Exotic plant invasions to the mediterranean region of

465CAUSES, HISTORY, AND IMPACTS OF PLANT INVASIONS IN CHILERevista Chilena de Historia Natural77: 465-483, 2004

Exotic plant invasions to the mediterranean region of Chile: causes,history and impacts

Invasión de plantas exóticas en la región mediterránea de Chile: causas, historia e impactos

JAVIER A. FIGUEROA*, SERGIO A. CASTRO, PABLO A. MARQUET & FABIAN M. JAKSIC

Centro de Estudios Avanzados en Ecología & Biodiversidad, Pontificia Universidad Católica de Chile, SantiagoCP 6513677, Chile

*Corresponding author: [email protected]

ABSTRACT

We review the literature on patterns, causes, processes and impacts of exotic plants, primarily in themediterranean region of Chile, considering three major non-independent drivers of the invasion process: (a)Availability of exotic species propagules, (b) attributes of the local communities in which exotic speciesestablish and through which they will eventually spread out, and (c) attributes of exotic species that eitherfacilitate or constraint their spread into new sites. Regarding availability of propagules, central Chile matorralpresents the communities with the greatest incidence of naturalized herbs, followed by the sclerophyllousforest and the espinal scrubland in the coastal range. In contrast, north-central communities have lowernumbers and proportions of naturalized species of herbs in their seed banks. Availability and persistence ofnaturalized herbs do not differ between aboveground vegetation and seed bank. Regarding attributes of localcommunities associated with the establishment and the spread of exotics, grazing regime and land use emergeas the most prominent causes that render them more prone to invasion by exotics. Evidence on the effect ofthe fire regime is contradictory and native species richness does not seem to be an important factor. Regardingattributes of exotic species seeds, results suggest that naturalized annuals germinate within a wide temperaturerange, are highly resistant to cold and dry conditions, and show some degree of physiological dormancy.Additionally, naturalized annuals are highly tolerant to poor soils, but are generally intolerant to shade. Thesegeneral attributes have largely determined the invasion process in the mediterranean region of Chile.Historical data indicate that an important number of exotic species were intentionally introduced, and that thespread of exotic is uncontrolled. It has been demonstrated that arrival time of exotics is of great relevance tounderstand present day spread of exotics in Chile, independent of their biogeographic origin. Exotic speciesmay cause strong disruptions of ecosystem processes and functions in Chile, as exemplified by exotic treeplantations, which have altered soil chemistry, nutrient cycling, water cycle, hydrology, microclimate, andfire frequency and intensity.

Key words: exotic species, plant invasions, naturalized plants, invasion history, ecosystem disruption.

RESUMEN

Revisamos la literatura sobre patrones, causas, procesos e impactos de las plantas exóticas, principalmente enla región mediterránea de Chile, considerando tres factores determinantes del proceso de invasión: (a)Disponibilidad de propágulos de las especies exóticas, (b) atributos de las comunidades locales en las cualeslas especies exóticas se establecen y a partir de las cuales eventualmente se expanden, y (c) atributos de lasespecies exóticas que facilitan o restringen su expansión a nuevos sitios. Con relación a la disponibilidad depropágulos, el matorral de Chile central presenta las comunidades con la mayor incidencia de hierbasnaturalizadas, seguido por el bosque esclerófilo y el espinal de la Cordillera de la Costa. En contraste, lascomunidades al norte de Chile central tienen menores números y proporciones de hierbas naturalizadas en susbancos de semilla. La disponibilidad y persistencia de hierbas naturalizadas no difiere entre la vegetaciónemergida y el banco de semillas. En cuanto a los atributos de las comunidades locales, asociadas alestablecimiento y expansión de las especies exóticas, tanto el régimen de pastoreo como el uso de la tierraemergen como los factores más prominentes en hacerlas susceptibles a la invasión por exóticas. La evidenciasobre el efecto del régimen de incendios es contradictoria y la riqueza de especies nativas tampoco aparececomo un factor importante. Con relación a la atributos de las semillas de especies exóticas, los resultadossugieren que las anuales naturalizadas germinan dentro de un amplio rango de temperaturas, que sonaltamente resistentes a las condiciones frías y secas, y que muestran un cierto grado de latencia fisiológica.Además, las anuales naturalizadas son altamente tolerantes a los suelos pobres, y generalmente intolerantes ala sombra. Estos atributos generales han sido determinantes en el proceso de invasión de la región

466 FIGUEROA ET AL.

mediterránea de Chile. Los datos históricos indican que un número importante de especies exóticas fueronintroducidas intencionalmente, y que su expansión no está controlada. Se ha demostrado que la fecha dearribo de las especies exóticas es de gran relevancia para entender su actual dispersión en Chile,independientemente de su origen biogeográfico. Las especies exóticas pueden causar grandes perturbacionesde procesos y funciones ecosistémicas en Chile, tal como lo ejemplifican las plantaciones de árboles exóticos,que han alterado la química del suelo, el ciclaje de nutrientes, el ciclo del agua, la hidrología, el microclima, yla frecuencia e intensidad de incendios.

Palabras clave: especies exóticas, invasiones de plantas, plantas naturalizadas, historia de invasión,perturbaciones ecosistémicas

INTRODUCTION

In the past five centuries, the rate ofinterchange of fauna and flora among distantregions of the planet has increased considerably(D’Antonio & Vitousek 1992, Lodge 1993,Williamson 1996). Either intentionally orinadvertently species of a wide spectrum oftaxonomic and geographic origins have beenrelocated by man, by facilitating their dispersalthrough previously insurmountablebiogeographic barriers (Mack et al. 2000, Sakaiet al. 2001). Once in their new habitat,introduced species may establish viablepopulations (Lodge 1993, Kolar & Lodge 2001)and in some cases, surpass the abundance andgeographic distribution of comparable nativespecies (Lodge 1993).

Although the existence of biological invasionshad been noted for some time (Darwin 1872,Elton 1958), it has only been in the last twodecades that a profound interest has developed,owing to the important ecological, economic andhuman health impacts of exotic species (Bright1996, Sakai et al. 2001, Mooney & Hobbs 2000,Pimentel et al. 2000, Mooney et al 2001). At theecological level, invasive species are capable ofmodifying the patterns of abundance anddistribution of native species in the community(Williamson 1996), to the point of causing thelocal extinction of native populations (Vitousek etal. 1996). This fact becomes more worrying if weconsider that present day rates of speciesintroductions are unprecedented in history, andthey are far from being under control (Williamson1996). The existing evidence suggests that greaterchanges in global diversity can be expected ifspecies introductions are not controlled,especially in the species-rich mediterranean-typeregions of the planet (Sala et al. 2000).

Vascular plants are among the mostubiquitous invaders of the biosphere (Elton1958, D’Antonio & Vitousek 1992, van Auken2000). The majority of these plants have beenintroduced for agricultural, sylvicultural,ornamental, or medicinal purposes (Williamson

1996), but many have been introducedaccidentally (Newsome & Noble 1986). InChile, close to 700 exotic vascular plant speciesare considered weeds in agro-ecosystems(Matthei 1995), and many of them have alsoestablished in natural and semi-naturalenvironments (Montenegro et al. 1991, Arroyoet al . 2000). The majority of these areconcentrated in the central region of Chile(Matthei 1995), which below 2,000 m elevationcorresponds to the mediterranean-type climatearea of the country (di Castri & Hajek 1976).Mediterranean ecosystems here and elsewhereare eco-regions with high floristic richness andendemism on a global level (Cowling et al.1996, Arroyo et al. 1999, Myers et al. 2000).

Despite the importance of invasions inChilean mediterranean-type ecosystems, little isknown about the underlying causes of theseinvasions, historical processes, and theirconsequences for native species and ecosystemfunctions. Here, we provide an exhaustivereview of the relevant literature, with thepurpose of assessing what we know and what arethe major gaps in our knowledge of the invasionprocesses in Chilean mediterranean-typeecosystems. For methodological and analyticalpurposes we concentrate on the causes ofinvasions and naturalizations in central Chile byfocusing on three major non-independent driversassociated to the spread of exotic species (Fig.1). We identify propagule availability, attributesof local communities, and attributes of exoticspecies as the three major interactingcomponents of the invasion processes in centralChile. The establishment and spread of exoticspecies depends on an initial availability ofpropagules that will initiate the process ofinvasion within a local community. For thisinitial colonization to be successful a matchbetween the attributes of the local community,which define its invasibility (e.g., disturbanceregime, abiotic and biotic characteristics) andthe ecological and physiological requirementsand tolerances of the exotic species, whichdefine their invasiveness, is required. Depending

467CAUSES, HISTORY, AND IMPACTS OF PLANT INVASIONS IN CHILE

on this, a given species will either establish andreproduce in a local community or becomelocally extinct. Each result will affect theavailability of propagules, thus recursivelyaffecting the process of invasion through time.In the following paragraphs we elaborate onwhat we know about these interactingcomponents of the invasion process and explorethe effects of invasive plants on differentecosystem functions in Chilean mediterraneanecosystems. Finally, we identify areas ofknowledge where research is scarce and/orurgent for a better understanding of theecological consequences of plant invasions inmediterranean-type ecosystems of Chile.

AVAILABILITY OF EXOTIC PLANT PROPAGULES

Established plant pool

Naturalized species in central Chile amount to18 % of the total flora and to 27 % in the case ofherbs (Arroyo et al. 2000). However, thispercentage varies at the scale of localcommunities in central Chile (Table 1). Forinstance, the frequency of naturalized herbs(e.g., Erodium spp., Medicago polymorpha,Malva nicaensis) was close to 45 % of theestablished vegetation in a managed “matorral”(Las Cardas, 30° S), from where domesticherbivores were excluded for five years(Lailhacar & Aylwin 1988, Lailhacar & Torres2002, Torres 1999). Further, in a pre-montanesclerophyllous matorral (San Carlos deApoquindo, 33° S), naturalized herbaceousspecies (e.g., E. cicutarium, Vulpia bromoides,Anthriscus caucalis, Geranium robertianum),represented approximately 50 % of the taxaestablished aboveground (Figueroa et al. inpress). Instead, in a protected semiarid thorn-scrub of northcentral Chile (Aucó, 31° S), only20 % of ephemeral species recorded (e.g., E.botrys , E. malacoides , Galium aparine)corresponded to naturalized species (Gutiérrez etal. 2000). In sum, the available evidencesuggests that the central Chilean matorral is oneof the communities with the greatest incidenceof naturalized herbaceous flora. Other authorshave suggested the same for the sclerophyllousforest and the espinal of the Coastal MountainRange, with frequencies of naturalized speciesabove 50 % (Montenegro et al. 1991).

Propagules stored in the soil

Assessing the availability of naturalized plantsfor an area requires not only knowing where

the flora came from in an establishedcommunity, but also information on thepropagule reserve in the soil (Thompson &Grime 1979, Holmes & Cowling 1997). Forinstance, the percentage of naturalized herbs inthe seed bank of the pre-montanesclerophyllous matorral at San Carlos deApoquindo (33° S) represents approximately 55% of the total number of herbaceous taxa(Figueroa et al. in press). Still, a number ofnaturalized species present in the seed bankwere not recorded among the established plantsat the site during the same season (e.g.,Aphanus arvensis , Nasturtium officinale ,Polygonum aviculare, Portulaca grandiflora).Close to 60 % of the total density of buriedseeds, including native and naturalized herbs inexposed successional areas belonged to theexotic grass Vulpia bromoides (Figueroa et al.in press). On the other hand, a managedgrassland of central Chile (Rinconada deMaipú, 32° S) (Olivares et al. 1994), hadalmost twice the concentration of buried seedsand greater dominance of naturalized herbs inthe seed bank than the pre-montane matorral ofSan Carlos de Apoquindo. Olivares et al.(1994) identified nine taxa in the seed bank, ofwhich eight were naturalized herbs (E. botrys,E. cicutarium, E. malacoides, Avena barbata,Hordeum murinum , Vulpia sp., Trifoliumglomeratum and Medicago polymorpha). In adeciduous matorral of semiarid central Chile(Fray Jorge, 30° S), naturalized annuals (e.g.,E. cicutarium, M. nicaensis) represented about20 % of the total number of seeds (Gutiérrez &Meserve 2003). A minor representation ofnaturalized species was found in the seed bankof a thorn-scrub matorral in north-central Chilewith high presence of ephemeral native species(Table 1), where the most abundant exoticsbelonged to Erodium spp. (Gutiérrez et al.2000). Finally, available information showsthat north-central Chilean communities havesmaller richness and proportion of naturalizedherbs in the seed bank than do central Chileancommunities. Nevertheless, there is not enoughevidence to suggest that the naturalized herbavailability and persistence differs stronglybetween the established vegetationaboveground and the seed bank, perhaps withthe exception of the steppe matorral of north-central Chile (see Table 1).

ATTRIBUTES OF THE LOCAL COMMUNITY

Diverse factors in the native community mayfacilitate the establishment of exotic plants

468 FIGUEROA ET AL.

(Hobbs 2000). For instance, the burning ofnative vegetation (Richardson et al. 1990,D’Antonio 2000, D’Antonio et al. 2001),grazing pressure (Whisenant & Uresk 1990,Stohlgren et al. 1999a, Holmgren 2002),changes in land use (Rudnicky & McDonnell1989, Kowarik 1990, Rapoport 1993, 2000,Drayton & Primack 1996) and low diversity ofthe native community (Elton 1958) mayincrease the susceptibility to invasion by exoticplants. Each of these factors is considered inmore detail below, with regard to informationavailable from central Chile.

Fire regime

The intentional burning of vegetation is awidely used agricultural technique that hasbeen applied since the Spanish conquest(Aronson et al. 1998). The natural present-dayvegetation did not evolve in response to naturalfires occurring during dry summers, as it did inother mediterranean-type climate regions(Muñoz & Fuentes 1989). It is widelyrecognized that fires in the matorral are eitherdirectly or indirectly caused by humans(CONAF 1998, Montenegro et al. 2002). At thesame time, the first reports of naturalized plantsin this region are contemporary with the quickspread of European culture in Chile.Notwithstanding, the introduction of plants andthe use of fire are not clearly related (Holmgren2002) but few experimental studies exist on the

effects of fire on the composition andabundance of naturalized plants in Chile(Keeley & Johnson 1977, Avila et al. 1981,Holmgren 2000a,b). Exotic invasive grasseshave replaced vast regions of evergreenmatorral in central Chile (Holmgren 2002),which is the likely underlying factor of highfrequency of fires (Kunst et al. 2003). There aresuggestions that invasive annual populationsrebound quickly after fires whereas nativeperennials recover slowly, but there is noagreement among authors on the importance offires in the invasibility of communities incentral Chile.

On one hand, in burned woodlands ofAcacia caven, one year after a wildfire, 44,200seedlings per m2 were recorded of thenaturalized annuals Vulpia , Koeleria andBromus (Trabaud 1991). Further, Avila et al.(1981) reported that fire increased theabundance of naturalized herbs such asErodium cicutarium , E. botrys , Stellariacuspidata, Discurainia cumingiana, Matricariachamonilla and Avena barbata in a matorral onthe Coastal Mountain Range (Cuesta Barriga,33° S). Recently, Sax (2002a) also showed thatfire favored exotic species richness and coverover native species in a xeric matorral. Theconclusions of these authors are concordantwith observations made in southern France andwestern North America, where naturalizedspecies that also occur in Chile, enhance thefrequency of fires (e.g., Arundo donax, Bromus

TABLE 1

Percent of exotic herb species recorded in communities of central Chile with regard to the totalnumber of herbs established on the ground and stored in the seed bank. Nd = no data. Percentageswere obtained from lists of species (flora) published by the authors cited, with exception of Sax(2002a) who reported the mean number of plants. All authors presented data at a medium- and

small-size scale, with exception of Arroyo et al. (2000) who recorded at a regional scalePorcentaje de hierbas exóticas establecidas en el suelo y almacenadas en el banco de semillas, considerando el número total

de hierbas registradas en comunidades de Chile central. Nd = no hay datos. Los porcentajes fueron obtenidos desde laslistas de especies que los autores publicaron, a excepción de Sax que informó el número promedio de plantas. Todos los

autores presentan datos a una escala de tamaño mediano y pequeño, a excepción de Arroyo que informó a una escalaregional

Community Location Exotics on the ground Exotics in the Referenceseed bank

Deciduous matorral 30° S 21 19 Gutiérrez & Meserve (2003)Atriplex matorral 30° S 45 Nd Lailhacar & Torres (2002)Steppe matorral 31° S 20 12 Gutiérrez et al. (2000)Managed grassland 32° S Nd 88 Olivares et al. (1994)Evergreen matorral 33° S 50 55 Figueroa et al. (in press)Xeric matorral 33° S 47 Nd Sax (2002a)Acacia espinal Coastal range > 50 Nd Montenegro et al. (1991)Central Chile 33-37° S 27 Nd Arroyo et al. (2000)


madritensis , B . tectorum , Carduuspycnocephalus , E . cicutarium , Geraniumrobertianum, Schismus barbatus, and Sonchusasper) (Trabaud 1991, Dukes & Mooney in thisspecial issue).

Nevertheless, there are contradictory data aswell. For instance, Keeley & Johnson (1977)and Holmgren et al. (2000a,b) showed that firein the Chilean matorral does not havedifferential effects on the relative abundanceand composition of exotic (e.g., Lophocloacristata, E. cicutarium, Medicago polymorpha)and native herbs (e.g., Bromus berterianus,Amsinkia hispida). Likely, the opposed viewson the effects of fire are due to confoundingfactors that affect community invasibility (e.g.,grazing, land use, species richness) and whoseinteraction determine the establishment ofexotic and native plant species. All theseeffects are difficult to sort out with traditionalmethods of vegetation sampling (Stohlgren etal. 1999b). Thus, this is a subject that needs tobe studied further by using experiments thatcontrol for multiple confounding factors.

Grazing regime

Rabbits, together with cattle, goats, and horses,introduced from Europe, are widely distributedin the country and represent the principalherbivores in the matorral (Jaksic 1998).Particularly, European rabbits have been shownto arrest the process of succession in the nativematorral (Fuentes et al. 1983). Although there isno conclusive evidence demonstrating thatrabbits reduce the richness of native plants, theirrelative abundance is surely reduced withrespect to that of naturalized species (Sáiz &Ojeda 1988, Holmgren et al. 2000a).Specifically, when matorral plots were subjectedto rabbit grazing, the native grass Bromusberterianus proved to be the most affectedspecies, losing 30 % more biomass than theintroduced grass Lophocloa cristata (Holmgrenet al. 2000a). In contrast to rabbits, native smallmammals have more limited effects on matorralvegetation (Fuentes et al. 1983).

Rabbits prefer to graze on exposed siteslacking shrub cover (Jaksic 1998). As the dietof rabbits consists mostly of native herbs, thisherbivore may be facilitating the growth ofnaturalized annual herbs in open spaces andoutside shrubs (Jaksic & Fuentes 1980). Thismay have resulted in the presently observedspatial segregation, with perennial native herbsrestricted to protected sites under the shrubcanopy, and with naturalized annual herbscommon on exposed sites outside shrubs

(Jaksic & Fuentes 1980). Nevertheless, thisspatial segregation of invasive versus nativeannual plants does not always occur (Table 2),and could be the result of differences innutrient availability and light. For example, in astudy of a semi-arid grassland (Las Cabras, 30°S), from where livestock had been excluded butthat was exposed to grazing by rabbits, thenaturalized annual species Medicagopolymorpha and Erodium moschatum wereconcentrated below the canopy or in theperiphery of Cassia coquimbensis and ofAcacia caven , respectively (Lailhacar &Aylwin 1988). In these abandoned grasslands,the spatial distribution of annual herbs wasassociated rather to organic matter contents ofsoils, Nitrogen availability, and soil pH(Lailhacar & Aylwin 1988), as well as to wateravailability, and shrub species cover andidentity (Lailhacar et al. 19991, Torres 1999,Lailhacar & Torres 2002).

With respect to exotic livestock, there isconsensus that its presence has enhancednaturalized spread to the detriment of nativeperennials and annuals (Lailhacar et al. 19991,Holmgren et al . 2000a,). Further, theintroduction and management of livestock mayhave provoked the replacement of nativehemicryptophytes by both native andnaturalized annuals, which have the advantageof resisting the most stressful periods of theyear as seeds (Lailhacar 1986). Most authorsconcur that naturalized plants of Eurasianorigin are better adapted and have greatertolerance to grazing by livestock because theyevolved under the pressure of indigenousEurasian livestock (Holmgren 2002).

In sum, it is evident that grazing bylivestock and rabbits has facilitated the spreadof naturalized plants in central Chile (Jaksic &Fuentes 1980, Lailhacar 1986, Lailhacar &Aylwin 1988, Sáiz & Ojeda 1988, Holmgren etal. 2000a, Holmgren 2002) increasing bothspecies invasiveness and communityinvasibility in central Chile. However, theputative effect of rabbits in promoting thespatial segregation of native perennial herbsand introduced annuals is not conclusive.

Land use

In Chile, the richness of exotic flora is directlyrelated to the density of roads (e.g., Cotula

1 LAILHACAR S, C TORRES & P AZÓCAR (1999) Theeffect of Atriplex species and rainfall variations on theherbaceous stratum in arid Chile. VI International Range-land Congress. Townsville, Queensland, Australia.

470 FIGUEROA ET AL.

australis, Hypochaeris radicata), and of urban(e.g., Lactuca serriola) and cultivated soils(e.g., Raphanus sativus) (Arroyo et al. 2000).Results of a comparative analysis betweencentral Chile and California, and comparisonsamong regions of Chile, suggest that plantnaturalization is more frequent in areas ofgreater urban population growth, and contraryto expectations, the amount of agricultural landdoes not have a significant effect (Matthei1995, Arroyo et al. 2000). This pattern couldemerge because roads facilitate the spread ofexotic plants, and urban centers representstorage sites for seeds that come from externaland internal markets.

Likewise, at the landscape scale, thedistribution of exotic plants was studied on ruralroads in two national parks in the AndeanCordillera (39° S) by Pauchard & Alaback(2004). This study showed that rural roads arefunctional corridors and serve as sources ofexotic propagules that facilitate the spread ofexotic species (e.g., Hypochaeris radicata,Agrostis capillaris, Rumex acetosella, Lotusuliginosus) into protected native communities.Therefore, it is important to consider thatchanges in land use may alter and modify theprocesses of invasion and availability of exoticplants (Hobbs 2000, Pauchard & Alaback 2004).

Notwithstanding the above, studies incentral Chile have not yet evaluated themechanisms underlying the spread of exoticspecies on converted soils. Changes in land useare directly correlated with disturbance anderosion increments (Hough 1995), soil and airtemperature (McDonnell et al. 1993), CO2 andO3 concentration (Sukopp 1998), precipitationlikelihood (Botkin & Beveridge 1997), as wellas nutrient, pollutant, pesticide, and herbicideretention and storage (Pouyat & McDonnell1991). Future experimental research in this areashould control for multiple factors associatedwith changes in soil and land use.

Native species richness

Elton (1958) suggested that species-richcommunities should be the most resistant tobiological invasions. Nevertheless, the study byArroyo et al. (2000) in central Chile did notprovide support for Elton’s original hypothesis.This region harbors a lower number of exoticspecies as compared to California, despitehaving a lower species richness of native plantsper surface area. However, Arroyo et al.’sresults may be considered more indicative thanrobust, given that in drawing comparisons atsuch large biogeographical scales, it is difficultto have an adequate number of replicates(Stohlgren et al. 1999a), and the differencebetween the number of exotic species in bothregions could also be strongly influenced bypropagule pressure (Kolar & Lodge 2001), thatpresumably is higher in California than in Chile.

In contrast, at the small scale of 1-m2 to400-m2 plots, Sax (2002a) concluded that, atleast in the dry matorral on the coast of centralChile, the richness of exotic species waspositively correlated with the diversity ofnative plants. This author suggested that bothnative and exotic species are respondingsimilarly to environmental conditions and thuscompetition may not be operating, or notcontrolling local species richness (but seeByers & Noonburg 2003). Several studies havesuggested that the causes that explain theincrease in exotic species richness should besimilar to those factors involved in the increaseof native species richness within the samecommunities (Pickard 1984, Rejmánek 1996,Wiser et al. 1998, Smith & Knapp 1999).Specifically, disturbances and fluctuatingresources in plant communities may facilitatethe coexistence of native and exotic species(Davis et al. 2000, Sax et al. 2002).

Finally, Elton’s original hypothesis has notbeen subjected to test at a regional scale in

TABLE 2

Main establishment site for exotic annual plants in matorral communities of central ChilePrincipal sitio de establecimiento de plantas anuales exóticas en comunidades de matorral de Chile central

Community Exotic species Establishment site Reference

Evergreen matorral Anthriscus caucalis Under the canopy Figueroa et al. (in press)Evergreen matorral Geranium robertianum Under the canopy Figueroa et al. (in press)Cassia matorral Medicago polymorpha Under the canopy Lailhacar & Aylwin (1988)Acacia matorral Erodium moschatum Canopy’s edge Lailhacar & Aylwin (1988)Atriplex matorral Erodium moschatum Canopy’s edge Torres (1999)Atriplex matorral Malva nicaensis Indifferent Torres (1999)Atriplex pruned matorral Erodium moschatum Under the canopy Torres (1999)


central Chile. The great variety of native andanthropogenic communities in the region couldbe an appropriate scenario for determining theeffect of plant naturalizations on local andregional extinction rates of native plants.

ATTRIBUTES OF NATURALIZED PLANTS

Most studies of species invasions use areductionist perspective in which thecharacteristics of exotic species are used topredict the success of invasion (Rejmánek2000). This approach suggests that a successfulinvader can be characterized by a combinationof traits, which would facilitate its spread intonew receiving habitats (Baker 1974, Noble1989, Reichard & Hamilton 1997). Theprincipal characteristics that have beenconsidered to facilitate the invasion of anexotic plant are: the capacity of asexualreproduction (Panetta 1993, Reichard &Hamilton 1997), the presence of perfectflowers, flowering period (Goodwin et al.1999), small-sized genome (Rejmánek 1996),fast growth of the juvenile period (Aronson etal. 1992, Rejmánek & Richardson 1996,Grotkopp et al. 2002), short generation time(Grotkopp et al. 2002), immediate and rapidgermination in a wide range of physicalconditions (Reichard & Hamilton 1997), smallseeds (Rejmánek & Richardson 1996, Grotkoppet al. 2002), high competitive ability (Bakker &Wilson 2001), together with ecophysiologicaladaptation to heterogeneous and stressfulenvironments (Goodwin et al. 1999). Below,we address what is known regarding these traitsamong exotic species present in central Chile.

Life-history traits

Few studies suggest that a specific life historytrait could have favored the invasion of exoticplant species in Chile. Montenegro et al.(1991), in a limited number of sites, found thatthe most frequent herbs in central Chile arethose with annual life cycles. Recently, it wassuggested that, because herbs with annual lifecycles are poorly represented in the native floraof central Chile, available sites are moresusceptible to the invasion of exotic plants thatpossess this life history trait (Holmgren et al.2000a). However, Arroyo et al. (2000) rejectedthis hypothesis at a biogeographical scale. Acomparison of exotic species with annual lifecycles in central Chile and California, with thelatter having a high representation of nativeannual species, showed that Chile is no more

susceptible to annual species introduction thanis California. Thus, high representation ofannual species at a geographical scale is likelyrelated to the high availability of annual speciesin the set of exotic flora that was introduced tocentral Chile from the start, and not necessarilyto an advantage of exotic plants with annuallife cycles over those exotics with perennial lifecycles.

On the other hand, preliminary results of acomparative analysis of the traits of thosespecies that have been introduced to Chileshow that of 143 exotic species on whichinformation is available, 95 % possesshermaphroditic flowers, 3.5 % of the taxa aremonoecious, and 1.5 % are dioecious. Inaddition, seed size, fruit shape, and seeddispersal mechanisms have been shown to beinconclusive traits regarding speciesinvasiveness (Castro & Figueroa unpublisheddata). However, these latter results should beinterpreted with caution because the analysisdid not compare between invasive and non-invasive naturalized species (see Rejmánek1999).

Competitive ability

Experimental evidence on resource competitionbetween exotic and native plants is scarce inChile. In the matorral, Fuentes et al. (1986)proposed that native woody seedlingestablishment in exposed areas is very hard inpart due to increased competition with grasses,which are mostly exotic species. Later,Holmgren et al. (2000a) in a matorral locatedon the foothills of the Andean Ranges showedthat the erect annual native grass Bromusberterianus is competitively dominant overexotic prostrate annuals such as Erodium spp.because the former reduces the amount ofphotosynthetically active light reaching the soilsurface. However, plant competitive abilitycould change if nutrient availability in the soilis limited. For example, exotic prostrateannuals are most successful in nutrient-poorsoils because they allocate resources to developa deeper root system than do native grassesand, in contrast, native grasses are significantlymore abundant in high-fertility soil, whichaffords unlimited nutrients (Holmgren et al.2000a). Recently, a study at a spatial scale <400 m2 in a xeric matorral on the coast ofcentral Chile, with relatively low cover ofwoody species, showed the existence of asignificant negative correlation betweenherbaceous cover of native and exotic species,as well as the lack of a significant relationship

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between woody cover and herbaceous richness(Sax 2002a). Thus, at least for thesecommunities in central Chile, it appears thatcompetition for light and nutrients betweennative and exotic herbs may be operating andaffecting their abundance, and that nativewoody species may be of minor importance instructuring these systems (Sax 2002a).

Regarding exotic tree plantations, largedifferences in species diversity andvegetational structure have been found betweennative forests and neighboring exoticPseudotsuga menziesii plantations (Frank &Finckh 1997). P. menziesii plantations areextremely poor in native plants, a pattern thatwas also described for plantations of the exoticPinus radiata (von Buch & Osorio 1987).Exotic P. menziesii and P. radiata displacenative epiphytes and vines because of themonostratified structure of the plantations,which hold only tree and herbaceous cover(von Buch & Osorio 1987, Frank & Finckh1997). However, these results should beinterpreted with caution because the observeddifferences between forest plantations andnative forests may be associated to forestmanagement strategies and not to thecompetitive ability of the respective species(Sax 2002b).

Similarly, Atriplex canescens, A halimus andA. nummularia in the arid region of centralChile, cause a reduction in richness and cover ofthe herbaceous stratum by reducing the amountof light reaching the soil (Torres 1999).However, when these shrubs are pruned andmanaged, they can enhance herbaceous richnessand vegetative cover due to a reduction in waterstress by facilitating mist condensation, andcontributing with an adequate concentration oforganic matter in leaf litter (Lailhacar et al.19892, Lailhacar & Torres 2002).

On the other hand, Matthei (1995) reportedthat an important number of exotic herbs havetoxic compounds. However, no evidence existsthat these toxins actually have negative effectson the survival or abundance of native or ofexotic plants. Despite this, Atriplexnummularia, a species that was introducedfrom Australia, was shown to have allelopathiceffects, inhibiting annual species in naturalgrasslands in arid northern Chile (Aliaga 1982).Further, phytotoxic chemicals that leach from

the leaves and litter of Eucalyptus species candirectly inhibit germination and delay seedlinggrowth of grasses in North America (del Moral& Muller 1970). But their effects are notknown for native vegetation in Chile.

In sum, for mediterranean-type ecosystemsof Chile,the available evidence suggests thatcompetitive ability of naturalized plants may beimportant in determining invasiveness at a localscale.

Ecophysiological tolerance

The invasiveness of exotic species is associatedwith wide tolerances to requirements forgermination (Reichard & Hamilton 1997). Inthis respect, investigations on Chileanmediterranean-type ecosystems are scarce andhave been carried out mainly with managedinvasive annuals. For instance, most invasiveannuals that are used for the management ofgrasslands in central Chile (e.g. , Avenabarbata, Hordeum murinum, Vulpia bromoides)are able to germinate under a wide range oftemperatures (Johnston et al. 1989, 1994,Olivares et al. 1990), and it is known that thegermination of Erodium invasive species ishighly tolerant to cold and dry conditions(Olivares et al. 1999). For example, thegermination in Erodium species starts at 1 °Cwhen water availability is high. Similarly,Vidiella & Armesto (1989) and Gutiérrez(1993) recorded in xeric environments of north-central Chile that naturalized ephemerals havegreater tolerance to water stress thangerminating native ephemerals, which in partmay explain the persistence of naturalizedannuals in those environments.

Regarding seed dormancy, it is known thatthe response of naturalized plants in centralChile is diverse (Figueroa & Jaksic 2004). Themajor naturalized species in central Chileshow physiological dormancy that can bebroken by chilling (e.g., Chenopodium album,Plantago lanceolata) and elevated temperature(e.g., Avena fatua , Poa annua , Stellariamedia). A less numerous group of naturalizedannuals shows physical dormancy (e.g. ,Erodium spp, Ipomoea purpurea). However,the number of naturalized species that doesnot show dormancy at the time of seeddispersal (e .g. , Cardus nutans , Vulpiabromoides) is not negligible. On the otherhand, published results indicate that thenaturalized annuals in central Chile cangerminate on a wide temperature range, andthat they are highly resistant to cold and dryconditions (Figueroa & Jaksic 2004).

2 LAILHACAR S, A CARRASCO, MA SADZAWKA & GCASTELLARO (1989) Effet de l’arbuste fourrager Atri-plex repanda Phil. sur fertilité du sol et sur la strate herba-ce é associée. XVI Congrès International de Herbages,Nice, France.


There are few experimental studies on growthand ecophysiology of naturalized plants in centralChile. Most have focused on unnaturalizedwoody exotic (Ovalle et al. 1996, Arredondo etal. 1998, Aronson et al. 2002) and annual herbsused in productive prairies (e.g., Lailhacar &Aylwin 1988, Torres 1999, Del Pozo et al.2002a,b). For example, invasive annual herbs arehighly tolerant to soils with low nutrientconcentrations (Squeo et al. 1994, Holmgren et al.2000a) but have low tolerances to shading(Lailhacar et al. 19991, Torres 1999). EvenMedicago polymorpha, which was successfullyintroduced from Europe, recruits on a widevariety of regions, soils, and habitats of Chile(Rihan 1988 in Del Pozo et al. 2002a,b). Thevegetative growth of this species increases withincreasing precipitation (Lailhacar et al. 19991),temperature (Del Pozo et al. 2002b), soil surfacepH (Torres 1999) and, contrary to many invasivespecies in Chile, has a high tolerance to shading(Lailhacar & Aylwin 1988, Torres 1999). Also,for Malvia nicaensis it has been shown thatgrowth increases in soils with high Nitrogencontent (Lailhacar & Aylwin 1988, Torres 1999).

In sum, the few available data for Chileanmediterranean-type ecosystems suggest that ingeneral naturalized annuals are tolerant togrowing in poor soil conditions but have a lowtolerance to shading. However, the naturalizedannual M. sativa stands as a remarkableexception, that additionally shows a significantecotypic differentiation in phenology andwinter “vigor”, along environmental gradientsin central Chile (Del Pozo et al. 2000, 2002a,b).

HISTORICAL PROCESSES

In addition to the drivers identified in Fig. 1,history seems to play a significant role in theintroduction success and spread of exoticspecies because it is possible that priorityeffects (e.g. , Drake et al . 1993) ormicroevolutionary changes leading to increasedinvasiveness may be operating. In this context,the history of the invasion process could be ofparamount importance for understandingcurrent and future trends in species invasions.Below we provide a summary of the history ofplant invasions in Chile and show thatwidespread exotic species were introducedearlier than more localized species.

Record of arrival of exotic plants

The Spanish conquest of Chile in the 16th

century marked the first deliberate

introductions of several Old World plant andanimal species into central Chile (Montenegroet al. 1991, Jaksic 1998). However, the firstscientific descriptions and collections of theChilean flora date from the 18th century, andwere carried out by naturalists interested in thedescription of the native flora, not on theintroduced elements. The emphasis on thediscovery of native plants with agricultural andmedicinal uses prevailed as the criterion ofcollection in the expeditions led by Louis E.Feuillée between 1708 and 1710 (Philippi1867) and those of Hipólito Ruiz and José A.Pavón between 1782 and 1783 (Ruiz & Pavón1798-1802). It is estimated that towards the endof the 18th century, numerous exotic plantswere already naturalized in Chile, as is the caseof Cardamine hirsuta, Medicago polymorpha,Spartium junceum and Bromus hordeaceus(Castro unpublished data).

More systematic efforts to expandknowledge on the diversity of plants startedwith the arrival of the French naturalist ClaudioGay in 1828 (Reiche 1901, Muñoz-Schick1991). Gay (1845-1854) performed a completefloristic inventory of Chile as part of his“Physical and political history of Chile,” whichincluded 146 naturalized plants. Philippi (1875)reported the presence of 180 naturalized plants,which he classified into four groups: (1)Marine coastal plants (e.g. , Cotulacoronopifolia); (2) aquatic or freshwater plants(e.g. , Rorippa nasturtium-aquaticum ,Callitriche terrestris); (3) accidentallyintroduced weeds (e.g. , Fumaria media ,Sisymbrium officinale, Erodium cicutarium, E.moschatum, E. malacoides, E. botrys); and (4)naturalized cultivated plants (e.g., Ranunculusrepens , Brassica nigra, Mentha piperita ,Holcus lanatus).

At the turn of the 20th century, Karl Reiche(1896-1911) published “Flora of Chile,”incorporating numerous plants that werenaturalized in central Chile, such as Cotulaaustralis, Chrysanthemum segetum and Lactucaserriola. Later, Baeza (1928)3 became one ofthe first botanists in Chile to show a specialinterest for naturalized species (which hereferred to as invasive species). This authorcalled attention to the growing importance ofthe naturalized flora in the country. In addition,Espinosa (1929) documented the presence ofLinaria vulgaris , Agrostemma githago ,Hypericum perforatum, Arctium minus, Cirsium

3 BAEZA VM (1928) Contribución al conocimiento de laflora advena de Chile: Apuntes Docentes. Instituto Peda-gógico, Universidad de Chile, Santiago, Chile. 33 pp.

474 FIGUEROA ET AL.

Fig. 1: Representation of interactions among three general causes of exotic plant invasions. Theexotic species pool is determined by exotic plant availability established above the ground and inthe seed bank of the soil. The native community attributes are represented by plant richness anddisturbance regime. Finally, species attributes determine exotic plant traits associated with theirsuccessful naturalization and further spread.Representación de las interacciones entre tres causas generales de la invasión de plantas exóticas. El conjunto de especiesexóticas es definido por la disponibilidad de plantas exóticas en la vegetación y en el banco de semillas del suelo. Losatributos de la comunidad nativa están representados por la riqueza de plantas y el régimen de perturbaciones. Finalmente,los atributos de las especies quedan definidos por los rasgos de las plantas exóticas asociados con su naturalización exitosay posterior expansión.

Exo

tic s

peci

es a

ttri

bute

s (p

hysi

olog

y, li

fe h

isto

ry) C

omm

unity attributes (richness, disturbances)

Exotic species pool


arvense and Pulchea absinthioides, as weeds incultivated lands in the central zone of Chile.

Later , Gunckel (1935) recorded thenaturalization of Lupinus arboreus and Telinemonspessulana, two Papilionaceae speciesinitially cultivated in the Botanical Garden atSantiago and which then spread throughoutcentral Chile. Garaventa (1937) recognizedRubus ulmifol ius , Acacia dealbata , A.melanoaxylon, Nicotiana glauca and Salixbabilonica as exotic plants that colonized bareground. Further, Drathen (1937) mentionedRubus ulmifolius and Ulex europaeus asspecies capable of excluding Alstroemeriaaurantiaca from established sites. Acevedo(1939) catalogued 13 species as exotic grassesin Chile (e.g., Agrostis verticillata, Bromusrigidus , Paspalum urvi l le i , Festucamegalura), indicating sites of collection, andaccessioning them in the Herbarium of theMuseo Nacional de Historia Natural (Muñoz-Schick et al. 1981). Navas (1973, 1976, 1979)undertook a complete f lorist ic s tudy ofSantiago’s basin, considering 21 collectionsites situated in a 100 x 40 km area, between33°12’ and 33°56’ S. She recorded anaturalized flora of 60 species among 229native species, but these figures should berevised in light of subsequent changes innomenclature.

The most recent and complete registry ofthe vascular flora of Chile is the “Catálogode la Flora Vascular de Chile” (Marticorena& Quezada 1985, 1987). A flora composedof 6 ,058 taxa including subspecies arecatalogued here, of which 582 correspond tonaturalized species. More recently, Matthei(1995) recorded 690 exotic plant speciesthat grow as weeds in croplands, causingimportant economic damages in productivelands . Us ing Mat the i (1995) a s the i rprincipal source of information, togetherwith the data base of the Chilean flora andsome local floristic studies (Henríquez et al.1995, Marticorena et al. 1998), Arroyo et al.(2000) p rov ided a ca ta logue o f 707naturalized plant species (12 % of the totalChilean flora). According to Matthei (1995)and Arroyo et al. (2000), the central regionsof Ch i l e ho ld c lose to 60 % of thenaturalized flora, thus constituting one ofthe most invaded areas of the country. Incentral Chile, the number of naturalizedspecies represents approximately 18 % ofthe flora that has been described for thisregion (Arroyo & Cavieres 1997).

In summary, the first exotic species wereintentionally introduced into the country, and it

seems that they have spread completelyuncontrolled. Thus, the proportion of exoticplants in the total flora of Chile will likelyincrease with more monitoring efforts.

Biogeographic origin of exotic plants

With respect to the origin of the exotic speciesin central Chile, ca. 70 % came from Eurasianand northern parts of Africa (Arroyo et al.2000). Another important source of exotic plantspecies is the rest of South and North America,especially from the subtropical regions, which intotal contribute 12 % of the exotic flora.Tropical regions contribute 8.7 %, while othersources such as South Africa, temperate regionsof the Northern Hemisphere, and Australasia,have each contributed less than 2.5 % of theexotic flora in central Chile. The high proportionof Eurasian-origin flora is remarkable (Fig. 2).This major biogeographical feature of theintroduced flora of central Chile is concordantwith the flora introduced to all regions ofmediterranean climate in the world (Groves1991), but is not necessarily concordant withothers climatic regions (Guillerm 1992). Thehigher percentage of Eurasian species in theexotic flora of central Chile may be due toseveral attributes: (1) Eurasian species possestraits associated to invasiveness, which allowedthem to quickly spread in mediterranean-typeecosystems in Chile during the last 450 years,(2) the historical use of land in central Chilemay have allowed for a higher invasibility oflocal communities, and (3) in central Chile,Eurasian plants presented higher arrival ratesand larger species-pool than plants of otherorigins, thus native communities have been incontact with a higher number of Eurasianexotics. This interesting problem will be dealtwith in the following section.

Propagation and spread exotic plants

In the beginning, the introduction of exoticplants was promoted enthusiastically by diversegovernmental agencies. Exotic plants wereimported through exchange programs withEuropean institutions with the purpose of usingthem in teaching, botanical medicine, and inthe search for new crop plants (Philippi 1881).Toward this aim, the grounds of the QuintaNormal de Agricultura, were set aside forteaching and research in agriculture, and usedas a testing site. This way, numerousintroduced plants were cultivated for theirstudy and propagation (Mostny-Glaser &Niemeyer-Fernández 1983). Philippi (1881,

476 FIGUEROA ET AL.

1884) catalogued approximately 2000 exoticplants that were being cultivated in thebotanical gardens of the Quinta Normal deAgricultura, although in time it came to holdmore than 3,000 species (Marticorena &Rodríguez 1995). A total of 43 speciesapparently “escaped” accidentally from thiscultivation site, among them Eschscholziacalifornica, Veronica verna and Centaureajacea, which are now naturalized and widelydistributed in central Chile (Matthei 1995).

On the other hand, the exact date ofintroduction as well as the number ofintroduction events are difficult to establish,given that many naturalized species have beenintroduced involuntarily in the country (Arroyoet al. 1995). Nevertheless, from 1854 onwards,a sustained increment occurred in the numberof exotic plants introduced to Chile, resultingin an annual rate of 2-3 new naturalized species(Matthei 1995), which is lower than the figures(four to six species per year) computed forother mediterranean-type ecosystem (Groves1991). Using the date in which each exoticspecies was first recorded and/or collected incontinental Chile, Arroyo et al. (2000) foundthat the date of introduction is related with thedegree of distribution of the species throughout

the country. Recently, Castro et al. (20034)showed that the extent of the geographicdistribution of naturalized species in Chileincreases with time since introduction into thecountry (Fig. 3), demonstrating that arrival timeof propagules is of great relevance tounderstand the present-day spread of exoticplants (see also Pysek et al . 2003),independently of their biogeographic origin.The exotic flora of European origin has beenexposed, for a long time, to a selectiveenvironment of anthropogenic thrust. Di Castri(1989) proposed that this European speciespool is highly invasive, because it has evolvedin response to drastic climatic and otherenvironmental changes, including intensiveagriculture. Castro et al. (20034) postulated thatthis hypothesis is not supported in Chile,because the exotic flora here originated fromdifferent regions and does not show differencesin their regional spread within the country.Thus, an alternative explanation for the amplespread of Eurasian flora in mediterraneanregions, and in Chile in particular, may beassociated to the high historical availability ofplants of this origin, due to an asymmetricalexchange in imports and exports to and fromthat region (Castro et al. 20034).

ECOSYSTEM IMPACT OF INVASIVE PLANTS IN

CENTRAL CHILE

Plant naturalization may alter ecosystems incentral Chile. An important ecosystem processthat could be altered by exotic legumes is thenitrogen fixation rate. Although publishedinformation does not exist for central Chile, thenitrogen-fixing annual legumes Medicagopolymorpha (Del Pozo et al. 2000), Trifoliumspp. and the shrubs Cytisus scoparius and Ulexeuropaeus may alter the abundance anddistribution of the native flora by enhancing thenitrogen contents of the soil. Ulex europaeus,which was introduced to Chile during the 19th

century (Philippi 1875), is a species that inhibitsthe regeneration of woody species in disturbednative forests. In contrast, Carduus nutans, aspecies native from central Chile, was shown toinhibit nitrogen fixation by the legume Trifolium

Fig. 2: Biogeographic origin of the exotic plantspecies in central Chile. Percentages of eachorigin are shown.Origen biogeográficos de las especies de plantas exóticas enChile central. Se muestran los porcentajes de cada origen.

Others7%

Australasian3%

Tropical America9%

SubtropicalAmerica

12%

Eurasian andnorthern of Africa

69%

4 CASTRO SA, FIGUEROA JA, MUÑOZ-SCHICK M &JAKSIC FM. 2003. Importancia de la fecha de introduc-ción como determinante de la distribución geográfica deplantas naturalizadas en Chile continental. XLVI ReuniónAnual de la Sociedad de Biología de Chile. XII ReuniónAnual de la Sociedad de Ecología de Chile, Puyehue. Bio-logical Research 38: R-21.


repens in Australia (Wardle et al. 1994).However, no studies have been conducted fordetermine if similar effects of C. nutans occuramong native legumes of central Chile.

Evidence also exists of naturalized speciesaltering other ecosystem-level processes, suchas the rate of methane release in wetlands (e.g.,Lythyrum salicaria), soil chemistry, andnutrient cycling in forests (e.g., Pseudotsugamenziesii) (Frank & Finckh 1997), andmodifications of the water cycle by changes ofevapotranspiration rates (Kremer & Running1996). In this respect, annual exotics such asAvena spp., Bromus spp. and Vulpia spp.,which have replaced native perennials speciesin mediterranean-type ecosystems in Chile, useless of the deep-water reserves, because theyhave shallower roots. As a consequence, thesespecies may have produced a significantdecrease in evapotranspiration in the matorralof central Chile. On the other hand, exoticforest plantations may have altered thehydrology (Canadell et al. 1996), annualevapotranspiration, and microclimate (Kremer& Running 1996) in large areas of the CoastalRange of central Chile (Lara & Veblen 1993).

There are species that could alter thefrequency and rates of disturbances in centralChile. For instance, Senecio mikanoides, a

species naturalized in Chile that in Californiaforms dikes that contain the flow of waterdecomposing organic matter; Cynodondactylon, which in Arizona stabilizes thesediments in streams, and Arundo donax, whichon the coast of California enhances thedeposition of sediments in rivers (see Dukes &Mooney in this special issue). Additionally, thereplacement of native forests by exotic forestplantations may have altered the frequency offires in the last 40 years (Montenegro et al.2002). Here, exotic plantations deserve aspecific mention, because Chile holds the mostextensive Pinus radiata plantations of theentire world (Lewis and Ferguson 1993).Approximately two million hectares areoccupied by species of Pinus spp. andEucalyptus spp., constituting a serious threatfor the maintenance of native biodiversity(Armesto et al. 1998) and thus likely candidatesfor strong ecosystem disruptions. These specieswere introduced for commercial purposes, andthus may not be considered as naturalized(Arroyo et al. 2000) or invasive (Kruger et al.1989). However, these plantations should bestudied, specially considering that the treesinvolved are likely altering large-scale spatialand temporal processes that native ecosystemshad never experienced before (Armesto et al.

Fig. 3: Mean number of administrative regions occupied by naturalized plants in Chile according tothe introduction year of 428 species (bars represent ± SD). ANOVA shows a significant differenceamong years (F1,3 = 12.1; P < 0.001).Media aritmética de regiones administrativas que son ocupadas por plantas naturalizadas en Chile, de acuerdo al año deintroducción de 428 especies (las barras representan ± DE). ANDEVA muestra una diferencia significativa entre años(F1,3 = 12,1; P < 0,001).

Introduction year

Num

ber

of a

dmin

istr

ativ

ere

gion

s7

6

5

4

3

2

1

01800-1849 1850-1899 1900-1949 1950-2000

478 FIGUEROA ET AL.

1998). Additionally, there is evidence of Pinusradiata reproducing and regenerating in nativeforest fragments (Bustamante et al. 2003).

CONCLUSIONS

Despite the fact that species naturalizations incentral Chile are cause of concern because oftheir widespread occurrence and large speciesnumbers, there are important gaps in ourknowledge of this phenomenon in Chile(Vázquez & Aragón 2002). In the last fewyears, the priority has been to determineregional patterns of naturalized plants andavailability at regional (Arroyo et al. 2000,Castro et al. 20034) and landscape scales(Pauchard & Alaback 2004), taxonomic andsystematic characteristics of introduced species(Matthei 1995), ecosystem regulation models ofvegetation (Holmgren 2002), and microscale-level patterns (Sax 2002a). Betterunderstanding of plant naturalizations could bereached by filling important gaps on the threemajor drivers of invasion (Fig.1), specially onthe historical processes and the ecosystemimpacts of exotic species.

For instance, in relation to the currentavailability of naturalized species in centralChile, which reaches up to 50 % of total florain evergreen matorral and Acacia espinal, it isimportant to answer the following unresolvedquestions. Is it possible to decrease the size ofthe exotic propagule pool to decrease invasionlikelihood in the most susceptiblecommunities? Is it possible to calculate thenaturalization rate assuming that we know theapproximate availability of exotic plants fromexogenous sources? In sum, Is the temporal andspatial pattern of exotic plant naturalizationdetermined and predictable by exotic propaguleavailability?

On the other hand, studies on the localcommunities and habitats invaded in Chile haveintensified during the last few years (Holmgrenet al. 2000a, Arroyo et al. 2000, Pauchard &Alaback 2004). However, further large-scalestudies are urgently required in order to providevaluable information to improve the presentnetwork of protected areas, and to identify sitesof high priority for the conservation of nativebiodiversity, which is threatened by exoticspecies (Pauchard & Alaback 2004). Conceptsdeveloped in the field of landscape ecology aretools that have been used successfully in thedevelopment of an ecological theory of plantinvasions (Rejmánek 1999). Also,metapopulation concepts and models could be

of great utility for explaining the persistence, atthe local and landscape scales, of abundant andrare exotic populations or the susceptibility ofdisturbed local habitats to increased propaguleavailabili ty and immigration of exotics(Marquet 2002).

With regard to species traits linked toinvasiveness, this is one of the invasionphenomena less well developed in Chile. Infact, it has practically been ignored, with theexception of the reportedly annual life historyof herbs. Further, genetic molecular tools couldbe of great utility for determining rates ofmutation, population genetic variability, andrates of dispersal (Novak & Mack 2001, Sakaiet al. 2001).

Interestingly, historical analyses of thepresence of exotic plants could help explainmany of the present-day regional distributionalpatterns of the naturalized flora in central Chile(Castro et al. 20034). In the same way, questionsof similar concern are still unresolved. Can wesay anything about the future spread of recentlynaturalized species, using our knowledge of thenaturalization history of exotic species? In short,How predictable is the process of invasion byexotic plants?

Finally, perhaps one of the areas that hasprovided the best theoretical and practical resultswith direct application to the management ofundesired species, has been the identification ofkey invading species that alter ecosystem-levelprocesses and mechanisms (Glyphis et al. 1981,Wheeler et al. 1987, Vitousek & Walker 1989,Gordon 1998, D’Antonio et al. 2001, Dukes &Mooney this special issue). However, we knowvery little about the impacts that widespreadnaturalized plants in Chile (e.g., Erodium spp.,Ulex europaeus, Pinus radiata) have on ecosystemfunction. This represents an open and urgent areafor research of plant invasions in the country.

The study of plant invasions is relevant in thefields of conservation biology, resourcemanagement, global change, and ecological,ecosystem, and evolutionary theory (Hobbs2000, Mack et al. 2000, Rejmánek 2000, Sakaiet al. 2001, Pysek et al. 2003). Notwithstandingrecent advances, the systematic study of plantinvasions in Chile lags far behind what it shouldbe (Vázquez & Aragón 2002). We call for an all-out effort to understand the impacts of invasiveexotic species in Chilean ecosystems.

ACKNOWLEDGMENTS

We thanks A. Pauchard and four anonymousreviewers whose comments on this article


improved it substantially. This study wasfunded by Fondecyt-Fondap 1501-0001. J.AFigueroa is supported by grants from the AWMellon Foundation and the Center forAdvanced Studies in Ecology & Biodiversity,Pontificia Universidad Católica de Chile. SACastro is supported by grants from the AWMellon Foundation. This is a contribution toresearch program of Fundación Entorno.

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Exotic plant invasions to the mediterranean region of