loss of mammalian species from the south american gran ... · loss of mammalian species from the...

REVIEW

Loss of mammalian species from the South American GranChaco: empty savanna syndrome?Maria E. PERIAGO* Instituto Multidisciplinario de Biología Vegetal (IMBIV), Consejo Nacional deInvestigaciones Científicas y Técnicas (CONICET), Facultad de Ciencias Exactas Físicas y Naturales,Universidad Nacional de Córdoba, Casilla de Correo 495, 5000, Córdoba, Argentina and Grupo deInvestigaciones de la Biodiversidad (GiB), Centro Científico y Tecnológico Mendoza (CCT), InstitutoArgentino de Investigaciones de Zonas Áridas (IADIZA), Av. Ruiz Leal s/n Parque General San Martín,CP 5500, Mendoza, Argentina. E-mail: [email protected]ónica CHILLO Grupo de Investigaciones de la Biodiversidad (GiB), Centro Científico y TecnológicoMendoza (CCT), Instituto Argentino de Investigaciones de Zonas Áridas (IADIZA) and ConsejoNacional de Investigaciones sCientíficas y Técnicas (CONICET), Av. Ruiz Leal s/n Parque General SanMartín, CP 5500, Mendoza, Argentina. E-mail: [email protected] A. OJEDA Grupo de Investigaciones de la Biodiversidad (GiB), Centro Científico y TecnológicoMendoza (CCT), Instituto Argentino de Investigaciones de Zonas Áridas (IADIZA) and ConsejoNacional de Investigaciones Científicas y Técnicas (CONICET), Av. Ruiz Leal s/n Parque General SanMartín, CP 5500, Mendoza, Argentina. E-mail: [email protected]

Keywordsdefaunation, ecosystem services, frugivores,habitat loss, herbivores

*Correspondence author.

Submitted: 1 November 2013Returned for revision: 6 January 2014Revision accepted: 9 September 2014Editor: KH

doi:10.1111/mam.12031

ABSTRACT

1. The Gran Chaco in central South America is a major savanna woodland eco-system. Accelerated changes in land use within it have resulted in a complexmatrix of areas with varying capabilities for sustaining wildlife. Furthermore,hunting and habitat loss increasingly threaten the functional diversity ofmammals found there.2. We assess the potential consequences of the loss of large and medium-sizednative mammalian herbivores and frugivores on Chacoan ecosystem functioning,focusing on their role and conservation status in the Argentine Chaco.3. Our review shows that almost 50% of the largest frugivorous mammals presentin the Argentine Chaco are threatened and exhibit declining population trends.Their decline may cause changes in vegetation composition, since almost 53% ofthe Chacoan woody plant species display endozoochory as their seed dispersalmechanism. Moreover, 80% of the largest herbivores are threatened, which mayalso lead to a compositional change in savanna vegetation.4. There is a significant void of information regarding the population statusof native mammals in the Argentine Chaco and the functional roles they play inthe ecosystem, and there are few studies examining the consequences of theirpotential loss.5. We express our concern with the major changes taking place in this subtropicalregion due to significant and rapid habitat transformations and emphasize theimportant role of ecological functionality in restoration and conservation plan-ning in the Gran Chaco.

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Mammal Review ISSN 0305-1838

41Mammal Review 45 (2015) 41–53 © 2014 The Mammal Society and John Wiley & Sons Ltd

INTRODUCTION

The Gran Chaco is one of the main biogeographical regionsin South America and the largest ecoregion after Amazonia(Dinerstein et al. 1995). This savanna woodland ecosystemextends through the present territories of Argentina,Bolivia, Paraguay and south western Brazil, between theParaguay and Paraná rivers and the Andean high plains(Fig. 1). The Gran Chaco is considered a vulnerableecoregion of great importance to conservation at both localand regional scales due to the high levels of endemism andmammalian species richness it harbours (Redford et al.1990, Mares 1992, Olson et al. 2001, Ojeda et al. 2002,Torres & Jayat 2010, Sandoval & Bárquez 2013). Chacoanvegetation ranges from dense, moist woodlands and thicketsthrough open shrublands to extensive treeless grasslands;the composing communities form a series of floristic, faunaland environmental gradients (Bucher 1982). Herbivory,along with rain and fire, are the main agents that structurethe vegetation of this ecosystem, resulting in an extensivesavanna interspersed with patches of forest (Bucher 1987,van der Waal et al. 2011). The balance between woody and

herbaceous cover is regulated by a combination of thesefactors (Bucher 1982, Augustine & McNaughton 2004,Staver et al. 2011, Hoffmann et al. 2012), as well as the evo-lutionary history of the savanna (Lehman et al. 2014).

The Gran Chaco is characterized by competing or coex-isting land uses produced by historical and contemporaryinteractions between socio-economic and intrinsic bio-physical characteristics (Morello & Saravia Toledo 1959a, b,Baldi & Jobbágy 2012). The impact of human activity islinked to the introduction of domestic cattle and deforesta-tion, which led to the elimination of fire-climax grasslandsas well as to the alteration of forest composition and struc-ture (Bucher 1982, Gasparri & Grau 2009). The replacementof grasslands by shrubs is attributed to a synergy betweenherbivores, climate and fire (Beerling & Osborne 2006), andthe degree to which each factor regulates the dynamics ofwoody plants can have significant implications on the con-servation and management of the savannas. More specifi-cally, the occurrence of these three factors can exhibitpositive feedbacks by removing and preventing forestencroachment and providing space for grasses that fuelmore fires. In the case of herbivores, however, negative feed-backs are also observed, as they select certain grasses, thusreducing the flammability of the system and therefore pro-moting tree survival (Beerling & Osborne 2006).

The mammals of savanna ecosystems are key compo-nents of their dynamics due to the roles they exert(McNaughton et al. 1988, Frank et al. 1998, Odadi et al.2011), and it is therefore essential to analyse how they copewith highly fragmented, human-influenced, unprotectedlandscapes. In particular, native herbivorous and frugivo-rous mammals are known to provide several ecosystem ser-vices to humans, including ecological (regulating ecosystemdynamics through seed dispersal of key plant species andplant recruitment), cultural (ecotourism, traditional usesand education) and provisioning (bush meat) services (duToit & Cumming 1999, Schipper et al. 2008). However,although more than 100 species of native mammal inhabitthe Gran Chaco (Anonymous 2005), there is an alarminglack of knowledge regarding their population status, theroles they play in ecosystem dynamics and the consequencesof their possible demise.

Subsistence and commercial hunting was identified as thesixth main challenge to Argentine Chacoan biodiversityconservation by the Nature Conservancy and other institu-tions (Anonymous 2005), after agricultural expansion, com-mercial forest exploitation, hydroelectric dams, livestockexpansion and fire (in the dry Chaco). Wild animals havealways represented important sources of food for manypeople in Latin America, as indicated in a thorough reviewregarding subsistence and commercial hunting by Robinsonand Redford (1991). In particular, subsistence hunting inthe Gran Chaco is a recurring activity (Ojeda & Mares 1982,

Fig. 1. Map of the South American Gran Chaco (Dinerstein et al.1995). The Argentine Chaco is the specific focus of this review.

Loss of Chacoan mammals M. E. Periago, V. Chillo and R. A. Ojeda

42 Mammal Review 45 (2015) 41–53 © 2014 The Mammal Society and John Wiley & Sons Ltd

Altrichter 2006), though there are no records of the impactof this practice on mammalian populations. Furthermore,the high level of wildlife exploitation (that may drivechange) raises a growing concern for the persistence ofpopulations of larger (>10 kg) mammalian species and foroverall species rarefaction in the richest biomes of Argen-tina, such as the Gran Chaco and Yungas (Mares & Ojeda1984, Ojeda et al. 2002).

According to Bucher and Huszar (1999), the case of theChaco can be extrapolated to all ecoregions of the develop-ing world, and its conservation has been ‘doomed to failure’for many years, unless high economic returns can beachieved from it in a sustainable manner. Moreover, theaccelerated expansion of the agricultural frontier in thesouthern portion of the Argentine Chaco, particularly inthe past 10 years, has led to the loss of remnant forest coverat an annual rate of 2.2%, one of the highest rates inrecorded history for such a limited area (Eva et al. 2004, Zaket al. 2004). Thus, most of the Chaco biome has been trans-formed into a highly fragmented mosaic of forest patches,dense thorny scrubs, semi-natural grassland and cultivatedland (Zak et al. 2004, Baxendale & Buzai 2009, Hoyos et al.2013). As a result, the Chacoan landscapes show a complexmixture of ecological conditions, with different regenera-tion possibilities and varying potential to sustain popula-tions of large and medium-sized mammalian species. In thiscontext, understanding the roles of mammals in key ecosys-tem processes is crucial, as ecosystem dynamics (e.g. post-disturbance and restoration trajectories) may be affected bytheir abundance (Harrison et al. 2013).

The purpose of our review is to assess the potential conse-quences for ecosystem dynamics of the loss of native Chacoanmammalian herbivores and frugivores due to rapid andincreasing habitat transformations and ongoing huntingpressures. We focus on the possible effects of losing the func-tional roles fulfilled by large and medium-sized mammalianspecies. Our working hypothesis is that the loss of locallythreatened large and medium-sized mammals in the Chacowould entail the loss of their functions in the ecosystem,because each species has a particular role in the woodlandsavanna dynamics. To test our hypothesis, we summarize thepopulation status and trophic ecology of native Chacoanmammals. We also suggest future directions for research, andmethods for the conservation of the Gran Chaco.

METHODS

This review focuses on the southern portion of the GranChaco, which is located in Argentina and comprises 55% ofthe total 1.2 million km2, encompassing both the dry andhumid Chaco ecoregions (Dinerstein et al. 1995). The dataused to identify the possible consequences of defaunationare derived from an extensive search of peer-reviewed litera-

ture on the role of mammals and the consequences ofdefaunation in different environments. We focus on 25 largeand medium-sized native mammalian species (c. 1–310 kg;frugivores and herbivores), including their conservationstatus, population trends and diet type. We performedsearches in Blackwell, Elsevier, Google Scholar, Scielo andScopus data bases, using different combinations of the fol-lowing keywords: ‘mammal’, ‘Chaco’, ‘function’, ‘herbivore’,‘frugivore’, ‘omnivore’, ‘disturbance’, ‘poaching’, ‘hunting’,‘logging’, ‘cattle’, ‘defaunation’ and ‘fire’. We also reviewedthesis manuscripts in universities and consulted severalregional and local mammal guides, as well as the Red List ofThreatened Species produced by the International Unionfor Conservation of Nature (Anonymous 2013) and theArgentine Red List of Threatened Mammals (Ojeda et al.2008). The complete list of articles consulted is available inthe reference section and in Supporting InformationAppendix S1.

LAND USE INTENSIFICATION IN THEARGENTINE CHACO

The Gran Chaco has a long history of colonization, land usechanges and interactions with wildlife, beginning with sub-sistence hunting by native people. However, over the last 200years, land use has changed to include more intensified prac-tices such as land fencing, livestock production, selectivelogging and intensive agriculture (Eva et al. 2004, Morelloet al. 2006, Hoyos et al. 2013). The combination of thesepractices has resulted in the replacement of grasslands andwoodlands with shrubs and completely eroded areas of baresoil (Morello et al. 2006, Baldi & Jobbágy 2012). In Argentina,agriculture is now expanding to almost every corner of theregion; large-scale agribusinesses mainly for soybean produc-tion are taking over regions previously considered unfit foragriculture (Gasparri & Grau 2009). This expansion, coupledwith climate change, technological advances (the use ofgenetically modified organisms, no-till farming, and pivotirrigation) and socioeconomic factors (high populationdensity, unstable land tenure structure and high land prices)has resulted in isolated patches of forest surrounded by pri-vately owned farms that exert daily pressures on native biodi-versity (Faleiro et al. 2013, Nori et al. 2013), with littleconsideration for long-term sustainability (Zak et al. 2008,Dobrovolski et al. 2011, Laurance et al. 2012).

Almost 40% of the Argentine Chaco has been transformedand only approximately 2% is protected under some type oflegislation (Brown et al. 2006). This is a problematic scenariofor those species whose geographic ranges are constantlybeing constrained to protected areas, especially in those areaswhere protection is neither effective nor guaranteed (Brownet al. 2006). An index of mammal conservation for the differ-ent ecoregions in Argentina, taking into account endemisms,

M. E. Periago, V. Chillo and R. A. Ojeda Loss of Chacoan mammals


vulnerability and taxonomic singularity, has suggested thatthe most urgent conservation priorities are the arid andsemi-arid biomes such as the Chaco and Patagonia, and thesubtropical Yungas forest (Ojeda et al. 2002).

DEFAUNATION AT A GLOBAL SCALE

Habitat loss or fragmentation threatens mammals throughthe loss of food (plants or prey), shelter and increased pre-dation risk (Pimm et al. 1988, Schipper et al. 2008). Largeanimals at higher trophic levels are most vulnerable tohabitat destruction and poaching, since they require largehome ranges and more prey, and because they usually moveacross or use unprotected areas (Duffy 2003). Althoughrarity is always a risk factor, being a common species doesnot necessarily guarantee protection from hunting if thespecies is of interest (Altrichter 2006). The effects ofdefaunation and empty forest syndrome have been welldocumented in tropical forests; several consequences of ver-tebrate loss on ecosystem dynamics have been identified(Table 1; Dirzo & Miranda 1990, Redford 1992, Wilkie et al.2011, Corlett 2012, Harrison et al. 2013). The main conse-quences of defaunation identified by Corlett (2012) includethe co-extinction of parasites, a reduction in environmentalheterogeneity, the release of competitors and prey (includ-ing plants) and a loss of quality and quantity in seed disper-sal services.

Frugivores and ecosystem dynamics

The causes and effects of the loss of frugivores in tropicalforests have been studied worldwide (Table 1). Frugivorousmammals impact ecosystem dynamics mainly by affectingplant regeneration due to seed dispersal and predation(Danell et al. 2006). For example, a decrease in populationsof seed-dispersing animals can cause seed clumping close toparent trees, which can lead to an increase in seed predationby insects or an increase in seed infections, negatively affect-ing species recruitment. On the other hand, an increase inseedling abundance has been reported in areas with lowabundance of seed predators (Table 1). Ultimately,frugivores can exert a negative effect on plant regenerationand distribution through predation, or a positive effectthrough seed dispersal, depending on whether the seedsconsumed are destroyed or favoured after passing throughthe digestive tract (Willson & Traveset 2000).

A recent review on the consequences of defaunation atthe community level in tropical forests showed that large-seeded species undergo reduced dispersal and increasedaggregation of seedlings with the parent individuals, butalso that diminished seed predation and herbivory maybuffer the negative effect of reduced dispersal (Kurten2013). Thus, the occurrence of higher or lower seedling

recruitment depends upon the life history of plant species.Nevertheless, the net effects of defaunation on the plantcommunity were found to be a reduction in species richnessand diversity and an increase in species dominance andenvironmental homogeneity (Corlett 2012, Kurten 2013).

Most studies on defaunation have been conducted inNeotropical rain forests (Table 1), where the percentage ofvertebrate-dispersed tree species in the canopy and sub-canopy is 51–98%, and as expected, defaunation can havesignificant implications on forest regeneration (Stoner &Henry 2009). A decrease in seed dispersal and seedlingabundance due to hunting and fragmentation has beenobserved in seasonal and subtropical forests (Table 1).Although these biomes are characterized by a higher per-centage of mechanically dispersed species, dispersal limita-tions can still have significant negative effects on forestregeneration (Leithead et al. 2012).

Herbivores and ecosystem dynamics

Herbivores are responsible, in part, for determining the het-erogeneity and biological diversity of a specific area, andcreate positive or negative feedbacks depending on the type,frequency and intensity of the disturbance (Table 1). Forexample, for savannas with a long evolutionary history ofgrazing, herbivory promotes the diversity of plant growthforms by suppressing the most vigorous species such asgrasses (Danell et al. 2006). Herbivores promote shootgrowth, increase light absorption by young and active tissueby removing old tissue and improve water-use efficiencyand soil status (Frank et al. 1998). In particular, ungulategrazers are able to maintain permanent grazing lawnsthrough a positive feedback loop that generates enhancedproductivity from a short sward, increasing grass strengthand competition for resources with woody seedlings andsaplings, thereby helping to maintain the grassland state(Bardgett & Wardle 2003).

Herbivores may regulate the structure of vegetation com-munities, as well as primary productivity, through directand indirect effects on ecosystem energy and nutrient flow(Wilkie et al. 2011). However, a plant’s response to her-bivory is highly dependent upon climatic constraints, herbi-vore diversity and biomass, and plant community (du Toit& Cumming 1999, Bardgett & Wardle 2003). For example,herbivores can cause absence of young trees in forests (Gill2006) and damage vegetation by defoliating, trampling,depositing dung and urine, and creating wallows (Hobbs2006). In the transition between forest and savanna, forexample, herbivory is considered to reduce tree cover in ananalogous manner to fire (a keystone factor), although in aless ubiquitous manner (Hoffmann et al. 2012). In thiscontext, the balance between woody and herbaceous plantsmay be regulated by the selective foraging of dominant



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herbivores and may result in changes in ecosystem trajec-tory (Augustine & McNaughton 1998, du Toit & Cumming1999, Wisdom et al. 2006).

LOSS OF CHACOAN MAMMALS AND ITSCONSEQUENCES

Species diversity has been significantly affected by theincreasing land use intensification processes that have beentaking place in the Gran Chaco during the past decades(Ojeda et al. 2002). This phenomenon is more marked inthe Argentine Chaco, which has been highly degraded, andwhere optimal habitats for large and medium-sized nativemammals no longer exist. Populations may begin to disap-pear or become less abundant in marginal areas as homeranges tend to contract, leaving deforested edge areas withfewer individuals (Ojeda et al. 2008). Moreover, thesealready stressed populations are still subjected to intensivepoaching (Altrichter 2005, 2006). Accordingly, Chacoanmammals currently face three main threats, all of which aresevere: (1) the expansion of agricultural lands to the detri-ment of original habitats, (2) intense hunting pressure, and(3) competition with invasive species (Ceballos & Simonetti2002), including the European hare Lepus europaeus, Euro-pean wild boar Sus scrofa and several species of deer intro-duced for sport hunting.

The Gran Chaco is rapidly being transformed into a placewhere the ‘big things that run the world’ are in jeopardy; thelarger mammals that play key roles in regulating thesavanna woodland ecosystem are disappearing (Terborgh1988). Almost 70% of the large and medium-sized nativemammals the geographical ranges of which include theArgentine Chaco have decreasing or unknown populationtrends at the global level: 36% of the species are consideredendangered, vulnerable or near threatened (Table 2;Anonymous 2013). However, the scenario at a national levelis even worse (Ojeda et al. 2012): 52% of large andmedium-sized mammalian species native to Argentina areconsidered to be endangered, vulnerable or near threatened(Table 2). Discrepancies between global and national statusoccur in 10 species, and national categories are always moresevere (Table 2).

Chacoan plant strategies

The Chaco is a seasonal woodland that ranges from subtropi-cal to temperate regions; the harshest environmental condi-tions (water deficit stress) occur in the southernmost portion(dry Chaco). Although both of the dominant canopytree species, quebracho colorado Schinopsis balansae andquebracho blanco Aspidosperma quebracho-blanco, haveanemochory as their seed dispersal strategy, the Chaco ischaracterized by a high diversity of woody species (trees and

tall shrubs), of which approximately 53% are dispersed byendozoochory (Abraham de Noir et al. 2002). Thus, the localextinction of mammals may lead to changes in vegetationcomposition and landscape structure. Among the mostabundant woody species of the Argentine Chaco, 70% dis-perse their fruits rather than their seeds. Of those, 31% arefleshy fruits (e.g. Celtis ehrenbergiana, Condalia microphyllaand Zizyphus mistol) and 36% are dry-indehiscent fruits(e.g. Acacia aroma, Prosopis alba and Prosopis nigra) thatare mainly dispersed by mammals (Abraham de Noir et al.2002).

Fleshy fruits are also dispersed by ants and birds,which maypotentially buffer the negative effects of frugivorous mammalloss on the dispersal of these seeds. However, the largermammals that consume large quantities of seeds and are ableto disperse them further are among the most threatened (e.g.Chrysocyon brachyurus, Table 2). Thus, the compensatorycapacity of this ecological function may only occur (if it iseven possible) with an increase in the abundance of theremaining fauna, but very few mammals are increasing inabundance (Table 2). The potential redundancy of frugivo-rous mammals in the dispersal of the woody species withdry-indehiscent fruits is not easy to evaluate. For example,how many of these species disperse the fruits of a keystone treesuch as Prosopis sp.? Is a mammalian species responsible formost of the dispersal and seedling recruitment? Campos et al.(2008) showed that the passage of Prosopis seeds through thedigestive tract of a mammal can modify germination capacityand speed, with great variability among species. This variabil-ity limits our capacity to analyse potential redundancy indispersal and the role of non-threatened mammals in com-pensating for a given function. In light of this, and as stated byWotton and Kelly (2011), conserving the full range of dispers-ers within an ecosystem ensures that ecological redundancy isretained and provides a buffer to plant extinction.

Chacoan frugivores

The Argentine Chaco is inhabited by 17 native large andmedium-sized mammalian frugivores and omnivores, ofwhich nine are near threatened, vulnerable or endangered atthe Argentine national level (Table 2). Threatened speciesinclude several emblematic species, such as the largeCatagonus wagneri, Chrysocyon brachyurus, Mazama ameri-cana, Pecari tajacu, Tapirus terrestris and Tayassu pecari(Table 2). For these species, the Argentine Chaco is thesouthernmost part of their geographical range, where mostof them show a reduction in population size and rangeoccupancy (Table 2).

In particular, the tagua Catagonus wagneri has disap-peared from approximately 40% of its original geographicrange in the Argentine Chaco, and the remaining very frag-mented populations are in decline, mostly due to an intense



Tab

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Larg

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dm

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increase in deforestation (Altrichter & Boaglio 2004). Thecurrent estimate of the maned wolf Chrysocyon brachyuruspopulation in Argentina is around 660 individuals (Paulaet al. 2008). This seed disperser is the largest canid in SouthAmerica (Motta-Junior & Martins 2002); its primary threatsresult from, among other things, conflicts with humans,drastic reduction in habitat, and hunting for fur and forparts used in alternative medicine (Anonymous 2013). Thelowland tapir Tapirus terrestris, although common in theAmazon and even in some areas of Argentina, ‘seemsunlikely to persist anywhere humans occur at densities anygreater than 1 individual per km2’ due to ongoing popula-tion reductions attributed to deforestation, hunting andcompetition with livestock (Naveda et al. 2008). The pecca-ries Pecari tajacu and Tayassu pecari are considered seedpredators and dispersers via endozoochory of small seeds,expectoration of large seeds and epizoochory (Beck 2005,Lazure et al. 2010). The original range of the peccaries inthe so-called impenetrable portion of the Argentine Chaco,an area of 4 million hectares in the semiarid Chaco, hasbeen reduced by 68% (Altrichter & Boaglio 2004). Thewhite-lipped peccary Tayassu pecari currently exists in only21% of its historical global geographic range (Keuroghlianet al. 2013). The species is heavily hunted in its entire range;subsistence hunting is considered sustainable in some areasof Peru, where it is abundant, and not sustainable at all inother regions, such as the Argentine Chaco (Altrichter2005).

Thus, the ecosystem function of frugivory may be underthreat in the Argentine Chaco, since the mammals thatguarantee this function are all under threat and havedecreasing populations. As we hypothesized, the uniquenessof the function that these species perform makes it difficultto identify other non-threatened species that may compen-sate for its loss; there are only a few appropriate species withincreasing population trends, and they are much smaller insize (e.g. Chaetophractus villosus and Lycalopex gymnocercus,Table 2). This raises concerns regarding the potentialchanges in vegetation composition and structure, since adecrease in seed dispersal and tree seedlings has been foundin seasonal forests where large and medium-sized frugivoresare missing (Table 1).

Chacoan herbivores

Fifteen large and medium-sized mammals that inhabit theArgentine Chaco have herbivory as a primary or secondaryfeeding strategy; 10 of them are near threatened, vulnerableor endangered at the Argentine national level (Table 2). Ofthe 15 species, eight are mainly herbivorous and 50% ofthem are threatened. Moreover, the Chaco ecoregion is thesouthernmost part of the geographical range of 74% of theherbivorous species. Medium-sized species are the most

diverse in their dietary strategies, and it is possible to iden-tify certain degrees of functional complementarities in mainfood categories between species of similar body size(Table 2). For example, the Patagonian mara Dolichotispatagonum and the Chacoan cavy Pediolagus salinicola aretwo medium-sized herbivorous rodents with very similarecological characteristics. However, they differ in theirfeeding strategy: the mara is mainly a grazer and the cavy ismainly a browser (Chillo et al. 2010). The plains vizcachaLagostomus maximus, another medium-sized rodent, pres-ents different ecological characteristics with regard tohabitat use but has dietary similarities with the Patagonianmara (Table 2).

The largest (8–140 kg) herbivores are ungulates, of which78% have decreasing or unknown population trends(Table 2). The four largest herbivores in the Gran Chacoregion are also the most threatened and least abundant of theChacoan mammalian species (Blastocerus dichotomus, Lamaguanicoe, Tapirus terrestris and Ozotocerus bezoarticus). Inparticular, the Pampas deer Ozotocerus bezoarticus has suf-fered a 98% reduction in its historical global geographicalrange (Ojeda & Mares 1982, González et al. 1998) and isconsidered endangered at the national level (Table 2); itsdeclining populations are currently at high risk of extinctionin the wild (Ojeda et al. 2012). The main causes of populationdecline are habitat loss and hunting. Current estimates inArgentina suggest that approximately 1200–1400 individualsexist in four isolated populations, including one in the Argen-tine Chaco with about 170 individuals (Gonzalez & Merino2008). The current range of the guanaco Lama guanicoe, oncethe most widespread ungulate of the continent, has retractedby about 58% in Argentina, 75% in Chile and Peru, almostcompletely in Bolivia and Paraguay, and completely inEcuador, where the species is considered extinct (Baigún et al.2008). The Andean and Patagonian populations in Argentinaand Chile are recovering thanks to conservation efforts andare classified as being of least concern (Ojeda et al. 2012),however the remnant populations in the Chaco were alreadyheading towards extinction 20 years ago (Cunazza et al.1995). These Chacoan populations, which are spread betweenBolivia, Paraguay and Argentina, still face intense huntingpressure and habitat loss, and there is a clear need for tri-national conservation efforts (Baldi et al. 2008).

The densities of domestic ungulates are often higher thanthose of their wild counterparts in the Argentine Chaco, andthe movement of herbivores has changed due to fencing,artificial water provision and nutrient supplementation,which has limited the ability of plants to recover from defo-liation (Staver et al. 2011). Grassland responses to grazingdiffer between native and domestic (livestock) grazing, andthe positive feedbacks that help maintain grasslands underwildlife herbivory may change to those that may maintaindegradation in livestock production systems (du Toit &



Cumming 1999, Wisdom et al. 2006). The replacement ofnative with exotic herbivores eliminates the ecosystemservice the native species provide and may also promoteinvasions, which may even lead to exotic species facilitatingadditional invasions (Parker et al. 2006). In the Chaco, achanging land mosaic is rapidly emerging where domesticand wild herbivores share a limited resource. A long-termexclosure experiment in the semi-arid savanna of Kenya hasshown that cattle can reduce the intensity of use of sharedhabitats by native herbivores because of competition for acommon resource (Riginos et al. 2012). Taken together,these findings show that the role performed by large nativeherbivores may not be compensated for by livestock, butrather that livestock may lead to a different trajectory of thesystem. Here, as with frugivory, the function of herbivory ofhelping maintain the savanna woodland dynamics may beunder threat, since there may not be a compensatory alter-native in medium-sized native herbivores or in domesticcattle.

RESEARCH NEEDS AND CONCLUSION

Redford et al. (2011) urge researchers to try to understandspecies’ recent historic distribution, abundance, geneticdiversity and ecological roles and to ensure that these attri-butes are maintained over time. In this review, we haveidentified native mammals that inhabit the ArgentineChaco, whose feeding strategies include the consumption ofplants and whose populations are under ever-increasingthreats. Most of the species currently show declining popu-lations or are in danger of being vulnerable to threats in thenear future (Table 2). More importantly, we show that thefunctions they carry out in the ecosystem may be at risk aswell. Changes in vegetation structure and compositioncaused by human-induced disturbances, particularly indrylands worldwide, can result in a significant loss of mam-malian functional diversity (Chillo & Ojeda 2012). Impor-tant knowledge gaps exist regarding not only the populationstatus of these large and medium-sized native mammals,but also their functional roles and how, if at all, they areadapting to the rapid land use changes. In particular, wehave scant knowledge of whether these roles will or evencan be carried out by other species (Wright et al. 2007).

Understanding the role of large and medium-sized mam-malian herbivores and frugivores in an ecosystem can shedlight on its evolutionary and ecological history and, moreimportantly, on the potential consequences of nativemammal loss on ecosystem functioning. There is no doubtthat the South American Gran Chaco is undergoing acceler-ated land use changes and that its ensemble of larger nativemammals continues to suffer from hunting pressure. There-fore, the potential losses of functionally unique species couldlead to changes that severely undermine the dynamics of this

savanna woodland ecosystem (O’Gorman et al. 2011). Uncer-tainties in the consequences of losing functionally uniquespecies demand urgent attention, and therefore we list themajor challenges and future research needs for the conserva-tion of mammal functional diversity in the Gran Chaco.

First, there continues to be a void in baseline informationfor many of the species (occurrence, relative abundance andhabitat use). Research on biodiversity loss should includespecies-based and population-based approaches, as well asresearch on service-providing units grouping species thatperform similar ecosystem functions (Luck et al. 2003). Wealso need to have a clear understanding of the nature andstrength of the interactions between functionally uniquespecies in the food web (O’Gorman et al. 2011). In particu-lar, we must consider the potential effects of the loss offunctionally unique species in any restoration attempt, asthis loss may lead to a different restoration trajectory, aswell as strategies that favour the recolonization of largespecies (Anand & Desrochers 2004).

Second, hunting is a current threat to medium-sized andlarge mammals, and therefore, for conservation projects to besuccessful, they must include the knowledge of local peoplewhen assessing the distribution and abundances of the prin-cipal mammalian species included in their diet (e.g. brocketdeer, edentates, peccaries and tapir). Third, local and regionalforums must be established to enhance a fluid and continuousmultidisciplinary and multisectoral dialogue among differentChaco stakeholders, in order to produce stronger bases forlong-term management and conservation (Díaz et al. 2011).Fourth, any restoration attempt must include considerationof the importance of woody plants and the ecological servicesthey provide, such as shade, forage, soil stability, habitats forwildlife, and as a source of biodiversity and carbon storage(Kunst et al. 2012).

Lastly, protected areas in the Argentine Chaco are insuffi-cient and inefficient (Ojeda et al. 2002), especially becausethe degradation of matrix habitats surrounding protectedareas reduces their conservation capacity, even if habitat ismaintained within their administrative boundaries (Hansenet al. 2005). Unprotected areas are crucial to the overall con-servation strategy, and developing strategies for those areasis essential since, according to conservative predictions,more than 80% of the world’s land will remain outside pro-tected areas (Primack 2012). Although large-scale conserva-tion strategies, such as the identification of priorityecoregions and biodiversity hotspots, have been effectiveresponses in the right direction (Loyola et al. 2009), conser-vation management is still failing to protect functionallyunique species and the ecosystem processes needed tomaintain the system (Eken et al. 2004, McConkey et al.2012). Also, the Chaco region is commonly left out of manyof these prioritization schemes, including ConservationInternational’s ‘Biodiversity Hotspots’. Therefore, we



consider it necessary not only to create new protected areasand conservation corridors, but also to improve the effec-tiveness of established areas and privately owned surround-ing areas, for the protection of functionally diverse species.There is a particular need for the establishment of conserva-tion priorities aimed at minimizing population and speciesextinctions, reducing conservation conflicts, and preservingecosystem services (Ceballos et al. 2005).

In the South American Gran Chaco, we are losing speciesfaster than we learn how important they are, the roles theyplay or how their disappearance would affect the entire eco-system. We are currently experiencing a disruption in theequilibrium between mammalian herbivores, frugivores andtheir plant resources, and we probably already face ‘the irre-versible erosion of diversity at all levels’ (Terborgh 1988).Biodiversity is undergoing a global crisis in whichdefaunation and deforestation are commonly accepted con-sequences of human sprawl, and ecologists are alreadydiscussing the need for reforestation and refaunation(Oliveira-Santos & Fernandez 2011). It is with this in mindthat we urge governments with stakes in this vast area not tostand idle while destruction of this unique savanna wood-land ecosystem continues without regard for its biodiversityand conservation value. We consider that any efforts toprevent the disappearance of the South American GranChaco and to restore the savanna woodland dynamics musttake into account the ecological roles played by its nativemammals. We must concentrate future conservation effortson the native mammals and ecosystem dynamics of theChaco before it is too late.

ACKNOWLEDGEMENTS

We thank our institutions: Instituto Multidisciplinariode Biología Vegetal (IMBIV), Consejo Nacional deInvestigaciones Científicas y Técnicas (CONICET), Facultadde Ciencias Exactas Físicas y Naturales, Universidad Nacionalde Córdoba, Córdoba, Argentina, and Grupo deInvestigaciones de la Biodiversidad (GiB), Instituto Argentinode Investigaciones de Zonas Áridas (IADIZA), CentroCientífico y Tecnológico Mendoza (CCT). This contributionwas supported through grants of the National Council forScience & Technology (CONICET) and the Ministry ofScience & Technology (PIP 325; PICT 25778, 0455). We thankJ. Nori for his help with the figure, and Andrew Noss and theanonymous reviewers for their insight and comments.

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