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Amazonian exploitation revisited: ecological asymmetry and the policy pendulum

2007; Wiley; Volume: 5; Issue: 9 Linguagem: Inglês

10.1890/1540-9295(2007)5[457

1540-9309

Mark B. Bush, Miles R. Silman,

Land Use and Ecosystem Services

Frontiers in Ecology and the EnvironmentVolume 5, Issue 9 p. 457-465 Paleoecology ReviewFree Access Amazonian exploitation revisited: ecological asymmetry and the policy pendulum Mark B. Bush, Corresponding Author Mark B. Bush Department of Biological Sciences, Florida Institute of Technology, Melbourne, FL 32901* (E-mail: mbush@fit.edu)Search for more papers by this authorMiles R. Silman, Miles R. Silman Department of Biology, Wake Forest University, Winston Salem, NC 27104Search for more papers by this author Mark B. Bush, Corresponding Author Mark B. Bush Department of Biological Sciences, Florida Institute of Technology, Melbourne, FL 32901* (E-mail: mbush@fit.edu)Search for more papers by this authorMiles R. Silman, Miles R. Silman Department of Biology, Wake Forest University, Winston Salem, NC 27104Search for more papers by this author First published: 01 October 2007 https://doi.org/10.1890/070018Citations: 84AboutSectionsPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinkedInRedditWechat Abstract The influence of pre-Columbian human populations on Amazonian ecosystems is being actively debated. The longstanding view that Amazonia was only minimally impacted by human actions has been challenged, and a new paradigm of Amazonia as a "manufactured landscape" is emerging. If such disturbance was the norm until just 500 years ago, Amazonian ecosystems could be far more ecologically resilient to disturbance than previously supposed. Alternatively, if the "manufactured landscape" label is an overstatement, then policy that assumes such resilience may cause substantial and long-lasting ecological damage. We present paleoecological data suggesting a middle path, in which some areas were heavily modified, but most of Amazonia was minimally impacted. Bluffs adjacent to main river channels and highly seasonal areas appear to have been the most extensively settled locations. Away from areas where humans lived, their influence on ecosystems was very local. Consequently, we see no evidence suggesting that large areas at a distance from rivers or in the less seasonal parts of Amazonia were substantially altered by human activity. Extrapolating from sites of known human occupation to infer Amazon-wide landscape disturbance may therefore potentially lead to unrealistic projections of human impact and misguided policy. The first scientists to enter Amazonia encountered a wonderland of undescribed organisms living in what appeared to be unoccupied and untouched forest. Adjectives they used to describe the forest included "virgin", "pristine", and "timeless", a vision which became incorporated into scientific thinking. Explanations of high Amazonian diversity invoked the stability and the museum-like quality of unchanging environments that accumulated species and minimized extinctions (Stebbins 1974). Coupled with this view was the romantic idyll of hunter–gatherers living in harmony with nature. Such views have been altered by excavations of archaeological sites from the mouth of the Amazon to the High Andes, which reveal a long record of human occupation, ceramics manufacture, and agriculture (eg Roosevelt 1991; Roosevelt et al. 1991). For at least some groups, a trajectory of increasing populations and greater reliance on agriculture is evident for the past several thousand years. As anthropological and paleoecological knowledge of these systems has deepened, the view of Amazonia as untrammeled and changeless has disappeared (Clark 1996). In a nutshell: Pre-Columbian human influence on Amazonia was spatially heterogeneous, with some sites intensively altered The large majority of Amazonia was probably barely influenced by human activity Fossil pollen and charcoal data point to localized influence around widely scattered occupation sites rather than a uniform influence Arguments that the Amazon forest is a manufactured landscape, and hence resilient to human activity, are only locally true and should not be used to set regional management policy The realization that human populations throughout the Americas declined sharply following European contact altered expectations of the level of human disturbance and modification of systems prior to 1492. Indeed, a series of articles (eg Clark 1996; Erickson 2000; Heckenberger et al. 2003; Erickson 2006) and a recent book (Mann 2005) suggest that the pendulum of scientific opinion has swung from the extreme view of the Amazon as "virgin", has passed a midpoint of "disturbance localized around main waterways", and is now headed toward the other extreme of "widespread and pervasive human disturbance". The title of Heckenberger et al.'s (2003) article, Amazonia 1492: pristine forest or cultural parkland?, was deliberately provocative, but if taken literally depicts a simple dichotomy. We suggest the possibility of a middle path. Here, we provide an alternative interpretation of the existing data, and caution that uncritical acceptance of Amazonia as a manufactured landscape may be misguided and could lead to unsound policy. In Amazonia, there has been a commendable use of science by governments, particularly the Brazilian Government, to set conservation policy. Refuge theory was widely accepted in the mid-1980s and was used at the time, together with maps of diversity, to prioritize areas for conservation (Dinerstein et al. 1995). Although this theory is now largely discredited (Colinvaux et al. 2001), the basic biogeographic patterns of high local endemicity and diversity used to identify "refugia" also formed effective guides for the establishment of protected areas. Land-use policy must be founded on scientific knowledge, but scientific knowledge is subject to continual revision and modification. Consequently, when science appears to support policies that could irreversibly damage ecosystems, the science deserves additional scrutiny. Population size and human impact Estimates of human population in Amazonia at the time of European arrival range from one to 11 million, with a tendency toward higher values in more recent estimates (for overviews see Denevan [1996] and Mann [2005]). The population collapse that occurred between ca 1520 and 1600 AD may have reduced Amazonian populations by an astounding, yet plausible 95% (Denevan 1976). Diseases brought to Central America by the first Europeans spread into South America via trade among native peoples. It is probable that the Incan emperor Huayna Capac died when a deadly epidemic (probably smallpox) swept through the Andes in 1524–1525 (Figure 1), 6 years before the arrival of Pizarro, the first conquistador to enter Peru (Hemming 1970). Smallpox, measles, diptheria, and influenza ravaged the Andean populations over the next 50 years (Denevan 2003). While Spanish accounts describe scenes of bodies piled up and abandoned in Andean villages, nothing is known about epidemic diseases in the lowlands. However, the same genetic susceptibility to European diseases (Black 1992), known trade contact with Andean communities (Hemming 1970), and densely packed populations along major rivers (Smith 1990), make it likely that Amazonian populations were similarly devastated. Figure 1Open in figure viewerPowerPoint Annotated schematic diagram of human population in Amazonia. Low, medium, and high estimates are shown. At the heart of the discussion over pre-Columbian influence in Amazonia are contradictory estimates of human population size, cultural development, and the geographic extent of their influence. The initial European descriptions of Amazonian populations, their size, wealth, and societal sophistication, are at best incomplete and at worst misleading. Friar Gaspar de Carvajal, who accompanied Francisco de Orellana on the first European voyage down the Amazon River in 1541, was writing to impress the King of Spain. While he describes extensive settlements stretching for tens of kilometers along the river, and encounters with thousands of warriors, his credibility is undermined by fanciful descriptions of such curiosities as single-breasted, warrior women. Although the river was named for these "Amazons", they were never encountered in subsequent exploration. In stark contrast to Carvajal's account, Charles Marie de la Condamine, who traveled the Amazon in 1743, described a very different setting, in which isolated bands of people struggled for existence in the most basic circumstances (Smith 1990). Many subsequent visitors validated this portrayal of physical and cultural poverty, so different from the agrarian idyll described by Carvajal. However, in a similar debate over indigenous influence on the vegetation of New England, Foster and Motzkin (2003) caution against accepting eyewitness accounts that post-dated European arrival by > 100 years as proper reflections of conditions immediately prior to first contact. For many years, Carvajal's account was seen to be essentially unreliable (Smith 1990). However, there was renewed interest in the possibility of disease decimating this society, prompting Mann (2005) and others to suggest that both accounts were essentially true. Carvajal did witness dense populations, whereas Condamine was viewing the shattered remnants of a society in which 90–99% of the population had succumbed to smallpox and other European diseases (Smith 1990). If there had been large, settled populations in Amazonia for a thousand or more years prior to contact, this raises the question: "To what extent did human activities prior to the population collapse influence Amazonian ecosystems?" Drawing from the archeological literature, Mann (2005) elaborates a vision of Amazonia in which the area supported upwards of 10 million people, with great urban centers (eg Marajó Island, Santarém), and many other, smaller cities with well-developed infrastructure (eg those adjacent to the Xingu River and Lake Manacapuru). The banks of the main Amazon channel and tributaries such as the Rio Negro, Madeira, Xingu, and Tapajós, teemed with villages (Denevan 1996). Great transforming public works, such as the raised villages, causeways, and fish weirs of the Beni region of southern Amazonia, are attributed to large workforces and complex societal hierarchies (Balée 1989; Erickson 2000). A further legacy of human endeavor is the distinctive soil layering, up to 2 m deep, of black or brown soils with elevated nutrient availability, known as terra preta del Indio (Figure 2). These nutrient-rich black soils often contain broken ceramics and appear to have been altered by the addition of ash, green manure, or, in some cases, fish meal (Lehmann et al. 2003). Such soil modification by humans may have held the key to sustainable exploitation of the land. Figure 2Open in figure viewerPowerPoint Natural and modified Amazonian soils. (a) An oxisol and (b) a terra preta soil. Oxisols are the most common dry land soils in Amazonia and when modified with the addition of ash and organic waste are stained black to form terra preta. Some Amazonian locations were occupied for several thousand years. Shellfish and fish were undoubtedly important dietary components, but so too were maize and manioc. On most Amazonian soils, five harvests of maize in a span of 2–3 years exhausts the soil of essential nutrients. A fallow period of about 20–30 years is needed before the land can again support crops of maize (Kellman and Tackberry 1997). A prevailing view is that these villages remained occupied year after year at population densities too high to allow such long fallowing between periods of cultivation. The elevated nutrient availability (particularly phosphorus) of terra preta soils may have allowed near-permanent cultivation of these soils, potentially supporting a much larger human population density than the native soils (Glaser et al. 2001). Indeed, the terra preta model may offer insight into how Amazonia could withstand intensified agricultural exploitation in the future (Glaser et al. 2001). Based on a wide array of evidence, Balée (1989) estimated that 11% of Amazonian vegetation in pre-Columbian Amazonia was extensively used and altered by human activity. That use ranged from slash-and-burn agriculture to enrichment with fruit-bearing trees (eg Bactris gasipaes [peach palm], Bertholettia excelsa [Brazil nut], Annona spp [includes guanabana or sweet soursop], and Mauritia flexuosa [aguaje, moriche, or nontoca; a palm whose fruit is used to make a drink]). Inferring past human disturbance Fire is the oldest human tool for both small- and large-scale manipulation of the landscape, and one of the major sources of evidence for past human disturbance of tropical forest systems comes from fire histories. Charcoal is produced by forest fires and is gradually buried within a soil profile. Charcoal layers from soil pits can be radiocarbon dated, yielding an age estimate for fire events (generally ± 50–100 years). If old wood is burned, the resulting 14 C dating of charcoal overestimates the time since the fire (Gavin 2001). Sources of such old wood could be the heartwood of an old tree killed by the fire, or dating long-dead but undecomposed wood lying on the soil surface. As most tropical forest fires char bark but not heartwood (sensu Cochrane 2003), it is unlikely that heartwood from this source is represented in the charcoal. Also, because rapid rates of decay in the tropics lessen the fuel load of undecomposed heartwood lying on the forest floor compared to temperate or boreal settings, the probability of charcoal being composed of heartwood is similarly low. The charcoal ages in tropical forest soils are therefore likely to be reasonably representative of the actual fire date (taking into account the errors of 14 C dating). When 304 ages for Amazonian soil charcoal are plotted against time (Figure 3 a,b), the data strongly suggest an expansion of agricultural activity at ca 250 AD, then a series of peaks of fire activity between ca 700 and 1550 AD, followed by a sudden collapse at ca 1600 AD. One of the more surprising results of this analysis is that the highest peak of apparent fire activity is not at ca 1550 AD, but at ca 700–800 AD. Nevertheless, the trajectory of implied disturbance fits well with archaeological estimates of village expansion (eg Roosevelt 1980; Heckenberger et al. 1999). Figure 3Open in figure viewerPowerPoint Soil carbon data from Amazonia. (a) Sketch map showing major Amazonian rivers, locations of radiocarbon-dated soil charcoal, and terra preta. (b) Ages of 228 carbonized layers in Amazonian soils. Data are derived from published accounts of soil charcoal in Amazonia (Sanford et al. 1985; Saldarriaga and West 1986; Desjardins et al. 1996; Piperno and Becker 1996; Pessenda et al. 1998; Tardy 1998; Santos et al. 2000; Walker 2000; Francis and Knowles 2001; Neves et al. 2004; Pessenda et al. 2004; Hammond et al. 2006). All ages are expressed in calibrated calendar-years before present (Stuiver and Reimer 1993). Hammond et al. (2006) conducted the first systematic survey for soil charcoal in a 60 000-ha area of Guyana. Their analysis of > 280 soil profiles revealed charcoal in all of them. The authors considered it unlikely that these were natural fires – although this section of Guyana is subject to El Niño-related droughts – and concluded that there had been extensive human influence in upland eastern Amazonian forests within the past millennia. Pollen, charcoal, and phytolith data from Amazonian lakes also provide evidence for widespread human occupation prior to European contact (Figure 4), and there is virtually no sign of human presence at almost every site for the period 1500–1900 AD. However, these data do not portray the intensity or scale of land use at a local level. Figure 4Open in figure viewerPowerPoint Evidence of widespread pre-Columbian occupation in Amazonia. Map shows the known distribution of modified (terra preta) soils, lakes with paleoecological records with and without evidence of human occupation, the major archaeological settings of (1) Marajó Island, (2) Santarém, (3) the upper Xingu, (4) Manacapuru, and (5) the Beni. The region that Mann (2005) maps as having a high probability of dense settlement is shown. Terra preta data from Lehmann et al. (2003) with additional data from A Zimmerman. Pollen data from numerous authors summarized in Bush et al. (2004; see also Bush et al. 2007a). Within the archaeological community, a full spectrum of opinion can be found, from those suggesting minimal pre-contact disturbance (Meggers 1954, 2003) to those citing extensive local impacts (Denevan 1996), to those who believe in regional, even basin-wide, habitat modification (Erickson 2000). Some anthropologists are now referring to the forests of Amazonia as "a cultural parkland", "human created", or "built landscapes" (Erickson 2000; Heckenberger et al. 2003; Mann 2005). Indeed, Charles Clement, an anthropologist based at INPA (National Institute for Amazonian Research) in Brazil is quoted in Mann (2005) as stating, "I basically think [Amazonian lowland forest is] all human created". Clark Erickson is quoted in Mann (2005) as saying that "…built environment applies to almost [all], if not all, Neotropical landscapes". As these ideas are repeated they tend to gain credence, and may subsequently influence public perceptions and policy. But how robust are the data underlying the assertions of widespread alteration of Amazonia? The hypothesis of widespread Amazonian landscape management is based on analyses of archaeological sites and the assumption that there was a large pre-contact Amazonian population (> 10 million people). A caveat must be applied to these data, and indeed all of the data that we have to date about human disturbance in the Amazon, which is that they are derived from just a few locations, and do not represent either a systematic or a randomized sampling design. There is no ecological component predicting which forest was most likely to be occupied. Was disturbance spread evenly across all of Amazonia or concentrated near human habitation? Is it safe to extrapolate results from sites where we know human habitation occured to the rest of Amazonia? Ecologists are familiar with problems of scale. Indeed, "the problem of relating phenomena across scales is the central problem in biology and in all of science" (Levin 1992). Some general observations from ecology raise at least three concerns regarding how we may extrapolate data from the kind of dot map shown in Figures 3 and 4. First, landscapes are heterogeneous, and the resulting variability in environmental factors produces characteristic patterns of distribution and habitat use in nearly all species. Second, although species distributions can be widespread, their occurrence may be very local. For example, a dot map of the painted turtle (Chrysemys picta) would show that it is distributed across much of the continental US, but its actual occurrence is highly localized within a landscape. Third, a species can be widespread and also have a very substantial impact on the system where it is found, but this is not the same as saying that a species has a widespread, intense impact, or makes wholesale changes to the habitat in which it lives. Thus, extrapolating observations from dot maps can be dangerous, especially when the dots represent discrete activities of limited spatial extent (eg terra preta formation). A first step in making the conjectures that are so critical to ecosystem management in Amazonia is recognizing the potential sources of bias that affect what we infer from data. The data in Figure 4 have two major potential sources of bias. First, lakes used to study paleoecology may not accurately represent the landscape as a whole, because they are attractive places for human settlement – humans like to live by water now and, apparently, always have (eg Bush et al. 2007b). Also, while maps of terra preta sites are available, we have no data on the distribution of soil pits that did not show modified soils. It is a statistical certainty that when extrapolations about land use are made from known archaeological centers and exclude other samples, the analyses will exaggerate human impacts. So how do we go about painting a more accurate picture of past human impacts? Investigating occupation: the scale of impact Fossil pollen and charcoal records (Figure 5 a,b) derived from the analysis of lake sediments can provide detailed insights into Amazonian history. Pollen and spores released from plants and blown or washed into lakes become incorporated into the sediment. Year after year, the sediment accumulates, burying and preserving these plant microfossils in anoxic mud. Lake sediments are retrieved using coring rigs supported by inflatable boats. The vertical columns of mud and the buried layers of microfossils they contain record the composition of vegetation that grew around the lake. Neotropical pollen and spores can often be identified to genus, and sometimes even to species. The radius of land represented in the micro-fossil record – the vegetation directly represented in the record – depends on lake size. In the moderate-sized lakes we discuss here, the great majority of the pollen would have been derived within a few kilometers of the lake. Figure 5Open in figure viewerPowerPoint Markers of human occupation from Amazonian lake sediment. (a) A pollen grain of corn (Zea mays) and (b) microscopic charcoal fragments. During a forest fire, charcoal particles are created in both the smoke and the charred plant remains. This charcoal falls or is washed into nearby lakes. The finest fraction of charcoal reflects regional fire histories, whereas relatively large particles (ie those > 160 μm in length) indicate past fire in the adjacent watershed (Clark 1988). Today, fire is rare in most natural Amazon systems, and many sediments from undisturbed settings contain no charcoal. Finding evidence of regular burns may therefore indicate past hunting activity, where fire is used to drive game or improve its habitat, as a mechanism to clear forest for semi-permanent dwellings, or to increase populations of those light-demanding plants preferred by hunter–gatherers. Finding both charcoal and pollen from crops such as corn (Zea mays) or manioc (Manihot esculenta) is a clear indicator of past agriculture. Zea mays is not native to Amazonia, and its pollen is distinctive, due to its surface pattern and large size (commonly 80–110 μm). Maize pollen is particularly poorly dispersed, making it a good marker of local crop use. Given these two proxies for human activity – microfossils and charcoal – we can start to look at regional comparisons of where humans have altered the landscape (Figure 4). Of the 22 pollen and charcoal records from lakes shown as yellow squares, 13 contained evidence of pre-Columbian occupation. A minority of these sites lay within the area predicted by Mann (2005) to be heavily occupied, but this pattern may reflect the relative abundance of lakes suitable for paleoecological study as much as it does human distribution. Most of these lakes were chosen for the purpose of looking at the vegetation history of the particular area, not as a random or even representative sample of Amazonia. At the scale of Figure 4, it is not always possible to show individual lakes, and so if one or more lakes in a cluster show human activity, then the district is circled. At the broadest scale – whether a region shows human impacts or not – it appears that Amazonia was broadly, and possibly universally, influenced by people. Looking at the lake data on a finer scale, however, shows the dangers of extrapolation. Three lake districts in which multiple lakes have been analyzed provide similar spatial extents of human activity in widely separated Amazonian landscapes (Athens and Ward 1999; Weng et al. 2002; Bush et al. 2007 b,c). In two settings, Prainha and Maldonado (Figure 6 a,b), one lake has an unambiguous record of occupation and agricultural use from about 4000 years ago until ca 1600 AD. The third location, a swamp named Maxus 5, near Yasuni in Ecuador (Figure 6c), lies in wet forest that has very little seasonality. This site has a long record of charcoal in its sediment, while two neighboring wetlands have none. Human occupation in this landscape is more tentative than in the other settings, as no crop pollen or artifacts are associated with Maxus 5. Nevertheless, the discovery of charcoal at just one of three settings is a likely indicator of human activity. The forest at Yasuni receives ∼ 2800 mm of precipitation each year, with no distinct dry season, making natural fires exceptionally rare, if not totally absent. That only one of the three sites contains charcoal, and that the charcoal was found in multiple samples, adds strength to the suggestion by Athens and Ward (1999) that the charcoal was produced by local human activity. Figure 6Open in figure viewerPowerPoint A spatial context for pre-Columbian disturbance within three Amazonian lake districts. (a) Lakes near Prainha, Brazil (1°41′23.20″ S, 53°33′44.41″ W); (b) lakes near Puerto Maldonado, Peru (12°9′51.51″ S, 69°5′59.74″ W); (c) lakes near Yasuni, Ecuador (0°53′53.02″ S, 76°10′24.58″ W). In the Maldonado lake district, the paleoecological record of human activity at Lake Gentry is supported by the presence of stone tools and a midden adjacent to the lake. The paleoecological markers of human occupation at this lake, corn and manioc pollen and charcoal, indicate that agricultural activity in the region began around 4400 years ago, with as much as 3000 years of burning prior to that time. Similarly, at Lake Geral in the Prainha group, corn pollen was found regularly between 4000 and 400 years ago (Bush et al. 2000, 2007c), and regularly occurring charcoal appeared between 8000 and 400 years ago. However, in both the Maldonado and Prainha groups, other lakes showed either a small increase in charcoal abundance or no charcoal whatsoever, and none contained pollen from corn or manioc. These records suggest that human occupation and land conversion were local in nature. Sites within 3–5 km of an occupation center appeared to be quite heavily used but, beyond this, human influence declined markedly, so that at distances of 50 km there was no evidence of human activity. This pattern is very similar to that described by modern anthropologists, where hunting and land management is concentrated in a 1–3 km radius around the center of habitation (Glanz 1991; Apaza et al. 2002). The absence of humans in these records is also striking in another way. In both the Prainha and Maldonado lake districts, human population collapses followed European contact, as both crops and charcoal disappear from the records in the past 400 years. Notably, the apparent collapse is evident even at sites that were never visited by Europeans, providing unambiguous support for the anthropological and historical hypotheses of widespread epidemics. An overall picture is clear: the paleoecological data confirm that Amazonia was exploited by indigenous peoples who practiced agriculture and developed urban centers (Roosevelt 1980, 1991; Roosevelt et al. 1991; Heckenberger et al. 2007), and the populations collapsed shortly after European contact. However, the data do not support the extrapolation of observations from occupied sites to infer uniformly widespread impacts and landscape transformation. There is no doubt that humans are important transformers of Amazonian landscapes and have been so throughout much of the Holocene. Determining how widespread those effects were in the vast area of the Amazon basin, particularly those far from water, requires further study. Specifically, it requires a research program that integrates existing data with new samples taken in ways that allow inferences to be made about broader Amazonia. Two other observations emerge from analysis of the charcoal data from Amazonian soils. The peak of fire frequency was observed not when human populations were presumably at their largest (ie immediately prior to European contact), but at ca 700–800 AD (Figure 3b). This period was thought to be one of peak El Niño activity (Thompson 2000), when droughts beset Amazonia and forests were more highly flammable. It is highly probable that the great majority of these fires were human-induced, but that during periods of intense drought, large areas were burned (making them more likely to be detected today) when small-scale fires escaped to become wildfire. In this way, the spatial scale of human disturbance in Amazonia as a whole does not necessarily track the intensifying history of local land use in the most populous areas. The capacity of humans to disturb the system appears to have been strongly influenced by climatic conditions, not simply a growing human presence. In addition, the time for post-disturbance forest recovery in these settings is not the 500 years implied by the disease model, but > 1000 years. One model of human settlement in Amazonia does incorporate known and inferred densities at the landscape level, albeit through observations of the preferences of modern indigenous populations. Denevan (1996) proposed a bluff model of human occupation, in which indigenous peoples preferentially settled sandy bluffs alongside rivers and where there were views over wetlands. Denevan estimates that as many as 10