Abstract

Humans create habitable zones to allow settlement in inhospitable areas, sculpting landscapes to make travel, labor, and agriculture more efficient and harnessing the power and nutrients of plant and animal resources through domestication. However, each of these processes also creates new opportunities for other creatures to affect humans in return. In particular, pathogens have adapted to many various human settlement and subsistence strategies, effectively using anthropogenic systems to their advantage. In this chapter, we investigate how the domestication of animals and increasing sedentism in prehispanic Bolivia promoted circulation of pathogens. Paleopathological lesions and stature estimates from human skeletal remains demonstrate that while nutrition did not decrease with reliance on agricultural products, disease circulation escalated for people living in the Titicaca Basin between 1000 BCE and 400 CE.

Humans are expert habitat modifiers, causing extreme and sometimes calamitous impacts on other biota on local, regional, and global scales. However, as the chapters in this volume emphasize, humans are not immune to influential, external forces, ranging from hurricanes to rats. In this chapter, we focus on how the physical, social, and economic landscapes in which humans live facilitate disease circulation. In effect, human landscapes create and are created by complementary microbe-scapes (Harper and Armelagos 2013), which are dependent on variables of human lifestyle, relationships with wild and domesticated plants and animals, and local climates. When humans modify their landscapes and relationships to other organisms, they also modify their relationships to microbes, which can have important impacts for humans and microbes alike. In this chapter, we explore how microbe-scapes shift alongside changing human subsistence and settlement patterns.

Pathogen-Human Relationships

Like all animals, humans have been hosts to various pathogens, microbes, and parasites throughout our evolutionary history. In fact, the human body averages 10 trillion to 100 trillion microbes, which make their homes on skin and in mouths, guts, navels, vaginas, nostrils, and sinuses (Harper and Armelagos 2013). The majority of these tiny tagalongs have a neutral impact, while many help humans digest food and ward off other invaders, among other commensal tasks. However, some microbes cause harm when humans encounter them for the first time, when they proliferate, or when the host becomes immune-compromised. The most common pathogens humans encounter are various types of viruses, bacteria, parasites, and fungi (Meade and Emch 2010).

For pathogenic microbes to affect humans, several variables must be in place. First, the ecosystems of pathogens, the human host, and any necessary vectors or reservoir hosts must overlap. Many microbes have the potential to make humans ill but never or rarely encounter humans. In addition, there has to be an effective transmission route between human individuals for pathogens to spread to new hosts. This can be achieved in many ways: through a mobile vector (such as P. falciparum and other malarial-causing parasites), aerosol airborne transmission (such as various Coronaviridae spp. or Mycobacterium tuberculosis), water sources and fecal-oral routes (such as Vibrio cholerae and Escherichia coli), or a combination of the above (Guthman 1995; Meade and Emch 2010; Morawska and Milton 2020; Patz et al. 2004; Roberts and Buikstra 2003; Roberts and Manchester 2007).

Humans have carried some pathogens for a very long time, often referred to as “heirloom” species, such as Helicopter pylori, M. tuberculosis, and various intestinal parasites (Darling and Donoghue 2014; Larsen 1995, 2018). Many of these pathogens were previously assumed to have been acquired from domesticated animals and are therefore relatively recent additions to the human microbiome. However, new genetic research shows that humans more likely acquired them from wild animals (in particular, felids) long before animal domestication (Araújo et al. 2011; Harper and Armelagos 2013; Pearce-Duvet 2006; Tietze et al. 2019). Zoonotic diseases often transfer to humans after repeated interactions with the animal carriers (Muhlenbein 2016), elevating risk for both foraging groups hunting wild animals and groups with domesticated animals.

However, human relationships with heirloom and more recently acquired pathogens have changed dramatically over time, as human groups moved to new regions, encountered new ecosystems, and—perhaps most significant—modified landscapes and ecosystems to support human settlement and use (Barrett et al. 1998; Cohen and Armelagos 1984; Cohen and Crane-Kramer 2007; Pearce-Duvet 2006; see also Quintus et al., chapter 9, this volume). The transition to agriculture is linked to increases in human population density, close association with domesticated animals, and sedentary settlements (although the mechanism and timing of these developments have varied over time and space). Each of these processes revolutionized the microbe-scape humans lived in, no matter when or where they occurred. By fundamentally changing the overlapping ranges of pathogens, vectors, reservoir hosts, and human hosts, humans living in sedentary and/or agricultural communities altered disease landscapes in irrevocable ways.

Sedentary lifestyles of both foragers and farmers have historically led to increased infectious disease and parasitic loads (Barrett et al. 1998; Cohen and Armelagos 1984; Cohen and Crane-Kramer 2007; Darling and Donoghue 2014; Kent 1986; Larsen 1995, 2018; Larsen et al. 2019; Reinhard et al. 1985; Walker 1986). As a result of living in permanent villages, people confronted with issues of sanitation and increased contact with feces facilitated the transfer of intestinal parasites (Blom et al. 2005; Larsen et al. 2019; Reinhard et al. 1985). While many intestinal parasites were not novel to agricultural or sedentary groups (Araújo et al. 2011; Harper and Armelagos 2013; Pearce-Duvet 2006; Tietze et al. 2019), the frequency of transmission and risk of human exposure generally increased with denser populations and permanent settlements.

Sedentary living also facilitated the emergence and maintenance of new pathogens. Larger and denser sedentary populations could sustain epidemics, and pathogen circulation within dense populations could permit transformation to endemic forms (Armelagos et al. 1991; Larsen 2018; Patz et al. 2004). For example, measles (Variola spp.) requires large populations to support spread and circulation. Most closely related to bovine rinderpest and canine distemper, it is likely that the viruses that cause measles emerged from the creation of sedentary settlements and dense populations (McNeill 2010; Pearce-Duvet 2006). More recently, SARS-CoV-2 has been able to circulate globally and to have sustained infection rates, partially because of densely occupied spaces and rapid international travel (Kraemer et al. 2020; Morawska and Milton 2020). Both measles and coronavirus demonstrate how human behaviors and settlements can create and maintain disease spread.

Increased pathogen load and endemic childhood infections decrease bodily resources available for growth and development during childhood as the immune system demands more energy to fight off infection (McDade et al. 2008; Scrimshaw 2003; Scrimshaw et al. 1959). This relationship between nutrition and infection is particularly problematic for agricultural groups, as they are often at higher risk of more catastrophic food shortages. Farmers tend to consume a narrower range of resources than foragers or those using a mixed subsistence strategy, and the risk of crop failures or shortages is more severe. Plants themselves are susceptible to their own pathogens, as the density of agricultural field plants actually elevates the likelihood of experiencing epidemics of plant diseases (Stukenbrock and McDonald 2008). Surplus and grain storage may mitigate short-term food shortages caused by plant disease or other crop failures; however, recurring or long-term shortages can exhaust these supplies, leaving few alternatives. In addition, stored resources attract commensal pests, which may destroy stored human food stocks and are often themselves vectors for diseases (Armelagos et al. 1991).

It is clear that settlement patterns and reliance on agricultural products impact human exposure to pathogens in several ways. Human subsistence strategies and agriculture in particular are major drivers of human pathogen load because they are responsible for “(a) changing the transmission ecology of pre-existing human pathogens; (b) increasing the success of pre-existing pathogen vectors, resulting in novel interactions between humans and wildlife; [and] (c) providing a stable conduit for human infection by wildlife diseases by means of domesticated animals” (Pearce-Duvet 2006:378). However, these patterns are regionally, temporally, and culturally specific; and they depend on what resources humans exploited, the previously existing pathogen load, and other cultural practices that may have amplified or mitigated disease (Pinhasi and Stock 2011). To look at the impact of subsistence and settlement pattern change in situ, we present a case study from the Titicaca Basin of Bolivia and discuss potential microbe-scapes for foraging-herding populations and newly sedentary horticulturalists.

Titicaca Basin Microbe-Scapes

Microbe-scapes in the Titicaca Basin are greatly impacted by the local ecology. Lake Titicaca is at high altitude, approximately 3,810 m above sea level, yet it has a warming effect on the local ecology, raising local temperatures by approximately 8˚C (Chávez 2012; Stanish 2003). This makes the lake and surrounding areas hospitable for diverse plant and animal life. The lake itself is home to several indigenous species of catfish and other small fishes, frogs (including the 1 kg Titicaca frog), and many aquatic plants including algae and totora reeds (Erickson 2000; Junk 2007; Miller et al. 2010). The hillsides surrounding the lake reach over 4,200 m above sea level and include patchy grassland used by wild grazers (deer and wild camelids such as vicuña), domesticated camelids (llama and alpaca), and smaller mammalian and reptilian predators and prey (Andean cats, foxes, viscachas, wild and domesticated guinea pigs, and other small rodents and reptiles; Erickson 2000; Hutterer 2001; Moore et al. 1999).

The wild and domesticated animals of the lake basin are certainly not immune to pathogens. Modern catches of indigenous fish show that they carry parasites transferrable to humans; while archaeological studies have not documented these same parasites, paleoparasitology studies from other parts of Latin America have confirmed the presence of various parasitic species linked to fish and mollusk consumption (Araújo et al. 2011; Morrow and Reinhard 2016; Patrucco et al. 1983). In addition, mummified guinea pigs and dogs from prehispanic Peru show that these animals carried fleas that would have been able to spread plague and other flea-borne diseases (Dittmar et al. 2003). Both guinea pigs and camelids carry various intestinal parasites with the potential to spread to humans either through eating infected meat or through contact with animal feces (García J. et al. 2013; Kouam et al. 2015; Saeed et al. 2018). Finally, felid coprolites from Patagonia showed a diversity of parasites, many of which could have been transmitted to humans through close contact or sharing cave dwellings (Tietze et al. 2019).

While not all of these zoonotic pathogens will ultimately cause disease in humans, it is clear that close and repeated human contact with animals elevates risk of pathogen gene swapping and allows microbes to adapt to human physiology (Muehlenbein 2016). In fact, a modern study near Cusco, Peru, shows that children who spend significant time with llama and sheep herds share more similar gut bacteria and viruses with the animals than with non-herders in the region (Rojas et al. 2019). Similarly, peri-urban children in Lima, Peru, share a gut parasite, Giardia lamblia, with dogs living in the same area, likely because of infected water sources and close contact between animals and children (Cooper et al. 2010). Thus, we would expect that humans in the Titicaca Basin with exposure to animals would share some of their pathogens.

People have lived in the Titicaca Lake Basin for at least 10,000 years. During the late Preceramic Period (3000–1500 BCE), people relied on foraging wild resources (including hunting wild deer and camelids), fishing and collecting other lake resources such as aquatic plants and frogs, and harvesting wild crops and tubers. Isotopic analyses from late Preceramic peoples indicate a diet high in protein (Juengst et al. 2021), supported by evidence of lithics associated with hunting and faunal remains of wild animals (Craig 2011; Craig et al. 2010; Haas and Viviano Llave 2015; Juengst et al. 2017a). These people likely moved regularly throughout the lake basin and into lower regions (Capriles et al. 2014, 2016; Haas and Viviano Llave 2015). Around 1500 BCE, people in the Titicaca Basin were in the process of domesticating camelids to supplement their otherwise wild diet and to make use of other camelid resources, such as wool and dung (Aldenderfer 1989; Craig et al. 2010; Moore et al. 2007).

In the Early Horizon (EH) (1000 BCE–1 CE), people in the Titicaca Basin began to grow domesticated plants, thus supplementing their foraging, hunting, herding, and fishing activities. Some of the first plant domesticates included quinoa (Bruno and Whitehead 2003) and tubers such as potatoes and oka (Aldenderfer 1989). While these plants quickly became important to the diet, large quantities of fish were also consumed, as evidenced by fish bones and scales present at EH archaeological sites and isotopic signatures consistent with diets high in lake fish (Capriles et al. 2014; Juengst et al. 2021; Miller et al. 2010; Moore et al. 1999).

The household-level cultivation of plants was associated with the establishment of sedentary settlements, terraced field complexes, and civic architecture—all of which became increasingly elaborate during the Early Intermediate Period (EIP) (1–500 CE; Bandy 2004; Bruno and Whitehead 2003; Capriles et al. 2014; Chávez 1988; Chávez 2004; Roddick et al. 2014; Moore 2011; Moore et al. 2007). Quinoa and newly introduced maize became more common throughout the lake basin (Bruno and Whitehead 2003; Chávez and Thompson 2006; Murray 2005; Stanish 2003; Whitehead 1999). This reliance on terrestrial plants complemented a decrease in fish consumption (Capriles et al. 2014; Juengst et al. 2021).

It is clear from the archaeological evidence that diets and subsistence strategies shifted between the Preceramic and the EH/EIP. Alongside these dietary changes, people were modifying the landscape, creating terraces and permanent dwellings. All of these changes would have impacted the microbe-scape as well. Preceramic foragers were likely exposed to various zoonotic pathogens by eating lake fish and other wild animals, and they increased their exposure as they spent more time with camelids. As EH and EIP peoples began to rely on domesticated crops and animals and to permanently live in one place, they escalated their exposure and risk of zoonotic disease.

Discussion

Differences in pathological lesions and stature suggest that Titicaca Basin foragers and farmers experienced different microbe-scapes. Preceramic Period individuals were significantly less likely to develop periosteal reactions and more likely to achieve greater adult stature. These patterns of paleopathology and stature suggest that they encountered fewer stress-inducing pathogens, despite their regular interactions with animals. It is possible that a lack of pathology reflects rapid mortality, with these individuals dying from diseases prior to forming lesions (Wood et al. 1992). While we cannot entirely reject this scenario, the overall height and robusticity of the Preceramic individuals suggest that they were overall well-nourished and physically fit and that they should have been able to combat infectious disease. Likely, the lack of pathology among Preceramic foragers related to their residential mobility, which limited parasitic load and re-infection of individuals from others or animals.

Conversely, Early Horizon and Early Intermediate Period peoples lived in permanent villages and increased their contact with domesticated animals, including camelids and guinea pigs. The increase in periosteal reactions and decrease in adult stature suggest that this group was exposed to more pathogens and suffered from infectious disease more regularly. Notably, the rate of periosteal reactions observed for this group (44%) is higher than for many other forager and agricultural Andean groups (Andrushko et al. 2006; Gómez Mejía 2012; Klaus and Tam 2009; Lowman et al. 2019; Suby 2020; Ubelaker and Newson 2002; Williams and Murphy 2013). While rates of osteomyelitis and linear enamel hypoplasia were not statistically more common among EH and EIP burials, it is notable that the Preceramic individuals did not present either of these conditions. This may be a sample size issue, but given the increase in periosteal reactions and decrease in stature, we suggest that these lesions reflect a true difference in experiences with infection and childhood stress.

The new subsistence strategies and settlement patterns of EH and EIP peoples created opportunities for microbe transmission that were enhanced through sedentism. While we cannot determine exactly what microbes were causing disease for this group, we can imagine that changing contact rates with other people and animals and physically changing the landscape created new microbe-scapes unique to this place and time. For instance, direct transmission of pathogens from animal to human or human to human was possible based on new subsistence and settlement patterns. With domesticated guinea pigs and camelids, people spent more time near these animals, providing more opportunities for zoonotic diseases to mutate into human pathogenic forms (Muehlenbein 2016).

In addition, as seen elsewhere, sedentary settlements promoted waste accumulation that people with more mobile lifeways avoided. Additional risks for new EH and EIP farmers may have included the use of waste as fertilizer for newly created agricultural terraces (Chávez 2012) and/or camelid dung as a fuel source (Moore et al. 2007). Since wood is scarce at this altitude, camelid excrement may have been seen as a convenient fuel source and as relatively easy to collect from domesticated herds (Moore et al. 2007). By interacting more closely and regularly with human and animal fecal matter, risk of pathogen exposure and likelihood of transmission were elevated for these farmers.

Decreases in stature associated with agriculture are commonly documented around the world (Cohen and Armelagos 1984; Larsen 1995; Mummert et al. 2011) and in South America as well (Ubelaker and Newson 2002; Verano 1997). Traditionally, these decreases in stature have been broadly linked to the poor nutrition most commonly available from agricultural diets. Recently, Jonathan C. K. Wells and Jay T. Stock (2020) argued that the increased burden of disease associated with sedentary settlements and the change in diet prompted adaptations in life history and growth trajectories, with bodies allocating more energy toward reproduction and immune defense rather than investing in maintenance or growth. This interpretation also accounts for increased periosteal reactions as evidence of stronger immune defenses, as people were able to combat pathogens longer (Wells and Stock 2020). In brief, the increased burden of infectious disease with sedentary settlements prompted a lifelong adaptive change in resource allocation that has global implications.

Across the Andes, while some parasites had great antiquity, the frequency of intestinal parasite infection likely increased with sedentary settlements and agricultural diets (Verano 1997). Interestingly, this has not always coincided with decreases in overall health; there was no documented paleopathological change after the introduction of agriculture and camelid pastoralism in coastal Chile (DiGangi and Gruenthal-Rankin 2019). Continued health in that case was attributed to ongoing use of marine resources, which buffered the stress of agricultural diets. It is also possible that parasitic load was already elevated prior to the introduction of agriculture, based on evidence of fish-borne parasites (Araújo et al. 2011). In the Titicaca Basin, we also do not observe a decrease in nutritional health (Juengst et al. 2017b); however, in this case, it does not seem that adequate diets were able to buffer the other stresses of sedentism.

While stature decreased overall for EH and EIP peoples, females were especially impacted. Interestingly, during the Preceramic, there was no statistical difference in stature between male and female individuals. While humans typically do exhibit some sexual dimorphism in height, patterning of human sexual dimorphism is tied to many variables such as genetics, diet, and climate (Gray and Wolfe 1980; Gustafsson and Lindenfors 2009). Here, a new trend in sexual dimorphism emerged during the EH and EIP, with particularly short females. This could be due to a number of factors. First, EH and EIP females may have been particularly at risk of childhood infections or malnutrition, stunting their stature attainment. However, pathological lesions do not vary significantly between male and female individuals, and previous isotopic studies do not show significantly different diets for males and females during this time (Juengst et al. 2021).

Another possible explanation is the energy toll of menarche and pregnancy. This correlates with Wells and Stock’s (2020) life history hypothesis: due to the elevated pathogen load and changed nutritional source, energy was devoted to reproduction over growth. Rather than accelerating growth in stature during adolescence, female bodies may have diverted energy toward supporting reproductive processes and immune defense. Males may not have experienced these pressures as strongly, as their bodily energy investment in reproduction is comparatively less (Ellison 2003). Thus, adult females experienced growth stunting more strongly than males, reflected in the stature differentials presented here.

Conclusion

Overall, we can see that Preceramic foragers and EH and EIP agricultural communities navigated different microbe-scapes, which influenced the health and energy allocations of these peoples for both individuals and groups. Preceramic foragers were not immune to pathogens, likely acquiring parasites from wild camelids, cats, and fish through eating contaminated meat and exposure to feces. However, it is clear that the shift toward sedentary settlements and associated increases in contact with other people, domesticated animals, and fecal matter elevated pathogen load for EH and EIP communities. The combination of exposure to zoonoses, waste, and increased circulation of pathogens between sedentary groups likely resulted in elevated pathogen load for EH and EIP peoples, as reflected by the increase in lesions and decrease in height.

Even though most pathogens are not visible to the human eye, they are capable of having dramatic effects on human lives. Human relationships with these tiny organisms correlate with relationships to other natural forces, including animals, plants, and landscapes. These relationships can promote or limit the impact of disease on human groups, depending on how humans structure their economic, political, and social settings. Importantly, rarely do diseases affect groups evenly—some members of society (in this example, females) often feel the weight of pathogenic burdens more heavily. Understanding how human habitats and lifestyle choices alter microbe-scapes is vital because current human groups still struggle to prevent and control disease outbreaks and because these patterns can potentially reveal underlying social inequities in human societies.

References