acknowledged. Corn. western Ivory Coast. Field techniques for herpetofaunal community analysis. Trefaut Rodrigues.. M.S. 30: 133–165. Bull. The “Projet Autonome pour la Conservation du Parc National de Taï”. Ecotropica 4: 93–97. Jr. Research permission was given by the “Ministère de l’Enseignement Supérieur et de la Recherche Scientifique. A recent history of forest fragmentation in southwestern Ivory Coast. Sér. Y.S. W.” Working in TNP was kindly permitted by the Commandant K. R. Evaluation of pitfall trapping in northwestern forests: trap arrays with drift fences. U. 1999. 1978. N’Dri. Advantages and disadvantages of different methods are summarized in Tab. Corn.o. R. 2003. Terre Vie 32: 441–452. for specific questions (cf.. consequent long-term effects on forest structure. Rödel.J. J. L.. A plot study of forest floor litter frogs. C. Afr. A 41: 417–428.R. J. R. J. 7: 503–522.. Biodiv. Transect cutting and the use of transects should therefore be done with the necessary precautions.. ACKNOWLEDGMENTS This study is part of the BIOLOG-program of the German Ministry of Education and Science (BMBF. 2003) transects should be supplemented by specifically investigating aquatic breeding sites with the appropriate set of standardized techniques (Heyer et al.” of the Republic of Ivory Coast. Ann. Halliday. not only on their breeding sites but throughout the whole range of habitats used by them. This might affect densities of other mammals including possible seed dispersers with. Hillcoat provided valuable comments on the manuscript. & M.. Rev.. 109–117 in Heyer. & P. Herpetological survey of the Haute Dodo and Cavally forests. Bury. Wien.S. Inst. fond. Wildlife Management 51: 112–119. Donnelly.. 1994. & M. Rödel 1998a). Pp. H. a well visible path becomes established that at least in primary forests remains so for years.. & S. Memoir 28: 145–186. Hayek.G. W. Washington & London. Lienert. After using transects intensively for some time. Project W08 BIOTA-West.J. thus generating a much more complete picture of an amphibian community than is possible with other methods. L.. Smithsonian Institution Press. Grundzüge der Vegetationskunde. Global amphibian declines: a problem in applied ecology. 1979a. Trop. 364 pp. Basset. R. Richards. Barbault. Conserv. 1982. Amphibians and reptiles of Monts Doudou.RÖDEL & ERNST were more often seen on the transect path than in undisturbed forest. SVTS and SATS are especially useful for long-term studies.E. Fish and Wildlife Service 13.
17–44 in Davis. & R. Nature 410: 681–684.. Which methods are most effective for surveying rain forest herpetofauna? J..S. Henle.cnah. J. Grace. 2001.S. Reaser. http://www. Donnelly.R.A. L.P. A.F. The quest for natural forest management in Ghana. 654 pp.C. Parris. John Willey & Sons Chichester. Velasco. Standard methods for amphibians. 277–284 in Heyer. (eds.): Measuring and monitoring biological diversity. R. Kuzmin. R. New York. Ecological Methodology. & C.R. I.B. Harper Collins Publishers. Sampling amphibians in lentic habitats. McCune.E. Herpetol.A. & R. Entstehung. de Graaf.. Hayek...B.. Oxford.. Ibáñez. 1986.R. Analysis of ecological communities.): Measuring and monitoring biological diversity. Heyer.. B. Aufbau.. + 15 plates. 378 pp.W. 364 pp. Jaeger.. 364 pp.K.C. 2000.. Conserv. Côte d’Ivoire and Liberia. J. R. Nature 404: 752–755. A phylogenetic analysis of the Hyperoliidae (Anura): Treefrogs of Africa.. Doan. Conserv. Measuring and monitoring biological diversity.T. R. M.): Measuring and monitoring biological diversity.C.. & M. Foster (eds. Drewes. General Technical Report. B. Washington & London. 320 pp. McCarthy. Ecological traits predicting amphibian population declines in Central America. 1994..W. 1997. M. M.W.R. 1994.): Naturschutzrelevante Methoden der Feldherpetologie. L.. C. Washington & London. 11: 1211–1225. 18 pp.-A. 20 247 pp. McDiarmid. Pap.. Juterbock. 2003. 134 pp. K. Kuhn. 1994. Podloucky. Reeve.o. Kennzeichnung und Eigenschaften der landwirtschaftlich genutzten Böden der DDR.M. Quantitative evidence for global amphibian population declines. Belden.B.pdf Donnelly.org/ch/ch/1999/1/index. Lawson.htm.-A. Leonard. L.E.R.. Calif. Complex causes of amphibian population declines. K. 2001. & M.R.S.org/Herpetofauna_of_the_Iwokrama_Forest. Bury. & M. Transect sampling.A. Acad. Bodenkunde. systems and processes. (eds. Amphibian monitoring in Latin America: A protocol manual.D.M. Pp.W.. Donnelly.. Northwest Fauna Number 4.J.. Donnelly. A field survey manual for vertebrates. J. 139: 1–70. Kasparek Verlag.. 1984. Berlin.R. 1999. Pp. R. K.G.. K.. & M. Drift fence-associated sampling bias of amphibians at a Florida sandhills temporary pond. C.O. 25: 296–301.-L. Inger. Identifying effects of toe clipping on anuran return rates: the importance of statistical power. Foster.AMPHIBIAN MONITORING IN TROPICAL FORESTS Corn. 84–92 in Heyer. Foster. T. R. Schmidt. 1982.-A.und Tierschutzsicht..R. M.M. vi. Washington & London. Mertensiella 7. Chen. Bury. A.. Individualerkennung und Markierung mitteleuropäischer Amphibien und Reptilien: Übersicht und Bewertung der Methoden. Gleneden Beach. Pp. & L. Amphibians and reptiles: the herptiles.C. Declining Amphibian Population Task Force. M. M. P.. Alford. & R. 1997.ac.K. A.S. 1995. W.. & M. 3. (ed. MjM Software Design. Lips. M..C..... & A. SSAR. Standard methods for amphibians. Pearman. W. C. Veith (eds. Recherches sur la végétation et la flore de la région du Bas-Cavally (Côte d’Ivoire). W. Bender 1997.W. 1995.. L.. Plant ecology in West Africa. Tropenbos Series 13.R. 2001.. Flore du Parc National de Taï (Côte d’Ivoire). Smithsonian Institution Press. D. Hayek. 37: 72–81.L. Watkins.E.M. 1994. Forest Service.) 1994. Donnelly. C. Lieberoth. Watson.B. Mémoires O. Bayero University. Dodd.open. Quadrat sampling. Standard methods for amphibians.A. Earthwatch Institute (Europe). PNW-GTR-256. 161 pp. R. Parris.S. Sampling methods for terrestrial amphibians and reptiles. C.W. Houlahan. African forest biodiversity. W.E.. Herpetofauna of the Iwokrama Forest. Pp. W....J. J. López.. 133–184 in Henle.C. MN. & G. 2002.) 2002. Oregon.R. Review: amphibian surveys in forests and woodlands. Society for Northwestern Vertebrate Biology. J. & M.. Krebs. Lips. W. Heidelberg. J. & S. 2002. Empfehlungen aus Natur. K. U.S. Tropical amphibian monitoring: a comparison of methods for detecting inter-site variation in species composition. Auflage. Sci. 364 pp. 97–102 in Heyer. 1991.A. Hayek. Crump. J. DAPTF 2002. Amphibia-Reptilia 22: 275–289.. 364 pp.S. 1990. Schmidt-Loske. B. McDiarmid. 1989.L. Smithsonian Institution Press. & R.. Smithsonian Institution Press. Meyer.. 11 . Herpetol.H. Hayek. Pearman.S. Biol. Witters.. Parren. U. Howell. Jr.K. Foster (eds. Department of Agriculture. & M. R. PACPNT 2000. 1967. & L.. & J. Foster (eds. 115 (7). Pp.. Donnelly. 364 pp.M...H. http://www.A. P.S.A. Herpetologica 51: 325–337. Pp. Standard methods for amphibians. A.G. Madagascar. Washington & London. Correlates of amphibian diversity in an altered landscape of Amazonian Ecuador. 357 pp. Visual encounter surveys. Guyer. McDiarmid. Guillaumet. Donnelly.. Young. Smithsonian Institution Press. Wageningen. M. 17: 1078–1088. K. Occ.A. M. and the Seychelles Islands.A.. Hayek. Shoreview. R.): Measuring and monitoring biological diversity. Nigeria.. G.htm. & N.-A. 300 pp.R. Findlay. McDiarmid. Jaeger. P. K. 199 pp. K.K. 2001. & N. Biol. G... Techniques for marking amphibians. Olson. Contemporary Herpetology 1: http://www. Blaustein.P. Smithsonian Institution Press. Kiesecker. Washington & London. Scott. & R. J. New York a. McDiarmid. L.uk/daptf/index. Iwokrama.M.R..iwokrama.J. Standard methods for amphibians. 2003. Rheinbach.B. 103–107 in Heyer.
.-O. & J. J. Cambridge. Rödel. Ivory Coast. H.-O.S....RÖDEL & ERNST Perret. The social behaviour of anuran amphibians. M. Washington & London.-O. 1961 breeds in tree holes (Anura: Ranidae). Bufo taiensis n.H. 1994.D.G.. Rödel. Nature 410: 639–683. an ecological study. M.H.. 9. Les espèces de Phrynobatrachus (Anura. Academic Press.E.): Patterns of distribution of amphibians. M. Rodda. McDiarmid.. Arch.A.. A new Phrynobatrachus from the Upper Guinean rain forest. 2002. The treefrogs (Rhacophoridae) of West Africa. 1999. 32: 24-30.C. Ranidae) à éperon palpépral. Schiøtz. Smithsonian Institution Press. Edition Chimaira. A high validity census technique for herpetofaunal assemblages. Richards.A.. 2001. 364 pp. J. PhD Thesis. & W. Les communautés d’amphibiens dans le Parc National de Taï..-O. Poynton. G. Frankfurt /M. Hayek. Washington & London. 2002. 1994. Les anoures comme bio-indicateurs de l’état des habitats. A. 1988. 1967. Herpetozoa 11: 19–26.): Etat des recherches en cours dans le Parc National de Taï (PNT). Herpetol. P.S.D.-O. 2003. R. Salamandra 39: 91–110. Veith. Edition Chimaira. Herpetological survey of the Haute Dodo and Cavally forests.-O.. Gascon.C. Semlitsch. The amphibians of Mont Sangbé National Park. & M. 2003. Altig.. A spatial gradient analysis. herpetofauna 22 (125): 9–16. Wells. & R. and Seychelles.. 323 pp. Wageningen. 36: 561–571. B. 633 pp. Tano (eds.-A. M. Kaulquappengesellschaften ephemerer Savannengewässer in Westafrika. Structure and dynamics of an amphibian community. Rapport de Centre Suisse de la Recherche Scientifique. B. E.-O. W. Fritts. 1999. & R. Pounds. 37: 43–52. 1998a.W. 2003. 195 pp. Schiøtz. Treefrogs of Africa. McDiarmid. L.R. a global perspective. Ivory Coast. R.E. Biotropica 33: 502–510. Pp. U. 12 .. Quantitative sampling of amphibian larvae. Tropenbos Series 8. Rödel. van R. & M.K.-A.L. Côte d’Ivoire. Zimmerman.R. K. W. A. West Africa. R. Spolia zool. & R. Côte d’Ivoire. E. 217–448 in Long-term studies of vertebrate communities. O..R. Distribution of amphibians in Sub-Saharan Africa. Musei Haun. Duellman (ed. Rödel.): Measuring and monitoring biological diversity. 1998b.. & G. M. & Y. 2001. M. 142 pp.. Rödel.. including a description of a new reproductive mode for the genus. I. sp. Donnelly. 1996. Gibbons.. 1996. Standard methods for amphibians.A. Herpetol. 130–141 in Heyer. Sci. A reproductive mode so far unknown in African ranids: Phrynobatrachus guineensis Guibé & Lamotte. Forest gradients in West Africa.. J. Ernst. The tropical rain forest. L. Rompaey.L..P. Woodward. Scott. Salamandra 38: 245–268.. Herpetozoa 16: 23–39.C. J. Pp 483–539 in W. 1977. Evidence from a 16-year study of a natural pond. Smithsonian Institution Press. Abidjan. Rödel. Patterns of richness and abundances in a tropical African leaf-litter herpetofauna. Campbell.R. Pp 108–113 in Girardin.. Alford. R. Johns Hopkins University Press. 2000. 1993.A. Part I: Amphibians. western Ivory Coast. Herpetol. M. Le Parc National de Taï. First record of the genus Acanthixalus Laurent. 2000. Vonesh. R. including the description of a new species. Sempervira.. Frankfurt/M.W. Kosuch. 92–97 in Heyer. Madagascar.P. Rödel. Donnelly. The amphibians of Marahoué and Mont Péko National Parks. 25: 1–346. Hayek.K. Genève 41: 275–294.. Branch. Wageningen.A. Baltimore.R. A. Pechmann.. S. Guillaumet 1994. Koné. J.-O.-O. Rödel. Elfenbeinküste.W. Climate and amphibian declines. Ernst. Animal Behaviour 25: 666–693.. Cambridge University Press.W.H. 575 pp. Ernst. M. Riezebos.B. Standard methods for amphibians.. Pp. Shaffer. M. & R.. Ernst. M.-L. D.): Measuring and monitoring biological diversity.. J. 1944 from the Upper Guinean rain forest. J. Rev...D. J. M. Foster (eds. Rödel. 2001. Richards. Audio strip transects. & J.S.J. Foster (eds. Pp. & T. Vooren. M. West Africa. 364 pp. 350 pp.W. eine neue Kröte aus dem Taï-Nationalpark.
SRET = species recorded with VES/AES on the clearing around the SRET station. 2 Ranidae Hoplobatrachus occipitalis Amnirana albolabris Amnirana occidentalis Aubria occidentalis Ptychadena pumilio Ptychadena bibroni Ptychadena mascareniensis Ptychadena superciliaris Ptychadena aequiplicata Ptychadena longirostris Ptychadena sp.AMPHIBIAN MONITORING IN TROPICAL FORESTS APPENDIX. G = species recorded in southern TNP (Guiroutou. 2 Petropedetidae Phrynobatrachus accraensis Phrynobatrachus gutturosus Phrynobatrachus fraterculus Phrynobatrachus guineensis 3 Phrynobatrachus phyllophilus Phrynobatrachus liberiensis Phrynobatrachus alticola Phrynobatrachus alleni Phrynobatrachus plicatus TaïF G SRET TC TP TS VES/AES Trap guild 1 0 0 0 0 0 0 1 f 1 0 0 1 1 0 1 0 1 1 1 0 0 0 0 1 1 0 1 1 1 1 1 1 1 1 1 1 1 1 1 0 1 0 1 1 1 0 1 0 0 1 1 1 1 1 1 0 1 1 1 1 1 1 0 1 1 0 0 0 0 1 0 0 0 1 1 1 0 0 1 1 1 0 0 0 0 0 0 0 1 1 0 0 1 1 0 0 0 1 1 1 0 0 0 0 1 1 0 1 1 1 1 1 1 1 1 1 1 0 0 1 1 0 0 0 1 1 1 0 0 0 0 1 0 0 0 1 1 1 1 1 1 1 1 0 0 0 1 0 0 0 0 1 1 0 0 0 0 0 1 1 0 1 0 1 1 1 1 1 1 1 1 0 0 1 1 0 1 0 1 0 1 0 0 0 0 1 1 0 1 1 0 1 1 1 1 1 1 1 0 0 1 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 1 1 aq l l l l l f aq l l aq l l l l l l l l l l l. Perret 1988) but not recorded by us. VES/AES = species recorded via visual and acoustic encounter surveys in forest habitats near SRET. Trap = species recorded with pitfall and funnel traps. 7°10’ W). species Gymnophiona Caecilidae Geotrypetes seraphini Anura Pipidae Silurana tropicalis Bufonidae Bufo regularis Bufo maculatus Bufo togoensis Bufo taiensis Bufo superciliaris Hemisotidae Hemisus sp. 6 = recorded north of area under investigation. TC = all species recorded on transects. TP = all species recorded on transects in primary forest. 5°25’ N. a = arboreal species. f = fossorial species. a l l l l l 13 . 3 = Phrynobatrachus guineensis is a leaf litter frog but reproduces in small water-filled tree holes (Rödel 1998b). l = leaf litter species. TS = all species recorded on transects in secondary forest. 2003). 5 = treated as full species and not as subspecies of Hyperolius fusciventris due to sympatric occurrence in TNP (see Rödel & Branch 2002). 2 = determination not possible at present time. TaïF = species recorded in forest habitats around the SRET station. 1 = known from TNP (Schiøtz 1967. List of amphibian species recorded in Taï National Park (TNP). aq = aquatic species. other than transects. 4 = Acanthixalus sonjae lives aquatically in large water filled tree holes but forages in surrounding vegetation (Rödel et al.
2 2 Hyperoliidae Leptopelis hyloides Leptopelis occidentalis Leptopelis macrotis Hyperolius concolor Hyperolius guttulatus 6 Hyperolius picturatus Hyperolius sylvaticus Hyperolius zonatus Hyperolius fusciventris 5 Hyperolius lamtoensis 5 Hyperolius nienokouensis Hyperolius wermuthi 1 Hyperolius chlorosteus Afrixalus dorsalis Afrixalus nigeriensis Afrixalus vibekae Kassina lamottei Phlyctimantis boulengeri Acanthixalus sonjae 4 Rhacophoridae Chiromantis rufescens total 56 species in TNP TaïF 0 0 1 1 1 1 1 1 1 1 1 1 0 1 1 1 1 1 1 0 1 1 1 1 1 1 1 1 43 G 1 0 1 0 1 1 1 1 1 1 1 1 0 1 1 1 0 1 1 0 1 1 1 0 1 0 0 1 41 SRET 0 0 0 0 0 0 1 0 1 0 0 1 0 1 0 0 1 0 0 0 0 1 0 0 0 0 0 0 16 TC 0 0 1 1 1 1 1 1 1 1 1 1 0 0 1 1 0 1 0 0 1 1 1 1 1 0 1 1 37 TP 0 0 1 1 1 1 1 1 1 1 1 1 0 0 1 1 0 1 0 0 1 0 1 1 1 0 0 1 33 TS VES/AES Trap 0 0 1 0 1 1 1 1 1 1 1 0 0 0 1 1 0 0 0 0 1 1 1 0 0 0 1 1 28 0 0 1 0 1 1 1 1 1 1 1 1 0 1 1 1 1 1 1 0 1 1 1 1 1 1 1 1 39 0 0 1 0 0 0 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 10 guild l l l l l l l l a a a a a a a a a a a a a a a a l a a.RÖDEL & ERNST Appendix continued species Phrynobatrachus calcaratus Phrynobatrachus taiensis 1 Phrynobatrachus villiersi Phrynobatrachus annulatus Astylosternidae Astylosternus occidentalis Arthropleptidae Cardioglossa leucomystax Arthroleptis sp. 12 Arthroleptis sp. aq a 14 .
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