Biodiversity and Conservation Status of Atnphibians of Ecuador

Transcription

1 CHAPTER 6 Biodiversity and Conservation Status of Atnphibians of Ecuador Santiago R. Ron, Juan M. Guayasamin and Pablo A. Menendez-Guerrero I. Introduction II. Geography A. Western Lowlands (Costa) B. Andean Region (Sierra) C. Eastern Lowlands (Amazonian Region, Oriente) D. Insular Region (Galapagos Islands) Ill. Biogeography and Diversity A. Biogeographic Regions 1. Dry Shrub 2. Western Deciduous Forest 3. Chocoan Tropical Rainforest 4. Western Foothill Forest 5. Western Montane Forest 6. Paramo 7. Andean Shrub 8. Eastern Montane Forest 9. Eastern Foothill Forest 1. Amazonian Tropical Rainforest B. Diversity and Distributional Patterns of Ecuadorian Amphibians IV. Conservation A. Conservation Status of Ecuadorian Amphibians: Extinction Risk Categories B. Extinction Risk Categories Under Global Climatic Change 1. Effect of Climatic Change on the Size of Distribution Ranges 2. Species Extinction Risks Under Future Climatic Change C. Threatened Species 1. Conservation Status of Frogs of the Genus Ate/opus 2. Conservation Status of Frogs of the Genus Telmatobius 3. Conservation Status of Frogs of the Genus Hyloxalus 4. Conservation Status of Frogs of the Family Centrolenidae D. Potential Threats for Amphibians in Ecuador 1. Global Changes in Climate 2. Habitat Loss and Fragmentation 3. Infectious Diseases 4. Introduced Species 5. Contaminants E. Conservation Efforts 1. Indirect Efforts: Protection of Natural Habitats 2. Direct Efforts: Scientific Research and Conservation Projects V. Acknowledgments VI. References Abbreviations and acronyms used in the text and references: DBH=diameter (of trees) at breast height; ACAP =Amphibian Conservation Action Plan; AEE = Almanaque Electr6nico Ecuatoriano; CDC = Centro de Datos para Ia Conservaci6n; CIMMYT =The International Maize and Wheat Improvement Center; EPN = Escuela Politecnica Nacional (Quito); ESPE = Escuela Politecnica del Ejercito; FHGO = FundaciOn Herpetol6gica Gustavo Orces; GEF = Global Environment Facility; BIRF = Banco lnternacional de Reconstrucci6n y Fomento; INEC = lnstituto Nacional de Estadfsticas y Censos (Ecuador); INEFAN = lnstituto Ecuatoriano Forestal de Areas Naturales y Vida Silvestre; IUCN = International Union for the Conservation of Nature; MECN = Museo Ecuatoriano de Ciencias Naturales; MHNG = Museum d'histoire Naturelle, Geneva, Switzerland; NSPA = National System of Protected Natural Areas (Ecuador); PROMSA = Programa de Modernizaci6n de los Servicios Agropecuarios; QCAZ = Museo de Zoologfa de Ia Pontificia Universidad Cat61ica del Ecuador; SSG = Species Survival Commission; USFQ = Universidad San Francisco de Quito; UICN = Spanish acronym for the International Union for the Conservation of Nature

2 13 AMPHIBIAN BIOLOGY I. INTRODUCTION rrhe amphibian fauna of Ecuador is the third most diverse in the world with a total of.l 51 formally described species (Appendix I). The present work summarizes the geographic and biogeographic features of Ecuador in the context of its amphibian fauna. In addition, the patterns of distribution and diversity of Ecuadorian amphibians are analysed, their conservation status evaluated and possible causes for population declines discussed. Ecuador is located in northwestern South America, bordered by Colombia to the north and northeast, Peru to the south and southeast, and the Pacific Ocean to the west. It has an area of km 2 and a human population of (INEC 28), being the most densely populated country in South America (55 habitants/km 2 ). Since 195, the population of Ecuador has increased four times. The country has also suffered recent changes in its population distributional pattern. In 195, most of the human population lived in rural areas; nowadays, 61% live in urban areas (INEC 22). Geographically, Ecuador is divided by the Andes into three main continental regions (Fig. 1): the lowlands west from the Andes to the Pacific coast (Western Lowlands or Costa), the Andes (Sierra), and the lowlands from the base of the Andes eastward (Eastern Lowlands, Oriente, or Amazonian Region). In addition, Ecuador has one insular region- the Galapagos Islands. A. Western Lowlands (Costa) II. GEOGRAPHY Located between the Pacific Ocean and the western slopes of the Andes, the Costa consists of coastal lowlands, coastal mountains, and river valleys. A coastal cordillera, with maximum elevations of 8-9 m, roughly parallels the coast from approximately 1 o N to 2 S, terminating just west of the city of Guayaquil. Annual rainfall varies from north to south, with northern areas being extremely wet (3-4 mm) and southern areas much less so ( < 1 5 mm) (Ridgely and Greenfield 21) (Fig. 1 ). Humans have modified the Western Lowlands for centuries. The Costa is highly populated (5% of Ecuador's population) (INEC 22) and also is used extensively for agriculture, e.g. rice, bananas, oil palms (Fig. 2). Moreover, the rates of transformation and degradation of the ecosystems in this region are the highest in Ecuador (Dodson and Gentry 1991; Sierra and Stallings 1998). Major biogeographic regions in the Western Lowlands are Dry Shrub, Deciduous Forest, and Chocoan Tropical Rainforest (Fig. 2). B. Andean Region (Sierra) The Andes are the longest mountain range in the world, spanning nearly 8 km. They cross Ecuador from its northern border with Colombia to its southern border with Peru. They are the most distinctive feature of South American topography. The Ecuadorian Andes are divided into two main ranges, a western one (Cordillera Occidental) and an eastern one (Cordillera Oriental). Transverse mountain ridges interconnect these ranges forming ten inter-andean basins. The Sierra has at least thirty peaks of volcanic origin. The Cordillera Occidental has its northern limit in the dry valley of the Chota River and extends for about 5 km south to the valley of the Jubones River (Duellman 1979). Eight mountains reach elevations above 4 5 m in this range. Among them is Volcan Chimborazo ( m), the highest mountain in the Andes north of Peru. The elevational gradients in this range are precipitous, with changes from 4 m to 1 m between localities separated by a distance of only 3 km. The Cordillera Oriental extends from Nudo de Pasto in southern Colombia to the Huancabamba depression in northern Peru, with a total length of more than 6 km. Twelve

3 RON et al: BIODIVERSITI AND CONSERVATION STATUS OF AMPHIBIANS OF ECUADOR 131 Fig. 1. Elevation and mean annual precipitation in continental Ecuador. 81'W 8'W 79'W 78'W 77'W 76'W 75'W 2'N l'li N A 1'1-l O'N O'N 1'S 'S... 2'S 2'S 3'S Biogeographie Regions 3'S c::j Dry Shrub c:::::joeciruous Forest b:l Olocoan Tropical Rainforest 4'S c::j w estern Foothll Forest O western Montane Forest s - Paramo 5'S 5 1 km I I I I I I I I I Andean Shrub [22Ll Eastern IA ontane Forest -Eastern F oothid Forest [DID Amazonian Tropical Rainforest S' S 81'W 8'W 79'W 78'W 77'W 7 'W 7:. w Fig. 2. Biogeographic regions of Ecuador. This classification is a simplification of Sierra's (1999) system.

4 132 AMPHIBIAN BIOLOGY mountains reach elevations above 4 5 m. The highest are the snow-capped Volcan Cotopaxi (5 897 m) and Volcan Cayambe (5 79 m). The Cordillera Oriental is interrupted by the low valleys of Rio Pastaza, Rio Paute, and Rio Zamora. Three partly-disjunct highland areas rise to the east of Cordillera Oriental: Cordillera Napo-Galeras and Volcan Sumaco (3 732 m), Cordillera del Cutucu (2 2 m), and Cordillera del Condor (2 45 m). A latitudinal discontinuity in the volcanic activity of the Ecuadorian Andes occurs at 2 S as a consequence of a change of the subduction angle of the Nasca Plate beneath the South American Plate. North from 2 S, the mountain ranges are higher with many active volcanoes that are continuously erupting. South from 2 S all mountains are below 4 3 m (except for Volcan Sangay) and there has not been volcanic activity since the Miocene (Gregory-Wodzicki 2). The complex topography of the Ecuadorian Andes creates a landscape with extreme climatic differences. Precipitation gradients are severe with the highest annual rainfall in Ecuador occurring on the eastern slope of Cordillera Oriental (over 4 8 mm) contrasted by low precipitation at dry inter-andean basins under the influence of rain-shadows. Annual rainfall is relatively uniform in the northwest and on the eastern slope (as low as l 81 'W 8 'W 79 'W 78 'W 77 'W 76 'W 1 'N Colombia 1 ' N ' ' 1 'S 1 'S 2 'S 2 'S 3 'S Peru 3 'S 4 'S Natural vegetation c=j Mosaics (natural-agricultural) 4 'S 5 'S I II I I II I I.. Other c=j Agriculture and pastures 5 'S 5 1 km 81 'W 8 'W 79 'W 78 'W 77 'W 76 'W Fig. 3. Land cover in Ecuador (modified from AEE 2). "Mosaics" are mixtures of natural vegetation and either agricultural land or pastures (mostly devoted to raising cattle). "Other" includes urban areas, shrimp fanns, lakes, rivers, glaciers, and sand banks.

5 RON et al: BIODIVERSI1Y AND CONSERVATION STATUS OF AMPHIBIANS OF ECUADOR 133 mm). Temperature varies as a function of elevation and frosts occur above 3 m. The tree line occurs at m and permanent snow at m (Ridgely and Greenfield 21 ). Humans have modified Andean ecosystems during millennia; evidence of human presence in this region dates from 7-1 BC (van der Hammen and Correal-Urrego 1978; Brothwell and Burleigh 198). At present, more than five million people live in the Ecuadorian Andes (INEC 22). Human activities have produced an extensive deforestation of the original vegetation in the inter-andean valleys (Fig. 3). Moreover, large areas (including protected reserves such as Reserva Ecol6gica El Angel, Bosque Protector Cashca Totoras) have been reforested with exotic tree species (e.g., Eucalyptus globulus, Pinus radiata, P patula) that diminish the local diversity of the native flora (Bas lev and de Vries 1992). Virtually no effort has been made to use native species for reforestation. The western Andean slopes have significant portions of natural vegetation either completely cleared or fragmented, more so than do the eastern slopes (Fig. 3). The most pristine montane forests of the Andean region are those found on the ridges and peaks lying east of the main ridge of the Cordillera Oriental (e.g., Volcan Sumaco-Cordillera de Galeras, Cordillera de Cutucu, Cordillera del Condor) (Ridgely and Greenfield 21 ). Most of the external slopes of the Andes are uniformly humid, although both the Cordillera Occidental and Cordillera Oriental are incised by a few deep river valleys in which conditions may differ. In the Cordillera Occidental this occurs especially in the drainages of the Chota, G'uayllabamba, Chanchan, and Jubones rivers, portions of which are very arid. In the Cordillera Oriental, this occurs less frequently, although there is a relatively arid area in the Rio Pastaza valley near Banos in Tungurahua Province (Ridgely and Greenfield 21). Major biogeographic regions in the Andes are Eastern Foothill Forest, Eastern Montane Forest, Paramo, Andean Shrub, Western Montane Forest, and Western Foothill Forest. C. Eastern Lowlands (Amazonian Region, Oriente) The Oriente consists of an area that gradually descends eastwards from the foothills of the Andes, dropping to elevations of 2-4 m, and constitutes approximately 5% of the total area of Ecuador. Annual precipitation is generally greater than 2 mm and there are no ecologically dry habitats (Palacios et al. 1999) (Fig. 1 ). This region remains the most sparsely populated of Ecuador's three continental regions with only 4.5% of the human population (INEC 22). Although the Amazonian region still has a high proportion of undisturbed forest, human impact is considerable along roads (most of them constructed since the 197s for oil exploitation). Almost 2% of the original vegetation cover has been destroyed or severely fragmented in the Amazonian region below 6 m (estimate based on AEE 2). The only biogeographic region in the Eastern Lowlands is the Amazonian Tropical Rainforest. D. Insular Region (Galapagos Islands) The Galapagos Islands consist of a chain of large, medium, and small islands that have a combined area of about 8 km 2 The islands are located in the Pacific Ocean, approximately 1 km west of the continent of South America. All the islands are of volcanic origin, and some have active cones. The Galapagos have a remarkably seasonal climate, largely influenced by cool water masses originating off the coast of Peru and by warm water masses originating to the north (Colinvaux 1984; Houvenaghel 1984 in Grant 1999). There is a hot and wet period, from approximately January to May, and a cooler and drier period for the rest of the year (Grant 1999). On the large islands, proceeding from low elevations to progressively higher ones, the vegetation can be divided into ( 1) arid lands, (2) transitional forest, (3) moist forest, and (4) fern-sedge-grass vegetation (Grant 1999). Other vegetational types (e.g., mangroves) have restricted distribution (Grant 1999). No native amphibian species inhabit the Galapagos Islands, but recently numerous populations of the hylid frog Scinax quinquefasciatus have become established at Puerto Villamil (Isabela Island).

6 134 AMPHIBIAN BIOLOGY A. Biogeographic Regions III. BIOGEOGRAPHY AND DIVERSITY In the present classification, the vegetation types used to characterize the biogeographic regions of continental Ecuador are a simplification of Sierra's ( 1999) classification. In addition to the physiognomy of the vegetation, that system also considers the historic isolation between the western and eastern slopes of the Andes and the eastern and western lowlands. Table 1 shows the area, mean annual temperature, mean annual precipitation, amphibian species richness, and amphibian species density for each region. Figure 4 characterizes, in two-dimensional space, mean annual precipitation and mean annual temperature for each region. In the following account, Regions are listed in order of geographic position from west to east (Fig. 2). 1. Dry Shrub The Dry Shrub is characterized by a combination of warm and extremely dry conditions (Fig. 4). Annual precipitation can be as low as 6 mm (in the westernmost locality, Salinas, Guayas Province). The Dry Shrub covers an area of only 8 33 km 2 and is restricted to the coastal margin of central Ecuador. In some areas, grasses introduced for raising livestock have replaced native plants. In the drier habitats, xerophytic plants are dominant, especially cacti and other thorny plants (Geron et al. 1999). This region has the lowest diversity of amphibians anywhere in Ecuador (Table 1). 2. Western Deciduous Forest This Biogeographic Region lies between 5 m and 3 m (1 and 4 m in southern Ecuador) and covers km2 (1.3% of Ecuadorian territory). Conditions are drier and the terrain has lower tree densities than in evergreen forests. The trees are generally shorter Table 1. Amphibian diversity and climate in the Ecuadorian Biogeographic Regions (as defined in Figure 2). Annual averages of temperature and precipitation (standard deviations in parentheses) were calculated on digital climate maps from looo random point localities throughout Ecuador (AEE 2). Biogeographic Area of the Mean Annual Mean Annual Number Density Region region (km 2 ) Temperature ( C) Precipitation (mm) of species (species/1 km 2 ) Dry Shrub 8, (.66) 5 (393) Deciduous Forest 25, (1.32) 843 (3 16) Chocoan Tropical Rainforest 31, (.59) 2,86 (665) Western Foothill 15, (1.71) 2,2 18 (97) Forest Western Montane 21, (4.4) 1,187 (6 1) Forest Paramo 15, (2.3) 83 (277) Andean Shrub 11, (2.7) 8 17 (2 15) Eastern Montane 31, (4. 13) 1,691 (799) Forest Eastern Foothill Forest 13, (.91) 2,923 (1,23) Amazonian Tropical 73, (.8 1) 3,349 (555) Rainforest Galapagos Archipelago 7,96 1* <.1 Total for country 248, (5.78) 2,23 (1,177) (continental) * The only amphibian that occurs in the Galapagos is the hylid Scinax quinquefasciatus, an introduced species that established breeding colonies during the late 199s.

7 RON et al: BIODIVERSITY AND CONSERVATION STATUS OF AMPHIBIANS OF ECUADOR 135 x Amazonian Tropical Rainforest 1!1 Andean Shrub.c.. Chocoan Tropical Rainforest o Deciduous Forest ""' Dry Shrub Eastern Montane Forest Paramo o Weastern Foothill Forest v Eastern Foothill Forest + Weastern Montane Forest l l l...---l...---l------' _... Q) 2... D * ro '- Q) 17.5 c.. E Q) ro ::J 12.5 c: c: <( 1 c: ro Q) 7.5 ::2: X 1--,--,----,---r---r ,---,--r, ---r Annual Precipitation ( C) Fig. 4. Annual precipitation and mean annual temperature in Ecuadorian Biogeographic Regions (as defined in Figure 2). The values were measured from digital climate maps at localities throughout Ecuador. Forty random sites within each biogeographic region were chosen to characterize temperature and precipitation regimes (except for the Dry Shrub where 28 locations were measured). Table 2. Land cover (%) of natural and agriculturally influenced landscapes in the Ecuadorian Biogeographic Regions (as defined in Figure 2). Values are estimates based on digital maps of land cover in Ecuador (AEE 2). "Mosaics" are mixtures of natural vegetation and either agricultural land or pastures. "Other" includes urban areas, shrimp farms, lakes, rivers, glaciers, and sand banks. Mosaics Agriculture Biogeographic Region Natural Vegetation (Natural-Agricultural) and Pastures Other Dry Shrub Deciduous Forest Chocoan Tropical Rainforest Western Foothill Forest Western Montane Forest l.l Paramo Andean Shrub Eastern Montane Forest Eastern Foothill Forest Amazonian Tropical Rainforest

8 136 AMPHIBIAN BIOLOGY than 2 m with an understorey that can be dense with abundant herbaceous plants. Some tree species lose their leaves during the dry season (CerUn et al. 1999). Because of its dry conditions, amphibian diversity is low. Human impact on the natural cover has been severe. More than half of the land cover is being used for agriculture and raising cattle (Table 2). This habitat type is almost unrepresented in the Ecuadorian National System of Protected Areas. 3. Chocoan Tropical Rainforest This is the second largest Biogeographic Region in Ecuador with km 2 and elevations ranging from sea level to 3 m. It is absent in the lowlands of southwestern Ecuador due to predominantly dry conditions. The Chocoan Tropical Rainforest has a closed canopy with trees that can reach 3 m in height and with an understorey dominated by ferns and Araceae (Cer6n et al. 1999). Tree diversity is high (more than 1 species/ha with diameter at breast height [DBH] > 1 em) (Palacios et al. 1999), but lower than in the Amazonian Tropical Rainforest. The amphibian assemblages in this region share more species with Central American lowland rainforests than with those of the Amazon Basin (Ron 2). Only four species are shared between the Chocoan Tropical Rainforest and the Amazonian Tropical Rainforest: Hypsiboas boans, Phrynohyas venulosa, Trachycephalus typhonius, Rhinella marina, and R. margaritifera. Anthropogenic habitat degradation in this region is the highest in Ecuador; only 18.3% of the natural vegetation has not been cleared or severely fragmented (Table 2; Fig. 3). 4. Western Foothill Forest This Biogeographic Region covers km 2 in the western Andean slopes with an elevational range between 3 m and 1 3 m (4-1 m in southern Ecuador). This evergreen forest is structurally similar to its counterpart from the eastern Andean slope although the amphibian communities are highly differentiated with only three species shared between the Western and Eastern Foothill forests (Rhinella marina, R. margaritifera, and Hypsiboas boans). Moreover, genetic evidence suggests that populations of R. marina on different sides of the Andes may actually represent separate species (Slade and Moritz 1998). Plant endemism is high, especially between latitudes oo and 3 S (Cer6n et al. 1999). 5. Western Montane Forest This evergreen forest covers km 2 with an elevational range between 1 3 m and 3 4 m (1-3 m in southern Ecuador). The canopy is generally below 25 m with a high abundance of epiphytic plants (especially mosses, ferns, orchids, and bromeliads). At intermediate elevations, especially during the afternoon, the forests become misty and receive horizontal precipitation from low, overhanging clouds. These conditions are favourable for amphibians with direct development, especially Pristimantis. There are 19 amphibian species shared with the Eastern Montane Forest (13.9% of the 136 species recorded in the Western Montane Forest). Western Montane Forest is restricted to narrow stretches between the basin of the Mira River (close to the Colombian border) and the basins of the Chanchan and Chimbo rivers (2 S). It is replaced by drier habitats (principally Andean Shrub) south of 4 S, close to the border with Peru. Only 35% of its natural vegetation remains unaltered (Table 2; Fig. 3). 6. Paramo Paramo is the vegetation type that reaches the highest elevation. Depending on the region, its lower limit lies between 3 and 3 6 m. It covers ha (6.1% of the territory). Short herbaceous plants, generally forming tight clumps, dominate the vegetation. The plants are adapted to cold temperatures and to low availability of water. Open grassy areas are dominant but are mixed with small patches of forest or shrubs (Valencia et al. 1999). At higher elevations, the vegetation is restricted to sparse clumps on otherwise bare land. Because of the occurrence of frequent freezes, agriculture is limited and this has

9 Table 3. Categories of extinction risk (in percentages; from Appendix l) for amphibian species in the Ecuadorian Biogeographic Regions (as defined in Figure 2). For each species, the categories and the criteria for assignment correspond to those of the IUCN Red List Categories (IUCN 21 ). The percentages pertain only to "Data-Sufficient" species. Species described after 28 are not included in the analyses. Biogeographic Region Dry Shrub Deciduous Forest Chocoan Tropical Rainforest Western Foothill Forest Western Montane Forest Paramo Andean Shrub Eastern Montane Forest Eastern Foothill Forest Amazonian Tropical Rainforest No. of Species % Least Concern % Near Threatened % Vulnerable % No. of No. of % Critically Data-Sufficient Data-Deficient species (1%) Species l l :>:l z 1:1:1 t:i < ttl s t:i n z Vl ttl :>:l i-l z Vl i-l e Vl 'rj "1::1 ::r: ;; s; z Vl 'rj ttl n :>:l - -..]

10 138 AMPHIBIAN BIOLOGY (/) - 35 Q.) bf 3 - Ci3 25..c 5 2 z Year Eastern Montane Fig. 5. Relationship between percentages of threatened amphibian species versus mean annual temperature and average elevation across Ecuadorian Biogeographic Regions. ameliorated anthropogenic habitat degradation. In this region, only 21.1% of the natural vegetation has been cleared or severely fragmented, the lowest proportion for any region (Table 2; Fig. 3). However, the Paramo is the region with the highest proportion of endangered amphibians (Table 3; Fig. 5). Amphibians occur as high as 4 2m. 7. Andean Shrub This Biogeographic Region lies between 1 4 and 3 m and has an area of km 2 ; it is found in the inter-andean basins between the Cordillera Occidental and the Cordillera Oriental. As a result of rain-shadow effects from both mountain chains, the Andean Shrub has relatively low precipitation (Table 1). Although originally dominated by shrubs, most of the vegetation has been replaced by crops, pastures, or forests of exotic trees of the genus Eucalyptus and Pinus (Valencia et al. 1999). In dry valleys (e.g., Chota, Guayllabamba, and Patate) the native vegetation is spiny. Andean Shrub is almost unrepresented in the Ecuadorian National System of Protected Areas. Habitat degradation is severe; more than half the land cover is devoted to agriculture or to raising cattle (Table 2; Fig. 3). 8. Eastern Montane Forest This evergreen forest covers km 2 between 1 3 m and 3 6 m on the eastern Andean slopes. The vegetation is structurally similar to that from the Western Montane Forest. Above 2 9 m the soil of the forest is covered by moss and the trees are irregularly shaped with titled trunks branching from the base (Valencia et al. 1999). This region has more amphibian species than any other in Ecuador (Table 1). Montane forests (Eastern and Western) are the regions from which most new or unreported species of Ecuadorian amphibians have been found during the past few decades (Fig. 6).

11 RON et al: BIODIVERSITI AND CONSERVATION STATUS OF AMPHIBIANS OF ECUADOR 139 logs= log A; R 2 =.42 Montane and Foothill Forests I '...,,,,,, en,,,, en,,,,, Q), 2,, Amazonian Tropical c,'..... Rainforest.r:. I.... I (.)... c '... en 1.8 Q) Chocoan Tropical Q) 1.6 Rainforest '(3 Cl.. (/) > 1.4 Deciduous Forest 1.2 Dry Shrub log Area (km2) Fig. 6. Accumulated number of formally described species of amphibians in Ecuador ( ). 9. Eastern Foothill Forest Eastern Foothill Forest covers km2 between elevations of 6 m and 1 3 m. This evergreen forest is a mixture of tree species from the Andes and the lowlands of the Amazon Basin (Palacios et al. 1999). The canopy reaches up to 3 m in height and encloses a dense sub-canopy and understorey. Tree diversity is lower (13 species/ha, > 1 em DBH) (Palacios et al. 1999) than in the Evergreen Tropical Forest. Average annual precipitation is the second highest of all regions (2 833 mm). This region has the highest density of amphibian species in Ecuador (7.54 species/1 km2). 1. Amazonian Tropical Rainforest The Amazonian Tropical Rainforest is the most extensive Biogeographic Region in Ecuador with a total area of km 2 (29.8% of the Ecuadorian continental territory). It is restricted to elevations below 6 m and has the highest average annual precipitation of any region (3 349 mm). The dominant forest type, Terra Firme, is characterized by welldrained soils. The canopy is 1-3 m high, punctuated by emergent trees up to 4 m (and rarely 5 m); there are small gaps created by fallen trees (Palacios et al. 1999; Valencia et al. 24). Tree diversity is high with 2-3 species of trees/ha (> 1 em DBH) (Palacios et al. 1999; Valencia et al. 24). Other vegetation types in this region include varzea forest (flooded with white water), igap6 forest (flooded with black water), riparian woodland forest, river island scrub, and Mauritia flexuosa palm swamps (Palacios et al. 1999; Ridgely and Greenfield 2 1 ). Amphibian alpha diversity reaches its peak in the Amazonian Tropical Rainforest of Ecuador. One of the two most diverse amphibian faunas ever documented is Santa Cecilia, a locality in this region (Provincia de Sucumbios). At Santa Cecilia, 86 species of anurans were recorded in the late 196s in an area of approximately 3 km2 (Duellman 1978). The

12 14 AMPHIBIAN BIOLOGY forest at Santa Cecilia was logged in the 197s with a consequent decimation of its amphibian fauna. In Amazonian Ecuador, at least one additional locality Yasuni National Park is known to have anuran species richness in excess of 13 species (Ron 21-28; Bass et al. 21 ). B. Diversity and Distributional Patterns of Ecuadorian Amphibians The amphibian fauna of Ecuador is the third most diverse in the world with a total of 5 l formally described species. This surprisingly high number for a country l/2 the size of Brazil is likely to increase significantly as demonstrated by the rate of description of new species (Fig. 6); 97 species have been added since Moreover, the application of molecular techniques to the systematics of Neotropical amphibians indicates that there is a considerable number of cryptic species that have been overlooked by previous morphologically-based systematic accounts (Ron et al. 26). For example, Santos et al. (23) found seven cryptic species of Dendrobatidae from Ecuador, based on phylogenetic analyses of mitochondrial DNA (genes 12S and l6s rrna). That study included 38 described Ecuadorian species. Cryptic species have also been found by applying molecular methods to Engystomops (Cannatella et al. 1998; Ron et al. 24, 26, 28), centrolenids (Guayasamin et al. 28) and Gastrotheca (Duellman and Hillis 1987). In Ecuador, Anura is the most speciose order with 4 71 species (Appendix I). Gymnophiona and Caudata are comparatively minor components with 23 and 7 species respectively. Pristimantis is by far the most speciose genus in Ecuador; nearly one in every three species of anurans is a Pristimantis. The high diversity of Ecuadorian amphibians seems to be a consequence of the historical complexity and environmental heterogeneity that characterizes the landscape. The Andes are home to the richest assemblage of amphibian species in South America (753 species, 45% of the total) (Duellman 1999) and the diversity patterns observed in Ecuador are an extreme instance of this continental generalization. There are 389 species in the Ecuadorian Andes (over 3/4 of the total); 65% of these species are absent in the lowlands. This proportionally high diversity is retained even when the Eastern and Western Foothill Forests are excluded from the analysis: 56% of the Ecuadorian amphibians are distributed in Montane Forests, Andean Shrub, and Paramo regions (3 species); of these, 187 species are absent in Foothill Forests and lowland regions. Endemism is high. A total of 213 species (42.5%) are only found in Ecuador; the nonendemic species are shared in a higher proportion with Colombia (222) than with Peru (155). The lowlands to the east and west of the Andes (below the Foothill Forest) are home to 247 species, most of them distributed in the Tropical Rainforest (97.%). The Ecuadorian lowlands comprise 56.2% of the continental area of Ecuador, a percentage above their share of the total number of species (48.1%). The most diverse biogeographic regions in Ecuador are the Eastern Montane Forest (173 species), Amazonian Tropical Rainforest (164 species), and Western Montane Forest (136 species) (Table 1). Considering the high alpha diversity in the Amazonian Tropical Rainforests and the fact that it is the largest biogeographic region in Ecuador (twice the size of the second largest) (Table 1), it is surprising that its diversity is lower than that of the Eastern Montane Forest. The reason for this imbalance seems to be the generally more extensive distribution of lowland amphibians relative to those from the highlands (Pounds et al. 26). Although amphibian communities in the Andes typically have lower alpha diversities (Young et al. 24), their turnover of species across space is higher (McKnight et al. 27). This is consistent with the higher endemism among Andean biogeographic regions in Ecuador: in the Eastern Montane Forest, 53% of the species are endemic to Ecuador whereas in the Amazonian Tropical Rainforest only 16% are. To a lesser degree, the same pattern is evident in western Ecuador where 5% of the Western Montane species are endemic versus 34% in the Chocoan Tropical Rainforest. Regional endemism is shown in Figure 7. Interestingly, the Western and Eastern Montane forests have a higher number of species endemic to Ecuador and to a single region than all other regions combined.

13 RON et al: BIODIVERSITY AND CONSERVATION STATUS OF AMPHIBIANS OF ECUADOR 141 The relationship between area and species richness (in log space) for Ecuador's biogeographic regions is statistically significant (F = 6.27, df = 9, P =.37) (Fig. 8). The graph also shows that the Andean forests (Foothill and Montane, on the eastern and western slopes) have species richnesses higher than expected for their area; understandably, the opposite is true for the dry regions of western Ecuador, Dry Shrub and Western Deciduous Forest. Overall, the patterns of species richness and endemism highlight the importance of the conservation of montane habitats. Unfortunately, only a low proportion of Andean forested areas (especially those on the western slopes) are included in the Ecuadorian National System of Protected Areas (see section IV-E-1) (Fig. 7). The amount of rainfall explains 5% of the variation in the number of species among biogeographic regions. The relationship between both variables is statistically significant (Fig. 9; F = 8.963, df = 9, P =.22). Both Eastern Montane Forest and Western Montane Forest have species richness higher than expected from their annual precipitation (Fig. 9). In contrast, the following relationships are not significant: species density versus annual precipitation (F = 1.69, df = 9, P =.229); species number versus mean annual temperature (F =.17, df = 9, P =.899); species density versus mean annual temperature (F =.121, df = 9, P =.737). Patterns of regional species richness differ among taxonomic groups. The most diverse family of Ecuadorian amphibians (Strabomantidae, 169 species) reaches its highest species richness in the Eastern Montane Forest (77 species) and Western Montane Forest (63 species) 35 <U ) 3 45 r , 4 ---FOT-- Protected % ofnspa ro & % species,.a... \ c 25 t ' <U ,._:_ Cl.....,,, Fig. 7. (A) Number of species of amphibians endemic to Ecuador and restricted to a single Biogeographic Region. (B) Proportion of the area of the Ecuadorian Biogeographic Regions (as defined in Figure 2) included within the National System of Protected Areas (NSPA). The "% of NSPA" represents the proportional area that each Region occupies within the NSPA; the "% of species" represents the proportion of Ecuadorian amphibian species present in each region (total number of amphibian species in Ecuador = 455; richness values of 1% exclude species described after 24). The Western Montane Forest and the Eastern Foothill Forest have a low representation within the NSPA despite their high species richness and high endemism.

14 en en 14 Q) 12 c..c (.) :: 1 en 8 Q) (.) 6 Q) c. 4 (/) 2 AMPHIBIAN BIOLOGY Montane: Forests,,...,, '.,,,',.,,.,.. -, 'o Annual Rainfall (mm) 3 Fig. 8. Relationship between amphibian species richness and geographic area for Ecuadorian Biogeographic Regions (as defined in Figure 2). Montane and Foothill forests show higher species richness than predicted from their geographic extent; the opposite is true for dry habitats (Dry Shrub and Deciduous Forest). (Appendix I). The second most diverse family, Hylidae (82 species), reaches its highest species richness in the Amazonian Tropical Rainforest (53 species) and Eastern Foothill Forest (3 species). Hylids have more than twice the number of species in the Eastern Andean forests (Foothill and Montane) compared to the Western Andean forests (39 and 17 species, respectively). Strabomantids also have higher species richness in Eastern than in Western Andean forests (85 versus 7). In contrast, bufonids, centrolenids, and dendrobatids have similar species richnesses on both sides of the Andes. The regions with most dendrobatids are the Western Montane Forest (16 species) and Eastern Montane Forest (13 species). Centrolenids reach their highest richness in the Eastern Montane Forest (15) and Western Montane Forest (13 species). IV. CONSERVATION Little is known about the demography of populations of Ecuadorian amphibians. General ignorance about this topic is the most significant obstacle to assessment of their conservation status. This section reviews the scant information available, followed by a discussion of factors possibly threatening the amphibian fauna. Most reports of decline of amphibians in Ecuador are incidental accounts of unsuccessful efforts to find species in their natural range (e.g., Vial and Sailor 1993; Coloma 1995, 1996; Stebbins and Cohen 1995; Lotters 1996; Coloma et al. 2, 27). These observations have not been based on standardized survey techniques and for most regions and species the information is either non-existent or scant and inconclusive. Although methodologically limited, these reports are relevant for assessing changes in population sizes of species that historically have had high local abundance in regions of easy access. The absence of records of these species during extended periods, despite intensive searches, is an indication of population decline. Species that fall in this category are several Atelopus, centrolenids, and dendrobatids (see below). Fuelled by concerns generated by early reports, since 1999 programmes of population monitoring have been established and information on species' relative abundances and on

15 RON et al: BIODIVERSITY AND CONSERVATION STATUS OF AMPHIBIANS OF ECUADOR Q) 6 O'l..., ru c Q) u 1... Q) a ' ' 'A - \ \ \ \ - ' ' ' ' - -k- - Least Concern '-' Critically I..... I I j I.. A. 2 1 Fig. 9. Relationship between species richness and annual precipitation in Ecuadorian Biogeographic Regions (as in Figure 2). Montane and Foothill forests show higher species richness than predicted from th<;ir annual rainfall. changes in community composition have been generated at some localities (Funk et al. 23; Ron et al. 23; Bustamante et al. 25; Yanez-Mufioz and Meza-Ramos 26). Additionally, research into the causes of declines (climatic change; pathogens) (Ron and Merino-Viteri 2; Merino-Viteri 21; Ron et al. 23; Merino-Viteri et al. 25) also has been conducted. A. Conservation Status of Ecuadorian Amphibians: Categories of Risk of Extinction Categories of risk of extinction for all Ecuadorian species are shown in Appendix I. The categories and the criteria for assignment correspond to those of the IUCN Red List Categories (IUCN 21) and constitute a reviewed and updated version of those defined by Coloma, Ron, and Menendez-Guerrero for the Global Amphibian Assessment Project (IUCN et al. 26). The assessment only considered Ecuadorian populations and therefore categories could differ from evaluations that consider the species' entire distributional range. The criteria used to assess categories of risk of extinction include: (1) species' distributional polygons based on known localities of occurrence (extent of occurrence), and (2) habitat degradation and fragmentation within each species' distributional polygon, quantified from Sierra's ( 1999) map using Arc Map 8.3 (ESRI 23 ). Locality data for each species were obtained from natural history collections and from published records. The evaluation of extinction-risk categories involves a non-trivial component of subjectivity as demonstrated by inconsistencies among recent evaluations of N eo tropical amphibians. For example, La Marca et al. (25) allocated 63% of the species of Atelopus in the "Data Deficient" category (i.e., data insufficient to assess population trends) whereas the Global Amphibian Assessment allocated fewer than 5% (IUCN et al. 26). Controversies

16 144 AMPHIBIAN BIOLOGY about the categorization implemented by the Global Amphibian Assessment (Pimenta et al. 25; Stuart et al. 25) also stem from our still inadequate understanding of the systematics, distribution, and demography of Neotropical amphibians and the need to make choices between "evidentiary" versus "precautionary" approaches to cope with the lack of information. These uncertainties highlight the persisting need for population-survey data and systematics-oriented research. The evaluation presented herein also suffers from those shortcomings and the categories presented in Appendix I should be considered tentative. The number of threatened species in Ecuador is 142 (3.5%). The numbers for each category are: 38 Critically (8.2%), 64 (13.8%), 4 Vulnerable (8.6%), 61 Near Threatened (13.1%), and 127 Least Concern (27.3%). The extinction-risk category of 135 species (29.%) was not determined because the available data were insufficient for assessment of status (Data Deficient category). The Global Amphibian Assessment (IUCN et al. 26) categorized two Ecuadorian species as extinct (Atelopus ignescens and A. longirostris). Although between 5 and 25 species of Atelopus may be extinct (Coloma et al. 27), assignments to the Extinct category are premature until more exhaustive searches are conducted. Thus, here these species are placed in the Critically category. Overall, the Andean biogeographic regions contain the most threatened amphibian faunas (Table 3; Fig. 1 ). The regions with the highest number of or Critically Species are the Eastern Montane Forest (55 species) and the Western Montane Forest (4 species). The regions with the highest proportion of spec;ies either or Critically are the Paramo (6.%), and Andean Shrub (59.4%). Conversely, the regions with the lowest number and proportion of or Critically species are those from the lowlands (Table 3; Fig. 1). This elevational pattern matches the perceived lower occurrence of amphibian declines in the Neotropicallowlands (Young et al. 2 1 ). Interestingly, there is a negative, statistically significant, correlation between the proportion of threatened species and mean annual temperature (linear regression ANOVA's F = 17.4, df =9, P =.3) and elevation (F = 15.87, df = 9, P =.4) in the Ecuadorian Biogeographic Regions (Fig. 5 ). Overall, regions with lower temperature and higher elevation have a larger proportion of endangered species. It is unclear what mechanisms, if any, could mediate these relationships. One causal agent may be climatic change because the increase in atmospheric temperature is expected to be more severe at high elevations in the Andes relative to the lowlands (Bradley et al. 24; see section IV D-1 ). An additional contributing factor could be size of distributional range. It has been shown that the size of amphibian distributions in the New World decreases dramatically at higher elevations (supplemental material in Pounds et al. 26). Thus, as a result of their expected smaller size, populations living at high elevations would have greater probability of extinction if they are affected by disease, climatic change, environmental contaminants, 1 Andean C/) C/) Q) Shrub,.."" Q)... O Andean / - 75 T5... Shrub a. / Q) / a...., Q:, < (j) / / (j) Paramo Paramo -c -c Montane Forests Q) Q) c 5 O _,.. Montane c 5 Q) Q) ro 9;; >- Fo ro Q) Q) c ' Choco 25 FoothUI.c Foothill ' O Forests Forests <?)..._ c... O E Amazon Amazon Median Altitude (m) Median Annual Temperature ("C) Fig. 1. Percentage of species of amphibians belonging to categories of risk of extinction in Ecuadorian Biogeographic Regions (total number of species per region = 1%).

17 RON et al: BIODIVERSITI AND CONSERVATION STATUS OF AMPHIBIANS OF ECUADOR 145 and other risk factors. Finally, the observed pattern could also be explained by a disease that is more virulent, or has higher transmission rates, at low temperatures. Batrachochytrium dendrobatidis' thermal optimum (17-25 oq (Piotrowski et al. 24) is above the average temperature of the regions with the highest proportion of threatened species in Ecuador; B. dendrobatidis' thermal optimum overlaps with the temperature of Andean Foothill forests and lowland regions where the proportion of threatened species is lower (Table 1). Analyses of the changes in assemblage structure in seven Andean localities reveal nonrandom patterns of population declines among taxonomic groups (Bustamante et al. 25). Comparisons between population surveys carried out before 1989 (mainly during the late 196s-early 197s) with surveys after 1999 show that the number of species of Strabomantidae (formerly "Eleutherodactylus") remained unchanged for all localities combined (28 species). In contrast, none of seven species of Atelopus were recorded after 2. Out of 12 species of Centrolenidae, 11 were less abundant and nine were completely absent in the recent surveys; similarly, all four species of Dendrobatidae declined and three were completely absent. Gastrotheca (four species) were present only at four out of nine historic localities. Atelopus, some Gastrotheca, Centrolenidae, and Dendrobatidae unlike the directdeveloping Pristimantis, have aquatic larvae. The higher occurrence of population declines among species with aquatic larvae reported by Bustamante et al. (25) is similar to patterns of change in amphibian assemblages in Central America (Lips et al. 23). B. Categories of Risk of Extinction Under Global Climatic Change 1. Effect of Climatic Change on the Size of Distributional Ranges Understanding how species will cope with projected future climatic change is of central importance for effective conservation and for management of biodiversity (Hannah et al. 22). During the past decade, species-climate "envelope" models have been used in a number of studies to predict the likely redistribution of species under a range of future scenarios of climatic change (e.g., Huntley et al. 1995; Peterson et al. 22; Thomas et al. 24; Araujo et al. 25; Malcom et al. 26). Only a few of these studies, however, have focused on amphibians (e.g., Teixeira and Arntzen 22; Parra-Olea et al. 25; Araujo et al. 26). The present authors evaluated the effect of climatic change on the distributions of 87 amphibian species with species-climate "envelope" models. The modelled species were those endemic to Ecuador and with the number of known unique localities greater than five. Species distributions were predicted under a scenario of climatic change that simulated conditions of doubled atmospheric levels of C 2 relative to preindustrial levels (climatic models from Duffy et al. [23] and Govindasamy et al. [23]). Doubled C 2 levels are expected to be reached in 5 years (IPCC, 21). Predicted distributions were built with the Maximum Entropy method (Maxent; see Phillips et al. [26] for a detailed description of the modelling procedure) under five dispersal scenarios: (1) no dispersal, (2) species dispersing at a rate of.2 km/year, (3) species dispersing at a rate of 1 km/year, (4) species dispersing at 1 km/year without crossing areas of cleared natural vegetation more than 1 km across, and (5) unlimited dispersal. Consequences of future climatic change on the distributions of Ecuadorian species are predicted to be rather severe under scenarios 1, 2, 3, and 4 (Fig. 11). If species were unable to disperse, by -25 amphibians would retain only 43% of their current distributional range (average change in area of the distribution range = -57%). Area of loss of range varied from 1% (Engystomops guayaco) to 95% (Atelopus longirostris, Hyloxalus sauli), highlighting greatly idiosyncratic responses across species. Under dispersal scenario 2 (.2 km/year), 82% of the species are expected to contract their ranges (average change in range = -36%). Under scenario 3 (1 km/year), 74% of the species will contract their ranges although average change in size of range is positive (3.9%). When current levels of habitat degradation and fragmentation were taken into account (scenario 4), the dispersal scenario

18 146 AMPHIBIAN BIOLOGY 15 5 r Temperature +..- co..- co..- co..- co..- co..- co..- (J) (J) C\J C\J (") (") '<t '<t L!) co co (J) (J) (J) (J) (J) (J) (J) (J) (J) (J) (J) Year co..- co... co... co L!) co co,..._,..._ co co (J) (J) (J) (J) (J) (J) (J)... (J) (J) E'.s 2 c 18 a. c:; 16 a.. 14 Cii :J c 12 <( COCJl (J)(J) (J)(J) Fig. 11. Percentage of species' range change between present and 25 under five dispersal scenarios: (1) ND = no dispersal; (2) MDD 1 km = maximum dispersal distance of 1 km; (3) MDD 5 km = maximum dispersal distance of 5 km; (4) MDD(HL-F) 5 km = maximum dispersal distance of 5 km considering habitat loss and fragmentation; and (5) UD = unlimited dispersal. The medians for the change in size of geographic range are shown (grey horizontal lines) with their respective 95% confidence interval (notches of boxes). The core boxes on boxplots indicate the interquartile range of data whereas the whisker lines extend to at most 1.5 the interquartile range from both ends of the box. Outliers are represented by asterisks. of 1 km/year resulted in a slightly higher number of species contracting their ranges (78%; Fig. 11) and an average change in range of -21.9%. Some species could extend their current distributions by more than 3% (e.g., Engystomops guayaco, Pristimantis glandulosus), whereas others will not gain new suitable habitat and are expected to contract their distributional ranges (e.g., Castro theca riobambae, Hyloxalus vertebralis, Osteocephalus fuscifacies ). If dispersion is assumed to be unlimited such that species' future distributions become the entire area projected by the climate-envelope model (scenario 5), 52% of the species are projected to substantially increase their distributional ranges (on average, an increase of 18% of range). Amphibians usually have low vagility and high site fidelity (Duellman and Trueb 1994; Sinsch 199; Blaustein et al. 1994b ), however, making the assumption of unlimited dispersal unrealistic, at least for some species. In Australia, Rhinella marina's rate of range expansion is 55 km/year (Phillips et al. 27), which falls under scenario 5 at the geographic scale of Ecuador. This high rate of expansion, however, seems to represent an extreme among anurans (Phillips et al. 27). Habitat destruction and fragmentation (which is occurring at a high rate) might drastically reduce suitable pathways for dispersal (e.g., Becker et al. 27) and could compromise the ability of amphibians to colonize suitable habitats under rapid climatic change (see section IV-D-1). The higher decrease in size of range in scenario 4 relative to scenario 3 is consistent with this prediction. Moreover, the estimates for scenario 4 are conservative because they are based on habitat-degradation levels of If the current deforestation rate is maintained (1.2% per year; see section IV-D-2), one would expect that less than one third of the natural vegetation present in 1996 will remain by 25. Overall, these results suggest that under most scenarios, global warming will exacerbate declines of

19 RON et al: BIODIVERSITY AND CONSERVATION STATUS OF AMPHIBIANS OF ECUADOR 147 Ecuadorian amphibian species and show the importance of rapid implementation of technologies for decreasing emissions of greenhouse gases to mitigate the effects of climatic change on amphibian diversity. 2. Species' Extinction Risks Under Future Climatic Change Over the past few years, a number of attempts at projecting effects of climatic change on biodiversity have used the IUCN Red List's criteria to estimate extinction risks based on projected shifts in range (e.g. Thomas et al. 24; Bomhard et al. 25; Thuiller et al. 25). Although the use of these criteria to identify species threatened by global warming remains highly controversial, some specific criteria (e.g. A3, B, D2) can be used to red-list species in the future (Akcakaya et al. 26). Furthermore, criterion A3(c) is probably the most straightforward way to assess species' risk of extinction under future climatic change (Akcakaya et al. 26). Appendix II shows the IUCN categories of extinction risk for 87 Ecuadorian endemic species for the year -25, according to the projected shifts in range based on speciesclimate envelope models under scenario 4. The evaluation is based on IUCN's Red-List criteria. For each species, current criteria were maintained except for criterion A3(c) (following Thuiller et al. 25) as well as criteria B1 and B2, which were reviewed according to projected changes on the size of distributional ranges. In line with criterion A3(c), the following thresholds were used: "Extinct" refers to a species with a projected loss of range of 1% in 5 years, "Critically " species have a projected loss of range of more than 8%, "" species have a projected range loss of more than 5%, "Vulnerable" species have a projected loss of range of more than 3%, "Near Threatened" species have a projected loss of range of less than 3% and species of "Least Concern" have no projected loss of range. Under the latter criteria (i.e. B 1 and B2), the quantitative thresholds specified in the IUCN Red List were applied. "Data Deficient" species were not re-evaluated because the modelling procedure does not increase the scant empirical data available. Our projections show that by -25 the number of threatened species will increase by 18%. Twenty six percent of the species will become Critically (up from 11% in the present), 51% (up from 38%), 8% Vulnerable (down from 17%), and 2% Near Threatened (down from 13%). Remarkably, just 3% of the species would be classified as low risk (down from 11% ). It should be emphasized that these results need cautious interpretation in the light of the many assumptions underlying the analyses. C. Threatened Species 1. Conservation Status of Frogs of the Genus Atelopus One of the taxonomic assemblages most affected by population declines worldwide is the genus Atelopus (La Marca et al. 25). These terrestrial, diurnal frogs are commonly associated with streams, where females deposit eggs and tadpoles develop (Reproductive Mode II, as defined by Duellman and Trueb [1994]). Habitats of these frogs include lowland tropical rainforests, cloud forests, and paramos at elevations as high as 4 5 m (Lotters 1996). The majority (7%) of the species are restricted to elevations > 1 m. Most have small distributional ranges and high regional endemism (Lotters 1996). At present, 21 described species in this genus are known to occur in Ecuador and at least 1 species are yet to be described (Coloma 25-27; Pounds et al. 26, L. A. Coloma, unpublished data). The following analysis of the conservation status of Atelopus pertains to these 31 species. Anecdotal information suggests that at least some species of Ecuadorian Atelopus were formerly locally abundant. In December 1864, the Spanish naturalist M. Jimenez de la Espada observed the occurrence of "thousands of individuals [A. ignescens] in the herbaceous and humid prairies close to streams, pools, and lakes" at Paramo del Antisana (Laguna de la Mica) Gimenez de la Espada 1875: 146). Field parties from the University of Kansas

20 148 AMPHIBIAN BIOLOGY documented high densities of Atelopus in the 196s and 197s (e.g., 194 individuals of A. ignescens [.81 individuals/person/min] at Ingaloma, Provincia de Pichincha, 3 78 m, 16 August 1968; 53 individuals of A. sp. (bomolochos complex;.88/pers/min) 2 km southwest of Santa Rosa, Provincia del Chimborazo, 3 7 m, 23 July 197; 53 individuals of A. sp. (bomolochos complex;.59 ind/pers/min) 11.2 km northwest of San Juan, Provincia del Chimborazo, 3 95 m, 12 July 1971 ). At Paramo del Anti sana, densities were as high as 5 individuals/m 2 in 1981 (Black 1982). In addition, there are reports of mass migrations that resulted in large numbers of individuals smashed across 1-8 km of highways in Provincia del Cotopaxi, Provincia del Tungurahua and Provincia de Bolivar in 1958, 1959 and 1985 (Peters 1973; Ron et al. 23). Despite their former abundance, efforts to find Atelopus above 1 5 m of elevation in the Andes of Ecuador since the mid 199s have been generally unsuccessful. Bustamante et al. (25) and Ron et al. (23) reported the absence of records of Atelopus in nearly 1 surveys at 21 localities in Ecuador between 1998 and 22. Except for one population of Atelopus sp. (spumarius complex) and one of Atelopus spumarius, records of Atelopus after 2 include only a few dozen individuals belonging to eleven species (see species accounts). Listed below is information suggesting population declines in Atelopus. Each species is accompanied by its distributional range, time of last documentation, population data (usually presence-absence at particular localities) and an estimate of the remaining natural vegetation within its range. In most cases, the population decline at a locality is inferred from the absence of the species after repeated visits. However, as Peters (1973) asserted, based on his observations of Atelopus in Ecuador during the 195s and 196s, the failure to record a species at a locality may be a consequence of seasonal fluctuations in local abundance or fluctuations in population size unrelated to long-term population declines. Therefore, the inference of a population decline based on absence data should be treated as tentative when it is based only on a few visits, especially if visits took place under similar environmental conditions. Estimates of remaining unaltered vegetation (i.e., natural vegetation that has not been cleared or fragmented) were obtained from a digital map of land use in Ecuador (AEE 2) within a radius of 5 km from the known localities for each species. Perhaps the best-documented case of population decline is that of Atelopus ignescens (reviewed by Ron et al. 23), an historically abundant species. This species is endemic to Ecuador. It was widely distributed in the northern and central Andes between 2 8 and 4 2 m elevation in Western Montane Forest, Andean Shrub, Paramo, and Eastern Montane Forest. It was recorded in areas heavily disturbed by humans such as backyards in Quito in 1959 and 1983 and in Latacunga in 1979 (]. A. Peters, L. A. Coloma, fieldnotes). This diurnal species was easily seen moving slowly on the ground. Perhaps as a consequence of its abundance, diurnal habits, and tolerance to habitat disturbance, it used to be well known by inhabitants of the Andes, especially Native Americans who live in the paramo. Unlike most Ecuadorian amphibians, Atelopus has a common name Uambato ), a word of Qui chua origin. The cultural prominence of Atelopus in the Ecuadorian Andes is exemplified by the fact that the third largest city in the Ecuadorian Andes, Ambato, was named after the A. ignescens that inhabited its main river. Despite its wide distribution, there is not a single record of Atelopus ignescens since 1988, except for a moribund tadpole presumably belonging to this species found in 1989, 22 km south of Ambato, Tungurahua Province. It is unlikely that the absence of records is a consequence of low search effort. Most known localities of A. ignescens are in regions of easy access that are visited frequently by herpetologists. Standardized surveys between 1999 and 21 with a search effort of person-minutes yielded no records even though they were carried out in regions where the natural vegetation remains undisturbed and the species was historically abundant (Ron et al. 23). Additional evidence of population decline comes from accounts by Native Americans who almost unanimously declare that Atelopus ignescens has not been seen for many years in the paramos, forests, and agricultural lands where they used to be abundant. Habitat degradation has been considerable with only 45.5% of the natural vegetation remaining unaltered at the known localities.

21 RON et al: BIODIVERSITI AND CONSERVATION STATUS OF AMPHIBIANS OF ECUADOR 149 Atelopus arthuri was only known from three nearby localities in Western Montane Forest in Bolivar Province and Chimborazo Province. Although regularly recorded at Bosque Protector Cashca-Totoras during the mid 198s, searches to find the species since 1989 have been unsuccessful despite great effort (e.g., per/min between 1999 and 22) (Bustamante et al. 25). Tadpoles of Gastrotheca pseustes collected at this locality in September 1999 tested positive for chytridiomycosis (Merino-Viteri 21). There are no records of A. arthuri from the type locality since the 19 specimens collected on 14 February 1959, by J. A. Peters (type series). Habitat degradation has been severe; only 15.4% of the natural vegetation remains unaltered. Atelopus balios was known from six localities in the lowlands of southwestern Ecuador. A single individual of this species was recently recorded (October 21 ) in the vicinities of Manta Real by a QCAZ party. Before this record, the species was recorded for the last time in 1995 at Rio Patul (Azuay and Caftar provinces). Five visits to Rio Patul and Manta Real failed to record this species between 1997 and 2; 51.6% of the natural vegetation remains unaltered at the five localities. Two specimens of this species collected at Rio Patul (elevation 35 m) in 1992 showed clinical signs of chytridiomycosis and tested positive for Batrachochytrium dendrobatidis (A. Blasco-Zuniga, P. A. Menendez-Guerrero, and C. Proafto Bolaftos, unpublished). Atelopus bomolochos sensu stricto (see also Atelopus sp. bomolochos complex) was known from six localities (Sevilla de Oro, Cuenca, Juncal-General Morales, Ingapirca, Sigsig, Cutchil) in the Interandean Region, in provinces Azuay and Caftar (Coloma et al. 27, Coloma 25-28). It had a small distribution encompassing Paramo, Montane Forest, and Andean Shrub (from latitude 1 3'S south to Azuay Province). It was recorded for the last time in 29 April 199 at Sigsig. One individual collected in Caftar Province in 198 tested positive for chytridiomycosis (Merino-Viteri 21) and is the oldest record of the chytrid in Ecuador. Atelopus sp. (bomolochos complex) used to be abundant, at least at some localities, in the Paramo region in Chimborazo and Bolivar provinces. For example, in October 1991 L. A. Coloma recorded 45 specimens at Laguna de Atillo in a single day. Some of those specimens were obviously unhealthy when found and a sample of five of them tested positive for chytridiomycosis (Merino-Viteri 21). Mterwards (1994, 1995, 21, 22, 23, 26), six visits to Laguna de Atillo failed to uncover A. sp. (tadpoles of Gastrotheca pseustes collected during the 21 visit also tested positive for chytridiomycosis after metamorphosing in captivity [S. R. Ron and L. Berger, unpublished]). The latest record for A. sp. was April 22 when a female (QCAZ 21123) was found in Laguna de Frutatian, Chimborazo Province, by D. Almeida-Reinoso. Four experienced herpetologists searching for several hours at the same locality in May 23 were unable to find the species (M. R. Bustamante, personal communication). As with A. ignescens, accounts by Native Americans also indicate the absence of A. sp. in the paramos and agricultural lands where the species used to be encountered frequently. Atelopus coynei was known from five localities in Western Foothill Forest, Western Montane Forest, and Andean Shrub (Pichincha, Imbabura, and Carchi provinces; elevational range m). It was recorded for the last time in 1984 at the headwaters of Rio Baboso, near Lita, Carchi Province (QCAZ, database). In 21, diurnal and nocturnal surveys (capture effort = 2 28 person-minutes) failed to record the species at one of its historic localities, Rio Faisanes (Bustamante et al. 25). Habitat degradation has been significant with only 18.4% of the natural vegetation remaining unaltered at the localities previously known to be inhabited by this species. Atelopus elegans is known from 13 localities in the Western Foothill Forest and Chocoan Tropical Rainforest (elevational range m) (Lotters 1996; QCAZ database). A photographic record of a single individual was made in 26 from the Alto Tambo region (Esmeraldas Province) and eight individuals were found in 29 near Durango (Esmeraldas Province) by a field party from QCAZ. The previous documented record was 1994 at La Mana (Cotopaxi Province; QCAZ database). At 5 km northwest of La Florida, Pichincha

22 15 AMPHIBIAN BIOLOGY Province, this species was not found during nine visits made by parties from QCAZ between 1989 and 22 (L. A. Coloma, fieldnotes; QCAZ database). Searches in the Rio Bogota region (2 832 per/min) by a QCAZ party in May 26 yielded no records. Additional visits by QCAZ parties to Rio Bogota-Lita and La Mana in 27 also yielded no records. Habitat degradation has been significant. Only 23.9% of the natural vegetation remains unaltered at the previously inhabited localities. Atelopus exiguus is known from Laguna de Zurucuchu ( = Llaviuco) and nearby localities in Paramo, Andean Shrub, and Eastern Montane Forest at Parque Nacional Cajas and Bosque Protector Mazan in southern Ecuador (Azuay Province; elevational range m). It used to be abundant until the mid 199s. At present, only two populations consisting of a few individuals are known to persist (Mazan Forest and Paramo Quimsacocha, Azuay Province) (Toral et al. 25, E. Arbelaez and A. Merino-Viteri 26 and 27 fieldnotes; Moore 28). On a visit to the Mazan Forest in September 27, two juveniles were found indicating that the population is breeding. (S. R. Ron fieldnotes). Anecdotal data of its abundance were provided by M. Read (cited by Coloma et al. 2). Only 53.6% of the natural vegetation remains unaltered at its known localities. Atelopus guanujo (Coloma 22) used to be common within its narrow distributional range at two localities in the upper Rio Chimbo valley ( m; Western Montane Forest) in Bolivar Province. Despite its conspicuous, bright orange coloration, A. guanujo has not been seen since 1988 (Coloma 22). Repeated efforts to find it during the 199s made by parties from QCAZ have been unsuccessful (Coloma 22). Habitat degradation has been severe with only 19.8% of the natural vegetation being unaltered at Guanujo (the type locality). Atelopus longirostris was known from 14 localities in Chocoan Tropical Rainforest, Western Foothill Forest, and Western Montane Forest below 2 5 m. In Rio Faisanes (Pichincha Province), a field party from the University of Kansas recorded eight individuals in 12 person-minutes of search in (W. E. Duellman, personal communication). The last record of this species was in 1989 (QCAZ ) from near San Francisco de Las Pampas. Although not all the localities were surveyed after 1989, repeated visits to San Francisco de Las Pampas, Mindo, Alto Tambo, and Rio Faisanes made by parties from QCAZ have been unsuccessful in finding this species (e.g., at Rio Faisanes in 21 a search effort of 2 28 person-minutes yielded no specimens) (Bustamante et al. 25). Atelopus longirostris was sympatric with A. mindoensis in the region of San Francisco de Las Pampas and at Mindo. Only 12.3% of the natural vegetation remains unaltered at the previously inhabited localities. Atelopus lynchi was mainly distributed in southern Colombia. In Ecuador, it was known only from Maldonado, a locality in Western Montane Forest, close to the Colombian border (Carchi Province; elevation 1 41 m). It was recorded for the last time in Ecuador in 1984 (University of Kansas Natural History Museum database). Three visits to Maldonado (between 1989 and 1999) made by QCAZ field parties have failed to find the species. At Maldonado, 89.9% of the vegetation cover remains unaltered. Atelopus mindoensis is known from more than ten localities in Western Foothill and Western Montane forests in northern Ecuador. Its elevational range is m (Peters 1973; QCAZ database). At Quebrada de Zapadores it was abundant in 1975 when a field party from the University of Kansas found 128 individuals with a capture effort of 2 44 person-minutes (W. E. Duellman, personal communication). It was recorded for the last time in 1989 (QCAZ 987) and repeated visits to three localities have yielded no specimens. Surveys at Quebrada de Zap adores in failed to record the species even though search effort was higher than in the 1975 surveys (3 479 person-minutes) (Bustamante et al. 25). Habitat degradation has been severe. None of the natural vegetation remains unaltered at the previously inhabited localities. Fragmented natural vegetation covers 59.7% of the area, with pastures and agricultural crops occupying the rest. Atelopus nanay is only known from the type locality, Paramo del Cajas, a protected area in the southwestern Andes of Ecuador and a nearby site, Patul (E. Arbelaez, unpublished).

23 RON et al: BIODIVERSITI' AND CONSERVATION STATUS OF AMPHIBIANS OF ECUADOR 151 Infrequent efforts to find A. nanay at Paramo del Cajas made by parties from QCAZ (nine visits between 1991 and 27) yielded no specimens. Nonetheless, one individual was sighted in 27 and seven females were found in March-May 28 at Patul (E. Arbelaez, unpublished). Individuals found since 28 have been brought to captivity by two institutions (Amaru Zoo and Balsa de los Sapos at QCAZ) as part of ex situ conservation efforts. A Telmatobius niger that was collected simultaneously with individuals of A. nanay in 1989 tested positive for chytridiomycosis. Tadpoles of Gastrotheca pseustes collected at the type locality in December 1999 also tested positive for this disease when allowed to metamorphose in the laboratory (Merino-Viteri 21). Habitat degradation has been low at the type locality of A. nanay (92% of the natural vegetation remains unaltered) but is heavily altered at Patul. Atelopus onorei was known from two localities in Western Montane Forest in Azuay province (2 5 m). It was recorded for the last time in 21 April 199 (QCAZ 344, 3442). Since 199, four visits to the type locality in November 1992, February 1993, April 1993 and October 1993 have failed to record this species (Coloma et al. 27). Atelopus palmatus is known from several localities in Eastern Montane Forest in N apo and Pastaza provinces. The taxonomic uncertainty that involves this species precludes an evaluation of its status (Quiguango-Ubillus and Coloma 27). Nonetheless, a population possibly belonging to this species was found in 26 at an elevation of 1 7 m, near Nueve de Octubre, Morona-Santiago province. Atelopus planispina was known from five localities in the Eastern Montane Forest (5-1 8 m) of Provincia de Napo, Sucumbios and Morona-Santiago provinces. It was recorded for the last time in 1988 at La Tercera, near El Reventador (MHNG ). In 1971, a field party from the University of Kansas found nine individuals at Rio Azuela (Sucumbios Province) with a search effort of 4 32 person-minutes (W. E. Duellman, personal communication). Surveys at the same locality in 2 and 21 failed to record the species even though capture effort was higher (5 449 person-minutes) (Bustamante et al. 25). Searches between 2 and 24 at the surroundings of Cascada de San Rafael (Napo Province) also failed to find the species. Only 53.5% of the natural vegetation remains unaltered at the previously inhabited localities. Atelopus petersi was known from four localities in Western and Eastern Montane Forest in Napo and Chimborazo provinces (elevational range m). It was recorded for the last time in November 8, 1996, 1 km east of Oyacachi (one individual found dead) Coloma et al. 27). Since 199, repeated visits to Atillo, Papallacta, and Oyacachi have failed to record this species. Most (78.6%) of the natural vegetation remains unaltered at the previously inhabited localities. An undescribed species of Atelopus (formerly included within A. ignescens) is distributed in the northern Andes of Ecuador, in Imbabura and Carchi provinces (elevational range m) and in southern Colombia (Departamento Narifio). Rueda-Almonacid et al. (24), pastuso provided information of its absence in southern Colombia and categorized the species as Critically. In Ecuador, this species was recorded for the last time in January 1993 near Laguna Cuicocha (Imbabura Province) and March 1993 at Paramo El Angel (QCAZ database). On 18 May 1975 a field party from the University of Kansas recorded 9 individuals (.5 ind/pers/min) at Paramo El Angel (Carchi Province; 3 35 m) indicating that the species was formerly abundant. One of two individuals found at El Angel in 1993 was evidently unhealthy (L. A. Coloma, fieldnotes) and tested positive for chytridiomycosis (Merino-Viteri 21). Individuals collected in the Cuicocha area in October 1992 and January 1993 also tested positive (Merino-Viteri 21 ). On 29 June 1993, six individuals were found dead and six alive in the Cuicocha region during one hour of searching (E. Almeida and E. Varela, park guards notes). Visits to Cuicocha in April and May 1996 and to El Angel in March and December 1997 and January 1999 failed to record the species. Only 45.5% of the natural vegetation remains unaltered at the previously inhabited localities.

24 152 AMPHIBIAN BIOLOGY The only species of Atelopus that has been regularly recorded in the field during the past decade is an undescribed species belonging to the A. spumarius complex. It is distributed in southeastern Ecuador between 7 and I 7 min the Eastern Foothill Forest and Eastern Montane Forest. Habitat degradation has been significant in the region with only 31.3% of the natural vegetation remaining unaltered. Five visits to a single locality (6.6 km north of Limon, Morona-Santiago Province) were made between 23 and 24 (QCAZ database; S. R. Ron and L. A. Coloma fieldnotes) and a systematic monitoring programme at this locality was carried out between November 24 and December 25. During the monitoring period, 219 individuals were found; there was a scarcity of tadpoles and juvenile stages (Salazar-Valenzuela, 27). At least 25 individuals were infected by chytrid fungus (Merino-Viteri et al. unpublished). During population surveys between December 27 and April 28, 79 individuals were recorded, several of which were recaptures from (D. Salazar-Valenzuela, unpublished). A centrolenid (Hyalinobatrachium pellucidum; QCAZ 2595) found moribund at the same locality tested positive for chytridiomycosis (Table 4). Table 4. Ecuadorian amphibian species reported to be positive for chytridiomycosis. Species Provincia: Locality Year of Collection Diagnosed by: Source Atelopus balios Canar: 1992 A. Blasco-Zuniga A. Blasco-Zuniga, Rio Patul Verified by P. A. Menendez-Guerrero, J. Longcore C. Proano-Bo1anos (unpublished) Atelopus bomolochos Canar: 198 A. Merino-Viteri Merino-Viteri (21) (sensu stricto) (unknown) Verified by S. R. Ron Atelopus bomolochos Chimborazo: 1991 L. Berger, Merino-Viteri (21) complex Lagunas de Atillo A. Merino-Viteri Atelopus Imbabura: Cuicocha 1992 L. Berger, Merino-Viteri (21) aff. ignescens A. Merino-Viteri Atelopus Imbabura: 9 km E Cuicocha 1993 L. Berger, Merino-Viteri (2 1) aff. ignescens A. Merino-Viteri Atelopus Carchi: 42 km Tulcan 1993 L. Berger, Merino-Viteri (2 1) aff. ignescens A. Merino-Viteri Atelopus sp. Pichincha: Otongoro 1987 L. Berger, S. Ron Present chapter Atelopus sp. Marana-Santiago: C. Proano, M. Levy Proano et al. (27) (spumarius complex) 6.6 km N from Lim6n Gastrotheca pseustes Azuay: 1998 L. Berger, Merino-Viteri (21) 4 km Laguna A. Merino-Viteri La Toreadora Gastrotheca pseustes Bolivar: 1999 L. Berger, Merino-Viteri (2 1) Cashca-Totoras A. Merino-Viteri Gastrotheca pseustes Chimborazo: 21 L. Berger, S. Ron Present chapter Lagunas de Atillo Gastrotheca pseustes Cotopaxi: 21 L. Berger, S. Ron Present chapter Limpiopungo Hyalinobatrachium Morona Santiago: 23 A. Merino-Viteri Ron (25) pellucidum 6.6 km N from Li.J.n6n Hyla larinopygion Carchi: 1989 L. Berger, Merino-Viteri (2 1) complex via Tulcan-Santa Barbara A. Merino-Viteri Telmatobius niger Azuay: 4 km 1989 L. Berger, Merino-Viteri (2 1) Laguna La Toreadora A. Merino-Viteri

25 RON et al: BIODIVERSilY AND CONSERVATION STATUS OF AMPHIBIANS OF ECUADOR 153 Atelopus spumarius was recorded in Ecuador for the first time in 1994 and is known from four localities in the Amazon Basin. At Rio Pucayacu at the Ecology Center Shanca Arajuno in the Puyo region (Pastaza Province), several adult individuals and tadpoles have been found between (L. A. Coloma, S. R. Ron, P. Pefia, fieldnotes). Markrecapture surveys carried out between July and December 29 recorded 94 individuals (Ron et al. unpublished). The most immediate threat to this population is deforestation, which is occurring at a rapid rate. Almost all (99.3%) the natural vegetation at the known localities (except Rio Pucayacu) remains unaltered. The status of the other species of Atelopus in Ecuador is less certain. Almost nothing is known about the status of populations of A. boulengeri, A. halihelos, A. nepiozomus and seven undescribed species. Field work in their distributional ranges has been extremely infrequent. The available information suggests that the populations of approximately 19 species of Ecuadorian Atelopus have declined. The statuses of the remaining 12 species are unknown. Habitat loss, climatic change and/or diseases, acting since the late 198s, are likely causes of population declines of Atelopus and other Andean amphibians. The fungal disease chytridiomycosis has been reported in six species of Atelopus (Table 4). Atelopus infected with chytridiomycosis have been found in the field in an evidently unhealthy condition (Merino-Viteri 21; Ron et al. 23). In addition, there are records of chytridiomycosis between 198 and 23 from four localities where Atelopus occurred (elevational range -1-4 m; see Table 4). Findings of dozens of Atelopus sp. at the Limon population between December 27 and May 28 suggest that this population can persist in the presence of the chytrid. Infected individuals have been found in 25, 26, and 28 (Proafio et al. 27; Ron et al. unpublished). An alternative (or synergistic) factor that has been invoked to explain declines in Atelopus has been climatic change (Pounds et al. 26). Unusually dry and warm conditions along the Ecuadorian Andes prevailed in 1987, and 23, at the time when populations of Atelopus ignescens and other species were declining (Ron et al. 23; Merino Viteri et al. 25; see section IV-D-1). The declines of Atelopus in Ecuador are part of a general process that has affected this genus throughout most of its distributional range, including Costa Rica (Lips 1998), Panama (Lips 1999), Venezuela (La Marca and Lotters 1997; Bonaccorso et al. 23 ), Colombia (Rueda-Almonacid et al. 24) and Peru (Vial and Saylor 1993). Comprehensive reviews of the population status of the genus and possible causes for declines have been published recently (La Marca et al. 25; Pounds et al. 26). 2. Conservation Status of Frogs of the Genus Telmatobius Ecuador is inhabited by three endemic species of Telmatobius (central and southern Andes): T. cirrhacelis, T. niger and T. vellardi. Their population status has been addressed by Merino-Viteri et al. (25 ), who provided data on presence-absence at historic localities and discussed climatic changes and diseases as presumptive causes for population declines. Telmatobius have not been recorded in Ecuador since 1994 (data from 14 localities). Between 1985 and 199, 31% of the preserved specimens (except larvae) had some type of disease or abnormality. Additionally, 1% of tadpoles collected between 1989 and 1994 have morphological anomalies, including extra limbs, limb malformations, and epidermal disorders. Chytridiomycosis has been found in Telmatobius (Table 4) and symptoms of an unknown disease have also been reported (Merino-Viteri et al. 25 ). Analyses of climatic data from three meteorological stations from the Andes of southern Ecuador indicate the co-occurrence of high temperatures and low precipitation at the time when diseases were diagnosed and population declines presumptively occurred (Merino-Viteri et al. 25). Diseases and/or climatic abnormalities in the Ecuadorian Andes may have been involved in the population declines of Telmatobius in Ecuador during the late 198s and early 199s. Telmatobius cirrhacelis is known from Eastern Montane Forest at three localities in the Abra de Zamora (Loja and Zamora-Chinchipe provinces, elevational range

26 154 AMPHIBIAN BIOLOGY m) in southern Ecuador. This species has not been recorded since March 1987, despite ten surveys at the type locality. Telmatobius niger was widely distributed between Chimborazo Province in the north and Azuay Province in the south, in Western Montane Forest, Paramo, and Eastern Montane Forest. Its distributional area comprises 1 74 km 2 (elevational range m). Only 13.5% (1 444 km 2 ) of its estimated area of distribution is inside the Ecuadorian System of Natural Protected Areas, mostly at Parque Nacional Cajas (Merino-Viteri et al. 25). Telmatobius niger has not been recorded since The absence of records is puzzling considering its historically wide distribution (Merino-Viteri et al. 25). Telmatobius vellardi is known from six localities in Eastern Montane Forest, Paramo, and Andean Shrub (Loja and Zamora-Chinchipe provinces; elevational range m). Its estimated area of distribution (236.5 km 2 ) is mostly outside protected areas. The information available for evaluating the status of T. vellardi is scarce (Merino-Viteri et al. 25). This species was last recorded in 1987 near Centro Administrativo Cajanuma (Provincia de Loja; Merino-Viteri et al. 25). 3. Conservation Status of Frogs of the Genus Hyloxalus Coloma ( 1995) considered the status of populations of Hyloxalus (then Colostethus) jacobuspetersi, H. vertebralis, H. elachyhistus, H. awa, H. maquipucuna, H. lehmanni to be of concern, as well as that of three species from the Reventador area and the Quijos-Topo depression on the eastern slopes of Cordillera Oriental (H. Juliginosus, H. pulchellus, and H. shuar). Herein those accounts are updated. Hyloxalus jacobuspetersi was not recorded since 1989, in spite of its historically wide distribution in the higher parts of the Cordillera Occidental. Bustamante et al. (25) provided absence data for H. jacobuspetersi at Cashca-Totoras (Bolivar Province). Nonetheless, a small relictual population was found in 28 (M. Read, unpublished) in the environs of Quito. Hyloxalus pulchellus has been found recently at Yanayacu Reserve (Pichincha Province near Cosanga) and Rio Azuela (Napo Province) (Bustamante et al. 25). Overall, survey efforts have been scarce except in Papallacta and its surroundings. The most recent record at Papallacta is September Searches in 1996, 1997, 1999, 21 and 22 yielded no records. Hyloxalus vertebralis is absent from most of its historic range, particularly at Parque N acional del Cajas; populations have recently been recorded, however, at El Jordan, Paguancay, Azuay Province (Cordillera Oriental) and in the city of Cuenca (L. A. Coloma, fieldnotes, 24, 26; E. Arbelaez, fieldnotes, 27, 28). Habitat at El Jordan comprises pasturelands and secondary vegetation near human habitations, whereas at Cuenca an isolated population was found in a swampy pasture, surrounded by houses and streets inside an urbanized part of the city. Surveys petween 1988 and 24 in the vicinities of El Reventador and the Quijos-Topo depression on the eastern slopes of the Cordillera Oriental revealed the presence of H. bocagei and H. pulchellus, whereas H. fuliginosus, and H. shuar were not found (Bustamante et al. 25; QCAZ database). Hyloxalus awa from the western Andean slopes and tropical lowlands has been recorded frequently in the lower portion of its elevational range at localities such as Union del Toachi (Pichincha Province; 9 m). Bustamante et al. (25) provided absence data at Rio Faisanes ( m). Since the 199s, there have been significant survey efforts at localities where Hyloxalus lehmanni previously occurred (Tandapi, San Francisco de Las Pampas and surroundings). The surveys, carried out by field parties from QCAZ, have not yielded any records of the species. A similar case is that of H. whymperi which also occurred at San Francisco de Las Pampas. Hyloxalus delatorreae was monitored between September 25 and August 26 at

27 RON et al: BIODIVERSITI AND CONSERVATION STATUS OF AMPHIBIANS OF ECUADOR 155 Canon del Moran, Carchi Province, near its type locality (Yanez-Munoz and Meza-Ramos 26). They estimated a population size of 25 individuals. The status of other species from Montane and Foothill forests (H. anthracinus, H. chocoensis, H. elachyhistus, H. exasperatus, H. fallax, H. infraguttatus, H. maquipucuna, H. marmoreoventris, H. mystax, H. nexipus, H. peculiaris and H. pumilus), inhabiting regions over 1 m in elevation, is unknown because of poor sampling efforts. 4. Conservation Status of Glassfrogs (Family Centrolenidae) Although, precise data on the population changes experienced by glassfrogs are lacking, it is important to provide a first approximation of their conservation status. Herein, the focus is on the species listed as Critically (Appendix I). Species' names follow the proposal by Guayasamin et al. (29). Cochranella balionota has been reported from two localities in the provinces of Pichincha and Carchi at elevations between 1 4 and 1 54 m. It was relatively abundant at the type locality (3.5 km NE of Mindo) where 13 individuals were observed in two nights (7-8 April 1975) (Duellman, 1981). The last report of the species was on November 1984, and recent surveys near the type locality have failed to find this species (J. M. Guayasamin personal observations). Habitat around the town of Mindo is fragmented, but searches in pristine areas nearby (e.g., Mindo Biology Station) were also unsuccessful. Centrolene hallux is known from four localities in the Province of Pichincha (Ecuador) and one in the Department of Narino (Colombia). Recent surveys in Quebrada Zapadores (search effort 58 hours/person) (Bustamante et al. 25) and historical localities around Chiriboga have been unsuccessful in finding the species (J. M. Guayasamin personal observations). Recently (March 29), a population was found at Reserva Las Gralarias, in northwestern Ecuador. Centrolene buckleyi had an historical distribution that included the Andes of Colombia and Ecuador, to Huacambamba in the Piura department in northern Peru (Duellman and Wild, 1993). In Ecuador, this species was locally abundant at Papallacta, El Carmelo, Pilal6, and Saraguro (W. E. Duellman field notes; KU database). Other localities included interandean valleys, being the only glassfrog with historical records in Quito (last record in Quito in March 1983 from Chillogallo; L. A. Coloma and A. Almendariz, field notes). Bustamante et al. (25) systematically visited two historical localities where C. buckleyi was relatively common, Pilal6 and Bosque Protector Cashca-Totoras. Surveys during three years at Cashca-Totoras (search effort of hours/person) yielded only three tadpoles. At Pilal6, the species has not been observed in recent surveys (search effort of 36.6 hours/person) (Bustamante et al. 25). At present, C. buckleyi is known to persist at three localities: Yanayacu Biological Station (Napo Province), Sigchos (Cotopaxi Province), and Reserva Las Gralarias (Pichincha Province). Population declines are likely to be partly a consequence of habitat deterioration, especially in interandean valleys. At localities where natural vegetation still persists, reasons for declines remain unclear. Centrolene geckoideum was the first centrolenid to be described (Jimenez de la Espada, 1872). Also, this is the largest species of the family (maximum body size = 81 mm). In Ecuador, it is known from three localities in the north (Carchi and Pichincha provinces). Intensive field work at historical localities (Quebrada Zapadores and streams nearby) has failed to find this species (Bustamante et al. 25;]. M. Guayasamin personal observations). Natural vegetation at Quebrada Zapadores has been modified to pastures for cattle raising, but streams nearby seem relatively undisturbed. The last records of C. geckoideum in Ecuador are from Rio La Plata (Carchi provincia) on 25 July 1988, and a small population from Rio Guajalito Protected Forest (Pichincha Province) observed in 1998 and 1999 (Cisneros Heredia and McDiarmid, 27; Cisneros-Heredia and Yanez-Munoz, 27). In Ecuador, Centrolene heloderma has been recorded from four localities in the Pichincha Province at elevations between 1 96 and 2 16 m. This species seems to have had drastic

28 156 AMPHIBIAN BIOLOGY population declines. At the type locality (Quebrada Zapadores), it was last recorded in March This locality, as well as nearby streams, have been visited numerous times between 2 and 26 during wet and dry seasons with no records of the species (Bustamante 26;]. M. Guayasamin personal observations). Recently (March 29), a population was found at Reserva Las Gralarias, in northwestern Ecuador. Centrolene lynchi is known from six localities on the western Andean slope of the Andes. In most of its range, the species has not been recorded in the past 24 years (last record on 2 April 1984 from 1.4 km SW of Tandayapa) despite recent surveys at two historical localities where habitat has not been severely disturbed (Tandayapa, San Francisco de Las Pampas; J. M. Guayasamin, personal observations). However, a population was found recently at Reserva Las Gralarias. In Ecuador, Centrolene medemi is known from a single stream near Volcan Reventador at 1 49 m ( 19 March ). The lack of new reports in more than 3 years suggests a limited distribution and/or low densities. The habitat near Volcan Reventador is in relatively good condition. Centrolene pipilatum is endemic to cloud forests on the Amazonian slope of the Ecuadorian Andes at elevations between 1 42 and 1 91 m. The last confirmed report of this species was at Rio Salado on July Recent surveys at Rio Azuela (Bustamante et al. 25; J. M. Guayasamin, personal observations) and the type locality (16.5 km NNE of Santa Rosa; J. M. Guayasamin, personal observations) have failed to find the species. Hyalinobatrachium pellucidum is an endemic species of the Amazonian slopes of the Ecuadorian Andes, only known from two localities, Rio Azuela (Sucumbios Province) and 6.6 km N of Limon (Morona Santiago Province). At Rio Azuela, this species has not been seen since 1971, despite recent surveys (search effort 9.83 hours/person) (Bustamante et al. 25). Population densities at Limon are low and one specimen collected in 23 tested positive for chytridiomycosis (A. Merino personal communication, cited by Ron 25). Nymphargus anomalus is known from the type locality (a rivulet flowing into the Rio Azuela on the east slope of Volcan Reventador at 1 74 m), Volcan Sumaco, and Rio Yana Challuwa Yaku. At Rio Azuela, this species has not been found in more than 3 years (since 23 October 1971) despite recent surveys (search effort 9.83 hours/person) (Bustamante et al. 25). Only during 29, the present authors discovered the Sumaco and Yana Challuwa Yaku populations. Nymphargus megacheirus is endemic to the Amazonian slope of the Andes of Ecuador and Colombia at elevations between 1 3 and m. In Ecuador, this species has been reported from the provinces of Napo and Sucumbios. The last records of N. megacheirus correspond to specimens collected at Rio Azuela and Rio Salado on 24 February 1979 (USNM Database). Recent surveys at Rio Azuela have failed in finding the species (Bustamante et al. 25). The available information suggests that 11 species of glassfrogs are Critically, representing 24.4% of the diversity of the family in Ecuador. Additionally, Centrolene audax is and Hyalinobatrachium valerioi is Vulnerable. Eight species fall in the category of Least Concern, most of which are found in the Amazonian lowlands (Appendix I). The remaining 22 taxa are Data Deficient. Centrolenids inhabiting the Chocoan Tropical Rainforest and interandean valleys are likely to be affected by fragmentation and destruction of their habitat. Natural vegetation in the Choco has been reduced to only about 18% of its original area (Table 2), and the deforestation rate remains alarmingly high. Recent field work (22-29) in the Ecuadorian Choco resulted in ten new species records for Ecuador (Espadarana callistomma, Cochranella litoralis, C. mache, Rulyrana orejuela, Hyalinobatrachium aureoguttatum, H. fleischmanni, Nymphargus siren, Sachatamia albomaculata, Teratohyla pulverata, T. sornowi); given that these species are poorly known in Ecuador, they are listed as Data Deficient. However, it is likely

29 RON et al: BIODIVERSITI' AND CONSERVATION STATUS OF AMPHIBIANS OF ECUADOR 157 that these species are restricted to the Chocoan Tropical Rainforest. If that is the case, they should be considered as threatened. It is relevant that all Chocoan and most Amazonian glassfrogs have been observed in recent years, whereas several Andean species have not been seen in more than 2 years. All species listed as Critically are restricted to the Andes (Appendix I). Explaining the population declines of these 11 species is challenging. Habitat loss is likely to have affected some populations (e.g., Centrolene balionotum, C. buckleyi), but several others have disappeared from apparently undisturbed areas. At the moment, data needed to establish the causal factor for these declines and possible extinctions are lacking. Only for Hyalinobatrachium pellucidum is there evidence that may explain a possible population decline. An evidently unhealthy individual of H. pellucidum tested positive for the fungal disease chytridiomycosis (A. Merino-Viteri personal communication, cited by Ron 25). A possible link between the chytrid fungus (Batrachochytrium dendrobatidis) and subsequent mass mortality of amphibians has been reported from El Cope, Panama (Lips et al. 26) where B. dendrobatidis was discovered one month after an abrupt decline of amphibian density and species richness in both diurnal and nocturnal riparian amphibian communities (Lips et al. 26). Other possible factors affecting glassfrogs include climatic change and habitat degradation. Unfortunately, the lack of continuous historical records of population numbers makes it impossible to test for correlations between disease outbreaks, unusual climatic conditions, habitat degradation, and population crashes (_) g. - E Q) E... :::::l - c: 2 -C1:S... :;::::; Q).. C1:S a.. - E '(3 16 Q)... C1:S a_ 14 '4 :::::l 9 c: C1:S c: :::::l <( c: 12 c: c: <( C1:S Q) Precipitation J 6 5 Fig. '12. Mean annual temperature and annual precipitation in the Quito valley, Provincia del Pichincha, Ecuador between 1891 and 26 (updated from Ron et al. 23). Temperature and precipitation values for are from the Astronomical Observatory climate station; values for are predicted from climate at Izobamba and linear regressions between Izobamba and Astronomical Observatory (period ); see Ron et al. (23) for details. Both stations are in the Quito valley. The grey line is the worldwide average temperature. The late 198s and 199s were characterized by a combination of extremely dry and warm conditions in the Ecuadorian Andes (especially in 1987).

30 158 AMPHIBIAN BIOLOGY D. Potential Threats to Amphibians in Ecuador 1. Global Changes in Climate There is strong evidence indicating that ambient temperatures are increasing on a global scale with already noticeable effects on the distributions and/or phenology of plants, birds, insects, amphibians, and fish (Parmesan and Yohe 23). Temperatures in the Amazon Basin and on the Andean slopes could increase -3 oc over the next century (Boer et al. 21). At present, the global increase in mean annual temperature has been approximately. 76 oc (IPCC 27). The magnitude of increase, however, varies regionally. In the Ecuadorian Andes in particular, the rise in temperature seems to be much greater than the World average (Fig. 12) (Ron et al. 23; Merino-Viteri et al. 25). In the Quito valley, for example, temperature has increased 2.1 C during the past century (Ron et al. 23). In other Andean localities (urban and rural) in Ecuador, the increase has been comparable to, or even higher than, that observed in Quito (Merino-Viteri et al. 25 ). Amphibians are expected to be especially affected by simultaneously dry and warm climate because heat increases evaporative loss of water through the skin. Extreme combinations of dry and warm climate were prevalent within the distributional range of Atelopus ignescens during the late 198s, precisely when the last individuals of this species were seen alive (Ron et al. 23). Although a cause-and-effect link between climatic changes and the decline of Ecuadorian amphibians in the Andes has not been demonstrated, the co-occurrence of extreme climate and amphibian declines during the late 198s and 199s is compatible with that hypothesis. Because of the large magnitude of the increase in temperature in the Ecuadorian Andes, the effects on the biota are expected to be more severe and phylogenetically generalized than in other regions. When a species faces adverse changes in climate, possible outcomes are: (1) the individuals acclimatize homeostatically (no evolutionary change) to the new conditions, (2) the species adapts evolutionarily (via natural selection) to the new conditions, (3) the species changes its distributional range, tracking the movement of their climatic envelope, and/or (4) the species becomes extinct. Laboratory studies have documented a significant capacity of amphibians to acclimatize homeostatically to temperature changes (Brattstrom 1968, 197). Variation among species is substantial and is influenced by latitude and longitude. The capacity of acclimatization is positively correlated with size of geographic range (Brattstrom, 1968, 197). This suggests that species living in tropical mountains should have narrower homeostatic capacity because they tend to have smaller ranges (Pounds et al. 26). Interaction with other variables in nature (e.g., evaporative loss of water, disease) could also influence homeostatic responses in wild amphibians. The ex-situ evidence shows that homeostatic responses can be frequently within the range of observed climatic change (Brattstrom 1968, 197). Studies of wild amphibians are needed to understand interactions with other factors. Little is known about the capacity of amphibians to adapt evolutionarily to long-term climatic changes. However, climatic fluctuations in the Neotropical region during the Pleistocene and Holocene (including warmer-than-present conditions) might have been a selective force (both at the interspecific and intraspecific levels) favouring evolutionary plasticity capable of coping with climatic change. Under the third outcome mentioned above, Andean amphibians are expected to move upwards along elevational gradients. The capacity of amphibians to avoid extinction by tracking the movement of their climatic envelope will depend upon their dispersal ability (which, compared to that of other terrestrial vertebrates, is known to be generally poor; Duellman and Trueb [ 1994]) along slopes of mountain. Nevertheless, because of past climatic fluctuations, at least part of the Andean amphibian fauna should be suited to cope with long-term climatic change via dispersion. One factor that can make future scenarios of climatic change different from those of the past is the accompanying severe anthropogenic

31 RON et al: BIODIVERSITI AND CONSERVATION STATUS OF AMPHIBIANS OF ECUADOR 159 loss and fragmentation of habitat in the Andes (see section IV-D-2). Dispersion along elevational gradients will likely be hampered by the presence of unsuitable habitats between patches of natural vegetation. The interaction between global warming and habitat loss is exemplified by estimates of extinction under global warming to the year 25 showing a probability increase of as a consequence of habitat loss (Thomas et al. 24). The climate-linked epidemic hypothesis is an alternative scenario that correlates causally climatic change with amphibian population declines (Harvell et al. 22; Bosch et al. 27). This hypothesis posits that declines are a consequence of synergisms between pathogens and novel climatic conditions. During recent years, an increasing number of studies have reported results providing varying levels of support for this hypothesis (e.g., Pounds et al. 26; Alford et al. 27; Bosch et al. 27; Di Rosa et al. 27). Increased levels of ultraviolet radiation (UV) have also been linked to amphibian declines (e.g., Blaustein et al. 1994a; but see Licht 23) because UV can reduce survival of amphibian embryos (Blaustein et al. 1994a; Lizana and Pedraza 1998; Marco et al. 29). There is considerable variation among amphibian species in their sensitivity to ambient UV and therefore, the effect of this factor should vary among regions. In the tropical Andes, species potentially vulnerable to this factor are those that have aquatic embryos and larvae exposed to direct sunlight in shallow water (e.g., Atelopus, Telmatobius and Hyloxalus, especially in open habitats like the Paramo). On the other hand, species that have direct development (deposit eggs amidst soil and/or vegetation, hidden from direct or indirect sunlight) or are carried during early development by their mothers in a protective pouch (Pristimantis and Gastrotheca, respectively), should not be affected. Licht (23) questioned the importance of this factor because water and dissolved organic carbon provide a shield against UV radiation under a variety of natural conditions. 2. Loss and Fragmentation of Habitat Without doubt, one significant threat to Ecuadorian amphibians is loss of habitat (Table 2; Fig. 3). Humans have modified the inter-andean valleys and western lowlands for centuries, but this modification has been intensified by a sustained population growth (Ecuador has the highest human population density in South America). Since the 197s human impact has also become significant in Amazonian Ecuador as a result of petroleum extraction. Ecuador has the highest annual rate of deforestation in South America ( 1. 7%) (Food and Agriculture Organization of the United Nations 27). In the Deciduous Forest, Chocoan Tropical Rainforest, Western Foothill Forest, Western Montane Forest and Andean Shrub, more than 5% of the original vegetation has been cleared or severely fragmented (Table 2; Fig. 3). Most of the cleared areas have been devoted to agriculture and cattle production. Understandably, the regions where most of the natural habitat has been lost are those with the densest human populations. Impact by humans has been the most severe in the Ecuadorian Chocoan Tropical Rainforest (one of the world's biodiversity hotspots). Almost 85% of the natural vegetation there has either been cleared or fragmented. In this region, 15% of the amphibian species have been assigned to the category or Critically (Table 3). The Amazonian Tropical Rainforest has one of the highest proportions of natural vegetation cover (76.2%) (Table 2, Fig. 3) and concomitantly the highest proportion of species in the lower extinction-risk category "Least Concern" (82.7%). However, the link between the amount of remaining natural habitat and the risk of extinction is not always evident. For example, the Paramo region has one of the lowest proportions of vegetation cleared or fragmented (21.1%) and paradoxically one of the highest proportions of species facing high risk of extinction (6% are or Critically ). In the deciduous forest, only 26.7% of the natural vegetation remains unaltered but none of its 29 amphibian species is considered to be either or Critically. In fact, the regression between percentage of remaining natural habitat and percentage of threatened species at each region is non-significant (F =.13, df = 9, P =.725). However,

32 16 AMPHIBIAN BIOLOGY the regression between percentage of remaining natural habitat and the residuals from the regression between percentage of threatened species and mean temperature at each region is significant (F = 8.94, df == 9, P =.17). This indicates that loss of habitat is a good predictor of the regional proportion of endangered species, once the strong effect of temperature is removed. It should be noticed, however, that this correlation might be partly a consequence of the inclusion of habitat loss as one of several criteria used to evaluate categories of risk of extinction. Undoubtedly, loss of habitat has contributed to amphibian population declines in Ecuador but it cannot explain declines in seemingly pristine regions like those reported by Ron et al. (23). 3. Infectious Diseases Pathogens (especially viruses and fungi) are among the causes invoked to explain amphibian declines worldwide. Although half of the world's amphibian species inhabits the N eo tropical region and reports of declines are widespread (Young et al. 2 1 ), few efforts have been made to diagnose infectious diseases in wild amphibians, especially in South America. The first reports of Batrachochytrium dendrobatidis in South America are from Ecuador and Venezuela (Ron and Merino-Viteri 2; Merino-Viteri 2 1; Bonaccorso et al. 23; Ron 25). There have not been directed efforts to diagnose the presence of other diseases except for ranavirus at one locality in Argentina (Fox et al. 26). Below is a summary of what is known about B. dendrobatidis in Ecuador. Chytridiomycosis is a deadly disease that attacks the amphibian skin. Chytrids infect only keratinized parts of anurans (e.g., mouth parts in tadpoles and skin in postmetamorphic frogs) and cause death by interfering with osmoregulation (Berger et al. 29; Voyles et al. 29). Chytridiomycosis may have emerged as an epidemic disease because of a recent introduction, increase in virulence, and/or increased host susceptibility caused by other factors, such as environmental changes or yet-undetected co-infections. It has been suggested that it is linked to amphibian declines in all continents (e.g., Berger et al. 1998, 29; Lips 1999; Bosch et al. 21; Bradley et al. 22; Yang et al. 29). Ecuador is the first South American country where chytridiomycosis was diagnosed in wild amphibians (Ron and Merino-Viteri 2; Merino-Viteri 21). It has been found in nine species of anurans at ten localities throughout the Ecuadorian Andes (Table 4). Three localities are in Western Montane Forest, three in Paramo, and one in Andean shrub (biogeographic region for the remaining localities is uncertain). The earliest record of chytriciomycosis in Ecuador ( 198) pre-dates by several years the time when Atelopus declines first became noticeable in the Andes of Ecuador (late 198s) (Ron et al. 23). In fact, there are reports of sightings of abundant populations of Atelopus until the mid 198s (Ron et al. 23) even at the same province and in the species on which B. dendrobatidis was diagnosed in 198 (L. A. Coloma, personal observations). Eight out of ten species positive for chytridiomycosis are thought to have declined (Table 4). It is still unknown whether their declines are a consequence of chytridiomycosis. Finding a causal link is precluded by the impossibility of conducting bioassays to assess the virulence of the disease in species that have not been found for years despite intensive searches. Interestingly, although chytridiomycosis has been positively diagnosed in four populations of Gastrotheca pseustes, this species is still regularly found in nature (including localities positive for the chytrid). The persistence of wild populations despite the occurrence of the disease is puzzling and suggests that G. pseustes may have some level of resistance to the disease (resistance of amphibians to chytridiomycosis has been documented [e.g., Davidson et al. 23]). Alternatively, populations of Gastrotheca pseustes may in fact be declining although at a slower (and therefore less detectable) rate than is true for other species. Atelopus sp. from Limon also gives an example of persistence of a wild population of frogs in spite of the presence of the chytrid (D. Salazar-Valenzuela, unpublished; see section IV-C-1).

33 RON et al: BIODIVERSI'IY AND CONSERVATION STATUS OF AMPHIBIANS OF ECUADOR 161 The pattern of change in amphibian assemblages in several localities in the Andes (especially above 2 m) where species with aquatic larvae (Atelopus, centrolenids, dendrobatids) have disappeared while those with direct development (Pristimantis, Osornophryne) and marsupial pouches still persist (see section IV-A) is what would be expected from a disease that spreads aquatically, as seems to be the case for chytridiomycosis. 4. Introduced Species Introduced predatory fishes have been identified as possible factors contributing to amphibian declines (Knapp and Matthews 2; Vredenburg 24). Two exotic salmonid species (Salmo trutta and Onchorhynchus mykiss) have been introduced into Andean streams in Ecuador since the 195s and are widely distributed in paramos and montane forests (Ron et al. 23). It is unknown whether salmonids can feed on eggs, larvae, or adults of native amphibians. Although it is likely that salmonids may have contributed to amphibian declines in Andean ecosystems, the timing of their introduction suggests that they have not been the driving cause (Ron et al. 23). The bullfrog, Rana catesbeiana has been linked to declines of anurans in North America (reviewed by Kats and Ferrer 23). It was introduced into Ecuador during the mid 198s for meat production (Gallardo 24). At present, it is being found with increasing frequency in natural tropical ecosystems in Ecuador. The available evidence suggests that wild, breeding populations have become established in the eastern and western lowlands. Rana catesbeiana can affect native amphibians via predation, competition and as a vector for disease. 5. Contaminants Most of the Ecuadorian economy depends on oil production, agricultural products (e.g., banana, coffee, flowers, potatoes) and mining. These activities increase the level of contaminants in the environment and might affect amphibians (and other organisms). The list of contaminants includes heavy metals, pesticides, herbicides, fungicides, and fertilizers. Although there is no research on the effects of contaminants on amphibians in Ecuador, studies elsewhere suggest a negative impact (Marco and Ortiz-Santaliestra 29; Boone et al. 29; McCoy and Guilette 29; Luiselli and Lea 29). An estimate of two billion barrels of crude oil has been extracted from Ecuador's Amazonian Tropical Rainforest since the early 197s. As a consequence, millions of gallons of untreated toxic waste, gas, and oil have been released into the environment (Kimerling 1991 ). Studies of humans have shown increased incidence of cancer and spontaneous abortions in proximity to the Ecuadorian oil fields and concentrations of total petroleum hydrocarbons have been found above allowable limits (Hurting and San Sebastian 22; San Sebastian et al. 22). In amphibians, some metals can be lethal or induce sub-lethal effects such as slowing growth and development and altering behaviour (e.g. Blaustein et al. 1997; Lefcort et al. 1998, 1999; Raimondo et al. 1998). Heavy metals (contained in formation water from oil wells) are disposed without treatment into streams and rivers in the Amazonian Tropical Rainforest. One hypothesis for the decline of amphibian populations is that pesticides and their degradation products have induced gonadal changes (Stebbins and Cohen 1995; Hayes 2). For example, the herbicide atrazine induced hermaphroditism and demasculanized the larynges of exposed African clawed frog males (Xenopus laevis) (Hayes et al. 22). Atrazine is of common use in Ecuadorian agriculture. E. Conservation Efforts Efforts to conserve amphibians in Ecuador have focused mostly on habitat conservation, although some other conservation initiatives are currently underway. Conservation efforts can be classified in two categories: ( 1) indirect, or efforts that contribute to the conservation of Ecuadorian amphibians as a by-product of broad-spectrum actions to protect biodiversity, and (2) direct, or efforts specifically targeting the conservation of amphibians.

34 162 AMPHIBIAN BIOLOGY Table 5. Natural areas protected by the government of Ecuador Protected area Size (ha) Biogeographic region Province(s) Parque Nacional Cajas Paramo Azuay Parque Nacional Cotopaxi Paramo, Eastern Montane Forest Cotopaxi, Pichincha, Napo Parque Nacional Galapagos Galapagos Parque Nacional Llanganates Paramo Eastern Montane Forest, Tungurahua Cotopaxi, Napo, Pastaza, Parque Nacional Machalilla Western Foothill Forest, Deciduous Forest, Dry Shrub, Western Montane Forest Manabi Parque Nacional Podocarpus Eastern Montane Forest, Paramo, Andean Shrub Loja, Zamora Chinchipe Parque Nacional Sangay Paramo Eastern Montane Forest, Santiago, Tungurahua Caiiar, Chimborazo, Morona Parque Nacional Sumaco Napo Galeras Eastern Montane Forest, Eastern Foothill Forest, Amazonian Tropical Forest Napo Parque Nacional Yasuni 982 Amazonian Tropical Forest Orellana, Pastaza Recreaci6n Biol6gica Limoncocha Amazonian Tropical Rainforest Sucumbios Recreaci6n Ecol6gica Antisana 12 Western Montane Forest, Paramo Napo, Pichincha Recreaci6n Ecol6gica El Angel Paramo Carchi Recreaci6n Ecol6gica Cayambe Coca Eastern Montane Forest, Paramo, Eastern Foothill Forest, Amazonian Tropical Rainforest, Western Montane Forest Imbabura, Pichincha, Napo, Sucumbios Recreaci6n Ecol6gica Cayapas-Mataje 51 Chocoan Tropical Rainforest Esmeraldas Recreaci6n Ecol6gica Cotacachi Cayapas Western Foothill Forest, Western Montane Forest, Paramo, Chocoan Tropical Rainforest Esmeraldas, Imbabura Recreaci6n Ecol6gica Los Illinizas Western Montane Forest, Paramo Cotopaxi, Pichincha Recreaci6n Ecol6gica Mache-Chindul 7 Chocoan Tropical Rainforest, Western Foothill Forest, Western Montane Forest Esmeraldas, Manabi Recreaci6n Ecol6gica Manglares Dry Shrub, Deciduous Forest Guayas Churute Recreaci6n Geobotanica Pululahua Western Montane Forest Pichincha Recreaci6n Faunistica Chimborazo Paramo Tungurahua Chimborazo, Bolivar, Recreaci6n Faunistica Cuyabeno Amazon Tropical Rainforest Sucumbios, Napo Area de Recreaci6n El Boliche 227 Eastern Montane Forest, Paramo Cotopaxi

35 RON et al: BIODIVERSilY AND CONSERVATION STATUS OF AMPHIBIANS OF ECUADOR Indirect Efforts: Protection of Natural Habitats Habitat protection by itself does not guarantee the survival of species like Atelopus and Telmatobius and other endangered taxa that have declined in seemingly pristine areas. Nevertheless, the long-term survival of species that still persist in the wild depends on the conservation of natural habitats. Thus, viable conservation plans demand measures to secure protection of habitat. About 17% of the total area of Ecuador is protected by the National System of Protected Natural Areas (NSPA) (Table 5). The proportion of land protected by the government is high compared to most countries. An estimated 297 amphibian species (61.9%) is present in one or more of these protected areas. All Biogeographic Regions are represented in the NSPA although three of them only marginally so (.3% of the area of Deciduous Forest,.2% of Andean Shrub, and 3% of Chocoan Tropical Rainforest is protected) (Fig. 7). The low percentage of land protected in the Chocoan Tropical Rainforest is of particular concern because it also has high levels of anthropogenic modification of habitat (Table 2). The two regions with the highest proportional area protected are the Eastern Montane Forest (which also has the greatest species richness of amphibians) and Paramo; in both cases approximately one third of their area lies within the NSPA. The Andean forests (except the Eastern Montane Forest) have low levels of protection despite having high diversity and endemism of amphibians. Although the Western Montane Forest has 27.1 % of the Ecuadorian amphibian species (126), only 6% of the NSPA area belongs to this Biogeographic Region; the Eastern Foothill Forest has similar percentages (2.% of the species and 2.5% of the NSPA area). From the perspective of amphibian conservation, future efforts to create protected areas in Ecuador should focus on regions with a combination of low protection and high species richness and endemism (Western Foothill Forest, Western Montane Forest, Eastern Foothill Forest, and Chocoan Tropical Rainforest). In addition to the NSPA. there are several small private reserves that in some cases protect ecosystems not included in the NSPA. 2. Direct Efforts: Scientific R esearch and Conservation Projects In addition to conservation of habitat, actions needed to protect amphibians in Ecuador include intensive surveys of populations, in-situ studies of basic ecology, and ex-situ management of populations of endangered species. In Ecuador, some institutions involved in research and conservation of amphibians are: Museo de Zoologia de la Pontificia Universidad Cat6lica del Ecuador (QCAZ); Museo de Historia Natural Gustavo Orces V., Escuela Politecnica Nacional, Quito (EPN); Laboratorio de Anfibios y Reptiles, Universidad San Francisco de Quito (USFQ), Fundaci6n Herpetol6gica Gustavo Orces (FHGO), and Museo Ecuatoriano de Ciencias Naturales (MECN), among others. A summary of major ongoing projects is provided below: QCAZ is implementing a Strategic Plan for the Conservation of the Ecuadorian Amphibians in Risk of Extinction. Goals, results and activities defined within this initiative follow major guidelines of the global strategy for conservation of amphibians and the Amphibian Conservation Action Plan (ACAP) (IUCN/SSC Global Amphibian Specialist Group, and Declining Amphibian Populations Task Force, 25). Information of the Ecuadorian plan is summarized by Coloma (28) and available at: zoologia/vertebrados/amphibiawebec this initiative is available at balsasapos/ Museums, systematic and biogeographic studies: QCAZ holds the largest scientific collection of Ecuadorian amphibians (5 specimens) plus a tissue bank of about 2 samples. QCAZ also maintains a collection of about 5 species of living amphibians. EPN holds a collection of nearly 15 specimens. EPN and MECN have medium-sized collections

36 164 AMPHIBIAN BIOLOGY (15 and 8 specimens, respectively). FHGO and USFQ have smaller collections. Information from the QCAZ databases will be posted at QCAZ electronic Enciclopedia of Ecuadorian Amphibians, AmphibiaWebEcuador, which currently provides updated information about Ecuadorian amphibians including species accounts (available at zoologia.puce.edu.ec/vertebrados/anfibios.aspx). Population and natural history projects: Demographic studies are conducted to identify the species that have suffered, or are suffering, population declines and to determine the possible causes of those declines. Some of the results are already available (e.g., Ron and Merino-Viteri 2; Ron et al. 23; Bustamante et al. 25; Merino-Viteri et al. 25; Ron 25; Yanez-Munoz and Meza-Ramos 26). Field natural history studies are being conducted by QCAZ, EPN, MECN and other institutions. Some results are available through the AmphibiaWebEcuador web page. Public education: QCAZ organized a large exhibit of living amphibians: "Sapari: take an adventure in a world of frogs". This event, without precedent in public exhibits in Ecuador, lasted 9 days and was attended by 15 visitors. FHGO maintains a small permanent exhibit that includes Gastrotheca riobambae, Epipedobates anthonyi and other species. Ex-Situ Reproduction of Ecuadorian Amphibians: QCAZ is conducting a project FHGO have bred successfully Gastrotheca riobambae for educational purposes. Results of QCAZ captive colonies studies are research theses presented by Correa-Monge (1995), DelPino et al. (27), Quiguango-Ubillus ( 1996), Dfaz-Proano (1999) and Castillo-Trenn (24). Hyla, a private company, has bred G. riobambae, G. pseustes, and G. monticola for educational and commercial purposes. V. ACKNOWLEDGMENTS Chris W. Funk and C. R. Darst provided comments on earlier versions of this work. Rodrigo Sierra and C. H. Graham made available digital versions of maps. Santiago R. Ron's research at the University of Texas was funded by the University of Texas continuing fellowship and NSF IRCEB grant 7815 to D. C. Cannatella. Ailin Blasco-Zuniga made available unpublished records of Batrachochytrium dendrobatidis. Ernesto Arbelaez, A. Merino Viteri, M. Read, and D. Salazar-Valenzuela made available unpublished population records and field notes. VI. REFERENCES AEE, 2. "Almanaque ElectrUnico Ecuatoriano. InformaciOn Espacial para Aplicaciones Agropecuarias". PROMSA, Alianza Jatun Sacha/ CDC Ecuador, Mud Springs Geographers, CIMMYT, ESPE. Quito. Akcakaya, H. R., Butchart, S. H. M., Mace, G. M., Stuart, S. N. and Hilton-Taylor, C., 26. Use and misuse of the IUCN red list criteria in projecting climate change impacts on biodiversity. Global Change Biol. 12: Alford, R. A., Bradfield, K. S. and Richards, S. ]. 27. Global warming and amphibian losses. Nat. 447: E3-E4. Araujo, M. B., Pearson, R. G., Thuillers, W. and Erhard, M., 25. Validation of species-climate impact models under climate change. Global Change Biol. 11: Araujo, M. B, Thuiller, W. and Pearson, R. G., 26. Climate warming and the decline of amphibians and reptiles in Europe.]. Biogeog. 33: Bass, M. S., Finer, M., Jenkins, C. N., Kreft, H., Cisnerosheredia, D. F., McCracken, S. F., Pitman, N. C., English, P. H., Swing, K., Villa, G., Di Fiore, A., Voight, C. C., and Kunz, T H. Global conservation significance of Ecuador's Yasuni National Park. Plos One, 5, e8767. Baslev, H. and de Vries, T, Diversidad de la vegetaci6n en cuatro cuadrantes en el paramo arbustivo del Cotopaxi, Ecuador. Publicaciones del Museo Ecuatoriano de Ciencias Naturale, Serie Revista 3: Becker, C. G., Fonseca, C. R., Haddad, D. F. B., Batista, R. F. and Prado, P. I., 27. Habitat split and the global decline of amphibians. Sci. 318: Berger, L., Longcore, J. E., Speare, R., Hyatt., A. and Skerratt, L. F., 29. Fungal diseases of amphibians. Chapter 2 (Pp ) in "Amphibian Decline: Diseases, Parasites, Maladies and Pollution", vol. 8 in "Amphibian Biology", ed by H. Heatwole and J. W. Wilkinson. Surrrey Beatty & Sons, Baulkham Hills, Australia.

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