Biodiversity and Conservation 10: 1983–1996, 2001.© 2001 Kluwer Academic Publishers. Printed in the Netherlands.

Exotic species introductions into South America:an underestimated threat?

JON PAUL RODRÍGUEZCentro de Ecología, Instituto Venezolano de Investigaciones Científicas, Apartado 21827,Caracas 1020-A, Venezuela (e-mail: jonpaul@ivic.ve; fax: +58-212-5041088)

Received 5 September 2000; accepted in revised form 3 January 2001

Abstract. Prior studies on the latitudinal extent and ecological impact of exotic plant species suggestthat areas of high diversity, such as the Neotropics, may be relatively ‘resistant’ to invasions. To explorethe generality of this assertion and assess the impact of alien species on continental tropical faunas, Icompiled data for threatened Neotropical animals from the red data books of Bolivia, Brazil, Minas Gerais(a Brazilian state), Peru, and Venezuela. A total of 378 species (including both vertebrates and inverte-brates) were considered. For each taxon, I recorded whether it is threatened by habitat conversion, over-exploitation, and/or exotic species. As suggested by other researchers, exotic species introductions appearto be relatively unimportant in South America, threatening only 6% of animal taxa. However, many SouthAmerican animals are themselves either recent invaders or survivors of the Great American Biotic Inter-change (GABI) which began during the Pliocene. Here, I hypothesize that the GABI may have acted as an‘extinction filter,’ leaving faunal groups of mostly South American origin relatively more threatened by thecurrent wave of exotic invaders than those with prominent North American representation. The data supportthis prediction. For taxa whose current diversity patterns were not strongly influenced by the GABI, exoticspecies are indeed an important threat. For example, alien invaders threaten 29% of continental fishes and30% of amphibians, figures comparable to those recorded in temperate areas. As more information on theseless-studied taxa becomes available, the magnitude of the threat posed by exotic species introductions willprobably reveal itself to be large. Of critical importance is to assess the impact of invasions on biologicalrealms that have only been recently exposed to alien taxa, such as the aquatic faunas of the numerousdrainages that occur along the eastern and western slopes of the South American Andes. The results ofthese investigations provide predictions for similar research focussed on other continental tropical regionsof the world.

Key words: alien species, biological invasions, deforestation, exotic species introductions, extinctionthreats, habitat conversion, hunting, Neotropics, overexploitation, South America, threatened species

Introduction

Among the distinctive characteristics of the current biodiversity crisis is an increasingdegree of global ‘biotic homogenization’ (McKinney and Lockwood 1999; Rahel2000). The steady expansion of a relatively small number of species is graduallyreplacing the larger number that are declining as a consequence of human activi-ties. Second only to habitat conversion, exotic species introductions are one of themain threats to biodiversity worldwide (Elton 1958; Vitousek et al. 1997). Scientific

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interest in understanding the process of exotic invasions continues to grow in responseto their perceived role as a major extinction and economic threat (e.g., see Drake et al.1989; Carey et al. 1996; Kareiva 1996; Williamson 1999; Mack et al. 2000; Pimentelet al. 2000).

The proportion of exotic species successfully established in recipient communi-ties, however, is not uniformly distributed across the globe. Empirical studies of thelatitudinal extent of invading plants show that the continental tropics have accumu-lated fewer non-native species than temperate areas have (Rejmánek 1996; Lonsdale1999). Though the mechanisms underlying these patterns are not well understood,there is little evidence in support of the hypothesis that high species richness at lowerlatitudes is directly responsible for invasion resistance (as suggested, for example, byElton 1958; Moulton and Pimm 1986; Case 1991). Rather, it is more plausible that thehigh speed of ecological succession following a disturbance in tropical communitiesmay itself limit an invader’s likelihood of establishment and spread (Rejmánek 1996).Such latitudinal gradients do not appear to exist in offshore insular communities (Case1996; Rejmánek 1996; Lonsdale 1999), though both tropical and temperate oceanicislands seem to be especially sensitive to exotic species, and thus have attracted theattention of researchers concerned with biological invaders (Elton 1958; Vitousek1988; Drake et al. 1989).

Given that the continental tropics have accumulated fewer alien species than thetemperate zone has, does this mean that they are a lesser threat to biodiversity than inthe temperate zone? Existing evidence suggests that this may not be the case, partic-ularly in ecologically insular ecosystems. For example, the introduction of the Nileperch (Lates nilotica) and a few species of tilapia (but predominantly the ngege, Or-eochromis esculentus) into lake Victoria in east Africa caused the extinction of hun-dreds of endemic ciclids (Kaufman 1992; Witte et al. 1992; Ogutu-Ohwayo 1993).Likewise, the introduction of rainbow trout (Oncorhynchus mykiss), sea trout (Salmotrutta), and pejerey (Basilichthys bonariensis) into lake Titicaca in the Peru–Boliviaborder, caused the extinction of the endemic fish Orestias cuvieri and has causeddrastic declines of at least three other species in the same genus (Villwock 1986,1994).

Furthermore, the fact that the continental tropics have experienced fewer plantinvasions does not mean that the introduction of exotics should not affect other taxo-nomic groups in different ways. In the United States, for example, exotics are a mainthreat to 57% of imperiled plants, while they threaten 69% of the birds, only 4% ofthe crayfish and none of the tiger beetles (Wilcove et al. 1998). But despite a numberof studies in the continental tropics that examine the role of exotics as a risk factorat the national or sub-national level, or analyze the impact of biological invaderson a particular taxonomic group (e.g., Riedel 1965; Parsons 1972; Wurtsbaugh andTapia 1988; Witte et al. 1992; Señaris and Lasso 1993; Collar et al. 1994; Villw-ock 1994; Bonino 1995; Andrade 1998b; Chacón de Ulloa 1998; Díaz-Sarmientoand Alvarez-León 1998; Jaksic 1998; Lampo and De Leo 1998; Molur and Walker

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1998; Rodríguez and Rojas-Suárez 1998a; Rueda 1998; López-Rojas and Bonilla-Rivero 2000), a general assessment of the current impact of exotics that spans acrossa wide geographical region and includes a variety of taxonomic groups has not beenpreviously undertaken. The present study is devoted to evaluating the influence ofnon-native species on continental tropical faunas, by focusing on the impact of exoticson South American threatened animals.

Following its separation from Gondwanaland (∼100 million years ago), the SouthAmerican fauna evolved in isolation from the remaining landmasses on Earthuntil the Pliocene, roughly 3 million years ago. The emergence of the Central Amer-ican isthmus allowed the Great American Biotic Interchange (GABI) a massive epi-sode of biotic invasions involving North and South American faunas and floras (Stehliand Webb 1985; Vermeij 1991). Not all taxa were equally successful at invading,however, nor the biotas of both sub-continents equally affected. North Americaninvading mammals experienced a rapid diversification and gradually replaced theSouth American natives; roughly half of current South American mammal genera areof North American origin (Marshall et al. 1982; Mares 1985; Webb 1985; Marshall1988; Lessa and Fariña 1996). Data for birds are not as rich as those for mammals, butavailable evidence also suggests a net movement of taxa from north to south (Vuil-leumier 1985). In contrast, most of the exchange of herpetofauna was predominantlyfrom south to north and included significant movement prior to the emergence of thePanama isthmus. Within this group, only a few North American amphibians enteredSouth America, though several North American reptiles did (Duellman 1979, 1988;Vanzolini and Heyer 1985). In other taxa with limited dispersal, such as freshwa-ter fish, the process occurred at a slower rate. Thus, their current distributions areprobably more similar to those existing prior to the interchange (Bussing 1985).

Studies of extinction and endangered species tend to focus on the better-knowntaxonomic groups, such as birds and mammals, underestimating the risk to understud-ied taxa (McKinney 1999). If an analysis of the impact of exotics in South Americawere to focus mainly on birds and mammals, this could generate a distorted imageas most taxa in these groups are themselves either recent invaders or survivors of theGABI. Prior exposure to biotic exchanges may act as an ‘extinction filter’, decreasingtheir current sensitivity to biological invasions (Balmford 1996). Therefore, attentionshould perhaps focus on taxa whose current diversity patterns were not as stronglyinfluenced by such faunal exchange, such as freshwater fish and amphibians (Bussing1985; Vanzolini and Heyer 1985).

I explore the hypothesis that South American faunal groups relatively unaffectedby the GABI and thus of mostly South American origin should be more threatened bythe current wave of exotic invaders than those with significant North American repre-sentation. If this were the case, invaders may be of higher concern in the Neotropicsthan previously thought (e.g., see Collar et al. 1994; Jaksic 1998; Rodríguez andRojas-Suárez 1998a), and conservation strategies aimed at counteracting the effect ofinvaders may have to be designed taking into account both the taxon and region of

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interest. The results of these investigations provide a framework for similar researchfocused on other continental tropical regions of the world.

Methods

Most South American countries have published national Red Data Books or Red Listsof threatened animals (WCMC 1994). These are catalogues of threatened specieswhere each taxon is assigned to a category that reflects the magnitude of the extinctionrisk it faces (IUCN 1994). Only a few South American Red Data Books, howev-er, also include information about the threats to each taxon. The present analysis isbased on information compiled from five such Red Data Books: Bolivian vertebrates(Ergueta and de Morales 1996), Brazilian mammals (Fonseca et al. 1994), Peruvianterrestrial vertebrates (Pulido 1991), and vertebrates and invertebrates from Vene-zuela (Rodríguez and Rojas-Suárez 1998b) and the Brazilian state of Minas Gerais(Machado et al. 1998). Combined, these five books present information on nearly sev-en hundred animals, spanning 11 orders (Table 1). While not an exhaustive sample,this does cover a large diversity of taxa that extend across the Neotropics, providinga snapshot of current threats to biodiversity in the region.

A database was created to record the risk category assigned to each taxon in thefive Red Data Books, as well as to summarize the available information on their prin-cipal extinction threats. These books use either the most recent version of the WorldConservation Union’s system of red list categories (IUCN 1994), the version thatpreceded it (Groombridge 1993), or, in the case of the Peruvian book (Pulido 1991),a close approximation of the latter. All taxa whose status is not presently well known(e.g. those classified as ‘data deficient’), taxa assigned to an ambiguous category (e.g.

Table 1. Number of taxa included in the Red Data Books used in this study. Not allrow totals are equal to the sum of entries in that row, because some taxa are presentin more than one book simultaneously.

Class Bolivia Brazil Minas Gerais Peru Venezuela Total

Amphibia 2 11 11 24Aves 55 83 8 122 245Bivalvia 3 3Crustacea 12 12Gastropoda 5 5Insecta 27 48 75Mammalia 62 58 40 10 127 220Oligochaeta 3 3Onycophora 1 1Osteichthyes 26 3 16 45Reptilia 14 10 1 23 43

Total 159 58 178 19 367 676

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those classified as ‘rare’), or taxa whose degree of threat is not of high immediateconcern (e.g. those classified as ‘lower risk’) were removed from the database. Thus,the remaining taxa are classified in at least one of the five Red Data Books as ex-tinct (EX), extinct in the wild (EW?), critically endangered (CR), endangered (EN),or vulnerable (VU). Species in the latter three categories are commonly referred tojointly as ‘threatened’ (IUCN 1994). Consequently, the present analysis focuses onlyon South American animals that are threatened or extinct (including both EX andEW?).

Regarding extinction threats, I recorded whether each taxon was threatened byhabitat conversion, overexploitation, exotic species introductions, or some combi-nation of these three. Similar analyses by other authors have used slightly differentthreat classification schemes. For example, Wilson (1992) considers four categories– overexploitation, habitat conversion, exotic species introductions, and diseases car-ried by exotics – while Wilcove et al. (1998) add a fifth one – pollution. In the presentanalysis, diseases carried by exotics are included as part of the ‘exotic species’ cate-gory, while pollution is considered a form of habitat conversion. It was also recordedwhether taxa threatened by exotics were also restricted to islands or if they inhabitedin the mainland. The purpose of this simpler scheme is to facilitate the classificationof the threats to South American taxa. It is important to note that a threat was re-corded when the authors of each Red Data Book reported it either as a hypothesizedor observed cause of population decline. No attempt was made to verify the reportsin the Red Data Books or to estimate the relative importance of each threat to eachtaxon.

Results

The removal of taxa that did not meet the criteria outlined above reduced the num-ber of animals in the database from 676 to 378; one order, Bivalvia, was also lost.The remaining taxa are predominantly vertebrates (∼90%), with birds and mammalsaccounting for roughly 70% of all entries (Table 2).

The main threats to South American animals are habitat conversion and overex-ploitation, respectively (Table 2). Overall, exotic species appear to threaten a rela-tively small proportion of taxa (6%). In contrast, half of the imperiled species in theUnited States (Table 2) and 80% of endangered South African fynbos species (Arm-strong 1995) are considered threatened by biological invaders, while exotic specieswere implicated in the global extinction of a fifth of the mammals, a fifth of the birds,and roughly 40% of reptiles that have been documented since the 1600s (Nilsson1983).

A closer look at the results, however, reveals that the pattern might be more subtlethan is initially apparent. Though South American birds, mammals and reptiles –which overwhelm the database as a consequence of their numbers – do not appear

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Table 2. Proportion (%) of taxa in each class at risk due to the three main threats to South Amer-ican animals. Proportions add up to over one hundred percent because some taxa are affectedby more than one threat simultaneously. Included are only taxa classified as EX, EW?, CR, ENor VU (see text for abbreviations). For comparison, the last column presents equivalent figuresfor taxa threatened by exotic species in US (from Wilcove et al. 1998).

South American taxa threatened by (%)

Class n ExoticsHabitatconversion Over exploitation

Proportion threatenedby exotic species in US

Amphibia 20 30 100 45 27Aves 170 3 87 43 69Crustacea 4 75Gastropoda 1 100Insecta 30 93 7Mammalia 101 4 87 65 27Oligochaeta 3 100 33Onycophora 1 100Osteichthyes 21 24 67 38 53Reptilia 27 7 70 78 37

Total 378 6 86 48 49

to be very susceptible to exotic species, a much larger proportion of amphibians andfish are threatened by biological invaders. Moreover, if among the fishes only con-tinental species are considered, the proportion threatened by exotics increases from24 to 29%. The figures for birds, mammals and reptiles are in sharp contrast to theequivalent figures for North America, but the numbers for fish and amphibians arewithin the same order of magnitude (Table 2). Considering that fish and amphibiansare relatively less-studied groups, the threat posed by exotic species may be evenlarger than is apparent in this analysis. As mentioned above, these groups are alsopredominantly of South American origin, thus providing support to the hypothesisthat they should be relatively more sensitive to biological invasions than birds andmammals, which are mainly of North American origin. Of the 22 taxa examinedwhich are threatened by exotic species, only one of them is an island species (Ven-ezuela’s Margarita island blue crowned parakeet, Aratinga acuticaudata neoxena) –all others inhabit the mainland.

Discussion

The general trend in the results is according to the prediction: taxa of predominantlySouth American origin appear to be more sensitive to invasions than groups with moreprominent North American representation. Furthermore, the fact that South Ameri-can birds and mammals – two well-studied groups – are relatively not threatened byexotics further reinforces the predictions. Clearly, to be able to support this assertion

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with a greater degree of certainty will require additional research. Of particular im-portance is to examine factors other than extinction threats that may be generatingthe observed patterns. For example, certain natural history traits, such as dispersalability, physiology and behavior, may be correlated due to phylogenetic relatedness,thus influencing the susceptibility of certain taxa to biological invasions. Therefore,the results here discussed must be considered as preliminary and be used to postulatehypotheses for future testing.

Exotic species are largely absent from discussions about Neotropical wildlifemanagement and conservation (e.g., see Robinson and Redford 1991; Fang et al.1997), as well as from considerations pertaining fisheries management (e.g., seeWelcomme 1990). Recent issues (Vols. 3–6) of the journal Vida Silvestre Neotropical(1994–1997), do not include a single article that considers exotic species as a threatto regional biodiversity. One study discusses their role as agricultural pests (Bruggersand Zaccagnini 1994), another as vectors of human diseases (Villa et al. 1994), and athird is a general review of the risk of spreading exotic pathogens to wild populationsthrough captive breeding and reintroduction programs (Jiménez Pérez 1996).

There are at least three possible reasons why the impact of exotic species in SouthAmerica may be currently underestimated. First, relatively little research on exot-ic species has taken place in the tropics when compared with the temperate zone(Drake et al. 1989; Pysek 1995). An indicator of this trend is the disproportionaterepresentation of North American and European scientists in the Global BiodiversityAssessment (UNEP 1995) of the United Nations Environment Programme (Figure 1).Though many scientists that reside in the temperate zone also carry out research intropical regions, the difference in research resources available between the indus-trialized and developing world is a well-known fact (May 1998). It is also possiblethat the predominance of English may limit exchange of information with scientistsfrom the non English-speaking world. Further research, targeted at understanding thephenomenon of biological invasions in the Neotropics may reveal that the impact ofexotics is more ubiquitous than is reflected by current literature.

Second, historically, the focus of species conservation research in South Americahas been on large vertebrates, which tend to be threatened mainly by overexploitationand large-scale habitat conversion (Table 2; also see Mares and Ojeda 1984; Ojasti1993; Iriarte et al. 1997). The oldest South American Red List is the one for Chil-ean terrestrial vertebrates (Glade 1988). It took a decade more for threatened specieslists to incorporate invertebrates as well (e.g., Machado et al. 1998; São Paulo 1998;Rodríguez and Rojas-Suárez 1998b). In some cases, exotic species are not even con-sidered a topic worthwhile for scientific research. A recent survey of exotic speciesintroductions into Colombia concluded that (1) the general public is totally unawareof the consequences of exotic species introductions, (2) lack of scientific interest in‘non-native’ fauna resulted in their regularly being excluded from routine wildlifesurveys, and (3) studies of the effect of invaders on freshwater biotas and plants havenever been carried out (Andrade 1998a). Only in the temperate zone of South America

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have exotic species been the object of synthetic reviews (Bonino 1995; Jaksic 1998).In these cases, however, just terrestrial vertebrates are considered, and there is a clearbias towards larger vertebrates such as mammals and birds. In general, relative to ver-tebrates, the burden of proof seems to be higher for considering a plant or invertebrateas threatened (Wilcove et al. 1993), while extinction rates in freshwater ecosystemsmay be as high as five times larger than those observed for terrestrial species (Ricc-iardi and Rasmussen 1999).Thus, those species groups that appear to be more likelyto be sensitive to invaders in South America tend to be of lesser conservation interestand the threat of exotics goes unnoticed.

The third reason for the underestimation of the impact of exotics in South Americais a bias in regional science. Overexploitation and habitat conversion have dominatedthe scene of perceived threats to biodiversity in South America, thus scientists maybe more inclined to attribute a recently observed population decline to habitat de-gradation than to the introduction of an exotic species. For example, the cinereouswarbling-finch (Poospiza cinerea) is considered vulnerable in Minas Gerais (Brazil)as a consequence of vegetation changes mediated by the expansion of exotic grasses(Machado et al. 1998). Alien grasses have established themselves both in native andderived savannas in Central and South America. In combination with fire, these grass-es are able to trigger positive feedback loops that facilitate their establishment andspread, preventing the recovery of forest once converted into grassland (D’Antonioand Vitousek 1992). Such large scale habitat changes may mask the fact that theunderlying process is a biological invasion.

Although the present study has focussed on exotic species as a threat to conti-nental faunas, there exist great similarities between these results and the observationthat insular faunas tend to be relatively more sensitive to alien invaders than main-land faunas (Elton 1958; Vitousek 1988). I have argued that taxa of mainly SouthAmerican origin should be more sensitive than taxa with abundant North Americanrepresentatives, because they have evolved in the absence of recent invasion events.Though species diversity can be regionally high for these South American groups,it has accumulated locally as a consequence of in situ speciation rather than as aconsequence of dispersing taxa from other regions. Such locally-generated speciesassemblages – as is the case with the cyprinodontid fishes in lake Titicaca in thePeru-Bolivia border (Villwock 1986, 1994) – have proved to be highly sensitive toinvasion in other regions as well, regardless of whether they are from islands or con-tinents. Pimm (1998) discusses five well-known cases of major recent extinctions:Pacific island birds, flora of the Cape floristic region in South Africa, freshwatermussels and clams in North America, freshwater fish in North America, and Austra-lian mammals. In all these cases, exotic species introductions played a mayor role incausing extinction, and, until the relatively recent wave of biotic invasions mediatedby humans, the native taxa evolved in relative isolation from the influence of colo-nizing taxa from other regions (e.g., see Banarescu 1992; Cowling et al. 1996). Themain common feature between the cases presented by Pimm (1998) and those that I

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have discussed here is that sensitivity to invasions is associated with a long historyof ‘evolutionary insularity’, without major exposure to recent large-scale invasionevents.

Although the results of the present study conform to the predictions, they must betaken with caution. The sample size on which the analysis is based is small; only 22of the 378 taxa considered are threatened by exotics. Additionally, although exoticspecies are proposed as a threat to these taxa, they may not be the only or the mostimportant ones. For example, the current status of the amphibian species here con-sidered has been linked to the global amphibian decline phenomenon (La Marca andReinthaler 1991). Recent work suggests that such decline may be due to the spreadof an exotic fungal pathogen (Berger et al. 1998; Lips 1999), but it is still unclearwhether the South American species included in the present analysis have declinedas a consequence of this pathogen, or due to other causes such as habitat conversionor predation by introduced salmonid fishes (La Marca and Reinthaler 1991).

In conclusion, this study provides preliminary evidence to suggest that SouthAmerican faunas may be more sensitive to biological invasions than previously in-dicated in the literature. Additionally, taxonomic groups of predominantly SouthAmerican origin whose current biogeographical patterns were not strongly influencedby the GABI appear to be especially susceptible. Among these groups are amphibiansand freshwater fish. Future research should focus on these understudied taxa, partic-ularly in regions were faunas are known to have radiated locally and in isolationof taxa from other regions, such as Andean montane ecosystems (Descimon 1986;Vuilleumier 1986). Among the different taxa, the impact of introduced freshwaterfishes has probably been particularly underestimated. Hundreds of species of fisheshave been introduced into South American rivers and lakes, with very limited knowl-edge of their impact (e.g., Señaris and Lasso 1993; Villwock 1994; Díaz-Sarmientoand Alvarez-León 1998; Gutiérrez and Alvarado 1998). Previous experience in otherparts of the world suggests that the deliberate or accidental introduction of freshwaterfish is often followed by their rapid expansion through river networks, causing thedecline and often the extinction of numerous native taxa (Kaufman 1992; Allan andFlecker 1993; Wilcove and Bean 1994; Wilcove et al. 1994).

Acknowledgements

I am grateful to Jorge A. Ahumada and the Instituto de Investigación de RecursosBiológicos Alexander von Humboldt for their invitation to speak about exotic spe-cies introductions at the II Congreso Nacional de Conservación de la Biodiversidad(October, 1999, Universidad Javeriana, Bogotá, Colombia), and thus inspiring thispaper. The comments of Kathryn M. Rodríguez-Clark, Stuart Pimm, and two anon-ymous reviewers improved a previous version of the text. All remaining faults aremine, not theirs.

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References

Allan JD and Flecker AS (1993) Biodiversity conservation in running waters. BioScience 43: 32–43Andrade GI (1998a) Efecto de las especies introducidas y transplantadas sobre la biota local. In: Chaves

ME and Arango N (eds) Informe nacional sobre el estado de la biodiversidad 1997 – Colombia. TomoII. Causas de pérdida de biodiversidad, pp 93–95. Instituto de Investigación de Recursos BiológicosAlexander von Humboldt, PNUMA, Ministerio del Medio Ambiente, Santaféde Bogotá, Colombia

Andrade GI (1998b) Introducción de especies en ecosistemas terrestres. In: Chaves ME and Arango N (eds)Informe nacional sobre el estado de la biodiversidad 1997 – Colombia. Tomo II. Causas de pérdida debiodiversidad, pp 96–98. Instituto de Investigación de Recursos Biológicos Alexander von Humboldt,PNUMA, Ministerio del Medio Ambiente, Santaféde Bogotá, Colombia

Armstrong S (1995) Rare plants protect Cape’s water supplies. New Scientist 145: 8Balmford A (1996) Extinction filters and current resilience: the significance of past selection pressures for

conservation biology. Trends in Ecology and Evolution 11: 193–196Banarescu P (1992) Zoogeography of Fresh Waters, vol. 2. Distribution and Dispersal of Freshwater Ani-

mals in North America and Eurasia. AULA-Verlag, Wiesbaden, GermanyBerger L, Speare R, Daszak P, Green DE, Cunningham AA, Goggin CL, Slocombe R, Ragan MA, Hyatt

AD, McDonald KR, Hines HB, Lips KR, Marantelli G and Parkes H (1998) Chytridiomycosis causesamphibian mortality associated with population declines in the rain forests of Australia and CentralAmerica. Proceedings of the National Academy of Sciences USA 95: 9031–9036

Bonino NA (1995) Introduced mammals in Patagonia, southern Argentina: consequences, problems,and management considerations. In: Bissonette JA and Krausman PR (eds) Proceedings of the FirstInternational Wildlife Management Congress, pp 406–409. The Wildlife Society, Bethesda, Maryland

Bruggers RL and Zaccagnini ME (1994) Vertebrate pest problems related to agricultural production andapplied research in Argentina. Vida Silvestre Neotropical 3: 71–83

Bussing WA (1985) Patterns of distribution of the Central American ichthyofauna. In: Stehli FG andWebb SD (eds) The Great American Biotic Exchange, pp 453–473. Plenum Press, New York/London

Carey JR, Moyle PB, Rejmánek M and Vermeij G (eds) (1996) Invasion biology. Biological Conservation78: 1–214

Case TJ (1991) Invasion resistance, species build-up and community collapse in metapopulation modelswith interspecific competition. Biological Journal of the Linnean Society 42: 239–266

Case TJ (1996) Global patterns in the establishment and distribution of exotic birds. Biological Conserva-tion 78: 69–96

Chacón de Ulloa P (1998) Introducción de la hormiga loca en Colombia. In: Chaves ME and ArangoN (eds) Informe nacional sobre el estado de la biodiversidad 1997 – Colombia. Tomo II. Causas depérdida de biodiversidad, pp 99–100. Instituto de Investigación de Recursos Biológicos Alexander vonHumboldt, PNUMA, Ministerio del Medio Ambiente, Santaféde Bogotá, Colombia

Collar NJ, Crosby MJ and Stattersfield AJ (1994) Birds to Watch 2. The World List of Threatened Birds.BirdLife International, Cambridge, UK

Cowling RM, Rundel PW, Lamont BB, Arroyo MK and Arianoutsou M (1996) Plant diversity in Mediter-ranean-climate regions. Trends in Ecology and Evolution 11: 362–366

D’Antonio CM and Vitousek PM (1992) Biological invasions by exotic grasses, the grass/fire cycle, andglobal change. Annual Review of Ecology and Systematics 23: 63–87

Descimon H (1986) Origins of lepidopteran faunas in the high tropical Andes. In: Vuilleumier F and Mon-asterio M (eds) High Altitude Tropical Biogeography, pp 500–532. Oxford University Press, Oxford,UK

Díaz-Sarmiento JA and Alvarez-León R (1998) Fish diversity conservation in Colombia. In: Harvey B,Ross C, Greer D and Carolsfeld J (eds) Action Before Extinction, pp 215–222. World Fisheries Trust,Victoria, BC, Canada

Drake JA, Mooney HA, di Castri F, Groves RH, Kruger RH, Rejmanek FJ and Williamson M (eds) (1989)Biological Invasions: A Global Perspective. Wiley, New York

Duellman WE (1979) The South American herpetofauna: a panoramic view. In: Duellman WE (ed)The South American Herpetofauna: Its Origin, Evolution, and Dispersal, pp 1–28. Museum of NaturalHistory, The University of Kansas, Lawrence, Kansas

1994

Duellman WE (1988) Patterns of species diversity in anuran amphibians in the American tropics. Annalsof the Missouri Botanical Garden 75: 79–104

Elton CS (1958) The Ecology of Invasions by Animals and Plants. Methuen & Co., LondonErgueta P and de Morales C (eds) (1996) Libro rojo de los vertebrados de Bolivia. Centro de Datos para la

Conservación, La Paz, BoliviaFang TG, Bodmer RE, Aquino R and Valqui MH (eds) (1997) Manejo de fauna silvestre en la Ama-

zonía. Universidad Nacional de la Amazonía Peruana, University of Florida, UNDP/GEF, Instituto deEcología, La Paz, Bolivia

Fonseca GAB, Rylands AB, Costa CMR, Machado RB and Leite YLR (1994) Livro vermelho dosmamíferos brasileiros ameaçados de extinção. Fundação Biodivesitas, Belo Horizonte, Brazil

Glade AA (ed) (1988) Libro rojo de los vertebrados terrestres de Chile. Corporación Nacional Forestal,Santiago, Chile

Groombridge B (ed) (1993) 1994 IUCN Red List of Threatened Animals. IUCN, Gland, Switzerland/Cam-bridge, UK

Gutiérrez FP and Alvarado H (1998) Introducción de especies en ecosistemas acuáticos. In: Chaves MEand Arango N (eds) Informe nacional sobre el estado de la biodiversidad 1997 – Colombia. Tomo II.Causas de pérdida de biodiversidad, pp 106–110. Instituto de Investigación de Recursos BiológicosAlexander von Humboldt, PNUMA, Ministerio del Medio Ambiente, Santaféde Bogotá, Colombia

Iriarte JA, Feisinger P and Jaksic FM (1997) Trends in wildlife use and trade in Chile. Biological Conser-vation 81: 9–20

IUCN (1994) IUCN Red List Categories. IUCN Species Survival Commission, Gland, SwitzerlandJaksic FM (1998) Vertebrate invaders and their ecological impacts in Chile. Biodiversity and Conservation

7: 1427–1445Jiménez Pérez I (1996) Limitaciones de la reintroducción y cría en cautiverio como herramientas de con-

servación. Vida Silvestre Neotropical 5: 89–100Kareiva Pe (1996) Developing a predictive ecology for non-indigenous species and ecological invasions.

Ecology 77: 1651–1697Kaufman L (1992) Catastrophic change in species-rish freshwater ecosystems. BioScience 42: 846–858La Marca E and Reinthaler HP (1991) Population changes in Atelopus species of the cordillera de Mérida,

Venezuela. Herpetological Review 22: 125–128Lampo M and De Leo GA (1998) The invasion ecology of the toad Bufo marinus: from South America to

Australia. Ecological Applications 8: 388–396Lessa EP and Fariña RA (1996) Reassessment of extinction patterns among the Late Pleistocene mammals

of South America. Palaeontology 39: 651–662Lips KR (1999) Mass mortality and population declines of anurans at an upland site in western Panama.

Conservation Biology 13: 117–125Lonsdale WM (1999) Global patterns of plant invasions and the concept of invasibility. Ecology 80: 1522–

1536López-Rojas H and Bonilla-Rivero AL (2000) Anthropogenically induced fish diversity reduction in lake

Valencia basin, Venezuela. Biodiversity and Conservation 9: 757–765Machado ABM, da Fonseca GAB, Machado RB, Aguiar LMS and Lins LV (eds) (1998) Livro vermelho

das espécies ameaçadas de extinção da fauna de Minas Gerais. Fundação Biodiversitas, Belo Horizonte,Brazil

Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M and Bazzaz FA (2000) Biotic invasions: causes,epidemiology, global consequences, and control. Ecological Applications 10: 689–710

Mares MA (1985) Mammal faunas of xeric habitats and the Great American Interchange. In: Stehli FG andWebb SD (eds) The Great American Biotic Exchange, pp 489–520. Plenum Press, New York/London

Mares MA and Ojeda RA (1984) Faunal commercialization and conservation in South America. Bio-science 34: 580–584

Marshall LG (1988) Land mammals and the Great American Interchange. American Scientist 76: 380–388Marshall LG, Webb SD, Sepkoski JJ Jr and Raup DM (1982) Mammalian evolution and the Great Ameri-

can Interchange. Science 215: 1351–1357May RM (1998) The scientific investment of nations. Science 281: 49–51

1995

McKinney ML (1999) High rates of extinction and threat in poorly studied taxa. Conservation Biology 13:1273–1281

McKinney ML and Lockwood JL (1999) Biotic homogenization: a few winners replacing many loosers inthe next mass extinction. Trends in Ecology and Evolution 14: 450–453

Molur S and Walker S (1998) Conservation assessment of the herpetofauna of India – an overview. Hama-dryad 23: 169–178

Moulton MP and Pimm SL (1986) Species introductions to Hawaii. In: Mooney HA and Drake JA (eds)Ecology of Biological Invasions of North America and Hawaii, pp 231–249. Springer-Verlag, New York

Nilsson G (1983) The Endangered Species Handbook. Animaal Welfare Institute, Washington, DCOgutu-Ohwayo R (1993) The effects of predation by Nile perch, Lates niloticus L., on the fish of lake

Nabugabo, with suggestions for conservation of endangered endemic cichlids. Conservation Biology 7:701–711

Ojasti J (1993) Utilización de la fauna silvestre en América Latina. Situación y perspectivas para un manejosostenible. FAO, Rome

Parsons J (1972) Spread of African pasture grasses to the American tropics. Journal of Range Management25: 12–17

Pimentel D, Lach L, Zuniga R and Morrison D (2000) Environmental and economic costs of nonindigenousspecies in the United States. BioScience 50: 53–65

Pimm SL (1998) Extinction. In: Sutherland WJ (ed) Conservation Science and Action, pp 20–38. Black-well Science, Oxford, UK

Pulido V (1991) El Libro Rojo de La Fauna Silvestre del Perú. Instituto Nacional de Investigación Agrariay Agroindustrial, Lima, Perú

Pysek P (1995) Recent trends in studies on plant invasions (1974–1993). In: Pysek P, Prach K, Rejmánek Mand Wade M (eds) Plant Invasions – General Aspects and Special Problems, pp 223–236. SPB AcademicPublishing, Amsterdam

Rahel FJ (2000) Homogenization of fish faunas across the United States. Science 288: 854–856Rejmánek M (1996) Species richness and resistance to invasions. In: Orians GH, Dirzo R and Cushman JH

(eds) Biodiversity and Ecosystem Processes in Tropical Forests, pp 153–172. Springer-Verlag, BerlinRicciardi A and Rasmussen JB (1999) Extinction rates of North American freshwater fauna. Conservation

Biology 13: 1220–1222Riedel D (1965) Some remarks on the fecundity of Tilapia (T. mossambica Peters) and its introduction

into middle Central America (Nicaragua) together with a first contribution towards the limnology ofNicaragua. Hydrobiologia 25: 357–388

Robinson JG and Redford KH (eds) (1991) Neotropical Wildlife Use and Conservation. University ofChicago Press, Chicago

Rodríguez JP and Rojas-Suárez F (1998a) Fauna amenazada de Venezuela: causas pasadas, presiones ac-tuales y perspectivas futuras. Vida Silvestre Neotropical 7: 90–98

Rodríguez JP and Rojas-Suárez F (1998b) Libro rojo de la fauna Venezolana, segunda edición. PROVITA,Fundación Polar, Caracas

Rueda JV (1998b) Aspectos generales sobre la situación actual de las poblaciones adventicias de rana toro(Rana castbeiana) en el valle del Cauca. In: Chaves ME and Arango N (eds) Informe nacional sobre elestado de la biodiversidad 1997 – Colombia. Tomo II. Causas de pérdida de biodiversidad, pp 101–103.Instituto de Investigación de Recursos Biológicos Alexander von Humboldt, PNUMA, Ministerio delMedio Ambiente, Santafé de Bogotá, Colombia

São Paulo (1998) Fauna ameaçada no estado de São Paulo. Secretaria de Estado do Meio Ambiente, SãoPaulo, Brazil

Señaris JC and Lasso C (1993) Ecología alimentaria y reproductiva de la mojarra de río Caquetaia kra-ussii (Steindachner 1878) (Pisces; Cichlidae) en los llanos inindables de Venezuela. Publicaciones de laAsociación de Amigos de Doñana 2: 1–58

Stehli FG and Webb SD (eds) (1985) The Great American Biotic Exchange. Plenum Press, New York/Lon-don

UNEP (1995) Global Biodiversity Assessment. United Nations Environment Programme, CambridgeUniversity Press, Cambridge, UK

1996

Vanzolini PE and Heyer WR (1985) The American herpetofauna and the interchange. In: Stehli FG andWebb SD (eds) The Great American Biotic Exchange, pp 475–487. Plenum Press, New York/London

Vermeij GJ (1991) When biotas meet: understanding biotic exchange. Science 253: 1099–1104Villa B, Franco DW and Franco DC (1994) Population structure and reproductive characteristics of the

Norway rat (Rattus norvegicus) in some markets of Mexico city. Vida Silvestre Neotropical 3: 112–114Villwock W (1986) Speciation and adaptive radiation in Andean Orestias fishes. In: Vuilleumier F and

Monasterio M (eds) High Altitude Tropical Biogeography, pp 387–403. Oxford University Press,Oxford, UK

Villwock W (1994) Consecuencias de la introducción de peces exóticos sobre las especies nativas del lagoTiticaca. Ecología en Bolivia 23: 49–56

Vitousek PM (1988) Diversity and biological invasions of oceanic island. In: Wilson EO (ed) Biodiversity,pp 181–189. National Academy Press, Washington, DC

Vitousek PM, D’Antonio CM, Loope LL, Rejmánek M and Westbrooks R (1997) Introduced species:a significant component of human-caused global change. New Zealand Journal of Ecology 21: 1–16

Vuilleumier F (1985) Fossil and recent avifaunas and the interamerican interchange. In: Stehli FG andWebb SD (eds) The Great American Biotic Exchange, pp 387–424. Plenum Press, New York/London

Vuilleumier F (1986) Origins of the tropical avifaunas of the high Andes. In: Vuilleumier F and MonasterioM (eds) High Altitude Tropical Biogeography, pp 586–622. Oxford University Press, Oxford, UK

WCMC (1994) Biodiversity Data Sourcebook. World Conservation Press, Cambridge, UKWebb DS (1985) Late Cenozoic mammal dispersals between the Americas. In: Stehli FG and Webb SD

(eds) The Great American Biotic Exchange, pp 357–386. Plenum Press, New York/LondonWelcomme RL (1990) Status of fiheries in South American rivers. Interciencia 15: 337–245Wilcove DS and Bean MJ (eds) (1994) The Big Kill. Environmental Defense Fund, Washington, DCWilcove DS, McMillan M and Winston KC (1993) What exactly is an endangered species? An analysis of

the US endangered species list: 1985–1991. Conservation Biology 7: 87–93Wilcove DS, Fujita R and Goldburg B (1994) Enlightened fisheries management: solving problems instead

of creating them. In: Wilcove DS and J BM (eds) The Big Kill, pp 247–266. Environmental DefenseFund, Washington, DC

Wilcove DS, Rothstein D, Dubow J, Phillips A and Losos E (1998) Quantifying threats to imperiled speciesin the United States. BioScience 48: 607–615

Williamson M (1999) Invasions. Ecography 22: 5–12Wilson EO (1992) The Diversity of Life. W. W. Norton & Company, New York/LondonWitte F, Goldschmidt T, Wanink J, van Oijen M, Goudswaard K, Witte-Maas E and Bouton N (1992) The

destruction of an endemic species flock: quantitative data on the decline of the haplochromine cichlidsof lake Victoria. Environmental Biology of Fishes 34: 1–28

Wurtsbaugh WA and Tapia RA (1988) Mass mortality of fishes in Lake Titicaca (Peru-Bolivia) associatedwith the protozoan parasite Ichthyophthirius multifiliis. Transactions of the American Fisheries Society117: 213–217