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2012 Synthesizing Parasitology with Archaeology in Paleopathology Karl Reinhard University of Nebraska-Lincoln, [email protected]

Adauto Araujo Escola Nacional de Saúde Pública, [email protected]

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Reinhard, Karl and Araujo, Adauto, "Synthesizing Parasitology with Archaeology in Paleopathology" (2012). Karl Reinhard Papers/ Publications. 64. http://digitalcommons.unl.edu/natresreinhard/64

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Synthesizing Parasitology with Archaeology in Paleopathology Karl J. Reinhard and Adauto Araújo

Parasites furnish information about present day habits and ecology of their individual hosts. The same parasites hold promise of telling us something about host and geographical connections of long ago. They are simultaneously the product of an immediate environment and a long ancestry reflecting as- sociations of millions of years. Eventually there may be enough pieces to form a meaningful language which could be called parascript—the language of parasites which tells of themselves and their hosts both of today and yesterday. (Harold Manter 1966:70)

Introduction reconstruction of Albany, NY, based on analysis of medical documents, artifacts such as medicine bot- Parasitology is the study of organisms that are symbi- tles, archaeochemical analysis of sediments for evi- otic with other organisms. In this form of symbiosis, dence of medicines, reconstruction of sanitation, and the parasite species by definition benefits from the in- direct analysis of parasite eggs from various domes- teraction while the host is harmed to some degree. In tic contexts. In addition, archaeopalynology (Chaves actuality, some parasites benefit their hosts. The an- and Reinhard 2006) and archaeobotany (Reinhard et al. imals traditionally studied by parasitologists range 1985) reveal evidence of medicines used to treat par- from protozoa to arthropods, and include all types of asitic disease symptoms. In short, archaeoparasitolo- internal and external worms. Ticks, fleas, lice, and a gists sift through every imaginable type of archaeo- variety of insects that transmit parasites are also stud- logical residue that can provide any insight into the ied by parasitologists. Recently, a more holistic view culturally defined relationship between human hosts of parasitism appeared, including bacteria and viruses. and parasites. In doing so, we decipher the unique par- In essence, parasitology is the study of a certain kind ascript specific to human-parasite cultural evolution. of biological relationship that is very common in the natural world. The Americas and Archaeoparasitology Humans host hundreds of parasite species. The de- tails of the relationship between any parasite species Archaeoparasitology is a fusion of archaeology and and humans are defined by culture. Archaeology is the parasitology (Horne 1985). In North America archaeo- study of past humans and human culture. Therefore, parasitology began with excavations by archaeologists archaeoparasitology is the analysis of parasitism based such as J. Richard Ambler, Robert Heizer, Cynthia Ir- on archaeological evidence. As defined by Reinhard win-Williams, Jesse Jennings, Don Morris, Art Rohn, (2000a) and Reinhard and Araújo (2007), archaeopar- Steve Mrozowski, and Harry Shafer. These archaeolo- asitology derives data from physical evidence such as gists, among others, recognized the importance of cop- artifacts, documents, and art. In addition, ecoartifacts rolites for detailed data regarding diet and disease. such as coprolites, sediments, and human remains pro- Each of them focused graduate students and parasitol- vide direct evidence of parasitism. Fisher et al. (2007) ogists on analysis of coprolites. Thus, the distinct link- provide a holistic example of archaeoparasitological age of parasitological data to archaeological questions

751 752 R e i n h a r d a n d A r a ú j o i n A G l o b a l H i s t o r y o f P a l e o pa t h o l o g y (2012) comes from these researchers who took the relevant re- development of sanitation, and the overall health of mains from the field into the laboratory. prehistoric peoples adapting to a diversity of arid en- In the Great Basin, Robert Heizer (Hester 1982) vironments. Thus, the sponsorship of parasitological and Jesse Jennings (Aikens 1999) were prolific field re- research by archaeologists resulted in a distinct focus searchers. Jennings and his students excavated copro- of archaeoparasitology on human questions. lites from Danger Cave, Hogup Cave, Cowboy Cave, Dirty Shame Rockshelter, and other lesser known Archaeoparasitological Studies sites, including a number of sites in Glen Canyon. They were the first to analyze coprolites for dietary There have been distinct phases to archaeoparasitol- and parasite evidence collaborating with a parasitolo- ogy: exploratory (1910 to 1974), population (1976– gist, John Moore. Heizer excavated in the Great Basin 1987), and synthesis of archaeology and parasitology of Nevada and directed the California Archaeological (1987 onward). The exploratory phase was most influ- Survey at the University of California at Berkeley. He enced by the archaeologists noted above. Studies of promoted the interdisciplinary analysis of coprolites, ancient parasites, like many fields of paleopathology, especially those from Lovelock Cave. The late 1960s began as series of isolated case studies. In this explor- and the decade of the 1970s saw a shift of focus from atory phase, the discoveries were by themselves note- the Great Basin to the Ancestral Pueblo region of the worthy, and sometimes sensational, due to the novelty Colorado Plateau. National Park Service archaeologists of recovering parasites from archaeological remains. Art Rohn and Don Morris excavated coprolites from The exploratory period was rapidly supplanted by a Mug House, Mesa Verde, and Antelope House, Can- period of population comparison over geographic re- yon de Chelly, respectively. Cynthia Irwin-Williams gions, again influenced by these same archaeologists. (Wormington and Agogino 1994) also excavated cop- The synthesis phase was represented by the synthesis rolites from Salmon Ruin, and J. Richard Ambler, a stu- of “parasitological theory” and archaeology. Parasito- dent of Jennings, excavated coprolites from the region logical theory generated theoretical frameworks that of Navajo Mountain and Glen Canyon. were used to interpret archaeological parasite remains. Beyond the Ancestral Pueblo homeland, Harry Sha- fer, Vaughn Bryant, Donny Hamilton, and other Texas Early Exploration archaeologists were excavating coprolites from west Texas. Hundreds of coprolites were recovered from The exploratory phase began with the first parasitolog- Hinds Cave, Baker Cave, and other rockshelters in the ical study of archaeological remains in the Old World region. These researchers collaborated with parasitol- (Horne 1985). Ruffer (1910) reported the find of blood ogists and directed research into prehistoric parasit- fluke eggs in Egyptian mummies. In Diseases in An- ism among Texas hunter-gatherers (Reinhard 1990). tiquity, Brothwell and Sandison (1967) added parasi- Steve Mrozowski pioneered the scientific study of tology as a distinct part of paleopathology. Sandison latrine sediments from historic sites (Reinhard et al. (1967) described the relevance of the field to paleopa- 1986). He promoted the study of parasite eggs from thology, summarizing evidence from art and litera- latrine sediments. His focus was on the integration of ture. Taylor (1955) described the value of parasite ex- parasitological, palynological, and macrobotanical ev- amination of latrine sediments in medieval England, idence with historical documentation of urban devel- and Lambrecht (1967) summarized the evidence for the opment (Mrozowski 2006). Thus, Mrozowski’s efforts evolution of African sleeping sickness from South Af- inspired the search for evidence of parasitism in indus- rican ecological data. Alongside parasitological study, trializing societies. W.H.S. Jones (1967) examined ancient Greek texts to Because archaeologists directed the research, par- describe the antiquity of malaria in Greece. Later, di- asitological data addressed archaeological problems rect evidence of parasites was presented from latrine in North America (Reinhard 1992a). In a broad sense, excavations in Denmark (Nansen and J0rgensen 1977) the archaeological questions focused on zoonotic par- and England (Pike 1975). Samuels (1965) analyzed cop- asitism related to hunter-gatherer dietary practices, rolites from Mesa Verde, Colorado, and established zoonotic diseases from domestic animals, increase in protocols for laboratory analysis. Pike (1968) published human-specific crowd disease among farming peo- the results of analysis of parasitological examination of ples, transhumance patterns, cultural contact, paleo- Roman sites and showed the value of eggs in making pharmacology related to anthelmintics (vermifuges), cultural interpretations regarding ancient sites. S y n t h e s i z i n g P a r a s i t o l o g y w i t h A r c h a e o l o g y i n P a l e o p a t h o l o g y 753

These discoveries stimulated the interest of Amer- transition from hunter-gatherer populations to farm- ican archaeologists. Coprolites from Great Basin sites ing communities. Cockburn proposed that species were the focus of defining publications in the explor- that occasionally infected hunter-gatherer became ma- atory phase. Heizer and Napton ( 1969) summarized jor health hazards in agricultural communities. Cock- the analyses of coprolites from Lovelock Cave, Ne- burn also postulated a decline in food-borne zoonotic vada. At this site, archaeoparasitological study re- infections with agriculture. Both of these hypotheses vealed no evidence that hunter-gatherer lifeways lim- were verified by coprolite analysis. Thus, archaeopar- ited parasitism in some areas (Reinhard 1988). The asitology was established in population studies in arid antiquity of parasites was demonstrated by Fry and North America (Reinhard 1992b). Hall (1969), Fry and Moore (1969), and Moore et al. Population studies began in other regions from the (1969). In contrast to Lovelock Cave, Utah Great Basin 1970s onward. In Brazil, Luiz Fernando Ferreira di- hunter-gatherer coprolites were positive for zoonotic rected Adauto Araújo and Ulisses Confalonieri in a and human-specific parasites. Fry and Hall (1969) re- search for parasites in South American remains. Their ported the discovery of pinworm eggs in a 10,000-year- work resulted in the definition of the distribution of old coprolite from the Great Basin of Utah. Moore et al. ascarid, whipworm, and hookworm infections. In (1969) reported the discovery of acanthocephalans, also Peru, Duccio Bonavia working with archaeologists in the Great Basin, in 10,000-year-old coprolites. These Raul Patrucco and Raul Tello analyzed series of cop- early coprolite discoveries were sensational enough to rolites (Patrucco et al. 1983) and defined the antiquity be published in Science. Following Pike’s 1968 paper in of parasites in that region. In England, AKG Jones Nature, such publications illustrate that the novelty of (1979; 1982; 1983, 1985; 1986; Jones and Nicholson ancient parasite discoveries was so impressive that iso- 1988; Jones et al. 1988) built on pioneering work by lated case studies were published in the most presti- Pike (1967, 1975), Sandison (1967), and Taylor (1955) gious outlets. This inaugurated a line of research that to explore regional distributions of parasites in medi- focused on the search for zoonotic parasites, especially eval urban settings from England to Norway. He de- among hunter-gatherer remains. fined methods and theory for parasitological inves- Exploratory work in South America was also sen- tigations of latrine sediments. By comparing the egg sational. Allison et al. (1974) published the remark- quantities between archaeological deposits, he was able discovery of adult hookworms in a prehistoric able to document variation associated with different Peruvian mummy. Eggs were recovered from the in- site functions. He also showed that parasite eggs were testinal lumen and adult hookworms were found ad- part of the normal medieval urban background fauna herent to the intestinal mucosa. This was followed by and, thus, exposure to parasite infection was an un- a series of discoveries of hookworms in Brazil (Araújo avoidable aspect of medieval life. Furthermore, Bernd et al. 1981; Ferreira et al. 1980, 1983). These discov- Herrmann (1985, 1986) developed a quantitative anal- eries contradicted the prevailing conventional wis- ysis of German medieval villages to trace the distri- dom that hookworm was a historic introduction into bution of parasite species. the New World. The work of all of these pioneer- Researchers of the population phase had diverse ing researchers established parasitology as a part of theoretical perspectives. Jones’ theoretical framework paleopathology. emerged from environmental archaeology as practiced in the 1980s at the University of York’s Environmen- Comparison Between Populations tal Archaeology Unit, established formally in the mid- 1970s. It was composed of a variety of specialists who Population studies emerged in 1976 as students of Jen- sought to integrate diverse biological data sets to es- nings, Ambler, Shafer, and Bryant began their careers. tablish solid, holistic interpretations from archaeolog- Gary Fry (1977, 1980) and Henry Hall (1972, 1977) ical deposits. In addition, theoretically, Herrmann and completed their graduate work on coprolites from the Schulz (1986) defined the interpretive variables at play southwestern US. They established standard proto- that described parasite egg spectra in latrine sediments. cols for coprolite analysis that were followed by sub- These included the social group or groups that used sequent researchers. They also completed comparative specific latrines, the demographic makeup of those studies for hunter-gatherer sites and Ancestral Pueblo groups, differential egg production between species, sites in the Great Basin and the Colorado Plateau. Re- and the effects of soil chemistry and decay organism inhard (1985a, b, 1988) built his work on Cockburn’s on egg preservation. (1971) theory and defined the archaeoparasitological 754 R e i n h a r d a n d A r a ú j o i n A G l o b a l H i s t o r y o f P a l e o pa t h o l o g y (2012)

Horst Aspöck at the University of Vienna pioneered infection on an individual basis by calculating the archaeoparasitology in Austria (Aspöck, 2000). He and maximum number of eggs and nits cemented to hair his colleagues first analyzed parasite eggs from Otzi, shafts on the scalps of mummies. Lice nits and eggs the Iceman (Aspöck et al. 1995, 1996). Later, they pub- were quantified in 147 mummified individuals (Rein- lished a summary of the antiquity of parasite infection hard and Buikstra 2003). The distribution of nits and in central Europe (Aspöck et al. 1999). Trichuris trich- eggs on Chiribaya hosts reflected the negative bino- iura is the most ancient parasite and has been dated mial. This supports the statistical value of parasitolog- as early as 5,500 years ago, with Ascaris lumbricoi- ical data when large numbers of human remains can des and the hookworm Ancylostoma duodenale being be evaluated. dated to 3,500 years ago, the fish tapeworm, Diphyl- Beyond the epidemiological consistency of archae- ological data, other purely detailed epidemiologi- lobothrium, and the sheep liver fluke, Fasciola hepat- cal work was undertaken. Until the 19808, theories of ica, to 5,100 years ago, and the taeniid tapeworm and parasitology and epidemiology played small roles in the lancet liver fluke,Dicrocoelium dendriticum, dated the investigations of ancient parasitism. However, this to 2,000 years ago. changed with the incorporation of the theoretical con- In Japan, Matsui and his colleagues explored the an- structs of Cockburn (1971) and Pavlovsky (1966), as tiquity of parasitism from Jamon context to medieval reviewed by Reinhard (2008) and Reinhard and Bry- times (Matsui et al. 2003). This was an interdisciplin- ant (2008). Aidan Cockburn’s perceptions about the ary team that included experts in parasitology, zoo- sources of disease directed the development of par- archaeology, palynology, and archaeobotany. Within asitological study of Archaic and Ancestral Pueblo a few months of research, they identified a range of sites in the Southwest US. Cockburn (1967, 1971) pro- parasites including ascarid roundworms, whipworms, posed that the evolution of infectious diseases was de- Yokogawa flukes, Chinese liver flukes, and the beef termined by the evolution of human social complex- or pork tapeworms. By integrating the parasite evi- ity. Cockburn’s theories motivated Reinhard (1985a) dence with the other areas of expertise, they identified to test Cockburn’s ideas with archaeological remains. the use of anthelmintics and related patterns of diet Reinhard viewed the prehistoric Southwest as an ideal to disease, and immigration of people to Japan from experimental setting because there were several stages other countries. The development of sanitation in Ja- of cultural development represented by archaeologi- pan was defined. cal sites: hunter-gatherers with varying dietary strate- gies, dispersed horticultural hamlets, and large agricul- A Synthesis of Parasitology and tural villages. Reinhard (1985a, 1992 b) compared the Archaeoparasitology parasitic picture of Colorado Plateau Archaic peoples Overviews of parasitological theory are presented by to Ancestral Puebloan sites. He reified some of Cock- Price (1980) and Brooks and McLennan (1993). Synthe- burn’s theories that occasional infections in hunter- sis of parasitological theory and archaeological practice gatherers became major health hazards in agricultural emerged over a long period of time. The process was populations. Reinhard (1988) included the following sporadic as archaeological investigations recovered ap- explanations of why parasitic disease arose in Ances- propriate material for different aspects of the synthesis. tral Puebloans relative to earlier hunter-gatherers. Par- Perhaps most essential was a demonstration that asitism was limited in hunter-gatherers due to small prehistoric patterns fit the epidemiological features band size, its mobility, diffuse regional populations, of modern parasitic infection. Parasites are over-dis- and presence of natural anthelmintics. Hunter-gath- persed in natural populations. This means that a very erer parasitism was promoted by the consumption of small percentage of hosts harbor the majority of par- uncooked meat and insects. Parasitism was promoted asites. In parasitological terms, this phenomenon is in Ancestral Puebloan communities by contaminated best described by the negative binomial distribution water sources, concentrated populations, a more sed- (Anderson 1993). In order to validate the paleo epi- entary life, apartment -style living, establishment of demiological value of archaeoparasite data, this dis- large latrines, activities centered on water (agriculture), tribution had to be demonstrated with archaeological and activities that expanded wetlands, including irri- remains. Mummies of the Chiribaya culture of Peru gation of all types. were selected for study. Previously, Mumcuoglu and The work of E.N. Pavlovsky (1966), an epidemi- Zias (1988) had found lice nits in ancient louse combs. ologist, had a less immediate influence on archaeo- Reinhard and Buikstra (2003) were able to quantify parasitology. Pavlovsky developed the “doctrine of S y n t h e s i z i n g P a r a s i t o l o g y w i t h A r c h a e o l o g y i n P a l e o p a t h o l o g y 755 nidality,” deriving the term from the word “nidus” that the evolution of parasites parallels the evolution (plural “nidi”), which means “nest:’ (Many subsequent of their hosts. Therefore, the phylogeny of some para- researchers synonymize “nidus” with the Latin “fo- site taxa is congruent with the phylogeny of their host cus”). The doctrine of nidality establishes that each in- taxa. Thus, heirloom parasites have very ancient evo- fection results from the favorable overlap of host fac- lutionary origins. tors, parasite factors, and environmental factors, at the Souvenir parasites are those acquired relatively very least. The nidus is the specific area or focus of that recently in human prehistory through the break- interaction that results in infection. The key concept of down of ecological, behavioral, or geographical bar- nidality is that disease transmission has its own natural riers between humans and a parasite species. Sprent habitat. Thus the nidus exists under definite conditions (1962, 1969) specified animal domestication as a main of climate, vegetation, soil, and favorable microclimate source of souvenir parasites. Parasitological evidence in which host, pathogens, vectors, and reservoirs are from archaeological sites shows that heirloom para- associated as a biocenosis. The nidus can be permanent sites such as hookworm, whipworm, pinworm, and or seasonal. Humans can acquire a natural-nidal dis- a few other species do have a pre-Homo sapiens ori- ease of animals when they occupy or pass through bio- gin. The majority of parasites in archaeological sites cenoses of that infection. Pavlovsky applied the doc- are geographically circumscribed souvenir species. trine of nidality to explain the transmission of plague, Such souvenirs include thorny-headed worms in the tularemia, leptospirosis, arboviruses, tick-borne relaps- Great Basin (Moore et al. 1969), intestinal flukes in ing fever, and other diseases. Brazil (Sianto et al. 2005), ticks in northwestern Ari- The term pathoecology was coined by Karl R. Re- zona (Johnson et al. 2008), and fish tapeworm infec- inhard in 1974 (K.R. Reinhard 1974a, b). K. R. Rein- tion on the Pacific coast of Chile and Peru (Callen and hard, as an epidemiologist who worked on the history Cameron 1960). of infectious diseases in modern populations, applied Archaeoparasitology contributed to understand- pathoecology to the integrative study of historic cli- ing the evolution of the strategies of parasites. Un- mate and health records to define the impact of cli- til the 1990s, the general notion was that parasites mate variability on health patterns. Because statisti- evolved over time to have benign relationships with cally rigorous epidemiological data were not available their hosts and to develop a high degree of host spec- for these early historic periods, K. R. Reinhard (1974a) ificity. Parasitological work eventually showed that a suggested the term “retrospective pathoecology” for high degree of host specificity is lacking in most para- application to reconstructing the ecology of past dis- sites of humans. Of the 342 species of helminths clini- ease. The nidus concept, combined with the concept cally known to infect humans (Crompton 1999), only of pathoecology, is especially useful in exploring in- the beef tapeworm, pork tapeworm, hookworm, pin- fectious disease transmission evidenced in archaeo- worm, whipworm, and ascarid roundworm exhibit logical sites. high specificity to humans. The other hundreds of hel- As proposed by Martinson et al. (2003), Reinhard minth species that infect humans also infect other host (2008), and Reinhard and Bryant (2008), nidi can be dis- species. Most recently, Johnson et al. (2009) presented cerned in careful excavations in combination with eco- phylogenetic and experimental support of the hy- logical reconstruction. Nidi can be as finite as a Giar- pothesis that host specificity is an ancestral condition. dia-contaminated water point, or a single cave where Generalists evolved from specialist ancestors. Agosta cooking debris left by humans creates the biocenosis et al. (2010) present a case that there are pulses of gen- for Chagas disease transmission, or as large as a hu- eralization as parasites switch hosts. They assert that man feces-contaminated agricultural field where hook- climate changes and large-scale ecological perturba- worms complete embryonation in irrigated soil and ac- tions drive the mixing of species that increases rapid complish infection of sandal-wearing farmers. host switching. Both perspectives are borne out in the Another basic parasitological theoretical concept archaeological record. The majority of parasites found relates to souvenir and heirloom parasite taxa. Orig- in the archaeological record are opportunistic species inally defined by Sprent (1969), these concepts are that are generalists and therefore infect a variety of widely used by other parasitologists. Heirloom par- hosts. Humans became infected with them when they asites evolved from ancestral parasite species hosted intruded into nidi where these parasites existed. In by primate common ancestors of modern apes and hu- short, humans create their own ecological perturba- mans and even earlier mammalian ancestors. This fol- tions when they move into a new environment and lows the Fahrenholtz’s rule (Price 1980), which states change it through exploitation, agriculture, or animal 756 R e i n h a r d a n d A r a ú j o i n A G l o b a l H i s t o r y o f P a l e o pa t h o l o g y (2012) domestication. In these situations, zoonotic parasites Another example of paradigm shift resulting from ar- switch to humans. In contrast, the human-specific chaeological data is represented by investigation of parasites, such as hookworm, pinworm, and whip- Chagas disease as reviewed by Araújo and colleagues worm have been shown to be very ancient human- (2003, 2009). Chagas disease was once thought to have specific species, dispersed in antiquity throughout emerged in Andean cultures after animal domestica- the prehistoric world with human migrations. Inter- tion, but the growing body of evidence shows that estingly, it was once thought that Ascaris lumbricoides Chagas disease was distributed in North and South evolved in humans from the pig species Ascaris suum. America before agriculture. There are similar para- The discovery of ascarid eggs in 30,000-year-old hu- digm shifts for many other species (Reinhard 1990, man coprolites shows that humans were infected be- 1992a; Sianto et al. 2005, 2009). fore pig domestication and therefore this human-spe- cific parasite has an ancient evolutionary history with humans. Even the human-specific tapeworms noted Parasites and Paleopathology above evolved in ancient times, before the evolution Barrett et al. (1998) painted a picture of the state of of the genus Homo. Phylogenetic and ecological anal- human parasitism from a paleopathological perspec- ysis shows that these tapeworms evolved from inter- tive in broad-brush strokes. In their review, they define action between hominids and suids a million years three paleoepidemiological transitions, two of which ago (Hoberg 2006). occurred in the remote past. These include a rise in in- In an evolutionary context, Ferreira and his col- fectious diseases associated with the Neolithic Revo- leagues based their work on the parasitological theo- lution, and a shift from infectious to chronic disease ries of the times presented by Fonseca (1972) and Man- mortality associated in industrialized societies. Both ter (1967), who argued that the Arctic would prevent of these followed a Paleolithic pattern of low levels of the entry of pathogens into the New World with hu- parasitism in dispersed hunter-gatherer groups. Us- man migrations. According to the theory of heirloom and souvenir parasites, the most common modern ing archaeoparasitological data, we can fill in the de- parasites of humans, such as giant roundworm, whip- tails of these transitions, especially using archaeolog- worm, hookworm, and various flukes and tapeworms, ical data from the Americas. New World archaeology would have been absent in the New World because provides an ideal “laboratory” for the recovery of par- they could not have survived the migration of humans asites marking the transitions noted by Barrett et al. to the New World. By analyzing mummies and copro- (1998). Since hunter-gatherer, Neolithic, and industrial lites, Ferreira’s researchers discovered abundant evi- sites have been excavated for parasitological data, fur- dence of hookworm and whipworm infection (Araújo ther details can be added from Old World archaeolog- et al. 1981; Ferreira et al. 1980, 1983), disproving the hy- ical work. pothesis that a Beringean cold filter prevented the en- Barrett et al. (1998) note that “long-term coevolu- try of parasites (Araújo et al. 2008). tionary relationships between hominids and a heir- The use of archaeological parasites to evaluate para- loom parasite imply a good match between the par- sitological theory leads to a single conclusion from sev- asite’s mode of transmission, virulence, and lifecycle, eral perspectives. The evolution of heirloom, human- and the lifestyle and demographics of early foraging specific roundworms and tapeworms occurred very bands” (Barrett et aI1998:251). They suggest that pin- early in hominid evolution. The overwhelming num- worm and lice would be among the oldest of human ber of helminth parasites known from the archaeolog- parasites. These extremely intimate parasites of hu- ical and clinical literature are generalist souvenir para- mans would easily migrate to, and stay established sites that opportunistically infected humans as humans in, human populations in any biome. The archaeo- intruded into a variety of diverse nidi. parasitological work bears this out. Pinworm (Rein- Archaeoparasitology has redefined our percep- hard 1990) and lice (Araújo et al. 2000) arrived in the tions of the emergence and introduction of parasites New World with Paleolithic migrations. Interestingly, into the New World. Hookworm was once thought to whipworm, wireworm (Strongyloides stercoralis), and have been introduced into the New World with Af- hookworm also arrived with the earliest pre-Clovis rican slaves. As reviewed by Cox (2002), this percep- migrations (Araújo et al. 2008). Ascaris lumbricoides tion persisted for many years but has been dispelled has also been found in Paleolithic coprolites in France by hookworms recovered from archaeological sites. (Bouchet et al. 1996). The combined data shows that all S y n t h e s i z i n g P a r a s i t o l o g y w i t h A r c h a e o l o g y i n P a l e o p a t h o l o g y 757 of the heirloom, human-specific roundworms devel- The impact of early industrial societies can be eval- oped before or during Paleolithic times. The data also uated by analysis of latrine sediments from historical show that souvenir, generalist parasites also infected sites in the Americas. The arrival of Europeans resulted Paleolithic hunter-gatherers. Thorny-headed worms in the introduction of fecal-borne helminthiasis. Whip- and tapeworms are also found to have infected hunter- worm and ascarid eggs are present in latrines from ev- gatherer bands more than 10,000 years ago in Utah (Fry ery town and city from the Colonial Period onward 1977). However, as suggested by Barrett, early popu- (Fisher et al. 2007; Raymer and Reinhard 2006; Rein- lations were too small and dispersed to be chronically hard et al. 1987; Reinhard 1990, 2000b). Fisher et al. infected. This is borne out in New World archaeology (2007) studied in detail the emergence of fecal-borne by the fact that most hunter-gatherer coprolite series parasitism from colonial times to the 20th century in are nearly parasite-free (Reinhard et al. 1985; Reinhard Albany, New York, and showed that fecal-borne geo- 1992b). Therefore, for many parasite life cycles, hunter- helminths dominated. Infection peaks in the working gatherer behavior limited transmission only for those class neighborhoods in the 19th century. Other work parasite species that were tightly coevolved with hu- shows that parasitism in cities such as New York (Re- mans. The evolutionary pressure on human evolution inhard 2000b) and Philadelphia (Raymer and Rein- has also been explored for some parasites. Lambrecht hard 2006) was extremely common. Unpublished re- (1980, 1985) presented a particularly convincing case ports on file with Reinhard show decreased parasitism that forms of African sleeping sickness had a differen- in smaller towns, and absence of parasitism in rural tial role in the evolution of human resistance to the dis- farms. Therefore, the archaeological data recovered ease in different regions of Africa. from a variety of sites supports the general picture of The “Neolithic Revolution” is represented in the the emergence of parasitic disease proposed by Bar- Americas by many horticultural sites excavated in rett et al. (1998). drier regions. These sites contained mummies and coprolites, which have been extensively studied. In re- views of parasitic data, it is clear that horticulture and Current Centers for Archaeoparasitology sedentism did not by themselves result in a rise in par- asitism. The level of parasitism depended on a variety Archaeoparasitology training has foci in Canada and of factors including village plan, construction and lo- the United States. In keeping with the foundations of cation, use of irrigation versus dry farming, population the field, training is offered in archaeology or parasi- concentration, and the use of outdoor space (Hugot et tology programs. Allison Bain (2001) earned her doc- al. 1999: Reinhard 1990, 1992b, 2007, 2008; Reinhard torate at the Université Laval, Quebec, and currently and Bryant 2008). Prevalence and species diversity in- teaches in the environmental archaeology focus in the crease is associated with drought and environmental archaeology doctoral program at the same univer- collapse. The diversity of parasites among horticultur- sity. Her dissertation focus was on methods of recov- alists increased over hunter-gatherers and included ev- ery and interpretation of parasite eggs and insect re- idence of intestinal flukes, lung flukes, hymenolepidid mains. Rhonda Bathurst earned her doctorate from tapeworms associated with grain storage, tapeworms McMaster University and is currently on staff at the from uncooked meat, thorny-headed worms from in- University of Western Ontario (Bathurst 200Sa, b). The sects, wireworms from human-dog association, dog work of these two archaeoparasitologists is innovative tapeworm cyst disease, giardiasis, amoebiasis, body in method, application, and interpretation. Bain (2001) lice, and crab lice. Strangely, fecal-borne helminthiasis offers a comparative evaluation of diverse processing represented by whipworm and ascarids was relatively and quantification methods and an overview of the rare in the horticultural societies of the Americas. This Significance of archaeoparasitology, especially in his- can be explained by use of anthelmintics and behav- toric contexts. Bathurst (2005a, b) integrates zooarchae- ioral patterns (Leles et al. 2010). Therefore, although ology and archaeoparasitology through an innovative the general picture of “Neolithic” parasitism is vari- auger test system at a variety of coastal sites. In the able, there are sites that show a dramatic increase in United States Susan Jacobucci is an archaeopalynolo- parasitism diversity, especially associated with devel- gist and archaeoparasitologist trained at the Univer- opment of empires (Santoro et al. 2003) and environ- sity of Massachusetts, Boston, and currently works at mental perturbations (Reinhard 2007). Bone pathology the Andrew Fiske Memorial Center for Archaeologi- such as porotic hyperostosis is additionally associated cal Research, University of Massachusetts, Boston, di- with sites with high parasite diversity (Reinhard 2007). rected by Steve Mrozowski (Gallagher et al. 2007). Her 758 R e i n h a r d a n d A r a ú j o i n A G l o b a l H i s t o r y o f P a l e o pa t h o l o g y (2012) integration of pollen and parasite analyses builds on Cultural Properties, Chungnam Institute of History a long-standing tradition (Hevly et al. 1979; Reinhard and Culture, Hangang Institute of Cultural Heritages, et al. 1986). At the University of Nebraska, Lincoln, ar- and the Seoul Museum of History, parasitologists are chaeoparasitology is taught at the School of Natural examining a variety of archaeological deposits includ- Resources and the Manter Laboratory of Parasitology. ing from privies, in tombs, and within mummified re- In the near future, the Manter Laboratory will archive mains. Their papers cover methodological issues, ad- archaeoparasitological samples to preserve important dress interpretive problems, and approach the knotty specimens for future researchers. problem of differential preservation of parasite re- Independent of these centers of training, US archae- mains in tombs. Seo et al. (2009) and Shin et al. (2009) ological contractors are offering services in archaeo- provide literature reviews of the many papers that parasitology. Some of the work by these individuals is have come out of the Korean archaeoparasitological substandard because of inadequate training. The more collaborations during recent years. Their work is char- common errors we see in the archaeological “gray liter- acterized by refined diagnostic techniques combined ature” is misdiagnosis of parasite species and failure to with meticulous association of parasites with well-il- quantify the remains in a meaningful way. Therefore, lustrated archaeological contexts. This excellent inte- the emergence of contract archaeoparasitology threat- gration of parasitology and archaeology sets the ideal ens the integrity of the field. Archaeologists would be standards for such research. wise to employ only those individuals who have grad- Brazil has the longest history in archaeoparasitol- uate training in archaeoparasitology. ogy (Chapter 40). By the end of the 1970s Luiz Fer- Europe has several active laboratories. Andrew K. nando Ferreira and colleagues had published their first G. Jones is in the process of returning to parasite re- contribution to the study of parasites in ancient ma- search at York Archaeological Trust. Jones and stu- terial, naming it Paleoparasitology, a contribution to the dents have been working in Pompeii, Italy, and have study of parasites found in archaeological material in Brasil recently found human helminth eggs in calcareous (Ferreira et al. 1979). After this pioneering work, they “tufa-like” deposits that accumulated inside waste committed to the study of parasites in archaeological pipes and at the entrance to deep rubbish disposal and paleontological material, aiming to contribute to pits dug before the eruption of the volcano Vesuvius the study of the origin and evolution of infectious dis- in 79 CE. Parasite eggs, fly puparia, fish bones, and eases, not only in humankind, but also in other ani- even sherds of pottery have been in these materials. mals. With the development of their studies, and col- The work shows that Romans were infected with par- laboration with other research groups, a network was asites, even after the use of complicated sanitation established, mainly with the University of Nebraska– systems become common. It is noteworthy that three Lincoln and with the Laboratoire de Paléoparasitol- research groups have been established in France. At ogie, at the University of Reims, in France. The col- the University of Perpignan, Claude Combes, and laboration among these three laboratories was very Henry de Lumley have analyzed archaeological cop- productive, with researchers and students participat- rolites collected from sites in the Old World. Fran- ing in diverse scientific events, both of parasitology, coise Bouchet has also established her laboratory at such as those organized by the American Society of the University of Reims. She has trained several doc- Parasitologists, the North American Congress of Par- toral and postdoctoral students from France and Bra- asitology, Federación Latinoamericana de Parasitolo- zil including Sophie Dommelier-Espejo, Stephanie gia, Sociedade Brasileira de Parasitologia, as well as the Harter, Matthieu Le Bailly, Gino Chaves da Rocha, Paleopathology Association, American Anthropologi- and Marcelo Gonçalves. Matthieu Le Bailly has a new cal Association, International Council for Zoo archae- position at the University of Franche-Comté, where ology, and the World Congress of Mummy Studies. the French Scientific Centre has enabled him to estab- In South America three other laboratories have lish a new parasitology lab. appeared recently. In Argentina, Ricardo Guich6n, a One of the most active centers for archaeopara- bioanthropologist, and Martin Fugassa, a parasitolo- sitology is in South Korea at the Anthropology and gist, have created a laboratory of paleoparasitology in Paleopathology Lab, Seoul National University Col- the Universidad Nacional de Mar del Plata, dedicat- lege of Medicine — http://shinpaleopathology. ing their studies to the Patagonian region. They are blogspot.com/2009/11/publications-and-other- studying infectious diseases among prehistoric groups achievements.html . In cooperation with archaeol- in Patagonia, and the impact of new parasites on native ogists from the Foundation for the Preservation of populations when Europeans arrived to establish new S y n t h e s i z i n g P a r a s i t o l o g y w i t h A r c h a e o l o g y i n P a l e o p a t h o l o g y 759 colonies. Methodological contributions include exam- Anthropology Laboratories to recover ancient DNA ination of museum-curated sacra for parasites and the from coprolites. Preliminary work focusing on gut comparative analysis of burial sediments. bacteria has been published. (Tito et al. 2008) and At the University of Tarapad., Arica, in Chile, Ber- analysis of helminth DNA is ongoing. nardo Arriaza has created an archaeoparasitology re- search line to recover parasites in prehistoric popu- Conclusion lations who lived on the north coast of Chile. He is combining archaeology, anthropology, and parasitol- The interdisciplinary interest in archaeoparasitology ogy to understand the life of people who lived in the has created contributions in several areas. Work in the Atacama Desert, especially the Chinchorro (Arriaza et exploratory period and population study phases con- al. 2010). tributed to understanding the prehistoric distribution In Peru there is a recent proliferation of archaeo- of parasites and established an idea of the relative par- parasitology centers. Sonia Guillen at the Centro asite burden different cultures experienced in prehis- Mallqui has long fostered archaeoparasitological re- tory. These phases focused primarily on archaeological search (Holiday et al. 2003; Dittmar et al. 2003). Jane problems such as transhumance (including migra- Wheeler, now of CONOPA (an independent Peruvian tions), resource exploitation, anthelmintic parasite con- institution primarily dedicated to scientific research trol, sanitation, and other issues. The synthesis phase and development of the South American camelids, integrated archaeological data into developing parasi- established in 2001), conducted extensive parasito- tological theory established by Sprent and others. Ar- logical examinations of mummified llamas at San chaeoparasitology was especially relevant to defining Marcos’ Faculty of Veterinary Medicine in Lima. Her which parasites are heirloom species and which are PhD student, Eva Casas, coauthored the definitive souvenir species. These data also contributed to under- work on llama archaeoparasitology (Leguia and Ca- standing the parasite adaptation dichotomy of general- sas 1999). Since 2007 two new laboratories have been ists and specialists. The field has also contributed to ep- established. Ines Garate at the Universidad Nacional idemiological and paleopathological theory as defined Mayor de San Marcos has begun analysis of archae- by a variety of authors. Cockburn’s ideas regarding the ological remains for parasites, and Luis Huaman has evolution of pathogens was particularly well adapted included archaeoparasitology in his Paleobotany lab- to evaluation through archaeoparasitology. The more oratory at the Universdad Peruana Cayetano Here- recent construct presented by Barrett and colleagues dia. There, parasitology is taught as part of a holistic regarding stages of pathogen emergence is also con- analysis of plant remains to reconstruct ancient diet, ducive to testing through laboratories of archaeopara- environment, and disease. sitology. Of all theories, Pavlovsky’s nidus concept is By the end of the 1990s the laboratory at Fiocruz particularly adaptable to archaeology today. The indi- in Rio de Janeiro started to apply molecular biol- vidual nidi of prehistoric habitations can be defined in ogy techniques to ancient parasitological materials archaeological space and the pathogens can be recov- (Bastos et al. 1996; Ferreira et al. 2000) contempo- ered. Through archaeological method and paleopatho- raneously with research in Arica, Chile (Guhl et al. logical/epidemiological data, archaeoparasitology has 1999). In addition, molecular biology techniques be- made its most meaningful contributions and will con- gan to be used, mainly in Chagas disease research tinue to do so as a synthetic field. (Aufderheide et al. 2004). In North America, Dittmar et al. (2003) confirmed the diagnosis of Chagas dis- ease in a mummified body with megacolon described Acknowledgments — The final version of this chapter by Reinhard et al. (2003). However, PCR technique benefited greatly from discussions with the University was also applied to detect helminth infection in sed- of Nebraska parasitology faculty and students. In par- iments and coprolites (Iñiguez et al. 2003; Leles et al. ticular, Dan Brooks, John Janovy, Scott Gardner, and 2008, 2010) as performed by Loreille et al. (2001), Lo- Mary Lou Pritchard provided comments on broad as- reille & Bouchet (2003). The South Korean research pects of theory and also small errors in detail. We are is also sequencing Ascaris lumbcricoides and Trichu- all intellectual descendants of Harold Manter, who ris trichiura DNA, and the T. trichiura data have been founded parasitology at the University and our evo- published (Oh et al. 2010). Researchers at the Uni- lutionary perspective on parasites and hosts. versity of Nebraska–Lincoln have also begun collab- oration with the University of Oklahoma’s Molecular 760 R e i n h a r d a n d A r a ú j o i n A G l o b a l H i s t o r y o f P a l e o pa t h o l o g y (2012)

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