Evolutionary history of herbivory in the Patagonian steppe: The role of climate, ancient megafauna, and guanaco

Quaternary Science Reviews 220 (2019) 279e290

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Quaternary Science Reviews journal homepage: www.elsevier.com/locate/quascirev

Evolutionary history of herbivory in the Patagonian steppe: The role of climate, ancient megafauna, and guanaco
ndez a, *, Carlos Ríos b, Humberto L. Perotto-Baldivieso a Fidel Herna a b

Caesar Kleberg Wildlife Research Institute, Texas A&M UniversityeKingsville, Kingsville, TX 78363, USA Institute of Patagonia, University of Magallanes, Punta Arenas, Magallanes Province, Chile

a r t i c l e i n f o

a b s t r a c t

Article history: Received 12 December 2018 Received in revised form 1 June 2019 Accepted 8 July 2019 Available online 8 August 2019

Herbivory is an important ecological process than has influenced the evolution of grassland-savannah systems. The evolutionary history of herbivory largely determines how resilient plant communities are to herbivory, with communities evolving with a long history generally possessing plant adaptations that make them able to cope with such disturbance. Thus, the evolutionary history of herbivory can serve as an indicator of a system’s resilience to modern grazing. Determining this history, however, is problematic because quantitative measures of herbivory and knowledge of plant origin are needed over appropriate evolutionary time frames. Paleoecology offers a useful framework for assessing this evolutionary history of plant-herbivore interactions. The Patagonian steppe is a phytogeographic province of South America whose evolutionary history of herbivory has been debated. Past discussions have focused completely on the abundance of its sole large ungulate herbivoredthe guanaco (Lama guanicoe Müller 1776)dsince European colonization of the continent. Here we use a paleoecological approach to reconstruct the evolutionary history of herbivory and plant evolution in the Patagonian steppe over a much broader, geologic time frame (Cenozoic) to shed light on the matter. We examine the role of past climate, ancient megafauna, and guanaco in shaping the vegetation and briefly discuss how present land use may be misaligned with the steppe’s evolutionary history of herbivory. © 2019 Elsevier Ltd. All rights reserved.

Keywords: Evolutionary history of herbivory Grazing Guanaco Late-Pleistocene extinction Megafauna Patagonian steppe

1. Introduction Herbivory exerts a profound influence on ecosystems. Herbivores affect a variety of ecological processes such as nutrient cycles, trophic interactions, and plant-community dynamics (McNaughton, 1984; Hobbs, 1996). Prior to the Holocene (~11,700 ya), herbivory was a natural process that occurred solely via wild herbivores in places where plants and herbivores coevolved. The domestication of wild animals during the Neolithic (general global definition ~10,000e4000 ya) (Clutton-Brock, 1999), however, created landscapes whereby natural herbivory occurred increasingly in conjunction with domesticated herbivores. Today, grazing by domestic herbivores occurs globally and often on landscapes with little evolutionary history of herbivory (Holechek et al., 2011). How a plant community responds to grazing by domestic herbivores is, to a large degree, dependent on its evolutionary history

* Corresponding author.
ndez), carlos.rios@ E-mail addresses: fi[email protected] (F. Herna umag.cl (C. Ríos), [email protected] (H.L. Perotto-Baldivieso). https://doi.org/10.1016/j.quascirev.2019.07.014 0277-3791/© 2019 Elsevier Ltd. All rights reserved.

of herbivory (Milchunas et al., 1988). Plants evolving in communities with a long evolutionary history generally possess adaptations that make them resilient to grazing, whereas plants evolving in communities without such history often do not (Mack and Thompson, 1982). The evolutionary history of herbivory therefore can serve as an indicator of a system’s resiliency to grazing (Milchunas and Lauenroth, 1993). Unfortunately, determining a system’s evolutionary history of herbivory is problematic because quantitative measures of its native herbivores are needed over an evolutionary time period, as is knowledge of plant origin and evolution (Adler et al., 2004). Such data often are unavailable or have not been synthesized, and past studies have relied on subjective assessments to characterize the degree to which systems have been exposed to herbivory (Milchunas et al., 1988; Cingolani et al. 2005a). Paleoecology provides a useful framework for assessing the coevolution of plants and herbivores (Jacobs et al., 1999). Fossilized structures of plants such as pollen, phytoliths (plant silica bodies), leaves, stems, and floral parts serve as a record of ancient grasses € mberg, 2011). In addition, different sources of and grasslands (Stro

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paleozoological data such as fossils, tooth and skull morphology, enamel microwear, and stable carbon isotopes can be used to reconstruct the diets and communities of ancient herbivores (MacFadden, 2000). More recently, allometry has been used to estimate demographic parameters of paleoherbivores such as body mass, basal metabolic rate, density, and trophic relationships (Di ~ a, 2017). Because many of these data are Giacomo and Farin georeferenced, geographic information systems (GIS) can be used to synthesize these databases and provide a spatial and more quantitative view of paleoherbivory. The Patagonian steppe of South America is a phytogeographic province whose evolutionary history of herbivory has been debated. The guanaco (Lama guanicoe Müller 1776) has been the sole, large ungulate to inhabit the Patagonian steppe for the past ~10,000 years (Bucher, 1987). When Europeans arrived during the 1500s, guanaco populations in South America were estimated to be ~30e50 million (Raedeke, 1979). The evolutionary history of herbivory in Patagonian steppe therefore has been considered short because of the lack of generalist herbivores (Milchunas et al., 1988), long because of the presumed abundance of guanacos (Lauenroth, 1998), and unknown (Cingolani et al., 2005a). Here we use a paleoecological approach to reconstruct the evolutionary history of herbivory in Patagonian steppe and examine the role of climate, megaherbivores, and guanaco in shaping its vegetation. We begin with a concise literature review of the paleoclimate and flora of the Patagonian steppe during the Cenozoic to provide an environmental context for the evolution of plants and mammalian herbivores. We then reconstruct the paleoherbivore community prior to the late-Pleistocene extinction, and we synthesize these data using GIS to derive a spatial and more quantitative perspective of paleoherbivory. We discuss how the Patagonian landscape and guanaco may have responded following the megafaunal extinction and provide a synthesis of these paleoecological data to shed light on its evolutionary history of herbivory. Finally, we briefly discuss how contemporary grazing may be misaligned with the steppe’s evolutionary history of herbivory. 2. Literature review 2.1. Paleoclimate and vegetation transitions in southern South America Patagonia is a region in southern South America that encompasses ~39e55
S latitude. Patagonia spans three phytogeographic provinces, of which the Patagonian steppe and Monte comprise the majority of its area (Fig. 1). Patagonia consists of approximately 750,000 km2 and encompasses steppe and scrubland vegetation that is adapted to a cold (mean annual temperature ~12
C), arid (mean annual rainfall~300 mm), and windy (mean annual speed ~14e22 kmph) climate (Cibils and Borrelli, 2005). Three graminoids (Festuca, Stipa, and Poa) dominate throughout Patagonia; however, dominant shrubs (e.g., Mulinum, Lycium, Nassauvia, and Berberis)
n et al., 1998). The origin of the present xerovary regionally (Leo phytic community extends back to the Paleocene (~65 mya) when it occurred as isolated elements within a landscape dominated by subtropical rainforest (Barreda and Palazzesi, 2007). Two major eventsdthe establishment of the Antarctic Circumpolar Circulation and the Andean upliftdwere primarily responsible for the major shift in climate and vegetation from a tropical rainforest to the present-day semiarid steppe (Fig. 2). We begin our discussion of paleoclimate during the Paleocene, when the earth experienced one of its warmest climatic periods (Willis and McElwain, 2002). This time is considered essential for understanding the origin and distribution of modern plant communities because during this time continental plates moved to

their present location, mountain ranges formed, and global climate progressively cooled (Tallis, 1991). During the Paleocene, climatic conditions in southern South America were uniform with mean annual precipitation above 1100 mm and mean winter temperatures above 14
C (Iglesias et al., 2007). Such equitable climate resulted in a rainforest-dominated landscape comprised of highly diverse vegetation and abundant neotropical taxa (Barreda and Palazzesi, 2007). This warm, subtropical climate lasted until the middle Eocene (~50 mya) (Ortiz-Jaureguizar and Cladera, 2006), when the first major climatic eventd the establishment of the Antarctic Circumpolar Circulationdoccurred and ushered in a transition in climate and vegetation (Iglesias et al., 2011; Dunn et al., 2015). The Antarctic Circumpolar Circulation is an ocean current circulating around Antarctica. It came into existence when Antarctica became isolated from South America and Australia due to the establishment of the Drake Passage and Tasmanian Passage, respectively, thereby preventing warm equatorial currents from reaching southern polar regions (Willis and McElwain, 2002). The resulting progressive, cooling trend led to an expansion of temperate to cold-temperate biomes and an eruption of southern beech (Nothofagus) forests (Barreda and Palazzesi, 2007). Plant communities became homogenous and dominated by developing forests of Nothofagaceae with a fern and herb understory, indicating high rainfall and cold-temperate conditions. Grasses made their first appearance in Patagonia during this time (OrtizJaureguizar and Cladera, 2006) as evidenced by the discovery of a small monocotyledonous fragment (Berry, 1937). Climate warmed once again during the late Oligocene (~26 mya) and initiated a vegetation transition from one dominated by forests to one progressively dominated by shrubby and herbaceous plants (Barreda and Palazzesi, 2007). Nothofagus forests remained dominant in northwestern Patagonia, and tropical trees persisted as gallery forests in central Patagonia. Grasses, although clearly pre€ mberg, 2011; sent by now, remained in low abundance (Stro €mberg et al., 2013). Stro The Patagonian climate and flora experienced its second major transition at ~16 mya when the Andean uplift, which had been occurring since the Paleocene, reached a threshold elevation in the southern Andes and created an orographic rain-shadow that lead to considerable drying on the eastern foreland (Blisniuk et al., 2005). The formation of the southern Patagonian Andes, coupled with a decrease in temperature, created dry, cool conditions that resulted in radiation of xerophytic taxa (Iglesias et al., 2011). The last rainforest elements became rare or extinct by the late Miocene, and arid-adapted shrubs and herbs of asters, amaranths, and Ephedra began dominating the ground cover and had a pioneering role in repopulating the vast, open, nearly grassless landscape (Palazzesi and Barreda, 2012). Grasslandsdwhich virtually did not exist in Patagonia before the Quaternary (Palazzesi and Barreda 2012)d began to experience major expansion (Jacobs et al., 1999). By the end of the Pliocene, the landscape of South America was similar to its present form (Solbrig, 1976), and the Patagonian steppe assumed its modern appearance (Barreda and Palazzesi, 2007). Temperature fluctuations resulting from glacial and interglacial periods during the Pliocene and Pleistocene, in conjunction with the newly established rain shadow, produced the final marks on the landscape and resulted in the distinctive geography and flora that characterize Patagonia today: cool, temperate forest restricted to higher elevation areas with abundant rainfall in the west and arid steppe extending across the extra-Andean region to the east (Iglesias et al., 2011). 2.2. The ancient mammals of South America It was within this Cenozoic paleoenvironmentdone broadly


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Fig. 1. Vegetation communities of southern South America: A) current phytogeographic provinces (based on Cabrera, 1976), and B) predicted vegetation communities during late Pleistocene (based on Franca et al., 2015).

Fig. 2. Summary of key events in the evolutionary and geologic history of the Patagonian steppe.

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characterized by a progressively cooler, drier climatedthat the evolution of mammalian herbivores occurred in South America. Two general patterns characterize herbivore evolution in South America during this era: isolated speciation of the ancient inhabitants and a general tendency for massive body size. Following the breakup of Gondwanaland, South America was an island for much of the Cenozoic (Croft, 1999). The early Paleocene inhabitants consisted of only three mammalian groups: marsupials, xenarthrans, and a variety of “ungulates” (hoofed mammals) (Patterson and Pascual, 1968). Xenarthrans and ungulates comprised the herbivorous guild of South American fauna and were unlike that elsewhere in the world (Patterson and Pascual, 1972). Both groups were particularly diverse. Xenarthrans represented more than 180 genera and included armadillos, sloths, anteaters, and glyptodonts (Vizcaíno and Bargo, 2014). Ungulates comprised at least five orders that included an assemblage of strange herbivores: tapir-like astrapotheres, elephant-like pyrotheres, xenungulates (“strange ungulates”), camel-like liptoterns, and rodentand horse-like notoungluates. Notoungulates alone accounted for more than 140 genera (Croft, 1999). Two groups of waif immigrants (caviomorph rodents and platyrrhine primates) arrived in South America during the middle Oligocene to early Miocene (~34e26 mya) but with minimal disruption to the endemic South American fauna (Marshall, 1988). It was not until the late Pliocene (~3 mya), when the Isthmus of Panama emerged and connected the Americas after some 40 million years of independent evolution, that South American fauna radically changed as a result of the Great American ~ a et al., 2013). Biotic Interchange (Farin The Great American Biotic Interchange occurred over 2 million years and was nearly balanced in exchange: ~47 genera (13 families) from North America dispersed south and ~38 genera (15 families) from South America ventured north (Marshall, 1988; Webb, 2006). The North American immigrants, however, were considerably more successful and underwent explosive diversification in their new continent, whereas most South American immigrants eventually became extinct in North America. Consequently, South America experienced a considerable faunal turnover (Marshall et al., 1982). Xenarthrans largely were unaffected and remained diverse during the interchange (Vizcaíno and Bargo, 2014). Ungulates, however, essentially were supplanted by North American genera (Webb, 1976). The native ungulates decreased from thirteen genera to three while the immigrant group increased from 0 to fourteen genera (Webb, 1976). The new arrivals included camelids, cervids, equids, tapirs, peccaries, and gomphotheres (Marshall et al., 1982). Continued diversification of these North American lineages increased South American ungulate diversity to 23 genera by the late Pleistocene, with most ungulate genera (~85%) being of North American descent (Webb, 1976). It is uncertain why xenarthrans and ungulates faired differently. It is hypothesized that the large size and low metabolism of xenarthrans insulated them from competition with, and predation by, northern species (McDonald, 2005; Vizcaíno et al., 2012). Ungulates, on the other hand, although of moderate and large size, evolved with primitive marsupials as their only mammalian carnivores and therefore were naïve to the progressive carnivores (canids, felids, ursids) of North America (Webb, 2006). A second pattern in the evolution of South American mammalian herbivores during the Cenozoic was the general tendency for increased body size. This trend toward massive size was not unique to South America; however, the diversity and quantity of mega~ a et al., fauna evolving in South America were remarkable (Farin 2013). Gigantic herbivores such as astrapotheres (~1900 kg) and pyrotheres (~3500 kg) existed in South America during the Oligocene, but it was not until the Pleistocene that body size reached its peak (Vizcaíno et al., 2012). Of more than 120 genera, 40 genera

represented large herbivores (>100 kg), and twenty genera represented megaherbivores (>1000 kg) (Vizcaíno et al., 2012). One interesting feature of the South America megafaunal community was that it was dominated by xenarthrans. Unlike North America, Africa, and Eurasia where proboscideans, bovids, cervids, and-or equids dominated the large fauna (Smith et al., 2003), xenarthrans accounted for about 80% of megaherbivores in South America (Cione et al., 2003; Vizcaíno et al., 2012). In this respect, the megafaunal community of South America during the Pleistocene was singularly unique and contained no ancientdor moderndanalog (Vizcaíno et al., 2012). Despite such great diversity, South America lost about 80% of its largest (i.e., >44 kg) mammalian genera during the global extinctions of the late Pleistocene, an extinction rate far greater than that observed in any other continent (Barnosky and Lindsey, 2010). The exact cause for the mass extinction is debated but explanations include human arrival, climate change, and a synergistic combination of the two (Metcalf et al. 2016; Villavicencio et al., 2016). An interesting pattern of megafaunal extinction in South American is that the rapidity over which extinctions occurred appears to have increased from north to south (Barnosky and Lindsey, 2010). Extinctions occurred over a relatively wide time span (~10,000e40,000 years) in northern South America, a moderate time span (~5000 years) at mid-latitudes, and a narrow time span (~2000 years) in southern South America (Barnosky and Lindsey, 2010). In Patagonia, the mean time of extinction for megafauna appears to have been tightly clustered around ~12,000 years ago (Metcalf et al. 2016), with the region losing all of its megafauna and ~ a et al., 2013). In fact, only three most of its large herbivores (Farin ungulate taxa survived the extinction event in Patagonia: two cervids and one camelid. The cervidsdpudu (Pudu puda Molina 1782) and huemul (Hippocamelus bisulcus Molina 1782)dwere primarily forest dwelling species found at higher elevations. The camelid was the guanaco and inhabited the arid steppe. For the next ~10,000 years, the guanaco would be the only large ungulate to inhabit the Patagonian steppe until the introduction of sheep (Ovis aries) by Europeans during the late-1800s. 3. Methods The late-Pleistocene extinction transformed the herbivorous guild of the Patagonian steppe from a diverse assemblage of indigenous megafauna to a single, large ungulate species of North American descent. What effect the complete loss of the megafaunal community had on the Patagonian landscape, and how guanaco populations responded to the defaunation, shed valuable insight into the evolutionary history of herbivory of this phytogeographic province. Toward this end, we reconstructed the ancient community of large- (>44 kg) and mega-herbivores (>1000 kg) inhabiting the Patagonian steppe prior to the late-Pleistocene extinction and examined paleo-ecological processes that may have influenced guanaco populations following defaunation. We used seminal literature of South American paleofauna as initial references to identify ancient herbivores on the continent (e.g., Patterson and Pascual, 1972; Martin and Klein, 1984). We refined the list with studies specific to Patagonian fossil sites during the late Pleistocene (e.g., Miotti and Salemme, 1999; Barnosky and ~ a et al., 2013; Villavicencio et al., 2016) and Lindsey, 2010; Farin cross-referenced the list using The Paleobiology Database (www. fossilworks.org). We then used recent research on the global diversity of Pleistocene megafauna (e.g., Owen-Smith, 2013; Sandom et al., 2014; Faurby and Svenning, 2015) to obtain estimates of their geographic distributions (Sandom et al., 2014; Faurby and ~ a et al., Svenning, 2015), body mass (Smith et al., 2003; Farin 2013; Owen-Smith, 2013), density (Damuth, 1981; Di Giacomo


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~ a, 2017), and diet (MacFadden, 2000; Owen-Smith, 2013). and Farin We combined this information in a geographic information system to obtain spatial perspectives of paleoherbivory. The specific methodology to develop these spatial maps of paleoherbivory involved the following. We obtained estimates of body mass from published literature ~ a et al., 2013; Owen-Smith, 2013) and (Smith et al., 2003; Farin ~ a et al. (2013) and Di calculated population density as per Farin ~ a (2017). This methodology is based on the Giacomo and Farin model by Damuth (1981) and uses the equation, log D ¼ 0.75 (log m) þ 4.23 where D is population density (no. individuals/km2) and m is mass (g), to estimate density. We obtained estimated geographic distributions for the species from Faurby and Svenning (2015) (https://onlinelibrary.wiley.com/doi/full/10.1111/ddi.12369). We accessed the link provided by the Institut for Bioscience to acquire the data (https://megapast2future.github.io/PHYLACINE_1. 2/) and obtained.tif files for the geographic distribution of each species. We downloaded each species' global raster data, which were classified in a binary format: (1) to denote pixels within a given species distribution and (0) to denote pixels outside the distribution. We clipped each species' global raster to the boundaries of South America using ArcGIS 10.X (ESRI, The Redlands, CA) and added all individual raster layers using map algebra. This process resulted in a map of total species richness. To estimate total biomass, we multiplied the estimated density (no. of individuals/ km2) of a given species by the pixel resolution (10,000 km2) within its geographic distribution. We then replaced the pixel value (1) by the pixel density value. We multiplied pixel density (no. of individuals/10,000 km2) by the body mass of a given species and divided by 1000 to report biomass values as tons per 10,000 km2. We added the biomass layers across all species to obtain a map of total biomass. We conducted this general methodology to produce maps of paleoherbivory (species richness and biomass) for three categories of paleoherbivores (all species, xenarthans only, and non-xenarthans). 4. Results Patagonia appears to have possessed a rich assemblage of largeand mega-herbivores during the late Pleistocene based on recovered fossils and estimated species distributions (Faurby and Svenning, 2015). Sixteen species may have inhabited the Patagonian steppe, and an additional twenty-two species may have occurred to the north and west in the adjacent Monte, Espinal, Chaco, and Pampa provinces (Fig. 3; Supplemental Table 1). Xenarthrans dominated the community and comprised ~40% of large herbivores and ~80% megaherbivores (Supplemental Table 1). From an evolutionary-history-of-herbivory perspective, it is noteworthy that no bovid or proboscidean inhabited the Patagonian steppe. Bovids never dispersed into South America during the Great American Biotic Interchange (Webb, 2006). Proboscideans did disperse to South America during the interchange, but only two genera migrated sufficiently south for their geographic distributions to near the Patagonian steppe based on current evidence
et al., 2013). The mountain proboscidean (Lucas, 2013; Mothe (Cuvieronius hyodon) approached the steppe’s northwestern boundary, and the lowland proboscidean (Notiomastodon platensis) occurred to the north in the Espinal, Pampa, and Chaco provinces
and Avilla, 2015). The Patagonian and beyond (Lucas, 2013; Mothe steppe therefore evolved without the influence of these two keystone herbivores (i.e, bovids and proboscideans). Spatially, paleoherbivory decreased from north to south in terms of species richness and herbivore biomass (Figs. 4 and 5). Species richness was greatest in the Monte, Espinal, and Chaco provinces (Fig. 4A), and total biomass was 2e3 times greater in

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these northern provinces compared to the Patagonian steppe (Fig. 5A). The dominance of xenarthrans was evident when spatial patterns of paleoherbivory were compared without this group. The north-south gradient in paleoherbivory diminished when xenarthrans were excluded (Figs. 4B and 5B), and the level of herbivory as indexed by species richness (Fig. 4C), and in particular total herbivore biomass (Fig. 5C), was considerably reduced after the latePleistocene extinctions. Three general patterns therefore characterized paleoherbivory in the Patagonian steppe during the late Pleistocene: dominance by xenarthrans, an absence of bovids and proboscideans, and a decreasing north-to-south gradient in species richness and total herbivore biomass. 5. Discussion How these unique patterns of paleoherbivory (i.e., dominance by xenarthrans, lack of keystone megaherbivores, and latitudinal gradient in herbivory) impacted evolution of the Patagonian steppe may be understood by evaluating how the system responded to extinction of the megafaunal community. 5.1. Vegetation response to defaunation It is well known that modern megaherbivores such as elephants, rhinoceros, and bison can act as keystone species and exert profound influence on plant communities (Owen-Smith, 1987; Hobbs, 1996). For example, African elephants (Loxodonta africana Blumenbach 1797) create openings in forests and wooded areas and thereby influence landscape structure by maintaining savannas via woody-plant suppression (Dublin et al., 1990). In North America, bison (Bison bison Linnaeus 1758) create heterogeneous landscapes and maintain herbaceous-species diversity via pyric-herbivory processes (Knapp et al., 1999). In this ecosystem, natural fires historically burned across the Great Plains, which influenced bison grazing pattern by concentrating bison on recently burned patches, which in turn influenced the extent and intensity of future fire (Fuhlendorf and Engle, 2001). This interactive, pyric-herbivory process profoundly influenced the diversity and spatial patterns of vegetation on the grasslands of the Great Plains (Fuhlendorf and Engle, 2001). It therefore is conceivable that Pleistocene megaherbivores also may have acted as ecosystem engineers similar to modern megaherbivores (Owen-Smith, 1987). Research indeed suggests that ancient megaherbivores may have acted as keystone herbivores and influenced vegetation structure (Malhi et al., 2016), nutrient diffusion (Doughty et al., 2013), and fire frequency (Johnson, 2009), and that their extinction may have triggered broad-scale changes in plant-community structure (Bakker et al., 2016). However, it appears unlikely that Patagonian megaherbivores, which appeared to be dominated by xenarthrans, acted as ecosystem engineers and triggered sweeping landscape changes following their extinction. Present-day xenarthrans are characterized by a very low metabolism and a dental morphology characterized by low occlusal surface area for triturating food (Vizcaíno et al., 2006). They also possess lower energetic requirements (basal metabolism is ~40e60% of other placental mammals), and thus the ancient xenarthran megaherbivores may have required lower food intake compared to placental herbivores of similar size (McDonald, 2005; Vizcaíno et al., 2006). Consequently, the vegetation impact by these unique megaherbivores may have been less compared to other systems where megaherbivores such as proboscideans dominated, a condition deemed necessary for ancient defaunation to trigger broad-scale structural changes (Barnosky et al., 2016). Indeed, research investigating ecological-state shifts following megafaunal extinction provides evidence for this perspectivedPleistocene defaunation triggered

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Fig. 3. Large (>44 kg) and megaherbivores (>1000 kg) inhabiting the Patagonian steppe during the late Pleistocene. Fauna indigenous to South America are in black; fauna immigrating from North America during the Great American Biotic Interchange are in green. Asterisks denote xenarthran families. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)

Fig. 4. Paleoherbivory in southern South America as indexed by species richness of large (>44 kg) and megaherbivores (>1000 kg) during the late Pleistocene for A) all species, B) non-xenarthran species, and C) extant species. These maps were developed only using species whose fossils have been documented in the Patagonian steppe and adjacent provinces; thus, the index of paleoherbivory is valid only for southern South America and not for the entire continent.

major ecological-state shifts in North America (northeastern US, northwestern US, and Alaska) but not in South America (Patagonian steppe and Pampas provinces) (Barnosky et al., 2016). 5.2. Guanaco population response to defaunation A second important question regarding the evolutionary history of herbivory in the Patagonian steppe is how guanaco populations

responded to the lack of competing herbivores following the latePleistocene extinction. By the time Europeans arrived to South America in the 1500s, guanaco populations were estimated to be 30e50 million (Raedeke, 1979). This estimate is somewhat tenuous, however, because it is based on sheep and cattle numbers occurring in southern South America during the industry boom of the 1900s. It is well documented that livestock numbers historically were in excess of the steppe’s natural capacity and created considerable


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Fig. 5. Spatial patterns of paleoherbivory as indexed by total herbivore biomass of large (>44 kg) and megaherbivores (>1000 kg) during the late Pleistocene for A) all species, B) non-xenarthran species, and C) extant species. These maps were developed only using species whose fossils have been documented in the Patagonian steppe and adjacent provinces; thus, the index of paleoherbivory is valid only for southern South America and not for the entire continent.

degradation (Cibils and Coughenour, 2001; Baldi et al., 2010). Thus, the estimate of aboriginal guanaco abundance based on historical sheep and cattle numbers likely is excessive. Nevertheless, it is undeniable that resources that once were partitioned amongst sixteen or more paleoherbivores during the Pleistocene now were at the disposal of only one. How did guanaco respond: did populations increase exponentially, largely unchecked, or were populations limited and-or regulated by ecological processes? Guanaco descended from a North American camelid (Hemiauchenia Gervais and Ameghino 1880) that immigrated to South America during the Great American Biotic Interchange (~3 mya) (Franklin, 1982). This ancestral form differentiated during the middle Pleistocene (~2 mya) into three lineages (Palaeolama Ger
lez vais 1869; Lama Cuvier 1800; and Vicugna Lesson 1842) (Gonza et al., 2006). The ancestral lineage (Hemiauchenia) and Palaeolama became extinct by the late Pleistocene; however, Lama and Vicugna ~ a (Vicugna survived and became the modern guanaco and vicun vicugna Molina 1782), respectively. From this origin in the Andes, the guanaco spread east and south across the Central Andean Plateau ~50,000 years ago (Marin et al., 2013). The Plateau limited gene flow between the ancestral and dispersing population, and the two subgroups differentiated genetically into a northwestern (Peruvian and Chilean altiplano) and southeastern (Bolivian Chaco and Patagonia) population (Marin et al., 2013). The northwestern population remained small and stable (effective population size < 5000 individuals), whereas the southeastern population increased and expanded (effective population size ~80,000e120,000 individuals) (Marin et al., 2013). Archaeological evidence suggests that guanacos inhabited Patagonia by at least ~13,600 years ago (Sarno et al., 2001). However, the Patagonian population became regionally extinct (~12,300 years ago) toward the end of the Pleistocene, and loss of this southernmost clade almost led to extinction of the species (Metcalf et al. 2016). Patagonia subsequently became re-populated by a discrete population of guanacos from the north ~10,500 years ago, and this latter group became the ancestors from which modern guanacos in Patagonia descended. This near extinction of guanaco is borne in the genetic diversity of the species, and it stands in stark contrast to the commonly held belief that guanacos survived the late-Pleistocene extinction relatively unscathed (Metcalf et al. 2016).

Following the megafaunal extinction, the guanaco existed as the sole large ungulate in the Patagonian steppe for the next ~10,000 years. Although such ecological conditions generally would have favored unrestricted population growth, co-existing along-side guanaco were two of its primary predatorsdpuma (Puma concolor Linnaeus 1771) and early humans (Homo sapiens Linnaeus 1758)d that also had survived the Pleistocene extinction. Generally, the role of predation in Pleistocene systems has been underappreciated (Janzen, 1983). Megaherbivores generally were believed to be immune to the effects of predation because of their large size (OwenSmith, 1988). However, recent research suggests that Pleistocene carnivores may have exerted strong, top-down pressure and limited herbivore populations (Ripple and Van Valkenburgh, 2010; Van Valkenburgh et al., 2016). In Patagonia, the mammalian carnivore guild during the late Pleistocene consisted of five species: sabretooth cat (Smilodon populator Lund 1842; ~400 kg), panther (Panthera onca mesembrina Cabrera 1934; ~140 kg), puma (~121 kg), a short-faced bear (Arctotherium tarijense Ameghino 1902; ~360 kg), and a large fox (Dusicyon avus Burmeister 1866; ~15 kg) (Prevosti and Vizcaíno, 2006; Prevosti and Martin, 2013). The short-faced bear was primarily an omnivore, and the large fox preyed mostly on small mammals, although both occasionally may have consumed guanaco (Prevosti and Martin, 2013). However, the three large felids commonly preyed on camelids (L. gracilis Gervais and Ameghino 1880; L. guanicoe, and L. c.f. owennii), and guanaco comprised the bulk of the puma diet much as it does today (Prevosti and Martin, 2013). In modern Patagonian landscapes, guanacos comprise as much as 50% of the total biomass consumed by pumas (Iriarte et al., 1991; Donadio et al., 2010). Pumas also increase their kill rate of guanaco in a sigmoid, density-dependent manner as guanaco abundance increases (Novaro and Walker, 2005). Such sigmoid (Type III) functional response has the capacity to regulate prey populations and maintain prey below carrying capacity (Holling, 1959). Thus, guanacos may have been regulated by large felids during the Pleistocene and by puma during the Holocene. Adding to this regulation possibility is the fact that puma predation was not the only source of major mortality sustained by guanaco during the Pleistocene and into the Holocene. Guanacos also represented a critical resource for early humans (De Nigris, 2004). Hunter-

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gatherers reached southern South America ~15,000e11,000 years ago just prior to the late-Pleistocene extinction (Barnosky and Lindsey, 2010). These early people relied heavily on guanacos as their principal quarry, and guanaco provided most of the raw materials for their food, clothing, housing, and artifacts (De Nigris, 2004). Initially, hunting pressure on guanaco may have been ephemeral both spatially and temporally because human occupation in Patagonia was transitory as glaciers advanced and receded during the Holocene (Borrero and Franco, 1997). However, as human populations established and their density increased, hunting pressure on guanaco amplified and exploitation became consistent, with much of the space use of early humans being dictated by guanaco movements (Wolverton et al., 2015). A third ecological process that may have influenced guanaco populations during the Holocene is their territorial behavior. The influence of territorial behavior on population limitation of large herbivores generally has received minimal consideration because most discussion has focused on the relative influence of top-down versus bottom-up processes (Krebs, 2009). However, territoriality can exert a strong influence on a species' population growth, and theoretical models indicate that territoriality results in equilibrium densities that are below those predicted by environmental carrying
pez-Sepulcre and Kokko, 2005). Territorial behavior is capacity (Lo known to be an important self-limiting mechanism in a variety of vertebrate taxa including fish, birds, and small mammals (Wolff,
pez-Sepulcre and Kokko, 2005). In guanaco, territorial 1997; Lo behavior occurs via its mating system (resource-defense polygyny), in which adult males defend territories where groups of females and their young reside until offspring become yearlings and are expelled by the territorial male (Raedeke, 1979; Franklin, 1982). Such mating system suggests that guanaco populations may have been self-limited by territoriality during the Holocene and may have occurred at densities below carrying capacity. Indeed, research indicates that the territorial behavior of guanaco can selflimit the species and stabilize populations in Patagonia at densities well below (~23 guanacos/km2) the carrying capacity predicted by the environment (~62 guanacos/km2) (Marino et al., 2016). It is important to note that these ecological processes influencing guanaco populations during the late Pleistocene and into the Holocene were not occurring in isolation but rather within an environmental context of considerable climatic and vegetation fluctuations. During the late Pleistocene, climate experienced abrupt alternations between warm (~18,000e15,000), cold (~14,700e12,700 years ago; Antarctic Cold Reversal), and warm (~11,400) periods (Markgraf, 1983; Glasser et al., 2004). Although climatic changes during the Holocene were less extreme, such warm-cool fluctuations continued (Mancini et al., 2008), with precipitation fluctuating between arid (200 mm) and more mesic (500 m) conditions ~12,500e1000 years ago (Tonello et al., 2009). Consequently, Holocene vegetation fluctuated between steppe and open/closed forest near the forest-steppe ecotone, and between steppe and shrubland in the extra-Andean region (Mancini, 1998, 2002; Iglesias et al., 2014). This environmental variability likely contributed to the local extinction-recolonization dynamics experienced by guanacos during the late Pleistocene-Holocene (Metcalf et al. 2016), in a manner very similar to how climatic fluctuations influenced faunal turnover in North America (Cooper et al., 2015). 5.3. Legacy effects of paleoherbivory and climate on Patagonian flora The possible limitation and-or regulation of guanaco populations during the Holocene suggests that the Patagonian steppe may have evolved under relatively low herbivorous pressure following the megafaunal extinction. One interesting peculiarity of

South American flora, however, that seemingly contrasts this perspective is the prevalence of shrub spinescence (Johnston, 1940). In the Chaco and Monte provinces, for example, structural defenses such as spines and thorns are common in legumes (Prosopis and Acacia) and cacti (Opuntia) (Bucher, 1987). Further south in the Patagonian steppe, several shrubs characteristic of the province such as calafate (Berberis spp.), neneo (Mullinum spinosum), and cola de piche (Nassauvia glomerulosa) also are spinescent. Such prevalence of structural defenses seems unnecessary considering the near absence of contemporary wild herbivores (Bucher, 1987). If guanacos indeed were limited or regulated by ecological processes during the Holocene, then why are some shrub species in the Patagonian steppe apparently so well defended (Lauenroth, 1998)? Two ecological processesdanachronistic adaptation to past herbivory and prolonged evolution in an arid climatedmay offer explanations for this apparent ecological paradox. Ecological anachronisms are adaptations present in living organisms that evolved in response to past interactions with extinct species (Barlow, 2002). One classic example of an ecological anachronism is the large, fleshy fruits of many neotropical trees in Central and South America (Janzen and Martin, 1982). Fruits of neotropical trees such as jicaro (Crescentia alata), soncoya (Annona purpurea), and guanacaste (Enterolobium cyclocarpumare) formed part of the extinct megafaunal diet and evolved traits such as large size, indehiscence, and sugar-, oil-, or nitrogen-rich pulp to ~es encourage their consumption (Janzen and Martin, 1982; Guimara et al., 2008). Such fruit traits were adaptive during the Pleistocene when megafauna existed; however, these fruit traits are anachronistic in modern landscapes where effective dispersal agents are lacking (Janzen and Martin, 1982). Similarly, structural defenses of South American shrubs and trees are considered to be an anachronistic adaptation remaining from past herbivory of extinct megafauna (Bucher, 1987). Prior to the expansion of grasslands during the late Miocene, browsing was the dominant feeding strategy of ancient herbivores in the Americas (Janis et al., 2000). Browsers formed an extraordinarily diverse and abundant assemblage of paleoherbivores that relied heavily on mast, leaves, and stems of woody plants (Janis et al., 2000). In South America, Pleistocene herbivores played an important role as defoliators of shrubs and trees in the Matorral of Chile (Fuentes et al., 1987) and the Chaco and Monte provinces of Argentina (Bucher, 1987). Browse constituted a common dietary component of ~60 and 70% of the paleoherbivores in the Patagonian steppe and northern provinces, respectively (Supplemental Table 1), and formed an important component of the guanaco diet during the Holocene (Barberena et al., 2009; Gil et al., 2016). A general, spatial pattern of woody-plant spinescence occurring in southern South America is that woody plants with a predominantly Chacoan distribution generally possess larger, denser thorns than species with peripheral distributions (Bucher, 1987). The degree of spinescence in the Chaco is said to rival that of African savannas and be exceptional in that spines and thorns of Chacoan trees cover the entire plant rather than decreasing with height as plants grow beyond the reach of herbivores (Bucher, 1987). Such lack of retrogressive heteroblasty (i.e., decreasing spinescence with increasing plant height) in Chacoan trees is thought to be the result of past browsing by extinct megaherbivores (Bucher, 1987). The observation that this general region of greatest woody-plant spinescence (i.e., Chaco) spatially coincides with the highest levels of paleoherbivory indexed by our spatial maps provides support for the hypothesis that shrub spinescence may represent an anachronistic adaptation to past herbivory. A second explanation for the prevalence of woody-plant spinescence in southern South America may be the prolonged


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evolution of plants in an arid climate. Climate exerts a profound influence on plant morphology and community structure (Mooney, 1977). In xeric environments, plants often evolve small leaves, resinous coatings, and-or a deciduous habit as adaptations to minimize heat or water stress (Gates, 1968). Arid-adapted plants also often evolve spines or thorns to guard against the loss of valuable tissue in a resource-challenged environment (Whitford, 2002). A general trend in plant spinescence is for the prevalence of thorns, spines, and prickles to increase with increasing aridity (Mooney, 1977). The percentage of individuals possessing thorns in the Matorral of Chile, for example, increases as environments progress from montane (11%) to desert (38%), a pattern also documented along a similar environmental transition in California (0%e 55%, respectively) (Parsons and Moldenke, 1975). This paralleling trend of increasing spinescence with increasing aridity in both Chile and California is particularly instructive because vegetation structure has converged in geographically distant but climatically similar areas, despite possessing plants of different evolutionary origins (Mooney, 1977). In Patagonia, the richness and diversity of spinescent shrubs also increases as aridity intensifies along environmental gradients (Moreno et al., 2010). Given that aridity has characterized the Patagonian steppe for at least the past ~16 million years (Blisniuk et al., 2005), the Patagonian flora has been exposed to this selection pressure for millennia thus providing ample time for the evolution of plant spinescence. 5.4. Relative influence of paleoherbivory and climate on the evolution of Patagonian flora It is important to note that the influence of past climate and herbivory on the evolution of Patagonian flora is not mutually exclusive. Both climate and herbivory likely played an interactive role in the evolution of the flora and, although it is difficult to discern with certainty which factor exerted a greater influence, studies of plant phylogeography and plant functional traits can provide valuable insight. The Patagonian flora has been shaped by two primary events: Andean orogeny and Pleistocene glaciations (Sede et al., 2012). Andean orogeny created the rain shadow that led to the expansion of arid-adapted plants (Barreda and Palazzesi, 2007), and glaciations caused decreased temperature and increased continentality that influenced plant survival and geographic distributions (Rabassa, 2008). Glacial episodes in southern South America were relatively less severe than in North America, and large portions of the Patagonian steppe remained ice free (Markgraf et al., 1995). Consequently, many key Patagonian species as Hordeum (Jakob et al., 2009), Poa (Leva et al., 2013), Bromus (Leva et al., 2013), Mulinum (Sede et al., 2012), and Anarthrophyllum (Cosacov et al., 2013) survived glaciations in situ, while other species such as
rsic et al., 2011; Nicola et al., Nassauvia persisted in refugia (Se 2014). This phylogeographic history contrasts that of North America where certain flora survived glacial and inter-glacial periods by contraction and expansion of geographic ranges (Hewitt, 2004). The Patagonian steppe therefore may represent an old vegetation unit that extends back to the Andean uplift (Jakob et al., 2009), persisting through aridity and glaciations since at least ~16 mya and evolving under these climatic influences well before the large influx of North American ungulates entered the continent (~3 mya). Further evidence of the possible greater influence of climate on the evolution of the Patagonian flora is provided by plant functional traits (Adler et al., 2006). Plant functional traits are features such as leaf toughness, plant height, and spinescence that impact fitness indirectly through their effects on growth, reproduction, and survival (Violle et al., 2007). Functional traits therefore represent legacies of, or adaptations to, past selection pressures. Herbivory,

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for example, tends to favor grasses with an annual life history, short stature, and stoloniferous architecture and select against grasses that are perennial, tall, and caespitose (tussock), although plant functional-trait responses can be climate and region specific (Díaz et al., 2001, 2006). Similarly, aridity tends to result in grasses with scleromorphic features such as rolled leaves, increased leaf hardness, and increased leaf angles that are particularly beneficial in harsh environments (Groom et al., 2004; Hanley et al., 2007). It has been suggested that sclerophylly (i.e., thickened, hardened leaves) also could be an adaptation to herbivory (Coughenour, 1985; Turner, 1994); however, sclerophylly represents a more effective defense against invertebrate herbivores than vertebrate herbivores for whom structural deterrents are more effective (Hanley et al., 2007). Nevertheless, given these general tendencies, the cold, arid, and windy climate of the Patagonian steppe suggests that natural selection would have resulted in plants with scleromorphic features (e.g., high cellulose, high leaf-tensile strength) and either a tall, caespitose architecture if evolving under low herbivorous pressure or short, stoloniferous architecture if evolving under high herbivorous pressure. Research indicates that dominant grasses in the Patagonian steppe indeed are sclerophyllous (Cingolani et al. 2005b) and possess an erect, caespitose architec
n et al., 1998; Cibils and Borrelli, 2005), indicative of ture (Leo evolution under an arid, windy climate and low herbivorous pressure. In addition, dominant grasses in Patagonia are of similar height as dominant graminoids in the sagebrush steppe of North America (a climatically similar province with a known short evolutionary history of herbivory) but possess greater cellulose concentrations likely a result of the windier conditions in Patagonia (Adler et al., 2004; Cingolani et al. 2005b). Thus, both phylogeographic and plant functional-trait studies provide general evidence that climate may have exerted a greater relative influence on the evolution of the Patagonian flora than herbivory (Adler et al., 2006) and that climate resulting from orogeny and glaciations was a crucial factor influencing the demography and diversification of the flora (Rabassa, 2008; Cosacov et al., 2013; Nicola et al., 2014).

6. Conclusions The Patagonian steppe possesses a unique evolutionary history of herbivory. Past discussions of this evolutionary history have been focused solely on the guanaco and its pre-European abundance. However, a broader perspective of the co-evolution of plants and mammalian herbivoresdone spanning 65 million years from the Paleocene to the Holocenedpermits a much richer assessment. In doing so, we learn that the ancient inhabitants of South America (marsupials, xenarthrans, and “ungulates”) were a rare assemblage of mammals that evolved into a unique community of megafauna during some 40 million years of isolated evolution. We also learn that herbivory in the Patagonian steppe transitioned from this diverse, indigenous community of megafauna during much of the Tertiary to a depauperate system consisting of a single, large herbivore of North American descent (guanaco) from the latePleistocene extinction onward. This broader, geological perspective surfaces several key considerations regarding the evolutionary history of herbivory in the Patagonian steppe, namely:  The Pleistocene megafaunal community was dominated by xenarthrans, a group of megaherbivores characterized by low metabolism and low dental occlusal surface area for triturating food.  No bovid immigrated to South America during the Great American Biotic Interchange and only two proboscideans dispersed sufficiently south to approach the Patagonian steppe.

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The Patagonian steppe therefore evolved without the important influence of these two keystone herbivores.  Unlike regions of North America, no ecological-state shifts occurred in the Patagonian steppe following the megafaunal extinction thereby also indicating the general lack of keystone, herbivorous processes.  The guanaco, the only large ungulate survivor to inhabit the Patagonian steppe after the megafaunal extinction, also almost became extinct. This is in sharp contrast to the commonly held belief that guanaco survived the late-Pleistocene extinction relatively unscathed. Collectively, the paleoecological evidence suggests that the Patagonian steppe likely evolved under low herbivorous pressure as suggested by Milchunas et al. (1988). This is in contrast to the extensive Mammoth steppe that developed in the northern hemisphere under similar climatic influences (monsoonal rainshadow) (Guthrie, 2001) but was inhabited by a diversity of grazing megaherbivores such as mammoth (Mammuthus), bison (Bison), and horse (Equus) that may have created strong disturbance regimes that may have maintained steppe productivity (Zimov et al., 2012). Field studies investigating the effects of livestock grazing on Patagonian steppe support this general perspective of low herbivorous pressure and, more importantly, results of these field studies match the theoretical predictions of the Milchunas et al. (1988) model for a system with such evolutionary history (Cingolani et al., 2005a). Prolonged and intensive grazing by domestic livestock has decreased overall productivity of the steppe (Aguiar et al., 1996). In addition, overgrazing has resulted in desertification of ~35% of the Patagonian steppe (del Valle et al., 1998). Consequently, conservation and the long-term sustainability of the Patagonian steppe will involve the deliberate reconciliation of present grazing regimes with the past evolutionary history of herbivory in this province. Acknowledgements This research was supported by the US Fulbright Scholar Pro
ndez. We thank gram via a teaching and research award to F. Herna the Caesar Kleberg Wildlife Research Institute at Texas A&M University-Kingsville and the Instituto de la Patagonia de la Universidad de Magallanes for providing financial and logistical support during the Fulbright Award. FH was supported by the Alfred C. Glassell, Jr. Endowed Professorship in Quail Research and the R. M. Kleberg, Jr. Center for Quail Research during this research. F. C. Bryant, M. C. Downey, J. T. Edwards, T. E. Fulbright, G. M. Gasparini, D. G. Hewitt, W. K. Lauenroth, and R. Lira provided helpful comments on an earlier version of this manuscript. This manuscript is Caesar Kleberg Wildlife Research Institute Publication Number 18e129. Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi.org/10.1016/j.quascirev.2019.07.014. References Adler, P.B., Milchunas, D.G., Lauenroth, W.K., Sala, O.E., Burke, I.C., 2004. Functional traits of graminoids in semi-arid steppes: a test of grazing histories. J. Appl. Ecol. 41, 653e663. Adler, P.B., Garbulsky, M.F., Paruelo, J.M., Lauenroth, W.K., 2006. Do abiotic differences explain contrasting graminoid functional traits in sagebrush steppe, USA and Patagonian steppe, Argentina? J. Arid Environ. 65, 62e82. Aguiar, M.R., Paruelo, J.M., Sala, O.E., Lauenroth, W.K., 1996. Ecosystem responses to changes in plant functional type composition: an example from Patagonian steppe. J. Veg. Sci. 7, 381e390. Bakker, E.S., Gill, J.L., Johnson, C.N., Vera, F.W.M., Sandom, C.J., Asner, G.P.,

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