Journal of Biogeography (J. Biogeogr.

) (2004) 31, 18291839

ORIGINAL ARTICLE

Biological diversication in a complex region: a spatial analysis of faunistic diversity and biogeography of the Andes of Colombia
n Gustavo H. Kattan1*, Padu Franco1,2, Vladimir Rojas1,2 and Germa Morales2

n EcoAndina/Colombia Program of Fundacio the Wildlife Conservation Society, Cali, and 2 a, Universidad del Departamento de Biolog Valle, Cali, Colombia

ABSTRACT

Aim Understanding large-scale patterns of beta diversity and endemism is essential for ecoregional conservation planning. We present a study of spatial patterns of faunal diversication and biogeographical relationships in the Andean region of Colombia. This region has a great geomorphological complexity, as it is formed by several mountain ranges with different geologic origins. We hypothesize that this complexity results in a high turnover in species composition among subregions. Location The Andean region of Colombia, including the Santa Marta and Macarena mountain ranges. Methods The region was divided into subregions, represented by the eastern and western slopes of each of the three Andean cordilleras, the Cauca and Magdalena , Macarena and valley bottoms, and the peripheral mountain ranges of Perija Sierra Nevada de Santa Marta. Species lists for ve animal taxa (rodents, bats, birds, frogs and butteries) were compiled for each subregion and similarities in species composition were determined by cluster analysis. To explore biogeographical relationships, species were classied into one of four distributional categories: endemic, tropical Andean, Andean-Central American and wide continental distribution. Results The highest species richness in the region was found in the Pacic and eastern versants of the Andes, and the lowest in the Cauca and Magdalena valley bottoms. Inter-Andean slopes were intermediate in species richness. However, when species richness was calculated per unit area, the most diverse regions were the Santa Marta and Macarena ranges, the Cauca Valley watershed and the Pacic slope. Although each taxonomic group had a different branching pattern, -Sierra dendrograms indicated ve common subregional clusterings: (1) Perija Nevada, (2) the Pacic slope, (3) the eastern Andean slope, (4) the Cauca and Magdalena valley bottoms, and (5) the inter-Andean slopes. Clustering patterns of inter-Andean slopes varied among taxa. In birds, bats and rodents, grouping was by opposite slopes of the same valley, whereas frogs were grouped by mountain ranges and butteries by valleys and their respective slopes. Seventyve per cent of species in all taxa were found in less than ve subregions. The fauna of the Magdalena and Cauca valley bottoms was composed mostly of lowland species with wide geographical distributions, whereas the cordilleran fauna was mostly restricted to the tropical Andes. Main conclusions The western and eastern versants of the Andes have the highest species richness, but are also the largest subregions. On a per unit area basis, the peripheral ranges (Santa Marta and Macarena) are the richest, followed by the western portion of the Andes (the Cauca Valley watershed and the Pacic versant). Clustering patterns in dendrograms suggest two major patterns of
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*Correspondence: Gustavo Kattan, Apartado reo 25527, Cali, Colombia. Ae E-mail: gkattan@wcs.org

2004 Blackwell Publishing Ltd www.blackwellpublishing.com/jbi

G. H. Kattan et al.

differentiation of the Andean fauna: one elevational (lowlands vs. highlands) and one horizontal (among ranges and/or slopes). Biogeographical afnities of the inter-Andean valley bottoms are with the lowland faunas of tropical America. In contrast, Andean faunas diversied locally, resulting in the evolution of a large number of endemic species, particularly among the less vagile taxa. Three different main branches of Andean fauna can be recognized, one conned to the Pacic, another to the eastern (Amazonian-Llanos) versant of the Andes, and the third one composed by the inter-Andean slopes of the Cauca and Magdalena valleys. The identication of ve main biogeographical units in the Andean region of Colombia has important implications for the conservation of the regional biota. Conservation initiatives that seek to preserve representative samples of the regional biodiversity should take into account the patterns of diversication described here, and the evolutionary processes that gave rise to these patterns. Keywords Andes, Colombia, biodiversity, biotic diversication, ecoregional planning, protected area planning, speciation.
RESUMEN

biotic

radiation,

El conocimiento de los patrones de diversidad beta y endemismo a gran escala culo se presenta n ecorregional. En este art espacial es esencial para la planicacio n de la fauna y de sus un estudio de los patrones espaciales de diversicacio as perife cas en la regio n andina de Colombia y serran ricas. relaciones biogeogra n es de una gran complejidad geomorfolo gica, ya que esta conformada Esta regio as de diferentes or genes geolo gicos. Nuestra hipo por varias cordilleras y serran n de especies entre las tesis es que esta complejidad genera una alta composicio n andina de Colombia (incluyendo la Sierra Nevada de Santa subregiones. La regio a de La Macarena), fue dividida en subregiones, constituidas por Marta y la serran las vertientes oriental y occidental de cada una de las tres cordilleras, las planicies as de Perija y La Macarena y la de los valles del Cauca y Magdalena, las serran Sierra Nevada de Santa Marta. Para cada una de estas subregiones compilamos la micos: roedores, murcie lagos, aves, lista de especies para cinco grupos taxono n de ranas y mariposas. En cada grupo, determinamos la similitud en composicio especies por medio de analisis de agrupamiento (cluster analysis). Con el cas, clasicamos las especies en objectivo de explorar las relaciones biogeogra as de distribucio n geogra ca: ende mica, Andes tropicales, andinacuatro categor n amplia. La riqueza de especies ma s alta se encocentroamericana y distribucio ca y oriental de los Andes, y la ma en las vertientes Pac s baja en los valles ntro del Cauca y Magdalena. Las vertientes interandinas presentaron una riqueza rea las subregiones ma s diversas fueron intermedia. Sin embargo, por unidad de a La Macarena y Santa Marta, el valle del Cauca y sus vertientes, y la vertiente del co. Aunque el ana lisis arrojo diferentes patrones de agrupamiento para cada Pac grupo taxonomico, en los dendrogramas se destacan cinco ramas: (1) Perija co, (3) la vertiente oriental de los Andes, (4) Sierra Nevada, (2) la vertiente Pac las planicies de los dos valles, y (5) las vertientes interandinas. Los patrones de laagrupamiento de las vertientes interandinas fueron variables. En aves, murcie gos y roedores, las vertientes opuestas de cada valle resultaron muy cercanas en n de especies; en cambio, en las ranas se agruparon primero las dos composicio con sus respecvertientes de cada cordillera; en mariposas, cada valle se agrupo compuesta tivas vertientes. La fauna de las planicies del Cauca y Magdalena esta cas. principalmente por especies de tierras bajas y amplias distribuciones geogra

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Biological diversication in the Colombian Andes

compuesta principalmente por La fauna de las cordilleras, en cambio, esta especies restringidas a los Andes tropicales. Los patrones de agrupamiento en los n de la fauna dendrogramas sugieren dos patrones principales de diferenciacio n vertical (tierras bajas versus tierras altas) y otro horizontal andina: un patro (entre cordilleras y entre vertientes). Las planicies interandinas del Cauca y ca con la fauna de tierras bajas del tro pico Magdalena tienen anidad biogeogra n local, lo americano, mientras que las faunas andinas muestran una diversicacio n de un gran nu mero de especies ende micas, cual ha resultado en la evolucio viles. Se pueden reconocer tres grandes particularmente en los taxones menos mo co, ramas en la fauna propiamente andina: una connada a la vertiente del Pac otra a la vertiente oriental de los Andes, y una tercera compuesta por las vertientes n de cinco interandinas de los valles del Cauca y Magdalena. La identicacio cas en la regio n andina de Colombia tiene imporgrandes unidades biogeogra n de la biota regional. Las iniciativas de tantes implicaciones para la conservacio n que buscan preservar muestras representativas de la diversidad conservacio lo los patrones de diversidad descritos en este regional deben tener en cuenta no so culo, sino tambie n los procesos evolutivos que originaron estos patrones. art Palabras clave tica, radiacio n bio tica, Andes, Colombia, biodiversidad, biodiversidad bio n ecoregional, planicacio n de a reas protegidas, especiacio n. planicacio

INTRODUCTION Rising at the crossroads between two continents, the northern Andes have played a key role in the diversication of the tropical South American biota. For organisms such as vascular plants, birds and amphibians, two major foci of diversication on a continental scale have been identied, one centred in the Amazon basin and another centred in the northern Andes , 1994; Duellman, 1999). Uplift of the (Gentry, 1982; Fjeldsa Andes led to an explosive radiation of plant families of Gondwanan origin, originating almost half of all Neotropical plant species (Gentry, 1982). Diversities of frogs and birds in the northern Andes (427 and >1400 species, respectively) easily surpass Amazonian diversities (305 and c. 1000 species) , 1994; Duellman, 1999). Considering that the area of (Fjeldsa the northern Andes (490,000 km2, from the Huancabamba Depression in northern Peru to the Venezuelan Andes) is 14 times smaller than the area of the Amazon basin (6,869,000 km2), it is evident that the region is a hotspot that requires high priority in global conservation initiatives (Myers et al., 2000). The biological diversity of the northern Andes is the result of three major historical events (Gentry, 1982; Marshall & Sempere, 1993). First, the uplift of mountain ranges in a complex series of orogenic processes, caused innumerable vicariance events, and created an incredibly diverse array of new environments that provided fertile grounds for biotic radiation and diversication. Secondly, the connection with North America fostered a biotic interchange that enriched the autochthonous South American biota with new taxa,

particularly in the upper elevations; many of these taxa just reached the northern Andes and diversied there (e.g. Magnoliaceae; Gentry, 1982). Thirdly, the climatic uctuations during the Pleistocene likely produced cycles of range contraction and expansion that resulted in fragmentation and isolation of populations, with subsequent speciation and radiation events. As a result of these events, not only is regional diversity very high, but levels of endemism also are extraordinary (Adams, 1986; Bibby et al., 1992; Lynch et al., 1997; Duellman, 1999). The northern Andes reach their maximum geomorphological complexity in Colombia, where they are divided into three main ranges (the Western, Central and Eastern Cordilleras), separated by the sedimentary basins of the Cauca and Magdalena river valleys (Fig. 1). Several peripheral mountain ranges of different geological origins add to the physical complexity and biological diversity of the region. Encompassing 11 degrees of latitude and a little over 300,000 km2, the Colombian Andes harbour more than 10,000 species of plants, 1200 species of birds, 400 species of frogs, and 270 species of rodents and bats, representing up to 10% or more of the worlds biota in some taxa (Rangel, 1997a,b). Unfortunately, this region is also under intense pressure. Seventy per cent of the human population of Colombia is concentrated in the Andean region, and natural ecosystems have been extensively pez, 1996; Cavelier, 1997). transformed (Kattan & Alvarez-Lo The design and implementation of conservation schemes aimed at preserving a representative sample of regional biodiversity require understanding the spatial patterns of diversication and large-scale beta diversity, i.e. spatial 1831

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G. H. Kattan et al.

Figure 1 Map of the Andean region of Colombia, showing the three branches of the Andes and other subregions used for the spatial analysis of diversity (only the western is or Colombian portion of Serrania de Perija shown; the eastern half of this range lies in Venezuela). In addition to the subregions indicated, each branch of the Andes was divided into a western and an eastern slope.

turnover in species composition. If the regional biota is relatively homogeneous in its history and species composition, then a small number of areas will sufce to ensure complete representation. But if the biota is spatially heterogeneous, then more strategically located areas will be required to cover the regional variation. Here we present results of a study of the patterns of spatial diversication and geographical distribution of some groups of animals (rodents, bats, birds, frogs and butteries) of the Colombian Andes. Differences in geology, topography and climate suggest that the history and composition of the biota might differ among ranges or even between slopes of the same range. Our primary objective was to determine the degree of similarity in species composition and patterns of geographical distribution among different subregions composing the Colombian Andes. This information could then be used in making decisions about the areas required to obtain adequate representation of the regional biodiversity in a protected area system. STUDY AREA At their southern end, the Colombian Andes form a single high-rising massif (the Macizo Colombiano), which is the continuation of the main axis of the Ecuadorian Andes. North 1832

of this point, the three-pronged conguration and south north axes of the mountain chains give origin to three westfacing and three east-facing slopes, and two deep inter-Andean valleys (Fig. 1). The west-facing slope of the Western range forms the Pacic versant, which is continuous into northern Ecuador and is extremely humid, due to interception of humid coastal winds. The Andes here rise abruptly from the Pacic coast, so the lowlands are restricted to a narrow coastal corridor. The eastern slope of the Eastern range, on the contrary, faces the Amazonian lowlands in its southern half, and the llanos or savannas of Colombia and Venezuela in its northern half. The eastern Andean slope is also generally humid, as it intercepts the north-eastern trade winds. The interior-facing (inter-Andean) slopes of the Andes form the slopes of the Cauca Valley, between the Western and Central Cordilleras, and the Magdalena Valley, between the Central and Eastern Cordilleras. Humidity patterns in the Cauca and Magdalena valleys are more variable. The valley bottoms tend to be dry, but the range summits are humid. Rain shadow phenomena create subxerophytic (semi-arid) pockets, particularly in the foothills. At its northern end, the Eastern range bifurcates into the rida Andes, which extends north-east into Venezuela, and Me a de Perija , which extends northward the low-rising Serran

Journal of Biogeography 31, 18291839, 2004 Blackwell Publishing Ltd

Biological diversication in the Colombian Andes (Fig. 1). Also included in our analyses are two separate mountain ranges, the Santa Marta massif (Sierra Nevada de a de Santa Marta) on the Caribbean coast, and the small Serran La Macarena east of the Andes. The three ranges of the Colombian Andes, as well as the a de La Sierra Nevada de Santa Marta and the Serran Macarena, have different geological histories and resulted rgl, 1961; Irving, 1975). La from different orogenic events (Bu Macarena is part of the Guianan Shield and is the oldest range. North Andean orogenesis started in the late Paleozoic, when the ancestral Central Cordillera was insinuated at the western margin of a miogeosyncline. The Central Cordillera was emergent but low during the Cretaceous. Orogeny of the Western Cordillera can be traced to the end of the Mesozoic, and of the Eastern Cordillera to the middle Tertiary. Andean folding during the Miocene gave rise to the present conguration of three Cordilleras and the two sedimentary basins of the Cauca and Magdalena valleys. Present elevations were reached during the PliocenePleistocene. Initial orogeny of the Santa Marta mountains can also be traced to the late Paleozoic, but vertical uplifting to present altitudes occurred in late Tertiary time. METHODS To determine patterns of biotic differentiation, we divided the Andean region of Colombia into subregions, dened as the eastern and western slopes of each of the three ranges, the as of Perija , two inter-Andean valley bottoms, and the Serran Santa Marta and La Macarena (Fig. 1). This subdivision follows, with some modications, the classication of bioge ndez ographical provinces of Colombia proposed by Herna Camacho et al. (1992). The Pacic versant was further subdivided into an upper Pacic slope (>1000 m elevation) and a lower Pacic slope (2001000 m elev.). This subdivision was made to allow comparisons with the Cauca Valley slopes, as this valleys bottom lies at 1000 m elevation. The lower limit of 200 m was chosen to exclude the lowland, coastal biota from the analysis. Likewise, the lower limit on the eastern versant of the Andes was set at 500 m of elevation to exclude the lowland Amazonian biota (the Magdalena Valley lies at an average of 500 m in its mid portion, and descends rapidly northward). Species lists were compiled for each of the subregions from published national lists (Hilty & Brown, 1986; Ruiz et al., 1996; Alberico et al., 2000), complemented by literature surveys to include new species or records that have appeared after the monographs publication; buttery lists were not available and were compiled de novo by three experts. Major criteria for selecting study taxa were having a reasonable knowledge of species distributions and that lists could be obtained. In butteries we included the families Papilionidae, Pieridae (genus Catasticta), Nymphalidae [subfamilies Charaxinae, Heliconiinae, Ithomiinae, Morphinae, Brassolinae and Satyrinae (tribe Pronophilini)], Lycaenidae and Riodinidae. A species was assigned as present in a subregion if it had records in at least one locality. This may overestimate the geographical distribution of some species within the subregion, but as we are concerned with largescale patterns of distribution, this does not affect our analyses. To determine present similarities in species composition among subregions, we constructed dendrograms using cluster analyses of presenceabsence matrices with the SPSS statistical package. We used Jaccards coefcient of similarity (J) as a distance measure, and centroid clustering. Jaccards coefcient is dened as J c/(a+b)c), where a is the number of species in site A, b the number of species in site B, and c the number of shared species. This index equals 1 in cases of complete similarity, and 0 if the sites have no species in common. To explore biogeographical relationships, we assigned each species to a geographical distribution category, dened as follows: Endemic (E), species with geographical ranges restricted to <50,000 km2 (in many cases, particularly in frogs, known ranges are restricted to one or a few localities); Tropical Andean (TA), species that are distributed in the tropical Andes; Andean-Central American (CA), species that are distributed in the tropical Andes and Central American mountains; and wide distribution (WD), species that are widely distributed in tropical America or in the entire continent. RESULTS In general, the humid western (Pacic) and eastern (Amazonian-Llanos) versants of the Andes were the richest both in total number of species and number of endemics for the ve taxonomic groups, although the Central Cordillera also was very rich, and even surpassed the eastern versant in frog richness (Table 1). Conversely, the lowest numbers were found in the dry inter-Andean valley bottoms. The inter-Andean slopes of the Cauca and Magdalena valleys were intermediate (Table 1). Species richness in the ve taxonomic groups correlated with area of the subregions (Fig. 2). However, a different picture emerged when species richness was tallied per unit area (Table 2). Although the Pacic versant was still very rich, the richest regions were the peripheral mountain ranges of Macarena and Santa Marta. Per unit area, the eastern versant of the Andes and the Magdalena Valley watershed (including the slopes and valley bottom) were poor when contrasted with the Cauca Valley watershed, which emerged as a relatively rich region. Dendrograms showing the clustering of subregions for the different taxa are shown in Fig. 3. Although each taxonomic group had a particular pattern of clustering, the following common patterns of differentiation could be identied: a de Perija grouped with Sierra Nevada de Santa 1. Serran Marta in a separate branch in birds, bats and butteries were not available for frogs). In (separate data on Perija shared a higher proportion of species with Santa general, Perija Marta (J ranged from 0.39 to 0.86) than with the rest of the 1833

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G. H. Kattan et al.
Table 1 Number of species (endemics in parenthesis) of ve animal taxa in different subregions of the Colombian Andes
Subregion Butteries (61) (72) (105) (55) (53) (25) (15) (29) (48) (62) (90) (73) (76) (266) Frogs 163 124 233 23 48 23 NA 12 38 82 80 52 69 464 (110) (62) (142) (10) (20) (16) Birds Rodents Bats (26) 40 (18) 26 (30) 46 (5) 18 (4) 27 (26) 21 (9) 43 (0) 20 (14) 32 (15) 42 (16) 46 (9) 53 (12) 72 (73) 107 (3) (1) (4) (1) (4) (2) (3) (0) (3) (3) (3) (4) (4) (11) 65 87 101 46 58 94 103 84 60 62 72 77 126 166

Upper Pacic 210 Lower Pacic 364 Pacic (all) 490 Cauca Valley 212 Magdalena Valley 173 Santa Marta 161 Perija 124 Macarena 138 Western east* 273 Central west* 266 Central east* 385 Eastern west* 241 Eastern east* 658 Total 1334

740 590 850 298 345 637 429 (3) 561 (22) 484 (53) 434 (45) 523 (29) 499 (32) 791 (283) 1426

NA, not available. *Refers to the range and slope.

Eastern Cordillera (J 0.100.62). The only exception was grouped with the rest of the Eastern rodents, for which Perija Cordillera. 2. The western (Pacic) and eastern (Amazonian-Llanos) versants of the Andes branched as separate entities and were divergent in species composition; the only exception was butteries, in which the Lower Pacic region clustered with the eastern Andean slope, suggesting a shared foothills buttery a de La Macarena fauna on both anks of the Andes. Serran clustered with the eastern slope of the Andes in all groups except rodents (clustering of Macarena with Santa Marta in rodents may reect poor knowledge). The proportion of species shared between the Pacic and Eastern versants was intermediate in vagile groups such as birds (J 0.36) and bats

(J 0.50), but it was as low as J 0.04 in sedentary organisms such as frogs. The upper Pacic slope formed one unit with the lower Pacic in birds, frogs and bats, but it was more similar to the inter-Andean slopes in butteries and rodents. 3. The Cauca and Magdalena valley bottoms clustered together and were relatively similar for all groups (J 0.360.65) except butteries (J 0.27). 4. The inter-Andean slopes of the Cauca and Magdalena watersheds tended to group together in all taxa. However, there were some important differences among taxa in the clustering patterns of the different slopes. In birds, bats and rodents, grouping was by opposite slopes of the same valley, whereas frogs grouped by mountain ranges, and butteries grouped by valley bottoms and their respective slopes (Fig. 3). Thus, ve different faunistic subregions can be recognized: -Santa Marta, (2) the Pacic versant, (3) the Eastern (1) Perija versant, (4) the Cauca and Magdalena valley bottoms, and (5) the inter-Andean slopes (although we treat this subregion as a unit, it shows considerable internal heterogeneity). Differences in composition among subregions can be emphasized by examining how many subregions each species occurs in a measure of endemicity (Fig. 4). Seventy-ve per cent of the species in the ve taxonomic groups occurred in ve or less subregions, and 36% (i.e. 1225 of 3434 species in the ve groups) occurred in only one subregion. In contrast, very few species occurred in more than 10 subregions. Chiroptera was the only taxon with a dominance of widely distributed species. We also examined the patterns of distribution of species in each of the subregions, to explore biogeographical relationships (Fig. 5). In the case of rodents, the Pacic fauna was predominately composed of species with CA or WDs; widely distributed species were also well represented in the valleys and the Eastern slope, whereas species of TA distribution were

Frogs (R = 0.17)

Number of species

Birds (R = 0.22)
20,000 40,000
2

60,000 80,000

20,000 40,000
2

60,000 80,000

Butterflies (R = 0.61)

Bats (R = 0.13)

Rodents (R = 0.73)
20,000 40,000 60,000 80,000 20,000 40,000 60,000 80,000

Figure 2 Speciesarea relationships for ve taxonomic groups in different subregions of the Andean region of Colombia. In all cases, regressions on untransformed axes produced higher R2 values than loglog regressions. The extreme outlier in the frogs plot is the Pacic slope of the Andes, which is extremely rich in this taxon.

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Biological diversication in the Colombian Andes

Table 2 Area (in km2) and number of species per unit area (10)2) for ve animal taxa in different subregions of the Colombian Andes
Subregion Pacic (all) Cauca Valley Magdalena Valley Santa Marta Perija Macarena Western east* Central west* Central east* Eastern west* Eastern east* Area 36771 6780 19375 5998 5693 2888 14388 18995 51956 54232 60989 Butteries Frogs Birds Rodents Bats 2.53 3.13 0.90 2.68 2.18 4.78 1.90 1.40 0.74 0.44 1.08 1.21 0.34 0.25 0.38 NA 0.42 0.26 0.43 0.15 0.10 0.11 4.38 4.39 1.78 10.62 7.54 19.42 3.36 2.28 1.01 0.92 1.30 0.24 0.27 0.14 0.35 0.76 0.69 0.22 0.22 0.09 0.10 0.12 0.52 0.68 0.30 1.57 1.81 2.91 0.41 0.33 0.14 0.14 0.21

better represented in the Andean and Eastern slopes. Frogs were noteworthy for the dominance of the endemic species category in all regions, in contrast to bats, which in general had very wide geographical distributions. Butteries also had a large proportion of species with wide geographical distributions in all subregions, but one-third to one half or more of the species were endemic or restricted to the tropical Andes, and relatively few have Central American relations. In birds, there is a strong representation of CA and widely distributed species in all subregions, but TA species represent an important proportion in the Pacic, Eastern and inter-Andean slopes. DISCUSSION The Eastern and Pacic (the Chocoan biogeographical region) versants of the Andes have usually been recognized as biodiversity hotspots (Rangel, 1997a,b). In absolute numbers, our results agree with this assessment. However, on a per unit

NA, not available. *Refers to the range and slope.

Birds

Frogs

Bats

Rodents

Butterflies

Figure 3 Dendrograms showing similarity in species composition among subregions composing the Colombian Andes.
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G. H. Kattan et al.
300 200 100 0 1 800 600 400 200 25 69 1013

Frogs
80 60 40 20 0 Pacific 100 80 60 40 20 0

EN Rodents

TA

CA

WD

Birds

Valleys Bats

EastSlope

AndSlopes

Number of species

0 1 800 600 400 200 0 1 80 60 40 20 0 1 60 25 69 1013 25 69 1013 25 69 1013

Percent of species

Pacific 80 60 40 20 0 Pacific 80 60 40 20 0 Pacific 80 60 40 20 0 Pacific

Valleys Frogs

EastSlope

CV Slopes MV Slopes

Butterflies

Valleys Birds

WestC

CentC

EastC

Bats

Valleys Butterflies

EastSlope

AndSlopes

Rodents
40 20 0 1 25 69 1013

Cauca V

Magd V

East

Subregion
Figure 5 Patterns of geographical distribution of species in different subregional clusters, as dened by dendrograms in Fig. 3. Categories of geographical distribution are: EN, endemic; TA, tropical Andean distribution; CA, Andean-Central American distribution; WD, wide distribution (South and Central America).

Number of subregions
Figure 4 Patterns of distribution of species in ve taxonomic groups, in subregions composing the Colombian Andes. The graph shows the number of species occurring in different numbers of subregions.

area basis, the mountain ranges of Santa Marta and Macarena turn out to be the real hotspots. In addition, an important result is that by this measure the Cauca Valley watershed (including the valleys slopes and bottom) is an extremely rich region. One caveat is that this may reect poor knowledge of some regions (e.g. the eastern slope of the Andes), but the pattern holds true for relatively well-known groups such as birds and frogs. Moreover, the pattern is expected from the speciesarea relationship. From a conservation perspective, regions with a high species density (number of species per unit area) are more vulnerable, because many unique species could be extirpated by destroying a relatively small area. In any case, our results indicate that each of the ve subregions identied here tend to have distinct faunas. Clustering patterns of subregions suggest two major patterns of differentiation of the Andean fauna. The rst one is elevational, evidenced by the differentiation of lowland faunas in the valley bottoms and highland faunas in the Andean slopes. The second one is horizontal, represented by the divergence of faunas among ranges or even among slopes of the same range. The Cauca and Magdalena valley bottoms have typically lowland biotas, with a high proportion of species of 1836

wide geographical distributions, whereas the highlands have autochthonous Andean biotas, which are more restricted in their distribution (Renjifo et al., 1997; Stotz, 1998). The only exception to this pattern are butteries; here, each valley and its corresponding slopes form a different unit (probably related to the numerical dominance of Nymphalid butteries, which tend to have wide altitudinal distributions). At a continental scale, one major effect of the emergence of the Andes was the differentiation of CisAndean (Amazonian), Andean and TransAndean (Chocoan-Central American) biotas (Lynch, , 1994; Tyler et al., 1979; Gentry, 1982; Brown, 1987; Fjeldsa 1994; Duellman, 1999). Our results indicate that even within the Andean region, there is a differentiation between Pacic, inter-Andean and Eastern versant faunas. The diversication of the Andean biota is likely a combination of vicariance events, and local radiation and subsequent dispersal of taxa. As the Andes emerged, the fauna and ora radiated to ll the new environments that were generated. The Neotropical bird fauna underwent an explosive radiation in , 1994), the TA region starting in the upper Miocene (Fjeldsa resulting in distinct avifaunas in the highlands and lowlands (Renjifo et al., 1997). The great diversication of the northern Andes is a result of their topographic and climatic complexity,

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Biological diversication in the Colombian Andes and the high proportion of endemisms is associated with , vicariance in regions of high recent diversication (Fjeldsa 1994). Probably in no other group is the effect of the Andean uplifting more dramatic as in frogs. The nonsynchronous uplifting of the three Colombian Cordilleras fragmented populations and promoted allopatric speciation (Lynch et al., 1997). This horizontal diversication resulted not only in high diversity, but also in high levels of endemism (Fig. 5). One example serves to illustrate this. The Andean frog fauna is dominated by the genus Eleutherodactylus, the most speciose vertebrate genus. Of the 176 eleutherodactylines known from Colombia in 1997, 82 (46%) were endemic to the Andes; 27 were endemic to the Western Cordillera, 22 to the Central Cordillera, nine were shared by these two ranges, and 24 were endemic to the Eastern Cordillera (Lynch et al., 1997; since this paper, many species have been added to the Colombian frog fauna). Montane faunas have further diversied by altitude. Distinct elevational belts have been identied for the Andean biota, and species replacement along elevational gradients is a welldocumented phenomenon in many taxa (Terborgh, 1971; Patterson et al., 1998; Stotz, 1998; Medina et al., 2002). For instance, elevational ranges in a great proportion of Andean birds are 1500 m or less, and species turnover at different localities along altitudinal ranges in the Central Andes is 3050% (G. Kattan & P. Franco, unpubl. data). Species turnover in frog communities may be 60% or more (Restrepo & Alberico, 1994). Similar patterns of differentiation have been described for some groups of butteries. For example, Pronophiline butteries, a group of Satyrid butteries with their highest diversity in the cloud forests of the northern Andes, show a double pattern of speciation. Forty-eight of 125 species in the Colombian Andes show allopatric speciation, with close allies at similar altitudes in different ranges, whereas 61 species have parapatric distribution of close relatives at different elevational belts on the same slope (Adams, 1986). In addition to the radiation of autochthonous South American groups, the Andean biota was enriched by the immigration of taxa from North America, which occurred in a series of waves during the last few million years. Although this contribution is not considerable in birds (only 5% of the South American avifauna is composed of groups that invaded from , 1994), the contribution of these invaders is the north; Fjeldsa important in other taxonomic groups. The diversity of South American rodents, for example, is the result of radiation in two different groups. Hystricognath rodents (agoutis, porcupines and allies) are hypothesized to have arrived either from Africa or North America, sometime in the Eocene, and radiated in the lowlands east of the Andes, where they presently have their highest diversity (Wood, 1985; Reig, 1986; Eisenberg, 1989; Marshall & Sempere, 1993). Some species have invaded the Andes, but few are exclusively Andean. However, the Andes have played a key role in the radiation of the diverse sigmodontine rodents (> 250 species of Neotropical mice and rats). The rst wave of sigmodontine invasion from North America likely occurred as far back as the Miocene. Subsequent uplifting of the Andes during the Miocene orogenic phase set the stage for the radiation of an oryzomine stock in the northern Andes, which then dispersed south through the Andes, and north into Central America. From an oryzomine ancestor, an akodont stock was derived and radiated in the southern Andes, which in turn dispersed back into the northern Andes (Hershkovitz, 1966; Reig, 1986; Marshall & Sempere, 1993; Patterson, 1999). Thus, rodent diversity in the tropical Andes is the result of a complex history of multiple waves of invasion and radiation, and topographic complexity has been an important factor in this diversication (Marshall & Sempere, 1993; Patterson, 1999). The patterns of diversication and regional differentiation described here have important implications for conserving the extraordinary Andean biodiversity. The richness of the Andean biota is due to beta diversity, i.e. the spatial turnover in species composition that may occur over short distances (Gentry, 1982; , 1994; Patterson et al., 1998; Stotz, 1998). Although Fjeldsa alpha diversity may be low at a given Andean locality in comparison with Amazonian localities, landscape diversities in the Andes may even surpass Amazonian diversities. Much of this high species turnover is due to altitudinal gradients, as species turnover is rapid across elevational belts. But at larger scales, differences in species composition among mountain ranges or even between slopes of the same range result in high regional diversities. Our work showed the existence of at least ve different faunistic subregions, widely divergent in their species composition and afnities and in their evolutionary histories. Conservation efforts should take into account these regional patterns of diversication, in order to ensure representation not only of the present biological diversity, but also of the evolutionary processes that gave rise to this diversity. ACKNOWLEDGMENTS This work was done as part of a biodiversity analysis for the northern Andes, sponsored by the World Wildlife Fund, as part of the development of a biodiversity vision for the Northern Andes Ecoregional Complex. We thank the WWF Colombia ofce, in particular Mary Lou Higgins and Olga a Herna ndez, for supporting this work in various ways. Luc a Isabel Herrera, Mar a Dolores Heredia, Luis We thank Mar n Salazar for compiling lists of Miguel Constantino and Julia frogs and butteries, and for contributing unpublished information. We also thank several anonymous reviewers for making suggestions and pointing out literature that greatly improved this manuscript. WCSs long-term work in the Colombian Andes has been mostly supported by the John D. and Catherine T. MacArthur Foundation. REFERENCES Adams, M.J. (1986) Pronophiline butteries (Satyridae) of the three Andean Cordilleras of Colombia. Zoological Journal of the Linnean Society, 87, 235320. 1837

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G. H. Kattan et al. ndez Camacho, J. & Mun oz Alberico, M., Cadena, A., Herna feros (Synapsida: Theria) de Saba, Y. (2000) Mam Colombia. Biota Colombiana, 1, 4375. Bibby, C.J., Collar, N.J., Crosby, M.J., Heath, M.F., Imboden, C., Johnson, T.H., Long, A.J., Statterseld, A.J. & Thirgood, S.J. (1992) Putting biodiversity on the map: priority areas for global conservation. International Council for Bird Preservation, Cambridge, UK. Brown, K.S. (1987) Biogeography and evolution of Neotropical butteries. Biogeography and Quaternary history in tropical America (ed. by T.C. Whitmore and G.T. Prance), pp. 66104. Clarendon Press, Oxford. gica de Colombia. Revista de la rgl, H. (1961) Historia geolo Bu Academia Colombiana de Ciencias, 11, 137191. Cavelier, J. (1997) Selvas y bosques montanos. Informe nacional sobre el estado de la biodiversidad, tomo I (ed. by M.E. Chaves n de and N. Arango), pp. 3855. Instituto de Investigacio gicosA.Von Humboldt, Bogota , Colombia. 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Patterson, B.D., Stotz, D.F., Solari, S., Fitzpatrick, J.W. & Pacheco, V. (1998) Contrasting patterns of elevational zonation for birds and mammals in the Andes of southeastern Peru. Journal of Biogeography, 25, 593607. Rangel, J.O. (1997a) Diversidad de la ora de Colombia. Informe Nacional sobre el estado de la biodiversidad, tomo I (ed. by M.E. Chaves and N. Arango), pp. 323336. Instituto n de Recursos Biolo gicos A.von Humboldt, de Investigacio , Colombia. Bogota Rangel, J.O. (1997b) Diversidad de la fauna de Colombia. Informe Nacional sobre el estado de la biodiversidad, tomo I (ed. by M.E. Chaves and N. Arango), pp. 337365. Instituto n de Recursos Biolo gicos A. von Humboldt, de Investigacio , Colombia. Bogota Reig, O.A. (1986) Diversity patterns and differentiation of high Andean rodents. High altitude tropical biogeography (ed. by F. Vuilleumier and M. Monasterio), pp. 404439. Oxford University Press, New York. 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BIOSKETCHES Dr Gustavo H. Kattan is the coordinator of the Colombia Program of the Wildlife Conservation Society. His interests focus on the conservation of Andean ecosystems, and he conducts research on macroecology, community ecology and population biology of endangered species. Padu Franco is a recent graduate from the biology program at Universidad del Valle. His research interests include macroecology and behavioural ecology. Vladimir Rojas recently received his MSc from Universidad del Valle. His Senior thesis focused on the biogeography of Colombian mammals, and his Masters thesis was on the biogeography of birds associated to wetlands. n Morales recently received his MSc from Universidad del Valle. His interests include the biogeography and conservation of Germa Andean fauna.

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