Biogeography of the Llanos de Moxos : natural and anthropogenic determinants

Biogeography of the Llanos de Moxos: natural and anthropogenic determinants The Llanos de Moxos are an enclave of non-forest biota in the Amazonian lowlands of Bolivia where elements from the Gran Chaco, the Cerrados, and other source areas inhabit landscapes where indigenous peoples created numerous earthworks. While local relief features and geomorphology are often, at least in part, a result of pre-Hispanic human agency, the general patterns of biological diversity in the Llanos de Moxos are determined by longer histories of climatic, geologic, fluvial, and biological processes that well predate the human presence. The flora and fauna of the Moxos wetlands, grasslands, and savannas include many elements from the Cerrados and other extra-Amazonian open formations. While the flora shows low levels of endemicity, the fauna includes several endemic vertebrates associated with forest islands. The Moxos biota largely dates back to the Miocene. In terms of human impact, the introduction of cattle and cattle ranching is likely the most significant event in terms of the present-day landscape and ecology.


Roberto Langstroth Plotkin, South Riding 1 Introduction
Prior to the arrival of Europeans in the Americas, the human inhabitants of the Llanos de Moxos constructed diverse earthworks such as mounds and causeways, raised agricultural fields in the savannas and managed the landscape using fire and other tools (Denevan 1966;Langstroth 1996;Lombardo & Prümers 2010;Lombardo et al. 2011). Erickson (2008) considers the Llanos de Moxos to be an example of an Amazonian «domesticated landscape» and, based on evidence from Moxos, claims that «nature in Amazonia more closely resembles a garden than a pristine, natural wilderness.» These arguments presume that Moxos is representative of Amazonia and also discount the roles of longer-term physical and biological processes in play since the Miocene when extensive non-forest ecosystems originated east of the Andean Cordillera (cf. Hoorn et al. 2010;Latrubesse et al. 2010). This paper presents a review of the biogeography of the Llanos de Moxos and examines the explanatory power of the «domesticated landscape» hypothesis relative to the long-term natural processes in the region and its relevance to understanding Amazonia.

Phytogeography of the Llanos de Moxos
The Llanos de Moxos (also known as the Beni Savannas) are an enclave of open formations -herbaceous wetlands, grasslands, savannas, and woodlands -surrounded by the forests of the Upper Madeira basin (Fig. 1). Navarro (2002) considered the Beni Savannas a unique biogeographic province within the Brazilian-Paranense Region, distinct from the Pantanal and Cerrado provinces, and not part of the Amazonian Region in a biogeographic sense. However, floristic endemism appears to be low; Hanagarth & Beck (1996) identified a total of 14 endemic vascular plant species in the Beni Savannas.
Typical Moxos landscapes include three vegetationtopography units: alturas, semialturas, and bajíos (Beck 1983, Fig. 2). These are analogous to the «bancobajío-estero» sequence of the lower Orinoco Llanos. Alturas are uplands (natural levees) with forests of evergreen and deciduous species of genera such as Acacia, Albizia, Ampelocera, Anadenanthera, Attalea, Navarro 2002). Forests in these dissected «upland» landscapes are limited to narrow stream valleys below the level of the savannas, rather than occurring upon positive relief features as in the southern Moxos landscapes (Hanagarth 1993). A transitional belt occurs between the Cerrados of the Forebulge and the active whitewater floodbasins where the palaeochannels of the Beni river cut across the plains of southern Moxos, such as at the Barba Azul Nature Reserve (BANR) on the Omi river ( Fig. 1 and 4).
The forests surrounding the Llanos de Moxos vary greatly in floristic composition and geoecological relationships, including humid Pre-Andean forests along the southwestern margins near the foothills of the Andes, seasonal Chiquitano dry forest and Guarayos transitional forests to the southeast, humid Iténez forests to the east, the Rondonian forests to the east, the Acrean forests to the north, and the Madre de Dios forests to the west. These variations in contact zones result in a great diversity of forest elements in the meander belt forests, gallery forests, and forest island archipelagos that traverse the Llanos de Moxos.  (Voss et al. 2005). The rat Hylaeamys acritus is known only from the savannas of the Beni and Santa Cruz departments of Bolivia (Emmons & Patton 2005). The rats Juscelinomys guaporensis and J. huanchacae were described from the Huanchaca savannas (Emmons 1999) but are also in the Iténez savannas. In contrast to the Cerrado ties of the above, an unnamed clade of Calomys endemic to the Beni is most closely related to C. fecundus from the Subandean Chaco, not C. callosus of the Cerrados and Chiquitanía (Almeida et al. 2007).

Zoogeography of the Llanos de Moxos
Extra-Amazonian dry forest primates are common such as Alouatta caraya, Aotus azarae, and Callicebus donacophilus in the woodlands, forest islands, and gallery forests of the Moxos region, as well as two endemic primates, the Beni titi monkey (Callicebus modestus) and the Olalla brothers' titi monkey (C. olallae). Vos (2006) identified divergence events for these latter species at approximately 6 million years and 3 million years, similar to the divergence time of the blue-throated macaws noted above. These characteristic elements of the Llanos de Moxos are clearly products of evolutionary histories linked to the rise of the Moxos savannas during the Miocene and the subsequent isolation of their forest habitats from surrounding source areas, and not consequences of landscape domestication.
The presence of Cerrado lizards and small rodents, species with relatively low dispersal abilities across forest barriers, in isolated savannas of the Southwestern Amazon Basin suggests an ancient connectivity with the Precambrian Shield region to the east. Late Miocene environments of the southwestern Amazon basin were dominated by grasslands, swamps, and gallery forests, with seasonal climates and hyper-avulsive rivers, similar to the modern Llanos de Moxos (Latrubesse et al. 2010;Plotzki et al. 2011). These early non-forest ecosystems were likely in contact with the open-formations of the Precambrian Shield region in the past. The development of forest corridors along the major rivers such as the Iténez (Guaporé) and the Beni occurred only after these rivers established their present meander belts.

Subregional differentiation of the Llanos de Moxos
Hanagarth & Beck (1996), Hanagarth & Szwagrzak (1998, and Navarro (2002) have identified a major biogeographic division of the Beni savannas into northern and southern zones, which correspond to the Beni Cerrados and the Llanos de Moxos sensu stricto, respectively. Additional subregions are evident, each with unique characters that reflect natural variations in the geology, water and sediment chemistry, erosional and depositional regimes, climate, and other physical factors that affect vegetation, fauna, and land uses by the peoples who settled these landscapes (Fig.  1).
The southwestern region (SW Moxos) between the Beni and Mamoré rivers is influenced by rivers which carry base-and salt-rich Andean sediments, as evidenced by the abundance of Copernicia palms and an absence of Mauritia palms. Vegetation at Espíritu (Fig. 1) is floristically more similar to the Pantanal than to the nearby Iturralde pampas or Cerrados on the Bolivian Precambrian Shield (Hanagarth & Beck 1996). SW Moxos includes many archaeological raised fields and causeways and is presently densely populated by indigenous peoples, Andean colonists, and cattle ranches, presumably linked to the availability of young alluvial soils derived from whitewater rivers (Lombardo et al. 2011). Flooding in this subregion is also greater in magnitude and frequency, which is also likely related to the abundance of earthworks constructed as flood-avoidance strategies as suggested by   To the north of SW Moxos lies a Transitional Zone traversed by SW-NE to E-W trending palaeochannels related to the migration of the Beni river (Hanagarth 1993). Small, underfit rivers such as the Omi occupy portions of these palaeochannels. The interfluvial zones between these palaeochannels are not subjected to recent sedimentation and the soils are strongly leached, especially on the alturas and semialturas where the vegetation takes on a strong Cerrado character (Fig. 4).
Further north, the land is higher due to the deformation of the underlying Precambrian Shield, creating a feature known as the Beni Forebulge. These higher surfaces are dissected by streams and while not subject to sedimentation are occasionally inundated by rainwater ponding on the flat interfluves. This subregion comprises the heart of the Beni Cerrados that occupy an area of nearly 27,200 km 2 (Ibisch et al. 2008). East of the Mamoré, Cerrados occupy interfluvial uplands of the San Ramón-San Joaquín district where the soils are rich in ferralitic concretions («cascajo»). The woody species at Sheraton (Fig. 1) include all of the 27 most common Cerrado species of Brazil and 90% of the 65 species from a Cerrado near Cuiabá, Brazil (Hanagarth & Beck 1996). Despite the dystrophic soils of the Cerrado, the largest raised fields are actually in this subregion, not in the Llanos de Moxos sensu stricto, and the abandoned platforms presently support woody species intolerant of waterlogged soils (Fig. 7).
The northeastern boundary of the Llanos de Moxos is formed by the Iténez (Guaporé) river that drains the Precambrian uplands of Rondônia and Santa Cruz (Plotzki et al. 2011). The Baures subregion occupies the plains of the southern Iténez basin and is characterized by a combination of whitewater, blackwater, and clearwater rivers. While there are few raised fields (e.g., 12.8 km NW of Bella Vista, 13.200417°S, 63.793976°W), there are many elaborate earthworks such as ringed mounds and zigzag causeways. The forest islands in the Baures region are generally lateritic uplands within a flooded herbaceous savanna mosaic. In contrast to the true Moxos subregion, Mauritia palms are prevalent in the permanently waterlogged acidic soils of the Baures region. While data on the biota of the Baures open formations are nearly inexistent, significant aspects of the Baures subregion include large populations of giant otters and marsh deer, a result of the historically low human population density in these remote and wet savannas. Precambrian rock outcrops of the Baures subregion such as Cerro Orícore and the Serranía de San Simón are likely to harbor undescribed endemic elements, particularly Tropidurus lizards (personal observation).
The southeastern zone of the Llanos de Moxos (SE Moxos) between the Mamoré and San Pablo rivers has a complex Quaternary fluvial history (related to the migration of the Río Grande), resulting in a mosaic of savannas, palaeolevee forests, and partiallyinfilled oriented lakes. SE Moxos presents the greatest concentration of large earthmound complexes (e.g., Ibiato, Ibibate, Casarabe, Perro Muerto, etc.), largely upon naturally elevated, forested palaeolevees, not in savannas (Langstroth 1996;Lombardo & Prümers 2010). The soils are formed from Andean sediments of the Río Grande basin and are consequently relatively rich in bases and have high salt contents as evidenced by the abundance of Copernicia palm savannas. The extensive semialtura woodlands and natural levee forests of SE Moxos are dominated by dry forest elements such as Anadenanthera colubrina, Astronium fraxinifolium, Cordia glabrata, Piptadenia robusta, and Sterculia apetala, indicating their connectivity with the Chiquitano dry forests (Langstroth 1996). The abundance of natural levee surfaces with fertile, well drained soils suitable for upland agriculture may well explain the near-absence of archaeological raised field sites in this region as suggested by , as well as the recent boom in agricultural colonization and deforestation along the Trinidad-Santa Cruz highway.
The savannas west of the Beni River in the departments of La Paz (Bolivia) and Madre de Dios (Peru) are a distinct subregion that includes the Pampas del Heath and the Pampas de Iturralde. The savannas at El Dorado share nearly as many plant species with the Cerrados (21% Sørensen index) as with nearby Espíritu (22% Sørensen index) (Hanagarth & Beck 1996). Mamani et al. (2010) note that the Pampas del Heath are floristically distinct from the «Cerrado de Ixiamas», the former having only two Cerrado species but the latter with high Cerrado affinity. While these savannas support Blastocerus, Chrysocyon, Kunsia, and Ozotoceros, other widespread savanna faunal elements such as Rhea and Tropidurus appear to be absent. The Pampas de Heath and the Pampas de Iturralde bear no evidence of archaeological earthworks and have been occupied historically by forest-dwelling peoples (Denevan 1966(Denevan , 1980.

Llanos de Moxos as «domesticated landscape» and its relevance to understanding of «Amazonia»
Erickson (2008) supports his «domesticated landscape» argument largely on his research in savanna landscapes of the Llanos de Moxos. As demonstrated above, the Llanos de Moxos are not typical of «Amazonia» in any ecological or biological sense and cannot be considered «Amazonian» except in a watershed sense. Any generalization about «Amazonia» based on the Llanos de Moxos is thus inherently flawed and inaccurate. However, the major pre-Columbian population centers of the Amazon basin were located in the seasonal peripheries or flooded savannas, not in the center of the humid forests (Bush & Silman 2008;Meggers 2003). Rather than supporting arguments for agricultural intensification and high population in Amazonian forests, the evidence from the Llanos de Moxos and other savanna and wetland landscapes such as Marajó Island, the Coastal Savannas of the Guianas, and the Alto Xingu region were areas that provided greater opportunities for the development of intensive landscape management in the tropical lowlands of South America. Erickson (2008) does not imply that species were domesticated in Moxos but rather that the landscape itself was reorganized and improved for the needs of the people who inhabited it. In reality, there is little to suggest that the Llanos de Moxos ecosystems are managed systems or even feral systems, or by any other means garden-like in nature, despite the existence of numerous archaeological earthworks of great cultural significance. These earthworks are situated in landscapes which are the result of Neogene geology of the Andean Foreland Basin, the impermeability of the sedimentary cover, and the highly seasonal rainfall regime. Despite the large number of earthworks and the extensive use of fire, the overall configuration of wetland and upland ecosystems in Moxos is not determined by human agency. On finer scales, the vegetation may locally be influenced by earthworks, but more often reflects natural relief, including features created by earthworms, ants, termites, cattle, and plants themselves (Mayle et al. 2007).
The most significant long-term human impacts on the ecology and biodiversity of the Llanos de Moxos are the introduction of cattle in 1682 and the advance of the fossil fuel powered agricultural frontier in the first decade of the 21 st century. However, even the sunflower, rice, and soybean fields will eventually be abandoned just as the pre-Columbian raised fields and Jesuit-era cotton fields were abandoned before them. The natural processes which define the landscapes and ecology -inundation, drought, and fire -will likely return the transformed landscapes back to wetlands, savannas, and forests inhabited by largely native species of flora and fauna, along with the cattle.
Despite the construction of elaborate earthworks, the use of fire, hunting, the introduction of cattle, and agricultural land conversion humans have not significantly altered the essential structure, function, or spatial organization of the physical and biological systems of the Llanos de Moxos landscapes. The species assemblages continue to be dominated by native species, many with origins in the Miocene and Pliocene that pre-date the dispersal of hominids out of Africa, let alone the arrival of humans in the Americas. The biodiversity and biogeography of the Llanos de Moxos cannot be explained as an artifact of landscape domestication or the biological colonization of abandoned earthworks. In contrast, the past and present patterns of human settlement and utilization of the Moxos landscapes are more significantly associated with the natural patterns of inundation, drainage, soils composition, and biological resources.