INTRODUCTION
The Neotropical region has the largest number of described mammal species worldwide (1617; Burgin et al. 2018). Of these, 269 species make up the Order Carnivora after aquatic families Odobenidae, Otariidae and Phocidae are excluded. Twenty-seven species of terrestrial carnivores (hereafter “carnivores”) inhabit Argentina (Teta et al. 2018), representing 10.0% and 38.6% of the global and Neotropical carnivore diversity, respectively (Burgin et al. 2018). The greatest diversity of native, extant carnivores in Argentina is concentrated in the Family Felidae (11 species), followed by Mustelidae (8), Canidae (5), Procyonidae (2) and Mephitidae (1) (Table 1).
Seven of the carnivore species present in Argentina are globally categorized as threatened by the IUCN, whereas eleven species are consid ered threatened at the national level (Table 1). Habitat loss, degradation and fragmentation, as well as harvesting are the main threats to mammals in Argentina (SAyDS & SAREM 2019). Understanding underlying causes of these threats and species’ responses can guide the design of conservation actions. However, research on carnivore conservation challenges has had unequal coverage in Argentina in terms of threats, taxonomy and geography.
In this overview, we evaluate what topics have been the subject of carnivore conservation research in Argentina over the past 25 years (1994-2018). Also, we identify thematic and taxonomic gaps and discuss what research may be important to address conservation and management needs. We do not attempt to conduct an exhaustive literature review but to describe main research lines, illustrating them with relevant publications.
CONFLICTS WITH LIVESTOCK PRODUCTION
Contributions in this field focused on methods to monitor canid populations (e.g., Novaro et al. 2000a), testing for selective methods to control “problem” carnivores (Travaini et al. 2001), assessing the impacts of hunting on canid populations in ranches (Novaro 1995), or understanding perceptions and attitudes of livestock producers towards carnivores (Travaini et al. 2000). Interest in this topic has recently revived, seeking to diagnose conflicts (e.g., Guerisoli et al. 2017; Gáspero et al. 2018) or design management options that minimize livestock and carnivore mortality, including the use of guard dogs (e.g., González et al. 2012) and negative reinforcement with distasteful agents to create food aversion (Nielsen et al. 2015).
HUMAN-MODIFIED LANDSCAPES
Ecological and demographic responses. At the community level, the effects of human- induced landscape changes on habitat use by carnivores were studied in various eco-regions (e.g., Caruso et al. 2016; Cruz et al. 2019).
At the population level, the ecological (e.g., Farias & Kittlein 2008; Paviolo et al. 2018) and demographic (e.g. Novaro et al. 2005; Pereira & Novaro 2014) responses to livestock management, agriculture, deforestation, or hunting pressure were also evaluated. Studies on this topic greatly differ in their levels of detail and in their temporal and spatial scales of application.
Hunting. Acting synergistically with habitat loss, poaching (i.e., illegal hunting) threatens several carnivores (e.g., Paviolo et al. 2016; Quiroga et al. 2016). Retaliatory killing has also been identified as a frequent source of mortality of carnivores (e.g., Funes et al. 2006; Carrera et al. 2012). In a culpeo (Lycalopex culpaeus) population that occurred in a landscape with interspersed sheep and cattle ranches in Patagonia, source-sink dynamics occurred as hunting to protect sheep created population sinks and culpeo protection on cattle ranches generated sources (Novaro et al. 2005). This type of dynamics may sustain other hunted car nivores in landscapes dominated by productive activities (Travaini et al. 2010). Lethal control of carnivores through state bounty systems was ineffective in reducing livestock losses (e.g., Llanos et al. 2014), possibly because source- sink dynamics leads to rapid recolonization by dispersers, suggesting the need to better understand and respond to human-carnivore interactions in productive landscapes.
Roads. Local assessments of carnivore road-kill mortalities have been conducted (e.g., Cuyckens et al. 2016; Bauni et al. 2017). However, knowl edge on the extent, magnitude, and population effects of road-kill mortality throughout most of the Argentine territory is unavailable; as is the influence of age, sex, body size, activity, or diet on the probability of being killed on roads. Also, no long-term or large-scale research has focused on issues such as road characteristics or temporal and spatial factors that modulate carnivore road-kill mortalities. As a result, mitigation measures to reduce fatalities have been extremely scarce in Argentina (e.g., Varela 2015).
Exotic species. Exotic species have become new prey for native carnivores (e.g., Pia et al. 2003; Palacios et al. 2012). In southern Pampas grasslands, the availability of horse carcasses may increase the density and affect the spatial organization of Pampas foxes Lycalopex gymnocercus (Luengos-Vidal et al. 2012). In parts of northern Patagonia, due to hunting and competition with introduced livestock and lagomorphs, the biomass of large- and medium- sized native herbivores (such as guanacos Lama guanicoe and rheas Pterocnemia pennata) has decreased, making their representation as prey and sources of carrion in carnivore diets very low (i.e., < 7%), a process termed ecological extinction (Novaro et al. 2000b). In this area, introduced lagomorphs greatly affect trophic webs, modifying the strength of predator-prey relationships and altering community dynamics (Barbar 2016). In contrast, in protected areas and abandoned ranches in southern Patagonia, where guanacos and other native prey have recovered in recent years, both native and in troduced prey play important roles in carnivore diets (Zanón-Martínez et al. 2012). Similarly, in protected and remote areas of northwestern Argentina, native prey still play important roles in the diet of carnivores, but domestic and invasive species are often consumed (Walker et al. 2007; Donadio et al. 2010).
Trophic segregation appears to facilitate the coexistence between the only species of wild carnivore introduced in Argentina, the American mink Neovison vison, and two native ones: the lesser grison Galictis cuja in northwestern Patagonia (Delibes et al. 2003) and the southern river otter Lontra provocax in Tierra del Fuego (Gomez et al. 2010; Valenzuela et al. 2013). The recent invasion of chinook salmon in Tierra del Fuego could provide a new prey for both the southern river otter and the mink (Riccialdelli et al. 2017), with unknown consequences for the regional trophic web.
Domestic and feral dogs have been recorded as predators of native carnivores (e.g., Lucherini & Merino 2008; Pereira et al. 2010). Predation of native carnivores by dogs is probably widespread in Argentina, the country with the largest number of dogs per capita in the world (Mestel 2017), although events are likely underreported in the scientific literature (authors, op. cit.). In addition to killing and displacing native carnivores, free-ranging dogs frequently attack livestock and can exacerbate conflicts between native carnivores and people (A. Schiavini, pers. com.; Montecino-Latorre & San Martin 2018).
Pathogens of domestic cats and dogs that are widely present in rural areas (i.e., canine distemper virus, canine parvovirus) are potential threats to native carnivores (e.g., Martino et al. 2004; Uhart et al. 2012). Despite the importance of this process, infection spillover from domestic to native carnivores has been poorly studied in Argentina. Antibody titers for canine distemper virus and canine parvovirus were also found in American mink in southern Patagonia, although the epidemiological importance of this finding is poorly understood (Martino et al. 2017).
TROPHIC CASCADES
Despite the importance of understanding and protecting the role of predation in ecosystems (Estes et al. 2011), few studies have been conducted on community-level trophic cascades. In the southern Puna, vicunas Vicugna vicugna avoid canyons with high risk of predation by pumas Puma concolor, leading to increased plant complexity in canyons (Donadio & Buskirk 2016). Similarly, the risk of predation by pumas may have a significant impact on guanaco population fitness, affecting forage consumption and habitat selection (Marino 2010) by this dominant native herbivore of the steppe and Monte. In northernmost Pata gonian steppe pumas do not move seasonally following migratory guanacos, their preferred prey (Gelin et al. 2017). Predictions about significant impacts on prey populations due to predation by pumas and culpeos based on indirect assessments of kill rates (Novaro & Walker 2005) require further testing.
PREDICTIVE MODELS
The distribution of some carnivores, including the poorly known bush dog Speothos venaticus (DeMatteo & Loiselle 2008), Andean cat Leopardus jacobita (Marino et al. 2011), and Patagonian weasel Lyncodon patagonicus (Schiaffini et al. 2013) have been analyzed considering climatic, environmental and human-related variables to infer ecological requirements and predict geographic and climatic ranges. Conservation models for carnivore populations facing different threats in Argentina were also developed, including a landscape specifically designed for jaguar (Panthera onca) conservation and management in the Atlantic Forest (De Angelo et al. 2013), an analysis of the possible impacts of climate change on the potential distribution and viability of some carnivore populations (e.g., Canepuccia et al. 2008; Torres et al. 2013; Cuyckens et al. 2015), and the identification of corridors to avoid jaguar population fragmentation (e.g., Martinez-Pardo et al. 2017).
GENETICS
Studies using molecular genetic tools in Argentina during the last 25 years have applications in conservation, especially those characterizing taxonomic units and determining Evolutionary Significant Units (ESUs) and Management Units (MUs), the genetic base for conservation plans. Based on genetic studies of the Argentinian populations of the maned wolf, only one MU was recognized (Raimondi 2013). Moreover, the two maned wolf population sources proposed by Pautasso (2009) (“Bajos Submeridionales” and “Bañados del Río Dulce/ Laguna Mar Chiquita”) showed little genetic variation, pointing to another population (“Iberá”) as the most variable and thus most plausible stronghold for the species in Argentina (Raimondi 2013).
The once continuous historical distribution of the jaguar in Argentina has been reduced to three, apparently separate populations (Yungas, Chaco and Atlantic Forest ecoregions). The jaguar population of the Atlantic Forest of Argentina has already lost genetic diversity but still has higher allelic richness than other smaller populations of the Brazilian Atlantic Forest, from which it is currently isolated and has differentiated by genetic drift rather than adaptive evolution (Haag et al. 2010). A preliminary comparison of the three Argentinian wild populations with captive jaguars in Argentinian zoos (Font 2016; P. Mirol, unpublished) indicated very similar genetic variability in both groups, amongst the lowest estimated for the species. The low genetic effective size of the captive population (6.8), much lower than its number of individuals (37), and the significant genetic differentiation among the three wild populations (P. Mirol, unpublished), suggest the urgent establishment of corridors connecting these populations in northern Argentina to avoid increasing genetic loss and potential fitness reduction.
Lower genetic variability and higher relatedness in comparison with Brazilian populations, as well as a positive association between habitat quality and heterozygosity, were found in Neotropical river otters Lontra longicaudis inhabiting an area of high human impact (Trigila et al. 2015). For southern river otters in Patagonia, two subpopulations deserving conservation attention were postulated, with one of them appearing not to have suffered a human-induced population bottleneck of the sort experienced by other otter species (Centrón et al. 2008).
The rare Andean cat showed extremely low mitochondrial and nuclear genetic diversity throughout its range (Cossios et al. 2012). The geographic structure of this cat’s genetic diver sity was strong, but differed from that of other Andean species, something perhaps explained by isolation in high-altitude “islands” and use of corridors inaccessible to other species. Cossios et al. recognized two ESUs; the southern ESU, at lower elevation in northwestern Patagonia, may be highly endangered due to its smaller range, high conflict with livestock producers (Novaro et al. 2010), and increasing impact from the largest hydrocarbon operation in Argentina (Walker et al. 2013).
Scat detection by trained dogs and posterior genetic analyses allowed species identification and analyses of genetic diversity and habitat use by five carnivore species (bush dogs, jaguars, pumas, ocelots Leopardus pardalis and southern tiger cats L. guttulus) in the Atlantic Forest of Argentina (DeMatteo et al. 2014a; 2014b). Results for the endangered bush dog suggested more tolerance to disturbed habitat than previously thought, but incipient genetic differentiation and possible dispersal limitation between two portions of the Misiones Green Corridor (DeMatteo et al. 2014b).
WHAT NEXT?
We identify five broad research topics and tools that we believe could help carnivore conservation significantly in the near future in Argentina:
Under-studied species. Almost all Argentine carnivore species have been the subject of at least one study with conservation implications, with the exception of very rare (and possibly locally extinct) giant otters Pteronura brasiliensis, marine otters Lontra felina, and greater grisons Galictis vittata. Other species have a very poor representation in terms of research (e.g., Patagonian weasel, tayra Eira barbara). Basic understanding of distributions, biological needs, and threats of these poorly studied species is necessary to determine potential conservation actions. Additionally, periodic assessments of species knowledge and conservation priorities (e.g., Lucherini et al. 2004) are essential to update research needs.
Human-wildlife conflicts. Human-wildlife conflicts here addressed are widespread in productive lands of Argentina, which encompass >50% of its territory (Trading Economics 2019). In addition, interactions among threats may quickly escalate in local or regional importance in the near future, deserving special attention. For example, fracking will likely exacerbate the impact of traditional hydrocarbon extraction and desertification, causing habitat degrada tion and threatening water resources affecting regions and species beyond the Patagonian Andean cat (Walker et al. 2013). Human–carnivore conflicts will likely increase in Argentina due to increasing demand for agricultural products and consequent land-use change, so novel in terventions that promote coexistence based on robust scientific evidence and applicable to local socio-economic conditions are urgently needed. A thorough understanding of the impacts of the overall and emerging threats to carnivore populations will allow stakeholders to do more than just respond to crises, instead establishing pre-emptive management actions based on the needs of carnivores and other wildlife.
Climate change. Climate is rapidly changing worldwide (Barros et al. 2015), exacerbating other threats and triggering new challenges for conservation. Understanding the spatial structure, dynamics and trends of carnivore populations and their ecosystem-level interactions is key to predicting the consequences of climate change, identifying practical measures to reduce and adapt to anticipated effects, and improving our capacity to conserve carnivores (Mawdsley et al. 2009). For example, the development of connectivity models taking into account climate change and landscape change projections, like agriculture expansion, will improve the design of corridors to minimize the effects of fragmentation on carnivores (Correa-Ayram et al. 2016). Another possible interaction with climate change is the exacerbation of carnivore-livestock conflicts. As forage availability declines during droughts or floods and livestock herds become nutritionally stressed, livestock can become more vulnerable to predation. Thus, we must increase our ability to predict and adapt to these events, as well as have new effective tools to protect livestock.
Citizen science / Volunteer work. Citizen science and participatory volunteer networks are becoming increasingly common to assist carnivore research and monitoring activities (Silvertown 2012). For example, when testing tools for carnivore conflict mitigation, active and continued engagement of local people has been crucial, as demonstrated in trials with livestock-guard dogs in Patagonia (González et al. 2012). The jaguar and puma populations of the Upper Paraná Atlantic Forest ecoregion of Argentina, Brazil and Paraguay were mapped and monitored with a volunteer network comprising > 100 volunteers (De Angelo et al. 2011). A similar initiative is currently being implemented in the Argentine Chaco to monitor jaguars (V. Quiroga, pers. comm.). Citizen science and conservation initiatives will become more common in Argentina and the Neotropics, particularly with charismatic species that attract public attention, as new technologies facilitate communication, data acquisition and processing (Silvertown 2012).
Rewilding. Several carnivore species have become regionally or locally extinct, the distributions of some carnivores have been drastically reduced, and their native prey have been depleted. For example, the jaguar currently occupies less than 5% of its original area (Di Bitetti et al. 2016) and it is considered ecologically extinct in the Chaco (Quiroga et al. 2014). The restoration of ecosystems through keystone species reintroductions, referred to as rewilding, is an increasingly used technique to restore ecosystem processes and services (Svenning et al. 2016). A large rewilding initiative is taking place in Argentina, in the Iberá National Park (Root-Bernstein et al. 2017). Two critically endangered large carnivores, the jaguar and the giant otter, are targets of reintroduction efforts, together with other mammal and bird species (Zamboni et al. 2017). Research and monitoring of ecological and genetic aspects of reintroduced populations and their communities, as well as social attitudes toward this rewilding program should provide the foundations for success of future rewilding projects in Latin America (Root-Bernstein et al. 2017).
Innovative strategies are required to prevent future loss of carnivore habitats and populations, and to mitigate human-carnivore conflict in the face of expanding human demands, land-use intensification, climate change, and exotic species introductions. Addressing the great conservation challenges that carnivores face through well-planned research and appropriate management actions will help secure the diversity and valuable ecological roles of carnivores in Argentina.