VOLUMEN 42 (2) • DICIEMBRE 2012

REVISTA DE LA SOCIEDAD ESPAÑOLA PARA EL ESTUDIO DE LOS PASTOS

Grazing Systems and Biodiversity in Latin American Areas: Colombia, Chile and Mexico Coordinated by

Sergio Guevara Sada and Javier Laborde

Cover photography credits: Gerardo Sánchez Vigil Mariano Guevara Moreno-Casasola Adi E. Lazos R.

VOLUMEN 42 (2) • DICIEMBRE 2012

To Lucina Hernández García (1960-2013), enthusiastic woman and researcher on environmental history of livestock in Mexico.

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GRAZING SYSTEMS AND BIODIVERSITY IN LATIN AMERICAN AREAS: COLOMBIA, CHILE AND MEXICO

Coordinated by

Sergio Guevara Sada and Javier Laborde

REVISTA DE LA SOCIEDAD ESPAÑOLA PARA EL ESTUDIO DE LOS PASTOS Bases de datos: http://polired.upm.es/index.php/pastos (España), AGRIS (Italia), CAB Abstracts (Reino Unido), CABI Full Text (Reino Unido), Catálogo LATINDEX (México), DIALNET (España), ICYT Ciencia y Tecnología (España)

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CONTENTS Page 1.- INTRODUCTION, ACKNOWLEDGEMENTS AND CONTRIBUTORS Introduction

S. GUEVARA S.................................................................................................... 125 Acknowledgements.............................................................................................. 131

List of contributors............................................................................................... 133 2.- CHAPTER 1. BIODIVERSITY

Flora of the Mediterranean Basin in the Chilean espinales: Evidence of colonization.

I. MARTÍN-FORÉS, M. A. CASADO, I. CASTRO, C. OVALLE, A. DEL POZO, B. ACOSTA-GALLO, L. SÁNCHEZ-JARDÓN AND J. MANUEL DE MIGUEL.............................................................................................................. 137 Historical, biogeographical and ecological factors explain the success of some native dung beetles after the introduction of cattle in Mexico.

M. E. FAVILA...................................................................................................... 161 3.- CHAPTER 2. LANDSCAPE

From tropical wetlands to pastures on the coast of the Gulf of Mexico.

P. MORENO-CASASOLA, H. LÓPEZ ROSAS AND K. RODRÍGUEZ MEDINA.............................................................................................................. 185 The mesoamerican rain forest environmental history. Livestock and landscape biodiversity at Los Tuxtlas, Mexico.

S. GUEVARA S. AND J. LABORDE.................................................................. 219 4.- CHAPTER 3. ENVIRONMENTAL HISTORY

Livestock farming in the Saquencipá Valley, New Kingdom of Granada, Colombia, in the 16th and 17th centuries.

K. G. MORA PACHECO..................................................................................... 251

The impact of raising cattle in the Totonacapan Region of Mexico: Historical development and approaches for sustainable cattle ranching.

B. ORTIZ ESPEJEL AND R. JIMÉNEZ MARCE.............................................. 273

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5.- FINAL REMARKS

S. GUEVARA S. .................................................................................................. 301

6.- IN MEMORIAM

Gaspar González y González, socio de honor y fundador de la SEEP.

JESÚS TREVIÑO................................................................................................ 307 7.-INSTRUCCIONES PARA AUTORES

Instrucciones para los autores de la Revista Pastos.............................................. 317

1 Introduction, Acknowledgments and Contributors

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INTRODUCTION Raising livestock is the most extensive productive system in the tropics and subtropics. The domestication of animals arose almost at the same time as the domestication of plants in different parts of the world. Both types of production created two large guilds, that of the crop farmers and that of the ranchers, who throughout history have battled over land use. This confrontation has produced different results over time and in different parts of the world, producing the environmental and cultural characteristics that are particular to each region.

In the Americas, we see the most recent episode in the crops vs. livestock battle. Throughout these enormous and diverse continents of mainly crop-oriented heritage, livestock burst onto the scene in the 16th century when the Europeans introduced domesticated animals large and small, changing a landscape that had been largely defined by the crop raising vernacular, and becoming the most powerful tool of European colonization.

Owing to its extent and profound effect on biological and cultural diversity, the ecology of raising livestock is essential to understanding the current landscape if we are to aspire to balanced and sustainable management of the soil, biodiversity and the natural resources of the Americas. We know little about the interaction between livestock — cattle, donkeys, horses, pigs, goats, fowl and bees— and local flora and fauna, or of the effect that environmental conditions have on the animals. The scarcity and fragmented nature of our knowledge mythifies the ecological impact of livestock and limits our possibilities and alternatives for their rational management. To scientists, raising livestock causes a monumental disturbance of ecosystems and landscapes that entails the disappearance of native species, facilitates the invasion of exotic species and causes irreversible changes in the physical structure and fertility of the soil.

From this perspective, the scientists reaction is extreme, they overlook the biodiversity associated with the cattle pastures, ignore their role in the structure and functioning of the landscape and the possibility of understanding certain mechanisms and ecological processes that facilitate the movement of the flora and fauna that maintain the diversity of natural systems

When speaking about livestock, we are referring to the diverse species of introduced herbivores: cattle, pigs, goats, sheep, donkeys, chickens and bees. Each has its own foraging habits and its impact depends on the ecogeographic region where it occurs, though it can generally be stated that cattle ranching is the most widespread and common livestock activity in the Americas and the Caribbean.

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The ecology and behavior of cattle in Europe, Asia and Africa have been under study for some time now, and the results are useful for understanding cattle ranching in the Americas. However, the huge diversity of American ecosystems in terms of their flora and fauna, and the short time that has elapsed since the introduction of cattle, compared to the long history of domestication on Europe, Asia and Africa, make for quite a different story.

The European colonists were cattle ranchers, as were their ancestors, who practiced mixed agriculture and herding from 4500 years before the discovery of America. They brought cattle to the Americas for the first time in the Antilles in 1512, to Mexico in 1520, to the Andes region in 1530 and to Florida in 1565. By the end of the 16th century cattle had spread as far west as New Mexico and by 1769, to upper California.

The Iberian cattle (Bos taurus) adapted to the American environment quickly, both on the arid and semiarid high plains, and in the humid lowlands, as evidenced by the fact that the herds doubled in size at a much higher rate than they did in Europe. From the 16th to the 19th centuries, Bos taurus —a fast, lean and average-sized beast— rapidly occupied each ecosystem, in contrast to the more robust British and French cattle, which progressed much more slowly. From the time of their introduction in the eastern United States, they only reached the center of the nation in the 19th century. The capacity of cattle to transform cellulose into meat, milk, fiber and leather gave them enormous efficiency and an aptitude for changing the environment, even on a continental level. On the arrival of the Spanish, the Mesoamerican landscape was molded by extensive and intensive crop growing activities. Permanent and shifting cultivation occupied large tracts of flat land, hillsides and ravines. Because of colonization, the indigenous population decreased and relocated, the best lands were abandoned, monocultures proliferated and herds of cattle spread, changing the landscapes, leaving only a few remnants of the natural ecosystems. Livestock became the main agent of transformation of nature in the Americas and some authors believe it was the determining factor in European colonization.

When livestock was introduced, some animals were left to roam free in the forests and rainforests from the last third of the 16th century, and continued to do so until the end of the 19th century. It was left to move freely on the islands and the mainland, and in particular pigs and cows adapted to the savannas, scrub, and the sparse and dense woodlands of warm, moist and dry temperate climates.

It is surprising that, over this period of 500 years, the domesticated European animals that roamed freely caused no severe damage to the original structure of the vegetation, nor did they cause any considerable changes in the species composition of ecosystems and natural formations. It seems that the number of head of cattle and their behavior

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adapted to the prevailing environmental conditions and to the carrying capacity of each of the natural systems they occupied.

This type of feral cattle still exists in parts of Mexico and the Caribbean, where for various reasons it continues to inhabit natural systems that are reasonably well preserved. One explanation of why these ecosystems remained in such good ecological conditions is that these large herbivores did not have to compete with or displace other species in the natural American ecosystems. Large herbivores disappeared from the continent en masse, with the exception of bison, moose, caribou and some deer in North America, and llamas and vicuñas in South America during the Pleistocene, leaving a void. Livestock filled this gap in natural grasslands, scrubland and dense forests in both dry and humid regions, fulfilling the task of dispersing fruit and seeds, preying on seedlings, reducing plant biomass and recycling soil nutrients. One might suppose that they contributed to maintaining local biodiversity, favoring those species adapted to the presence of herbivores for their dissemination and establishment.

The disappearance of large herbivores has been documented for arid and semiarid regions of the Americas. There, the presence of cattle, horses and donkeys has taken over the function of the extinct herbivores, rescuing tree species that might otherwise have disappeared had large livestock not arrived on the scene.

Calculations of the number of native herbivores that were present before the Pleistocene indicate there was an average of 21 animals per km2, with a variation of 15 to 50 animals per km2, each weighing approximately 450 kg. This would mean there was an average of five hectares per animal, with a range of two to seven hectares, suggesting a large carrying capacity, which would explain why the presence of livestock did not drastically change natural habitats in the Americas.

Unfortunately, we do not have similar calculations for the humid tropics, though everything seems to indicate that the carrying capacity of the forests was high. Recently, the rapid decline of the medium-sized to large wildlife species most affected and the decrease in their populations in the tropical rainforests of southern Veracruz over the past 25 years has been documented. This defaunation included wild herbivore species, the disappearance of which could change the physiognomy and species composition of the rainforest. From our point of view, the greatest decrease in herbivorous fauna occurred in the late 19th and early 20th centuries, about 100 years ago, when the feral cattle of Bos taurus, which had roamed freely in the area was removed and replaced by Bos indicus feedlot cattle. The disappearance of Bos taurus doubtless had a negative effect on the rainforest plant populations, which once again were left “widowed”, without their dispersers or primary consumers and carnivore populations, among others.

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This change in the species of cattle was the result of a trend toward intensive production in enclosures and planted pastures. Spanish breeds of B. taurus were removed from natural systems and new breeds of B. indicus introduced. This change induced a massive opening of pastures at the expense of the natural vegetation, and from that time onwards, cattle ranching has meant deforestation. The concentration of high densities of livestock modified the soil and pasture management facilitated the arrival and establishment of grass species associated with livestock from Africa and Asia. Habitats were simplified and an extensive and homogeneous system emerged, where vegetation was cleared to make way for fields and pastures, areas with physical conditions that led to the proliferation of both exotic and other secondary and weed species, which eventually colonized these open areas. In both the dry and humid tropics, clearing for fields has reduced the forest to very small fragments. Huge areas of the tropics are dominated by livestock landscapes within which there are fragments of the original forest that vary in size immersed in the pastures. The forest fragments that remain are on hilltops, very steep slopes, and on rocky terrain or where flooding occurs. Within the pastures a few trees from the original forest have been spared, some form strips along rivers to protect the channel, and some are used as living posts to tend barbed wire, or occur as solitary trees to provide shade for livestock.

This remnant of the forest is worked into livestock management in an incipient way. Over the past four decades, the expansion of pastures has been impressive. In ecological terms deforestation and forest fragmentation is very recent and has happened very quickly. Given the current degree of fragmentation, we do not know if the sections of forests that remain on the ranching landscapes can be conserved, or for how long. Nor do we know for certain which and how many of the forest species, or what kind of ecological processes, can continue to occur in these landscapes. Livestock management in fragmented landscapes must not only contemplate grass and cattle, but also the scattered cover provided by the native trees that are present as isolated trees, as well as the gallery vegetation and the protection of forest edges to facilitate the movement of the fauna, seed dispersal and pollen exchange among plants in dispersed populations.

This can lead to the maintenance of the structure and dynamics of this type of landscape, protecting a number of the species of the original forest in areas dedicated to raising cattle, which we could describe as a tropical dehesa, an agroforestry system that originated in the Mediterranean region where the timber, grazing, livestock and cultivation activities interact beneficially in economic and ecological terms. The importance of implementing this optimal landscape design and its new management rules becomes even more evident when we acknowledge that the entire

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area of dry and rain forest in Mexico, Central and South America and the Caribbean —which there is still in time to conserve in its current state— is now surrounded by fragmented livestock landscapes. In large part, the future success of the conservation of Neotropical forests depends on what we can achieve in the landscapes that surround these remnants, especially with regards to the maintenance and proliferation of the trees in pastures. In this context, cattle as herbivores that are potential fruit and seed dispersers could contribute to maintaining those fragments and the landscape in general, decreasing the isolation of species and their populations. Naturally, it would be necessary to reflect on the most appropriate breed of cattle for this purpose. Knowledge of the ecology and environmental history of livestock will allow us to understand the current American landscape and will open new perspectives for the management of biodiversity in livestock areas. This issue brings together a set original research articles that represent a substantial contribution to our understanding of the adaptation of livestock to American landscapes and ecosystems, and of the impact its management and development has had on biodiversity and on the landscape.

The contributions are organized into three chapters. In the chapter on Biodiversity, Irene Martín-Forés et al. analyze the Mediterranean region in Chile where more than 25% of the flora is not native. This is especially important in the espinales vegetation, agroforestry-pastoral systems that are very similar in their functioning to the Spanish dehesas and are of great ecological and socioeconomic interest. The native/nonnative characteristic of central Chile is compared with that of areas on the Iberian Peninsula, highlighting possible mechanisms (filters) that may have been acting on floristic colonization from the Mediterranean basin toward the Chilean Mediterranean zone. Evidence is provided by Mario Favila for the success of the introduction of livestock. The dung beetles of Mexico —and those of the Americas in general— were able to exploit livestock dung and incorporate it into the nutrient cycles of the tropical and temperate soils. This ability to make use of an exotic resource is explained in the context of the evolutionary, biogeographic and ecological history of these beetles.

In the Landscape chapter, Patricia Moreno-Casasola et al. explain how, from the beginning, wetlands were used for cattle grazing, and they describe the transformations occurring in grazed wetlands that convert them into flooded pastures. The degree of impact depends on the number of head of cattle, the time they are in the wetland, and modifications to hydroperiod and vegetation. The changes in the level of flooding, soil characteristics (organic matter, water retention, bulk density, pH, micro- and macronutrients) and floristic composition, are described, along with how all this affects the environmental services provided by wetlands.

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Sergio Guevara S. and Javier Laborde D. demonstrate that the Mesoamerican rainforest is home to high biological diversity, in spite of its being intensely fragmented and the isolation of the remnants of the rainforest. There, biodiversity is rich because of the good connectivity of the landscape, itself the result of natural events, traditional agricultural practices and, more recently, by cattle raising activities. This historical overview allows for landscape management to conserve the biodiversity and develop sustainable production systems.

In the third chapter on Environmental History, Katherinne Giselle Mora Pacheco challenges the traditionally accepted explanation that environmental problems in the Saquencipá Valley of Colombia originated during the colonial period from a combination of wheat monoculture, deforestation and the introduction and expansion of livestock. She indicates that low rainfall, the influence of dry winds and the presence of clay soils were factors that from pre-Hispanic times made most of the inhabitants prefer to live on the fertile riverbanks. Prior to the Conquest, slash and burn activities in the dry forests, the demand for firewood and the occupation of land that was less fertile or on slopes led to the loss of vegetation in specific areas, and this loss was notable, even before the arrival of the Spanish in the region.

Benjamín Ortiz Espejel and Rogelio Jiménez Marce describe the development of cattle ranching in the Totonacapan, an indigenous region on the Gulf of Mexico, examining the pros and cons of three models: indigenous, peasant and agroindustrial. From their analyses, they extract a proposal to build a model for the sustainable development of raising livestock in this type of region.

In this volume, a notable group of researchers propose a novel approach to the relationship between raising livestock and biodiversity in the Americas. This is a landscape comprised of plant and animal species —both native and those brought from the Mediterranean— where biodiversity has been managed in the American and European ways, and supported by the biological precedent resulting from the disappearance of the great abundance and species richness of large herbivores. This compilation opens a new vista for the investigation of the introduction of livestock to the Americas. Sergio Guevara Sada

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ACKNOWLEDGMENTS We wish to first thank Juan Piñeiro Andión because he, as the Director of PASTOS, the journal of the Spanish Society for the Study of Pastures (Sociedad Española para el Estudio de los Pastos), enthusiastically embraced the project of this special issue for the journal and waited, with infinite patience and great friendship, while it was being prepared. We are grateful to Bianca Delfosse, a member of our team, who did an impeccable job translating and revising the style of the manuscripts, working hard and applying her professional abilities to overcome linguistic challenges that seemed insurmountable. Allison M. Jermain always efficient and capable also translated and revised the manuscripts. Graciela Sánchez-Ríos, a valued member of our research team, compiled the contributions in an organized manner, with diligence and care, and formatted them, playing a key role in the production of the manuscript. Kerenha Hernández, our smiling and ever enthusiastic collaborator and participant in the project, organized the manuscripts and controlled communication with the authors with great tenacity, invariably providing superb design ideas. Our thanks also to Gerardo Sánchez Vigil, a most passionately involved colleague and accomplice, and Mariano Guevara Moreno-Casasola enthusiastic and inspired, both who generously provided the magnificent photographs that illustrate the cover of this issue. The Landscape Ecology project (Ecología del Paisaje) of the Red de Ecología Funcional of the Instituto de Ecología, A.C., provided the infrastructure and funding for the preparation of the manuscripts.

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LIST OF CONTRIBUTORS BELÉN ACOSTA-GALLO Universidad Complutense de Madrid, Departamento de Ecología, Facultad de Biología, España, [email protected] MIGUEL A. CASADO Universidad Complutense de Madrid, Departamento de Ecología, Facultad de Biología, España, [email protected] ISABEL CASTRO Universidad Autónoma de Madrid, Departamento de Ecología, Facultad de Ciencias, España, [email protected] JOSE MANUEL DE MIGUEL Universidad Complutense de Madrid, Departamento de Ecología, Facultad de Biología, España, [email protected] ALEJANDRO DEL POZO Facultad de Ciencias Agrarias, Universidad de Talca, Chile, [email protected] MARIO E. FAVILA Instituto de Ecología, A.C. Red de Ecoetología Carretera antigua a Coatepec 351, El Haya, Xalapa 91070, Veracruz, México, [email protected] SERGIO GUEVARA S. Instituto de Ecología, A.C. Red de Ecología Funcional Carretera antigua a Coatepec 351, El Haya, Xalapa 91070, Veracruz, México, [email protected] ROGELIO JIMENEZ MARCE Universidad Iberomericana, Puebla, Departamento de Ciencias Sociales. Boulevard del Niño Poblano 2901. U. Territorial Atlixcáyotl.CP. 72197 Puebla, Puebla, México, [email protected] JAVIER LABORDE Instituto de Ecología, A.C. Red de Ecología Funcional Carretera antigua a Coatepec 351, El Haya, Xalapa 91070, Veracruz, México, [email protected]

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HUGO LÓPEZ ROSAS Universidad Nacional Autónoma de México, Instituto de Ciencias del Mar y Limnología Estación El Carmen, Cd. del Carmen, Campeche, México, [email protected] IRENE MARTÍN-FORÉS Universidad Complutense de Madrid, Departamento de Ecología, Facultad de Biología, España, [email protected] KATHERINNE GISELLE MORA PACHECO Universidad Nacional de Colombia, Línea de Historia Ambiental IDEA y Departamento de Historia, Bogotá, Colombia, [email protected] PATRICIA MORENO-CASASOLA Instituto de Ecología, A.C. Red de Ecología Funcional Carretera antigua a Coatepec 351, El Haya, Xalapa 91070, Veracruz, México, [email protected] BENJAMÍN ORTIZ ESPEJEL Universidad Iberoamericana, Puebla. Departamento de Ciencias Sociales. Boulevard del Niño Poblano 2901. U. Territorial Atlixcáyotl.CP. 72197 Puebla, Puebla, México, [email protected] CARLOS OVALLE MOLINA. Instituto de Investigaciones Agropecuarias INIA, Centro Regional de Investigación La Platina, Santa Cruz, Chile, [email protected] KARLA RODRÍGUEZ MEDINA Instituto de Ecología, A.C. Red de Ecología Funcional Carretera antigua a Coatepec 351, El Haya, Xalapa 91070, Veracruz, México, [email protected] LAURA SÁNCHEZ-JARDÓN Universidad Complutense de Madrid, Departamento de Ecología, Facultad de Biología, España, [email protected]

2 Chapter 1. Biodiversity

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FLORA OF THE MEDITERRANEAN BASIN IN THE CHILEAN ESPINALES: EVIDENCE OF COLONISATION I. MARTÍN-FORÉS1, M. A. CASADO1*, I. CASTRO2, C. OVALLE3, A. DEL POZO4, B. ACOSTA-GALLO1, L. SÁNCHEZ-JARDÓN1 AND J. M. DE MIGUEL1 1

Departamento de Ecología. Facultad de Biología. Universidad Complutense de Madrid. Madrid (España). 2Departamento de Ecología. Facultad de Ciencias. Universidad Autónoma de Madrid. Madrid (España). 3Instituto de Investigaciones Agropecuarias INIA-La Cruz. La Cruz (Chile). 4Facultad de Ciencias Agrarias. Universidad de Talca. Talca (Chile). *Author for correspondence: M.A. Casado ([email protected]).

SUMMARY In Chile’s Mediterranean region, over 18% of plant species are alien. This is particularly noteworthy in some agrosilvopastoral systems such as the espinales, which are functionally very similar to the Spanish dehesas and are of great ecological and socioeconomic interest. In the present paper we analyse Chile’s non-native flora, considering three scales of analysis: national, regional (the central region, presenting a Mediterranean climate) and at community level (the espinales within the central region). We compare this flora with that recorded in areas of the Iberian Peninsula with similar lithological and geomorphological characteristics, and land use. We discuss possible mechanisms that might have been operating in the floristic colonisation from the Mediterranean Basin to Chile’s Mediterranean region. Key words: Alien plants, biogeography, Chile, life cycle, Spain. INTRODUCTION Historically, the transit of goods, domestic animals and people has favoured the flow of wild organisms around the planet (Lodge et al., 2006), a fact that is often associated with the introduction of cultural systems, which have contributed to generating new environmental and socioeconomic scenarios (Le Houérou, 1981; Hobbs, 1998; Grenon and Batisse, 1989). The current globalisation process is increasing landscape changes and ecosystem disruptions by human disturbance and therefore facilitating Bases de datos: http://polired.upm.es/index.php/pastos (España), AGRIS (Italia), CAB Abstracts (Reino Unido), CABI Full Text (Reino Unido), Catálogo LATINDEX (México), DIALNET (España), ICYT Ciencia y Tecnología (España)

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the transit of organisms (Paskoff and Manríquez, 1999; Rouget et al., 2003; Dukes and Monney, 2004; Schwartz et al., 2006). These ‘assisted dispersals’ enable species to cross biogeographical boundaries that have previously limited their distributions. Species that have been transported from one region to another are defined as alien or exotic to that newly occupied region (Richardson et al., 2000). Most of these species fail to establish self-perpetuating populations, but some of them do succeed and become naturalized (Sax and Brown, 2000). Regardless of the factors enabling establishment, the main consequence of this naturalisation is that alien species significantly contribute to the global floristic (taxonomic and phylogenetic) homogenization of regional floras (Winter et al., 2009). Despite the fact that introduction of species increases diversity at short temporal and small spatial scales, in the medium and long term, interactions with native species can lead to extinctions (Pyšek and Richardson, 2006). The net effect will depend upon the spatial and temporal scales considered and on the balance between naturalisations and extinctions (Sax et al., 2002). Nonetheless, the resulting ecological consequence is the coexistence of native species with exotic ones, quite often in the same community. The origin and composition of these novel communities are of great interest to understand their functioning and possible management. Transcontinental naturalisation in Chile’s flora Mediterranean-type ecosystems around the world offer a great chance to compare and understand the mechanisms determining the success of species introduced into a given region (Kruger et al., 1989; Groves and Di Castri, 1991). The different regions presenting a Mediterranean climate have had different environmental histories associated with the density of human populations as well as the time and intensity of the changes that people have caused in the territory. In the Mediterranean Basin, anthropic modification of the landscape is millenary; however, rates of species extinction and naturalisation are low in comparison with other Mediterranean regions (Greuter, 1994). This fact is explained as a process of co-evolution of plants with people (Di Castri, 1981). Conversely, other Mediterranean areas have undergone a rapid change following successive cultural colonisations, some of these relatively recent, a fact that accounts for the current ecological conditions threatening the biodiversity of these areas (Underwood et al., 2009).

As with other Mediterranean regions, Chile is recognised as a biodiversity hotspot (Ormazabal, 1993), with high levels of regional and national endemism, possibly related with its biogeographic isolation (Myers et al., 2000). Its flora comprises 5364 native taxa, including species and subspecies (Marticorena and Quezada, 1985; Marticorena and Rodriguez, 1995, 2001) and between 552 and 723 alien species, depending on the

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author considered (Arroyo et al., 2000; Castro and Jaksic, 2008). Paradoxically, despite the large amount of alien species present and their early colonisation, Chile has been considered a region that has been less invaded or is in an earlier stage of invasion than other Mediterranean regions of the world (Arroyo et al., 2000; Figueroa et al., 2004; Castro and Jaksic, 2008). The arrival of exotic species to Chile started with the European colonisation in the XVI century (Arroyo et al., 2000; Figueroa et al., 2004), which marked the first deliberate introduction of animals and plants (Montenegro et al., 1991; Jaksic, 1998). The rate of species entry in these early days is unknown, since the initial systematic botanic descriptions of flora date from the XVIII century and were performed by botanists who were more interested in describing the native species than the exotic ones (Gay, 1845-1854; Reiche, 1896-1911). By the end of the XVIII century, numerous exotic species had become naturalised in Chile (Figueroa et al., 2004), such as Cardamine hirsuta L., Medicago polymorpha L., Spartium junceum L. and Bromus hordeaceus L. (Castro et al., 2005). Although this species introduction has not been consistent over time, a rate of two to three species per year is estimated, which is lower than the four to six species recorded for other Mediterranean regions (Groves, 1991; Kloot, 1991, Rejmánek et al., 1991; Wu et al., 2003). Processes and mechanisms in species introduction Changes in land use constitute the main factor determining processes of colonisation and naturalisation of plant species (Le Houérou, 1991; Huston, 1994; Holmgrem et al., 2000). Among the most influential factors, deforestation, fires and particularly agricultural practices have been highlighted (Le Houérou, 1991; Cowling et al., 1996; Williamson, 1996; Hobbs, 1998). With regard to deforestation, although Chile still has one of the biggest areas of temperate forest in South America (Donoso, 1993), much of it has been deforested for pastures or croplands. This process started in the XVI century, although the main boom was during the middle of the XX century, with the expansion and intensification of wheat crops (Echeverría et al., 2006) and the spread of forestry plantations. In relation to fire, unlike other Mediterranean climate areas, fire has not constituted a factor of natural disturbance in Chile (Muñoz and Fuentes, 1989; GómezGonzález and Cavieres, 2009), a fact that accounts of the absence of specific adaptations in native species. Although there is evidence of fires of human origin in earliest settlements in the region, around 14 000 years ago, these were not significant until the arrival of the Spanish (Aronson et al., 1998; Aravena et al., 2003; Villa-Martínez et al., 2003). Subsequently, fires became more frequent and intense, and currently about 5000 ha of native scrubland are burnt each year, the vast majority of these fires being

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intentional (Gómez-González and Cavieres, 2009). It has been suggested that plant communities under novel fire regimes are more susceptible to invasion than those under a natural (historical) fire regime (Trabaud, 1991; D’Antonio, 2000). However, different studies that have analysed the effects of fire upon native and non-native Chilean flora appear to indicate that fire is not a relevant factor with regard to favouring non-native species (Keeley and Johnson, 1977; Holmgrem et al. 2000; Gómez-González et al., 2010). Fire does, however, constitute a notable advantage for the establishment of annual plants, which are poorly represented in Chile’s native flora (Arroyo et al., 1995). The implementation of European agricultural culture in the XVI century leaded to big changes in land uses and landscapes in Chile, the extent of which are yet not well known (Turner et al., 1995). The effects of agriculture have been both direct (ploughing, cropping and grazing) and indirect (fire and deforestation, employed as techniques for preparing the land for agriculture and livestock farming). Livestock was introduced into Chile, perhaps at the same time as the colonisation by Europeans. Other herbivores, however, such as rabbits and hares, were brought more recently, in the XIX century (Jaksic and Soriger, 1981). Several studies have associated the naturalisation of exotic plant species with grazing by both livestock (Holmgren et al., 2000; Pauchard and Alaback, 2004; Del Pozo et al., 2006; HilleRisLambers et al., 2010) and rabbits (Sáiz and Ojeda, 1988; Holmgren et al., 2000; Holmgren, 2002). The effect of grazing on native or non-native species has been characterised using morphofunctional plant traits, revealing differences in their response. For instance, grazing appears to favour some exotic creeping species, such as Erodium cicutarium (L.) L’Hér. and some leguminous species, in detriment to the upright ones, the latter more closely associated with native species (Holmgren et al., 2000). Grazing also favours substitution of native hemicryptophytes by both native and non-native annuals, capable of resisting periods of drought stress as seeds. Many exotic plants were also introduced associated with crops, and became widely distributed as a result of the importance of agriculture in the country (Castro et al., 2005). Crop fields, particularly along their succession stages following abandonment, constitute the ecosystems presenting the highest values for richness and cover of non-native plants in Chile (Figueroa et al., 2011). Since colonisation the introduction process has continued, although with different rates along time. Thus, Aronson et al. (1998) highlight an initial wave of exotic species from 1880 to 1920 associated with transformation of the landscape. Fuentes et al. (2008) recognise an initial phase (19101940) associated with intense development of agriculture (Cariola and Sunkel, 1982), as well as a second phase (1980-2000) related with a sharp increase in the mechanisation of farms and forest plantations at large scale. Matthei (1995) describes a sustained increase

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in the naturalisation of exotic species from 1894 to 1934 associated with wheat imported from other countries.

Although many species were accidentally introduced into Chile (Arroyo et al., 2000), many were taken for agricultural, medicinal, culinary and, more recently, ornamental purposes. Since the arrival of the Spanish, species were introduced associated with hay for livestock fodder and with wool and cereals. Endozoochory likely constitutes the most frequent mechanism of effective seed dispersal. However, during transit from Spain to Chile, exozoochory was probably the most effective means of dispersal, given the difference in time between the transoceanic voyage and the time required for seeds to pass through an animal’s digestive tract (generally less than 1 week; Malo and Suárez, 1997). Europe was not the only centre of introduction of non-native species to Chile. During the Gold Rush, in the middle of the XIX century, there was intense wheat trading with California (Davis, 1894), a fact which mobilised other species, together with grain and straw, in both directions (Le Houérou, 1991; Jiménez et al., 2008), especially from Chile to California. Comparative studies of transcontinental naturalisation Comparison of non-native floras between climatically similar regions constitutes a very useful tool for understanding aspects associated with the species naturalisation process (Pauchard et al., 2004, Hierro et al., 2005). It can help us to understand the effects of changes in the landscape associated with historical or cultural scenarios upon the naturalisation process (Kruger et al., 1989; Aschman, 1991). Among comparative studies of different regions with Mediterranean climates, those between Chile and California have been intensely analysed (e.g. Parsons, 1976; Arroyo et al., 1995; Holmgren et al., 2000; Pauchard et al., 2004; Jiménez et al., 2008). These researches highlight the large number of species common to both regions (386, which is 64% of Chile’s non-native flora; Pauchard et al., 2004), as well as the fact that their communities are undergoing different process of invasion with similar consequences of floristic homogenization (Figueroa et al., 2011). However, to date there have been no comparative studies between Chile and Spain, despite their climatic and geomorphological similarity, the historical relationships that favoured the entry of species into Chile and the large number of species common to both countries. Many of these naturalised species are associated with the espinal, an agroecosystem presenting a management system and structure similar to those of the Spanish dehesa (Ovalle and Avendaño, 1987; Ovalle et al., 1990). However, as these agricultural systems are similar in both countries, we are not fully aware of the mechanisms underlying the arrival of determined species and the subsequent naturalisation and spread thereof.

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The aim of this paper is to analyse the relative significance of the biogeographic origin, lifecycle and representativeness of taxonomic families in Chile’s non-native flora. We considered three scales of analysis: national, regional (the central zone presenting a Mediterranean climate) and community (the espinales within the central zones). In the third case, we also conducted a comparative study with Mediterranean grasslands from the Iberian Peninsula in order to identify the degree of similarity in the floristic composition of communities with comparable ecological and agronomic characteristics. MATERIAL AND METHODS Study area The espinal is an anthropic savannoid formation characterised by dispersed trees of Acacia caven Mol. (the espino) within an herbaceous matrix comprising mainly annual plants of Mediterranean origin (Olivares and Gastó, 1971; Ovalle et al., 2005; del Pozo et al., 2006). It supports a rural population of approximately 350 000 people, as well as the largest Chilean livestock: 800 000 sheep and 250 000 cows. It covers an area of two million hectares in Chile’s central zone, ranging along the Central Valley and the western slopes of the Coastal mountain range (Ovalle et al., 1999). It currently occupies mainly the dryland sectors (Figure 1), from the river Petorca (32° S), bordering on the arid Mediterranean region, to the river Laja (37º S), bordering on the perhumid region (Fuenzalida and Pisano, 1965; Di Castri, 1968; Quintanilla, 1981; Rodríguez et al., 1983). Further north, in the arid and perarid regions, some espinales can be found, preferentially located in valley bottoms (Follman and Matte, 1963; Rodríguez et al., 1983). Their distribution is associated with Mediterranean-climate areas, albeit with very variable annual rainfall, from 160-200 mm at its northern limit and up to 10001200 mm at the southern one. It presents high species diversity (Gulmon, 1977; Solbrig et al., 2002; Del Pozo et al., 2002) and to date, 215 species have been identified only in the Cauquenes region (Ovalle et al., 1987). It originated through changes in land uses after the Spanish conquest; the native sclerophyllous forest was cleared in order to open up land for agriculture and livestock farming, which favoured gradual invasion by the exotic species A. caven (Gulmon, 1977; Armesto and Pickett, 1985; Ovalle et al., 1990), possibly from South America’s Gran Chaco (Holmgren, 2002).

The espinal is an agrosilvopastoral system presenting much similarity with the Spanish dehesas and Portuguese montados. It has traditionally been based upon two models of management: continuous extensive grazing in flatlands, occasionally inundated during winter, and rotation of grazing and cereal cropping in the better drained hillsides (Ovalle et al., 2005). In the latter case, the espino is periodically cut

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down for firewood and charcoal. The land is subsequently ploughed for sowing cereal crops. After one or two years’ harvest, depending upon the fertility of the soil, the land is abandoned and colonised by herbaceous species, while shoots grow from the stump of the espino. In this phase, the land is used for extensive grazing with a low stocking rate of approximately one sheep/ha (Del Pozo et al., 2006). The grazing period prior to the following cropping cycle is variable, from three to 40 years, depending on the fertility of the soil.

FIGURE 1

Location of Chile (in grey) in South America and enlargement of the Central zone. The shaded area represents the main distribution areas of espinal (modified from Ovalle et al., 1999).

Localización de Chile (en gris) dentro de Sudamérica y ampliación de la Zona Central. La región sombreada representa el área de distribución de los espinales (modificado de Ovalle et al., 1999).

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The espinal is currently more degraded than in past times. In the first place, an increasingly greater area of the espinales in the Central Valley is being replaced by intensive irrigation agriculture. Furthermore, many owners have abandoned their traditional farming activities for forest plantations (approximately 80 000 ha/year), mainly of Pinus radiata D. Don or Eucalyptus globulus Labill. Finally, the territory still maintaining functional espinales has usually low fertility and soil erosion, leading to low agricultural production. At present, 40% of the area is occupied by espinales with very little tree cover (