The History of Biological
The History of Biological
W. Seth Carus
This article critically reviews the literature on the history of biological warfare, bioterrorism, and biocrimes. The first
serious effort to review this entire history, made in 1969, had numerous limitations. In recent decades, several authors
have filled many of the gaps in our understanding of the past use of biological agents (including both pathogens and
toxins), making it possible to reconstruct that history with greater fidelity than previously possible. Nevertheless, there are
numerous remaining gaps, and closer inspection indicates that some supposed uses of biological weapons never took
place or are poorly substantiated. Topics requiring additional research are identified.
W. Seth Carus, PhD, is Distinguished Research Fellow, Center for the Study of WMD, National Defense University, Ft. McNair,
Washington, DC.
219
THE HISTORY OF BIOLOGICAL WARFARE
understanding of that history is recent. Writing in 1960, during the Korean War are reviewed, but not histories of
the eminent biologist Theodor Rosebury, who knew more the Japanese or US offensive biological weapons programs.
than a little about biological weapons, asserted that ‘‘. Similarly, while some histories of the Soviet offensive bio-
although allegations are many, not a single one can be logical weapons program are mentioned, the focus is on
called fully authenticated.’’1 claims of their actual use. A systematic review of studies
It was not until a decade later that Milton Leitenberg focusing on programs requires its own lengthy survey.
published the first systematic survey of alleged biological For purposes of this essay, a biological weapon is defined
agent use in The Rise of CB Weapons, the first of the 6- as the combination of a biological agent with a means of
volume 1969 Stockholm International Peace Research delivery. The delivery system can be quite complex, as is the
Institute (SIPRI) study, The Problem of Chemical and Bio- case with bomblets in a ballistic missile, or extremely sim-
logical Warfare; A Study of the Historical, Technical, Mili- ple, as with a powder in an envelope or a liquid in a test
tary, Legal and Political Aspects of CBW, and Possible tube. The definition of biological agent used here is con-
Disarmament Measures.2 In 17 pages, supplemented by a 5- sistent with the coverage of the Biological and Toxin
page appendix, Leitenberg reviewed claims of BW during Weapons Convention (BWC): pathogenic microorganisms
the post-1914 era, although he mentioned some earlier or toxins (toxins are poisons produced by living matter).19
allegations as well. As such, his work provides a baseline for This contrasts with the perfectly reasonable preference
assessing how much we have learned about the history of of some authorities to limit biological agents only to
BW during the past 45 years.2 pathogenic microorganisms.
Leitenberg described 18 allegations (although the exact Use of higher order animals, such as insects or poisonous
count depends on how they are categorized), but carefully snakes, as weapons is not considered. BW normally refers to
avoided giving definitive conclusions about their validity. At the employment of biological agents in the context of wars,
least some claims, such as Japanese use of biological weapons armed conflicts between states, but in this essay it is taken to
during World War II, were supported by considerable evi- include all uses of biological agents to cause harm, such as
dence, suggesting that Leitenberg found them credible. by terrorists (‘‘bioterrorism’’), criminals (‘‘biocrimes’’), and
However, the final chapter of the SIPRI volume includes a clandestine state operatives during peacetime.
section, written by Julian Perry Robinson, titled, ‘‘The non- Some activities occasionally treated as BW, such as pol-
use of biological weapons,’’ suggesting others did not agree.2 luting water supplies with dead animals or waste, are not
Today, however, there is a substantial literature on the considered here. This essay follows the example of 2 re-
history of BW, including many short surveys that purport spected experts in the history of BW, Milton Leitenberg and
to cover the entire history,3-18 and scores of books and Mark Wheelis.2,20 This approach also follows the example of
articles written about some aspect of the topic. As a result, the jurist Hugo Grotius, who helped create modern inter-
many incidents unknown, or just barely known, a few de- national law. While Grotius condemned the use of poison in
cades ago are now well characterized, even if we sometimes warfare, he accepted that the pollution of water was equiv-
await the appearance of definitive accounts. Unfortunately, alent to the cutting off of water supplies by destroying aq-
this literature also reports on a number of claimed instances ueducts or diverting water in rivers and streams.21 While it is
of BW that almost certainly never occurred. As a result, possible that water contaminations were meant to spread
sorting through the allegations to obtain an accurate picture disease, it is clear that in most cases such acts were intended
remains difficult. simply to make water sources unavailable to opposing
This essay reviews the existing literature, highlighting armies. This was, according to some historians, a common
what appears to be the best writing on any given topic. It practice.22
identifies gaps in that literature and suggests areas needing Insects also are excluded as weapons, unless used as a
additional research. Finally, it flags incidents that appear in vector to spread a pathogen. Thus, the Japanese reliance on
some accounts, but that clearly never occurred or should be fleas to spread Yersinia pestis, the causative agent of plague,
treated with skepticism. is mentioned, but not the many false allegations that the
Germans and Allies spread Colorado potato beetles during
World War II.23 Nor do I discuss similar claims by the
Methodology Soviet bloc that the United States at various times dispersed
insects to attack agriculture.24 There is a small literature on
This essay focuses explicitly on books and articles that de- the use of insects as weapons, including a book-length study
scribe alleged instances of biological agent use, rather than by Jeffrey Lockwood.25 Unfortunately, that book must be
on BW programs. While understanding programs—how used with caution because of the author’s unfamiliarity with
countries and nonstate groups attempted to produce bio- the complexities of diplomacy and international law asso-
logical weapons—is important, this essay focuses on what is ciated with biological warfare, the uneven research, and an
known about incidents involving the employment of bio- unwillingness to forthrightly declare that many of the al-
logical agents. Hence, Japanese BW during World War II leged intentional releases of insects were fabricated for
and allegations that the United States resorted to BW political reasons.
Toxins are included in this survey. There are important modern era and the total absence of known BW incidents
differences between toxins, which are poisons of biological employing the techniques of advanced biotechnology.
origin, and chemical warfare agents. Chemical warfare One critical question requires further elaboration: What
agents are all man-made, while toxins are natural products. constitutes ‘‘proof’’ of the use of a biological agent? Rose-
Toxins are not volatile, in contrast to almost all chemical bury apparently thought evidence needed to be over-
warfare agents. Almost all toxins are not dermally active, whelmingly compelling when he argued that there had been
while most chemical warfare agents can penetrate the skin. no ‘‘fully authenticated’’ uses of BW: ‘‘In other words, no
Toxins operate through a wide variety of biochemical government, and no responsible government official who
pathways, while chemical warfare agents operate through a was free from duress at the time, has ever admitted waging
small range of toxic effects. For such reasons, some experts offensive biological warfare. No other evidence could be
prefer to view toxins as a category of substances different fully acceptable to all concerned.’’1(p228) This standard is
from either biological or chemical warfare agents.26 Purists clearly unsupportable. Indeed, few criminal cases adjudi-
would argue, perhaps correctly, that what is described in cated in the most scrupulous judicial settings could satisfy
this article is really biological and toxin warfare. this criterion, given that most perpetrators never admit guilt.
Some authors, such as Mark Wheelis, prefer to disregard What other evidence is acceptable for establishing intent?
toxins and focus just on infectious diseases.20 This is de- Admissions of guilt are unlikely, as perpetrators are unlikely
fensible, given the modern understanding of the role of to confess their misdeeds and governments are likely to ob-
pathogens in disease etiology. Toxins are much closer to fuscate their activities. Document destruction is one method
chemical poisons than to replicating entities, whether to hide culpability, as demonstrated by the Germans after
pathogens or infectious proteins (such as prions). Thus, it is World War I, the Japanese at the end of World War II, the
not surprising to learn that toxins were part of the Soviet white Rhodesians after they abandoned their bid for an in-
chemical weapons program, not its BW effort, with the dependent state, and the Bulgarians with documents related
significant exception of botulinum toxin.24 In contrast, to the Georgi Markov assassination. The problems are even
toxins were part of the US biological weapons program, more difficult when we consider alleged uses in the pre-
probably because the expertise in biological production modern era. Even if employment of BW was documented—a
processes resided there and not with the chemical experts.27 doubtful prospect—survival of that supporting evidence is
Ignoring toxins, however, leads to an anachronistic even more unlikely. Nor can allegations of BW by the sup-
perspective. Evidence for the germ theory only emerged in posed victims be accepted uncritically. There is a long
the last third of the 19th century. It is impossible to discuss modern history of false claims of BW. Misguided individuals
intentional spread of pathogens, as opposed to the inten- who thought that they were reporting a credible claim ad-
tional spread of disease, prior to that. Interest in the mo- vanced some allegations, while other claims were dissemi-
tivations for resorting to BW and reactions to intentional nated as deliberate misinformation.
disease, for example, make it desirable to look well before Attribution of biological attacks has begun to receive
the modern era. As will be evident, fears of intentional serious analytic attention.33 The focus often has been on the
disease, and the desire to use disease agents as weapons, are emerging science of bioforensics.34,35 Unfortunately, many
quite ancient. Understanding the sociocultural context of of the tools available to the bioforensics analyst may be
BW militates against too narrow a perspective, and requires useless for the exploration of past BW events. In some cases,
that we broaden our understanding of BW beyond a defi- however, should there be surviving biological samples, it
nition limited strictly to infectious disease. might be possible to reconstruct events using techniques
Moreover, until the study of infectious disease emerged unavailable even a few years ago. Recent studies have
as a scientific discipline in the late 19th century, it some- demonstrated that it is possible to identify infectious agents
times was difficult to differentiate between toxin poisoning from bone fragments and teeth from people who died
and pathogen infection. Thomas Heazel Parke, a British thousands of years ago, resulting in the emergence of pa-
Army physician, thought that poison arrows actually con- leomicrobiology as a new field of study.36,37 In particular,
taining strychnine (from a species of Strychnos plant) were paleomicrobiologists may be able to answer questions about
causing tetanus.28 The confusion is not surprising, since the causative agent of an outbreak, which could provide
strychnine and tetanus cause similar symptoms.29-31 telling evidence useful in reconstructing the historical event.
This essay divides the history of BW into 3 main eras: (1) Paleomicrobiology and bioforensics, however, cannot
prior to the germ theory (through the late 19th century); (2) determine whether an outbreak was natural or intentional.
the emergence of microbiology from the late 19th century Far more important are the answers to medical and public
through 1945; and (3) the modern era (1945 to the pres- health questions, which often are unavailable for past in-
ent). This differs from the breakdown suggested by other cidents. Is the claim consistent with what we know about
writers, such as Gregory Koblentz, who also would consider the natural ecology and etiology of the disease and with the
the invention of genetic engineering as the transition to a epidemiology of a natural outbreak? Is there reason to be-
new era.32 For purposes of this essay, such an additional lieve that the disease could be spread in the manner
division is not helpful, given the few instances of BW in the claimed? Did the perpetrators, whether state or nonstate,
have the scientific and technical capabilities to undertake remained unidentified. Thus, Snow tied cholera outbreaks
the claimed activities? Does an outbreak have a plausible to contaminated water supplies decades before Koch
natural explanation?38-41 demonstrated that Vibrio cholerae was responsible.46
Attribution is not just a technical matter, determined As a result, it is perhaps not surprising that theories of
solely by scientific or forensic evidence. Rather, it requires disease causation in most cultures over much of human his-
the integration of all sources of information, including tory were heavily imbued with magical thinking. Theories of
those that would be collected in the case of incidents not disease etiology often had little if any scientific plausibility.
related to BW. In essence, such a review requires an as- While this may suggest that such societies lacked the tools
sessment of all the available sources specific to the alleged essential to cause intentional disease, shamans and their
use in the broader historical context. From that perspective, equivalents often had special ‘‘knowledge’’ that supposedly
the evaluation is no different from any reconstruction of allowed them to inflict illness. Sometimes the shamans em-
any past event. Many of the studies cited below meet that ployed toxins capable of causing disease. Occasionally, em-
criterion, even if they may not definitively settle the ques- pirical observation led to theories of disease causation
tion of whether a particular event occurred. consistent with modern medicine, perhaps most evident with
smallpox. It is probably true, however, that people more
commonly relied on theories with no empiric validity.47
Biological Warfare Before An intriguing perspective on primitive concepts of dis-
the Germ Theory ease, relevant to the discussion here, is one offered a century
ago by the British ethnographer W. H. R. Rivers:
Some caution is needed when discussing BW prior to the
emergence of the germ theory in the late 19th century. The If we examine the beliefs of mankind in general concerning
cause of many diseases was unclear, and what we now know the causation of disease, we find that the causes may be
to be infectious diseases caused by pathogens often were grouped in three chief classes: (1) human agency, in which it
attributed to chemicals, environmental factors, host pa- is believed that disease is directly due to action on the part of
some human being; (2) the action of some spiritual or su-
thologies, or supernatural causes. Many doctors could not
pernatural being, or, more exactly, the action of some agent
distinguish between ‘‘fevers’’ associated with such diseases
who is not human, but is yet more or less definitely per-
as malaria, yellow fever, typhoid, and typhus. Only during sonified; and (3) what we ordinarily call natural causes.48(p7)
the 19th century did medicine learn to differentiate be-
tween these diseases, aided by the growing use of autopsies As Rivers noted then, and as many have confirmed since
to discern their differing pathologies. Even when it became then, it is common in indigenous societies to believe that
possible to more reliably distinguish between different some illness results from maleficent human intervention.49
diseases, which only happened in the early 19th century in The following account will suggest that such fears are not
the United States, the etiology of diseases was rarely un- limited to so-called primitive societies.
derstood.13,42
Only a few diseases, such as smallpox, were understood
sufficiently to enable a reasonably accurate theory of disease ‘‘Primitive’’ Warfare
transmission. A classic example is provided by yellow fever, Biological warfare probably originated in prehistory.
which was the source of much dispute during the 19th Careful study of indigenous societies during and after their
century.43 Even in the early 20th century, after Walter Reed contact with explorers and researchers suggests that toxins
and his team performed their experiments in Cuba, some and even pathogens were used in prehistoric warfare. Émile
authorities doubted that mosquitos were associated with Perrot’s 1913 book, Poisons de fle`ches et poisons d’e´preuve,
yellow fever.44 It is often forgotten that Walter Reed ex- which is an excellent survey, gives evidence of extensive
perimented to see if yellow fever could be transmitted by poison arrow use everywhere except Central America and
fomites (objects, such as blankets or clothing, contaminated Australia.50 H. D. Neuwinger, a toxicologist, more recently
with pathogens) soiled with the fluids of yellow fever vic- has argued that only the peoples of Australia and New
tims at the same time he and his colleagues undertook their Zealand did not use poisons.51 This perspective is sup-
more famous mosquito experiment.45 ported by David Jones, who in his monograph, Poison
Infectious diseases often were inexplicable even to experts Arrows: North American Indian Hunting and Warfare,
prior to scientific demonstration of the germ theory, which identifies 80 tribes that used poison arrows.52 The available
occurred primarily through the microbiological work of evidence suggests that many, perhaps most, indigenous
Louis Pasteur and Robert Koch and the epidemiologic societies used poison for hunting, fishing, and warfare, but
studies of John Snow. Pasteur and Koch proved that mi- there is too little information available to provide a more
croorganisms could cause disease and that certain diseases precise estimate of the prevalence of such usage.
resulted from infection with specific microorganisms. Snow Numerous articles and books, usually penned by an-
demonstrated that it was possible to understand routes of thropologists or ethnopharmacologists, explore some aspect
transmission even when the specific cause of the disease of poison use in primitive societies, but the only
comprehensive surveys are badly dated. Perrot’s compen- Scattered accounts suggest that it may have been rela-
dium appeared in 1913, while Louis Lewin’s Die Pfeilgifte tively common for indigenous peoples to use ‘‘poisons’’ that
was published in 1923.50,53 Perrot’s volume is uneven, apparently rely on the effects of pathogens, although the
providing excellent accounts for some parts of the world evidence is admittedly scattered. We have several descrip-
and cursory summaries for others (such as North America). tions of such poisons. A band of the Yavapai, a group in-
I have been unable to review Lewin’s study, but Neuwinger digenous to Arizona, reportedly prepared their war poison
found it more satisfactory than Perrot’s, perhaps because it in the following way:
gave more emphasis to the toxicology.51 In contrast, the
American microbiologist Ivan C. Hall found Perrot more Arrow poison was made by stuffing a piece of deer’s liver
useful in his studies of poisoned arrows, perhaps because with spiders, tarantulas, and a rattlesnake’s head. It was
Perrot recognized that some of the ‘‘poisons’’ might have then wrapped with yucca fiber, buried in the ground, and
relied on pathogens to achieve their fatal effect. There is no fire maintained over it. When rotten, it was exhumed, tied
with a string, and hung from the limb of a tree. Because of
comparable English review, although Neuwinger wrote a
stench it was hung well away from camp. There it dried for
book-length study of African ethnobiology, which appears
several days, and shrunk to only a fraction of its original
to be both comprehensive and up-to-date, although focused size. Next, a part of it was rubbed down with a stone on a
more on the biology and toxicology than on military or flat rock, a little water being added to make a paste. The
sociocultural issues. Jones’s book on North American poi- unused portion was rehung. The paste was applied to the
son arrows provides a short ‘‘World Survey of Arrow Poi- arrow points with a stick. One took care not to get the paste
soning.’’ He apparently was unaware of the studies by under his nails, lest he be poisoned. Arrows thus treated
Perrot, Lewin, or Neuwinger, which undermines the value were dried far from camp. The arrows were placed in a
of his review.52 special quiver.61(p224)
The claim that poison arrows were the norm in primitive
societies, not the exception, contrasts sharply with one of- Other Native Americans apparently used a similar tech-
fered by Leonard Cole, who studied the use of poison nique, which clearly was not intended to kill immediately
weapons in preparing an interesting study of the ‘‘poison because the ‘‘septic effect of such a preparation is likely to
taboo’’ and concluded that ‘‘most tribal groups did not have been much greater than the toxic.’’62(p417) According
use them.’’54(pp123-124) His conclusion came from negative to Jones, a common preparation involved getting rattle-
evidence: There were few mentions of poisoned weapons in snakes to bite into a liver, allowing the liver to rot, and then
an anthropological bibliography of warfare or in the En- making a paste that was spread on arrowheads.52 However,
cyclopedia of World Cultures,55,56 and the anthropological at least one contemporary observer was skeptical of the
studies that he consulted rarely mentioned poisons. His efficacy of this preparation.63 It might be interesting to
conclusion was clearly misguided, telling more about the undertake a test to determine whether there was an em-
interests of anthropologists than the history of poison use. pirical logic to these practices and, if so, the nature of the
As Jones noted in particular reference to the study of poison ‘‘poison’’ generated.
arrows among North American Indians, most scholars have Similar practices are widely reported. Cole, despite his
preferred to ignore or denigrate the subject.52 general skepticism, cites anthropological studies of 2 New
Why was poison so widely employed? According to one Guinea tribes who used rotting material in their arrow
theory, early bows and arrows were insufficiently powerful poisons.54 Little is known of their practices, but in the case
to reliably kill prey, especially large animals, unless they of the Kiwai Papuans, they used a ‘‘poison’’ consisting of
were poison-tipped. Using the right poisons, however, little more than contaminating arrow heads with rotting
hunters could use even wooden arrows to kill large game— flesh.64 Others have identified similar practices in East
even elephants and whales.57,58 From this perspective, the Africa.65,66 Perrot’s survey suggests that poisons prepared
spread of the bow and arrow was made possible only by the using decomposing flesh were found globally, although not
concomitant reliance on toxins.59 However, use of poison every group using toxins also used biological materials.50
arrows did not necessarily disappear with the development There have been several published experiments to test
of more effective combinations of bows and arrows, and poison arrows for the presence of pathogens. The most
there is documented use of iron arrowheads coated with recent identified by this author are 2 studies undertaken by
poison.60 Professor Hall. A 1927 test of 6 Bushman arrows revealed
Jones offers an interesting perspective on the use of that only 3 were coated with a toxin, while Bacillus histo-
poison arrows that is particularly germane to this study in lyticus was present in 5 of 6 arrows tested. Bacillus welchii
his monograph Poison Arrows. He suggests that poison ar- and Bacillus novyi also appeared, but only on a single arrow
rows relying on animal poisons were used in warfare, while for each of those pathogens. Tests confirmed that a solution
hunting relied on plant toxins. Moreover, animal poisons of the poison removed from the arrows was toxic, at least to
typically were allowed to putrefy before use, and they guinea pigs.67 Hall subsequently examined 2 Malayan
‘‘probably exert their principal effect by inducing gas-gan- blowgun darts and found no evidence of any known
grene, tetanus, and other severe infections.’’52(p64-65) pathogen, although there were some otherwise unknown
organisms cultured that appeared to have mild pathogenic bce, and the Arzawans retaliated in kind.78 This derives in
effects in inoculated guinea pigs.68 part from his earlier arguments that a ‘‘plague’’ outbreak
Similar studies were undertaken at about the same time affecting the entire region was caused by F. tularensis.79,80
by a team of Swedish researchers. In 1921, the ethnogra- While there is agreement that such an outbreak occurred,
pher Gustaf Bolinger returned to Sweden with poison ar- some scholars had speculated that the outbreak was bu-
rows obtained from the Guajiros, an indigenous people bonic plague or bacillary dysentery, although still others
located in Columbia and Venezuela. Reputedly, the poison argue that there is insufficient information in the ancient
was a product of the ‘‘decomposing cadavers of animals, source to support any diagnosis.81
snakes, toads, and such poisonous creatures.’’69(p153) Five Unfortunately, the evidence to support deliberate spread
years later, animal testing of the poison found that it pro- of disease by the Hittites is nonexistent. The only ‘‘proof’’
duced tetanus-like symptoms. A Swedish team consisting of of possible use of biological agents comes from descrip-
a bacteriologist, Gottfrid Thorell, and a toxinologist, C. G. tions of a scapegoat ritual practiced by the Hittites. Tre-
Santesson, determined that the ‘‘poison’’ coating contained visanato relies on a study by Professor O. R. Gurney, a
virulent Clostridium tetanus organisms.69 This study, which noted authority on that ancient society, while Mayor ref-
this author has not reviewed, was published in 1927.70 erences the similar work by Christopher Faraone, which
Finally, a French microbiologist, Félix Le Dantec, found refers to Gurney’s study but actually focuses on Greek
that arrows obtained from New Hebrides were contami- practices. Such rituals, widely practiced in the ancient
nated with bacille de Nicolaı¨er, the name then used by the world, sought to induce a divine being to end an epidemic,
French for the organism causing tetanus, Clostridium tetani. perhaps by transmitting it to their enemies. Gurney does
According to Le Dantec, the New Hebridians made their not directly associate that ritual with the so-called ‘‘Hittite
poison arrows by dipping the tip into soil obtained from plague’’ studied by Trevisanato, nor does he claim that the
crab burrows found in mangrove swamps. He found a practice had anything but symbolic significance.82,83 These
slight effect from very old arrows, but 6-month old arrows scapegoating rituals do not suggest actual transmission of
prepared in this way quickly produced lethal results in disease. The ritual is symbolic, not physical, and the rituals
laboratory animals.71,72 are best understood not as BW but rather as a mystical
understanding of disease causation (disease resulting from
the acts of a god) and as a desire to convince friendly deities
Early Civilizations both to lift the disease and to inflict it on enemy societies.82-
85
There are claims that some ancient societies deliberately Hence, there is simply no evidence to suggest that the
spread infectious diseases, but the evidence is scanty and Hittites waged biological warfare. Nonetheless, numerous
generally unconvincing. It is always difficult to definitively publications have reported that the Hittites had engaged in
determine the etiologic agent responsible for a disease biological warfare.14,86-89
outbreak by relying only on written sources, often written A second allegation of possible BW has arisen in the
by people with limited medical background. However, even context of the Peloponnesian War, fought between Athens
when it is possible to link a disease to an event, claims that and Sparta and their allies. Recently, a team of Greek re-
certain outbreaks were spread deliberately are poorly sub- searchers, led by Manolis J. Papagrigorakis, suggested that
stantiated. the famous ‘‘Plague of Athens,’’ which reportedly killed
A ubiquitous source of information on poisons in the one-third of the population during Sparta’s 4-year siege of
ancient world, whether chemical or biological in origin, is Athens, resulted from deliberate introduction of the or-
an often-cited book by Adrianne Mayor, Greek Fire, Poison ganism responsible for typhoid into the water supply.90
Arrows, and Scorpion Bombs.73 This work received mixed The causes of that outbreak have been intensely debated. In
reviews,74-77 but it should be used with caution, even recent years, it has been attributed to diseases as varied as
though it presents a wide body of original research. Mayor’s smallpox, typhus, measles, bubonic plague, Ebola virus,
real expertise is folklore, and she rarely assesses the accounts influenza combined with toxigenic staphylococci, and Rift
with the critical eye of either the scientist or the trained Valley fever, among the 30 odd theories advanced over the
historian. It is best used as a sourcebook for further re- years.91-93
search, not as a definitive text. What is the evidence to support the theory of intentional
These problems are evident in Mayor’s claim that the contamination? Papagrigorakis and his colleagues have
Hittites waged biological warfare.73 The first edition of her scientific evidence to support the involvement of a bio-
work based this on a reference to a scapegoating ritual logical agent in the outbreak. Genomic analysis of recov-
found in Hittite religious documents. In the second edi- ered DNA from a burial pit of plague victims thought to
tion, she also cited the research of Siro lgino Trevisanato, have died during the siege revealed the presence of Salmo-
who expanded on Mayor’s claim by identifying the disease nella enterica serovar Typhi organisms in the skeletal re-
transmitted as Francisella tularensis. According to Trevisa- mains of outbreak victims.94 The organism identified may
nato, the Hittites infected their Anatolian enemies, the have been an ancestral version of the modern strain.95
Arzawans, with F. tularensis during the late 13th century According to Thucydides, the Athenians suspected that the
Peloponnesians deliberately poisoned the city’s water sup- this likewise has putrefied, they mix the sediment, which is of
ply, which led Papagrigorakis to suggest that spies intro- a watery nature, with the corrupted blood of the viper, and
duced the pathogen. thus make it a deadly poison.103(p1294)
Others are more skeptical. Some worry that the genomic
evidence is not sufficiently strong to support the identification Similarly, a Roman author, Pliny, states, ‘‘In Scythia the
of Salmonella enterica serovar Typhi. The techniques to re- natives poison their arrows with vipers’ venom and human
construct DNA at the time Papagrigorakis and his team blood; this nefarious practice makes a wound incurable—by a
undertook their work have been heavily criticized, and only light touch it causes instant death.’’104(pp97-98) A third source,
the subsequent development of methods that can reconstruct Aelian, who relied at least in part on a lost work by Theo-
genomes from smaller fragments of DNA have started to phrastus of Eresus, noted that ‘‘the Scythians are even said to
silence the critics.96 Moreover, it is generally agreed that mix serum from the human body with the poison that they
Athens was probably suffering from outbreaks of multiple smear upon their arrows to drug them. This serum somehow
diseases, and there is no proof that typhoid fever was the floats on the surface of the blood [and they know a means of
disease associated with the ‘‘plague’’ outbreak.97,98 Pathogens separating it].’’105(p235) Unfortunately, the part of the text in
evolve, as does host response, and other critics argue that the brackets was corrupted, so the exact meaning is uncertain.105
epidemiology of the epidemic is inconsistent with typhoid Mayor attempts to reconstruct the production method
fever,99 although possible differences between the ancient and using these accounts, but it is unclear if she fully under-
modern strains of the pathogen might make it hard to rely too stands her sources. Her reconstruction of the recipe from
much on analogies to modern epidemiologic patterns. multiple accounts cannot be accepted without further jus-
The major problem, however, is the absence of any re- tification. For example, she claimed that the Scythians had a
liable evidence that the Peloponnesians either contaminated method of separating plasma from blood, while the ac-
the water supply or that such a contamination would have counts make clear that they drew on a component of de-
been effective or that anyone knew how to spread the dis- composed blood. Similarly, she asserts that the arrow
ease intentionally. The only reason to believe the outbreak poison included decomposed dung, even though the ac-
was intentional comes from a comment by Thucydides, count by Pseudo-Aristotle states only that the container of
who described the outbreak in detail: ‘‘The disease . the decomposing material was buried in a dung-hill.73
suddenly fell upon the city of Athens, and attacked first the More plausible are claims that toxins were used in war-
inhabitants of the Piraeus, so that the people there even said fare during this period. Arrow poison was used during the
that the Peloponnesians had put poison in their cisterns; for time of classical Greece and Rome, but apparently only by
there were as yet no public fountains there.’’100(p343) The ‘‘barbarians.’’
fact that some Athenians thought the water had been de- Some sources claim that during the 6th century bce the
liberately contaminated is meaningless; we know how often Assyrians contaminated the wells of their enemies with rye
such allegations are made with no supporting evidence. ergot (Claviceps purpurea), a parasitic fungus that grows on
Moreover, it is not evident that Thucydides believed the certain grains and grasses and produces hallucinogenic alka-
allegation even as he reported it.101 In the end, the hy- loids. This allegation first appeared in the Medical Manage-
pothesis advanced by Papagrigorakis and his colleagues is ment of Biological Casualties, a publication of the US Army
not supportable with the evidence that they provide. Medical Research Institute of Infectious Diseases (USAM-
A more plausible form of biological warfare involved RIID) in the mid-1990s, and was repeated in the 7th edition
Scythian arrow poison. The Scythians were a nomadic of that work released in 2011.87,106 Unfortunately, it provides
people who lived in what is now Ukraine and were famed no references, so it is impossible to know where the account
archers during the period of Classical Greece. Renata Rolle, originated. This account was subsequently picked up in the
an expert on Scythia, hypothesized that the poison probably popular press,107 and Guinness World Records even anointed it
was contaminated with organisms capable of causing gan- ‘‘the first incidence of biological warfare.’’108 Recent publica-
grene and tetanus.102 This interpretation is plausible, based tions repeat the claim.11,109,110
on the method for producing the poison. The fullest de- There is, however, no reason to believe that the Assyrians
scription of their arrow poison appeared in a work wrongly ever used ergot as a biological weapon. Mayor doubts the
attributed to Aristotle (hence, sometimes known as Pseudo- story, but cites no sources and provides no supporting ra-
Aristotle). tionale.73 Other historical writings by authors associated
with USAMRIID do not mention it.5,7,14,15 More funda-
mentally, it is not even certain that the Assyrians suffered
They say that the Scythian poison, in which that people dips
its arrows, is procured from the viper. The Scythians, it
from ergotism. According to some students of Assyria, they
would appear, watch those that are just bringing forth young, did not cultivate rye, which is the primary host for out-
and take them, and allow them to putrefy for some days. But breaks associated with consumption of C. purpurea. The
when the whole mass appears to them to have become suf- symptoms described in Assyrian texts could be ascribed to
ficiently rotten, they pour human blood into a little pot, and, other causes besides exposure to ergot.111,112 Nor is it clear
after covering it with a lid, bury it in a dung-hill. And when how the contamination would occur. Would the Assyrians
have carried quantities of infected grain to the territory of cases, the perpetrators allegedly used poisoned needles to
their enemies to dump into water supplies? Could such kill their victims.73
contamination even cause a toxic effect? On balance, it is Even a cursory reading of Dio Cassius shows that Mayor
best to reject this allegation, barring the emergence of far misinterprets his account. First, he does mention the inci-
more compelling evidence than now exists. dent (Book 67, Chapter 11), but imputes no political
Mayor reviews the accounts of the claimed poisoning of motivation. Nor was it described as a disease outbreak or a
the water supply of Cirrha during the First Sacred War. ‘‘plague.’’ This is what he says about the ‘‘epidemic’’:
The people of Cirrha stood accused of interfering with the
famous Oracle of Delphi. An alliance of Greek city-states During this period some had become accustomed to smear
besieged the city, finally destroying it after a 10-year-long needles with poison and then to prick with them whom-
siege ending around 585 bce. Mayor identified multiple soever they would. Many persons thus attacked died
sources supposedly describing this incident, differing in without even knowing the cause, and many of the mur-
important details, but all agreeing that the water was con- derers were informed against and punished. And this went
taminated with a poison; most identified hellebore as the on not only in Rome but over practically the entire civilized
world.118(Vol8,p343)
toxin employed, which led to the incapacitation of the city’s
defenders and their ultimate defeat.73
There is a rather serious problem, however, which Mayor There is nothing in this account to suggest any kind of
ignored. In 1978 a classicist, Noel Robertson, argued that infection. Rather, it is clear that the reference is to some
the First Sacred War never occurred, pointing out that toxin or mineral poison.
archeologists have been unable to identify a city that cor- The second passage in Dio Cassius (Book 73, Chapter
responds to Cirrha despite intensive efforts to find it, that 14) is more difficult to interpret. He does mention a disease
all the sources attesting to the incident were written at least outbreak, which is generally assumed to be a continuation
200 years after the supposed event, that some of the sources of the Antonine Plague that struck the Roman Empire
are problematic for other reasons, and that it may not even between 165 and 189 ce.119 However, it is not clear that he
be possible to use hellebore to cause a mass poisoning in the attributes its origins to poisoning.
way described.113 While some classicists disagree, others
accept Robertson’s arguments.114-116 This led one recent Moreover, a pestilence, as great as any I know, took place,
account to assert, ‘‘Whether or not the war took place, it for it should be noted that two thousand persons several
times died in Rome on a single day. Many more, not
seems clear that many details of the usual account were later
merely in the capital but throughout almost the entire
elaborations.’’117(p332) In other words, we should be cau-
empire, perished by the hands of scoundrels, who smeared
tious about accepting stories about the siege, such as the some deadly drugs on tiny needles, and, for pay, infected
claimed poisoning of the water. men with the poison by means of these instruments. The
These disputes suggest that Mayor’s account is highly same thing had happened before in the reign of Domitian.
problematic. This is reinforced by a closer look at how she But the death of these unfortunates was not regarded as of
uses her sources. For example, Mayor relies on an account any importance.118(Vol9,p101)
attributed to Thessalus, son of the great physician Hippoc-
rates, who ostensibly wrote the earliest account of the siege. The second sentence does not state that the poisoned
His version of the history mentioned the poisoning but did needles were the cause of the pestilence. Indeed, the choice
not name the specific poison used.73 As it happens, most of words (‘‘many more . perished’’) seems to suggest that
classical scholars seem to doubt that Thessalus actually wrote these were 2 simultaneous but disconnected events. Re-
the account, suspecting that it was written much later.113 inforcing this view is the reference to drugs and poisons,
In other words, even the best-documented incident of which suggests use of a toxin or mineral poison.
toxin warfare in the classical world may not have happened. The need for a new and more systematic account of the
Given that most people interested in BW lack the expertise use of toxins in early civilizations is evident in discussions of
to evaluate the sources and understand the historical con- changing perceptions of the legitimacy of poison as a
text of such incidents, even a well-informed reader of BW weapon of war. Significantly, it appears that use of poison
history is unlikely to know that there are reasons for cau- arrows largely disappeared in the transition from hunter-
tion. For this reason, if no other, Mayor has done the field a gatherer to nomadic to settled societies, albeit with a few
grave disservice. notable exceptions.
Similar problems emerge with Mayor’s claim that Rome While some authorities assert that the emergence of
suffered 2 intentionally started epidemics, based on refer- civilized societies was accompanied by a growing repug-
ences in the history written by Dio Cassius in the early 3rd nance for the use of poison in warfare,120 the evidence for
century ce. According to her account, Dio Cassius claims such claims is remarkably thin. Commentators note that
that ‘‘saboteurs’’ initiated the plagues ‘‘to spread chaos and the Hindu Laws of Manu decried the use of poison: ‘‘When
undermine unpopular emperors’ authority.’’73(p126) This he is engaged in battle, he must never slay his enemies with
happened first in 90-91 ce, and again in 189 ce. In both weapons that are treacherous, barbed or laced with poison
or whose tips are ablaze with fire.’’121(p101) A similar in- that these actions led to an outbreak among the besieged,
junction appears in yet another Vedic text, the Dharmasutra the evidence certainly does not come close to meeting
of Baudhayana: ‘‘The king should not turn back in battle or Rosebury’s standard of proof and may not even be ‘‘beyond
strike with barbed or poisoned weapons.’’122(p159) The role a reasonable doubt.’’ Bubonic plague typically is transmit-
of such injunctions is not self-evident to the casual reader ted through the bites of infected fleas. But fleas quickly
and has been the subject of considerable learned debate by leave a dead body as it cools down,129 so it is uncertain that
those expert in this literature.121 the catapulted bodies would have exposed the residents of
Certainly, the Indian manual of statecraft, Kautiliya’s Caffa through that route.
Arthasastra, which seems to date from the same era, is filled Ultimately, there are missing elements to the story, if we
with references to the use of poison. It is impossible to are to believe that the Mongols deliberately spread the
identify the various poisons mentioned in it, and we cannot disease. First, we need some evidence that the catapulting of
tell whether the ‘‘poisons’’ mentioned are real—that is, are the bodies was linked to a plan to spread disease, but we
they true toxic substances with identifiable physiological have no accounts from the Mongol perspective. Second,
effects, or are they merely magical in character? Whatever even if the Mongols intended to spread the disease, we do
the case, it is evident that the most influential ancient In- not know for certain that their actions were responsible for
dian guide to statecraft saw poisons as ordinary tools of the outbreak, although Wheelis may be correct that the
statecraft. It may be significant that it never mentions catapulted bodies could have been the cause.
poison in the context of battles, but rather confines its use Although Wheelis makes a compelling, but by no means
to clandestine uses, such as assassination of political ene- definitive, attribution, his research is a model that others
mies or the secret murder of enemy commanders.123-125 would do well to follow. He carefully researched the known
This is a subject worthy of considerably more attention, historical sources, providing as rich an account as possible
given its importance for our modern understanding of the given the limited amount of material available. Equally
norms and taboos associated with BW. Some prohibition important, he examined the issue from epidemiological and
on the use of poison is evident in at least some early civi- microbiological perspectives, drawing on what is scientifi-
lizations, but the significance is unclear, given indications cally known about the spread of Y. pestis. He also consid-
that poison was still used. Indeed, Richard Price, who ex- ered an alternative explanation for the spread of the disease,
amined the norms associated with chemical weapons, ar- and carefully caveated his conclusions.
gued that the prohibition against the use of poison in Wheelis makes a similarly careful assessment of 2 other
warfare dates to the early modern era and particularly to the incidents. He reviews the evidence associated with a pos-
writings of Grotius. According to Grotius, the ban on sible BW attack during the 1340 siege of Thun l’Eveque.
poisons reflected the desires of kings, who saw poison as the According to one account, the besieging French army used
weapon of the weak and a dangerous threat to their power.120 their siege engine to hurl dead horses into the castle. It is
This seems doubtful, given the apparent disappearance of unclear why they did so; they may have been merely trying
poison weapons from the arsenals of at least some societies to harass the defenders. Complicating matters, this account
thousands of years earlier. was written long after the event, while another version of
the battle, written by someone who was fighting with the
English army in the area at the time, does not mention the
Medieval and Early Modern Warfare catapulted horses.20 These considerations suggest that at
There are few references to BW during the medieval period. most this is a possible instance of BW.
Mark Wheelis identified only 4 alleged incidents between Finally, Wheelis also discusses the claim that the city of
1340 and 1710 in his excellent survey, ‘‘Biological Warfare Karlstein was subjected to a biological attack in 1422. At
Before 1914.’’20 It appears in an indispensable SIPRI publi- the time, the Catholic Church was attempting to suppress
cation, Biological and Toxin Weapons: Research, Development, the Hussites, which was seen as a heretical movement.
and Use from the Middle Ages to 1945, edited by Erhard Karlstein, the most important Catholic stronghold in
Geissler and John Ellis van Courtland Moon, which contains Hussite-dominated Bohemia, was besieged by the Hussites
a number of excellent studies that are referenced below.126 for 5 months in 1522. A history of the failed siege, written
The only alleged use of BW during the medieval period about 250 years after the event, claims that they catapulted
that Wheelis found totally credible occurred during the the dead bodies of soldiers into the city, along with 2,000
Mongol siege of the Genoese town of Caffa, a community ‘‘barrow-loads of waste.’’ The objective of these attacks is
in Crimea on the site of modern Feodosiya. Wheelis fo- not given, but Wheelis finds them to be plausible efforts to
cused on this episode in a separate article likely to remain cause disease. He also admits that an account relying on
the definitive account, superseding a 1966 study by Vincent unnamed sources and written so long after the event cannot
Derbes.127,128 The besieging Mongols reportedly cata- be considered very credible.20 Ultimately, it is difficult to
pulted the bodies of plague victims into the city, but our consider this a likely example of BW.
only account is Genoese, and we have nothing from a There are a few incidents not mentioned by Wheelis.
Mongol source. Hence, while Wheelis makes a strong case Many accounts repeat the story that Frederick Barbarossa,
the Holy Roman Emperor, employed BW while besieging failed to note that their French-language source also as-
the Italian city of Tortona in 1155. One source even claims serted, ‘‘Le caractère légendaire de cette accusation est évi-
that his capture of the city resulted from the effects of the dent’’ (‘‘The legendary nature of this accusation is
biological agents.3,130 However, a reading of the original obvious’’). Unfortunately, the source of the original accu-
accounts indicates that the emperor was attempting to sation (a 1602 publication) and the rebuttal (a 1740 pub-
make the town’s water supply undrinkable. In addition to lication) were both written in Latin and do not seem to
dumping the carcasses of dead men and animals into the have been translated into a modern language.137 Thus, the
water, he also contaminated it with sulphur and pitch, allegation was made more than a century after the alleged
hardly the actions of someone who wanted people to drink event, and no one has bothered to review the original
the water.22 sources for the claim (and the rebuttal), clarify the historical
There also is an alleged incident involving the Venetians context in which it supposedly occurred, or examine its
and the Byzantines.4,8 In 1171, the Venetians became scientific plausibility. Absent such research, this allegation
embroiled in a war with the Byzantine Empire. After the cannot be accepted as a historical fact.
Byzantines arrested Venetian subjects and seized their According to one researcher, in 1650 a Polish artillerist
property, the Venetians built a large fleet and mounted a by the name of Jan Kazimierz Siemienowicz ‘‘fired hollow
retaliatory strike against the Byzantines. They seized a artillery spheres filled with the saliva from rabid dogs at
number of cities along the Adriatic coast that were friendly enemy forces.’’14 Other sources repeat this claim.6,9,16 In
with the Byzantines, including Ragusa, a quasi-independent contrast, the Robertsons, who first published an English
city-state. The Venetians then wintered on the island of language version of this story, only claim that he designed
Chios while trying, unsuccessfully, to negotiate a settlement such a device.4 They ascribe the story to an article that
with the Byzantines. After many of the Venetians became ill appeared in a Norwegian language medical journal, which
due to a ‘‘plague’’ outbreak (which may not have resulted was not located for this survey.138
from Y. pestis infections), some of the Venetians feared that There is at least some reason to suspect the accuracy of all
the Byzantines must have caused the disease by poisoning these accounts. Siemienowicz published a Latin text on
their water supplies. However, there is no evidence to artillery, rocketry, and fireworks in 1650, Artis Magnae
support that theory.131,132 That an army would experi- Artilleriae pars prima (Great Art of Artillery, the First Part),
ence disease outbreaks is scarcely surprising, given that which was translated into English in 1729.139 Suspiciously,
until the 20th century, infectious diseases killed more the alleged year that he supposedly used his weapon cor-
soldiers than enemy action. Natural causes are the most responds with the publication date of the book, suggesting
plausible explanation for the disease. that the Robertsons are correct in claiming that Siemie-
It is sometimes asserted that medieval European armies nowicz described but did not construct such a weapon.
commonly catapulted the carcasses of animals that died of More significantly, while Siemienowicz described a poison
disease or even diseased human remains into castles or weapon, it bore no resemblance to any of the accounts
fortified cities (as allegedly done at Caffa).3 In contrast, offered in the literature. Book 4, Part II, Chapter XI of
Wheelis uncovered only a single incident involving dead Siemienowicz’s book is devoted to ‘‘Poisoned Balls.’’ In it,
animals and only a couple (including Caffa) involving he describes how to contaminate the surface of artillery shot
humans in the 500 years before 1914.20 This is a subject (not exploding shells) with poison, following a procedure
that might benefit from some explorations by scholars who he outlines for making fire-balls. For this purpose, he rec-
study medieval warfare. ommends combining wolf bane with poison extracted from
Other allegations simply require more investigation. a toad, along with mineral poisons (such as mercury or
Louis XIV of France supposedly gave an Italian ‘‘chemist’’ a arsenic), ‘‘to which may be added the Menstrua of Barren
pension to keep the secret of a ‘‘bacteriological weapon.’’4 Women, the Brains of Rats, Cats, Bears, the Foam of Mad-
The source of that account is an article in the Encyclopedia Dogs.,’’ and so on.139(pp294-295) Thus, the slobber of rabid
Britannica, written by a biographer of the French king.133 dogs is only one possible ingredient for this poison weapon
The article does not source the story, and others claim, and by no means an important one. Finally, Siemienowicz
more plausibly, that the suppressed weapon was an incen- makes clear that the use of such weapons is proscribed in
diary device.134,135 The event apparently was well known. warfare, at least against fellow Christians.
The French writer Fontenelle wrote a life of Martino Poli, Use of toxin weapons also appears rare during this pe-
the alleged inventor, mentioning the incident without riod. A 1947 article by a Chinese scholar, Wang Ling,
specifically describing the type of weapon involved.136 reports that the Chinese of the Song and Yuan dynasties
Without further evidence, there is no reason to accept the used what were called ‘‘poison-drug smoke balls,’’ which
claimed existence of a biological weapon. included mixtures of gunpowder and a number of poi-
Numerous accounts now repeat a story that in 1495 the sonous materials, including plant toxins (aconite, croton
Spanish provided an opposing French army with ‘‘wine oil, langtu). One incorporated several toxins, as well as
contaminated with the blood of leprosy patients.’’4(p370) metallic poisons, another ‘‘dried, powdered and sieved’’
However, the authors who reported this supposed event human feces. The feces could not have spread an infectious
disease, because the ‘‘balls’’ were boiled during their prep- tinely to biological attacks.20 His account is better than an
aration. Ling also reports that the Mongols who tried to earlier essay by Adrienne Mayor, who reviewed many such
invade Japan in the 13th century were armed with poison allegations, but she was more interested in the transmission
arrows, although we are not told what poisons were used.140 of legends than in authenticity of the stories.145 At best, her
Norman Grainger Bisset, a pharmacologist, identified research shows how often people have suspected malicious
numerous instances of such use of poison arrows, even intent as the cause of disease outbreaks.
though he denies having made a comprehensive survey of Wheelis mentions claims that indigenous peoples in the
the topic. The Chinese military continued to use poisoned Brazilian Amazon were infected with smallpox during this
arrows until relatively modern times, although apparently period, but he was unable to research Portuguese language
in relatively limited quantities and for specialized purposes. sources to confirm the reports.20 However, he pointed to a
A Chinese law from 1546 required the production of about published account by Claude Lévi-Strauss that suggests that
2 kilograms of an aconite-based poison, which Bisset Brazilian elite oral tradition holds that such attempts dated
thought sufficient to coat 30,000 arrows. Indigenous peo- as far back as the 16th century.146 Lévi-Strauss also told
ples continued to use poisoned arrows and crossbow bolts Wheelis in an interview that he heard from Brazilians that
until at least the 18th century. When the Chinese defeated such methods were employed in the 19th century as well.20
the Miao in 1726, they captured 30,000 poison arrows.141 In any case, reports of BW were rare in South America.
In any case, it is evident that in medieval Europe, and One account is almost certainly false. The latest edition of
perhaps elsewhere at the same time, the use of poison in Medical Management of Biological Casualties produced by
warfare was rare. One intriguing explanation deserving USAMRIID claims that the Spanish conquistador Pizarro
greater attention is suggested by the ethnographic studies gave the Incas smallpox-contaminated clothing.87 While it
mentioned earlier. If poisons were essential to make the is true that disease outbreaks devastated the Incas, the
early bow and arrow a viable weapon, then what happens smallpox epidemics occurred well before the Spanish at-
when the bow and arrow became a highly efficient killing tacked in 1532 (probably sometime before 1530). Some
machine? By the medieval period, technological advances historians also doubt that smallpox was the disease.147
made archers, often available in large numbers, highly ef- Noble David Cook, who extensively studied the causes of
fective in battle, even against armored opponents. Indeed, a disease in colonial America prior to 1650, argues that there
medieval longbow arrow could penetrate steel plate; the is no evidence that the Spanish ever intentionally tried to
British kings ordered hundreds of thousands of these arrows spread disease in the Americas.148
in preparation for their French campaigns. In a 1360 The best documented incident, and the only one from
campaign, the English supplied their army with 23,600 this era confirmed ‘‘beyond the shadow of a doubt,’’ was a
sheaves, each containing 24 arrows, or 566,400 arrows in 1763 British plot to spread disease through the transfer of
all.142 How necessary or useful were poisoned weapons in smallpox-contaminated fomites to Native Americans dur-
such a setting? How easy would it have been to poison so ing Pontiac’s War. Often attributed to Lord Amherst, the
many arrows? British commander in North America who advocated
At least one archeologist argues that poison arrows were spreading smallpox among hostile Indians, the evidence
used by Slavs in parts of Poland into the 14th century ce, suggests that the actual ‘‘attack’’ originated with and was
but that poison was abandoned in response to the re- executed by the men defending the loosely besieged Fort
quirement for arrows able to penetrate the improved armor Pitt. It appears that by the time Amherst wrote in support
adopted by soldiers in the late medieval era.143 of the plan, it had already been executed. Unlike most other
incidents, we do not need to infer culpability, because the
historian can refer to original documents describing what
the British did and why they did it. Fortunately, we have
Indigenous Peoples: some excellent histories, especially the recent writings of
Native Americans and Aborigines Elizabeth Fenn,149-151 who built on earlier scholarship
The most credible allegations of BW reviewed by Wheelis apparently unknown to the BW community.152,153 More
involved use of the smallpox virus against Native Ameri- recently, Erica Charters has tried to understand how the
cans. Indigenous peoples can be highly susceptible to in- British at the time understood the ethical implications of
fectious diseases because they often are immunologically intentional disease introduction, concluding that they rec-
naı̈ve and rarely have needed medical or public health ognized that it was outside the bounds of conventional rules
practices to combat them.144 Often they ascribed human of warfare.154
agency to disease outbreaks. Accordingly, it is not a surprise The 1763 incident thus constitutes the first well-
either that Native Americans might have been the target of documented instance of deliberate spread of an infectious
BW or that they would fear infectious disease. Nevertheless, disease. While we know the intent and the action (giving
Wheelis, almost certainly correctly, considers almost all of contaminated material to the Native Americans), we do not
the allegations doubtful, although oral traditions among know the result. It is possible that the smallpox outbreaks
Native Americans suggest that they were subjected rou- among the Indians resulted from other interactions, and
Wheelis provides several plausible alternative routes of This outbreak quickly spread widely through the Aborig-
transmission.20 inal population in southeast Australia. So devastating was
There is another alleged incident involving Native the impact that some modern historians believe that it
Americans that has in recent years received more attention made possible European settlement of Australia in the
than all the others combined. Wheelis mentions an alle- face of Aboriginal hostility. The cause of the outbreak
gation that an 1837 smallpox outbreak among the Man- has been a mystery, because the First Fleet was free of
dans resulted from the deliberate introduction of the smallpox.164-167
disease, only to dismiss it.20 He does not refer to the Several theories have been offered to explain the unex-
writings of Ward Churchill, a prolific author who wrote pected emergence of smallpox at that time. Some historians
several accounts of the outbreak, not all consistent with one believe its appearance might have resulted from infections
another, claiming that the US Army deliberately provided originating on Australia’s northern coast due to transmis-
smallpox virus–contaminated blankets to the Mandans in sion from Macassan fishermen known to visit there. Critics
1837, causing a major outbreak that killed possibly as many of this theory argue that it is unlikely that an unbroken
as 100,000 Indians.155 Subsequently, Churchill seems to chain of transmission could have been maintained for such
indicate that the number of victims might have been a distance.166 Another theory, that it might have been in-
400,000.156 troduced by a French exploration that visited Botany Bay in
Reviews of Churchill’s work demonstrate that his ac- early 1788, has not been explored in any detail. However,
counts of the outbreak are unsupportable.157-159 If they the French apparently made no mention of smallpox,
had been true, the 1837 smallpox outbreak would have which the British certainly would have recalled when trying
constituted history’s single most significant instance of BW. to understand the unexpected appearance of the dis-
While some contended that the critiques of Churchill’s ease.164,167 While the French ships were wrecked before
scholarship were highly politicized (because the University returning to Europe, they left behind records of their ac-
of Colorado launched its investigation in response to his tivities in the months before visiting Botany Bay.168
attacks on US policy following the 9/11 attacks), there The prevailing theory, however, is that the British almost
seems little doubt but that his conclusions related to BW certainly introduced the disease. It is known that the First
had no merit.160 Fleet’s physician had some bottled smallpox material, as an
There is at least one other incident that deserves more account of the expedition reported, ‘‘Our surgeons had
attention, although it may not be possible to learn more brought out variolous matter in bottles.’’164(p2) There was
about it. Wheelis mentions that Isaac McCoy, a respected considerable conflict between the whites and the Aborigines,
Baptist missionary and Indian agent, reported that he had resulting in the death of both settlers and members of the
evidence showing that in 1831 certain members of a wagon marine contingent protecting them. Moreover, the marines
train carrying trade goods from St. Louis to Santa Fe de- were woefully unprepared for their responsibilities, being
liberately spread smallpox among the Pawnee Indians, too few to protect the area being colonized and having ne-
causing thousands of deaths. Unfortunately, all we have is glected to bring sufficient stocks of ammunition and repair
the single account in McCoy’s memoirs. An affidavit he equipment.166,167
mentions does not appear to have survived.20,161 This is the Advocates that the introduction was intentional also refer
only credible 19th century claim of a deliberate attempt to back to the 1763 incident at Fort Pitt.166,167 This is more
spread smallpox among Native Americans, and it deserves problematic than they would suggest, given that it is un-
closer examination. clear how many people were aware of the incident at the
While actual attacks were rare, there were numerous time. It is unclear that anyone knew about this incident
instances in which someone, usually a white man but oc- until 1870, when the historian Francis Parkman described
casionally a Native American, threatened to deliberately the episode in the 6th edition of The Conspiracy of Pontiac
spread disease, usually smallpox.149,158 Wheelis describes and the Indian War After the Conquest of Canada.169
one such incident, involving a fur trader in the Pacific Equally important, advocates point to Fenn’s argument
Northwest in 1812, but there were others as well.162 Per- that the prevailing moral standards in British society did
haps also relevant to this discussion is the so-called Whit- not forbid genocidal practices against primitive peo-
man Massacre, an 1847 Indian attack on a white settlement ples.149,167 Fenn’s views, however, are contested, so they
that was sparked by belief among the Cayuse in the Pacific cannot be taken as the last word on the subject.154
Northwest that deliberate ‘‘poisoning’’ by Dr. Marcus Ultimately, we have a strong circumstantial case sup-
Whitman caused a measles epidemic that devastated the porting the theory that someone deliberately introduced
tribe.163 smallpox in the Aboriginal population. The strength of the
There also is one claimed use of biological agents against case depends heavily on the exclusion of alternative expla-
Aborigines in Australia. The first white settlers, convicts nations, and advocates have done yeoman’s work under-
transported by the so-called First Fleet, arrived at Botany mining those alternatives. Some of the arguments made by
Bay in January 1788. In April 1789, British authorities dis- some advocates go well beyond the available evidence.
covered a smallpox outbreak among the nearby Aborigines. Nevertheless, the extensive research into the disease, the
careful exclusion of alternative explanations, and the at- certain infectious diseases. As a result, better evidence is
tention to counterarguments make this a model exploration needed before concluding that the actions were intended to
of a possible instance of BW. cause disease.
Fenn reviews claims that the British tried to spread
smallpox during the American Revolution. While many
18th and 19th Century Wars Americans at the time clearly believed rumors of British
There are several claims that biological agents were em- efforts to spread smallpox, there generally is no supporting
ployed during 18th and 19th century wars. Most of these evidence. On several occasions, the British sent people
allegations are simply not credible. suffering from smallpox into areas held by the rebels, or
Some sources claim that the Russians hurled the bodies of allowed smallpox-infected people to be captured by the
plague victims into the city of Reval (now known as Tallinn) Americans. However, we do not know why the British
during a 1710 siege, causing a plague outbreak.2,4 The re- acted in that way. While it is possible that they were trying
ality appears to have been somewhat different. In 1710, the to spread disease, it is also possible that they were trying to
Russians were seizing Swedish-held territory on the Baltic rid themselves of the burden of dealing with smallpox pa-
coast. As part of that campaign, a 5,000-man Russian army tients. In only one instance did Fenn locate supporting
camped outside Reval in mid-August and cut the city off evidence that the British considered deliberate spread of the
from surrounding areas on August 22. However, the pres- disease: a letter sent to General Charles Cornwallis a few
ence of plague was detected on August 10 and was in full months before his defeat at Yorktown in 1781.149 For that
force by the time the Russians approached the city. About reason, there are grounds for skepticism. Philip Ranlet, who
three-quarters of the 20,000 people in the city had died by examined these claims in some detail, is skeptical, and
the time the epidemic ended. Although the Russians never correctly points out that fears of intentional smallpox are
assaulted Reval, they contaminated a stream that flowed into not matched by evidence to support them.173 Leitenberg in
the city with the corpses of their dead (not necessarily plague his original study mentioned a claim that the Americans
victims). It is not clear whether this was to cause disease, to also used smallpox against the British during the Revolu-
make the water undrinkable, or was merely a convenient tionary War.2 The source was a 1969 comment by the
way to dispose of the bodies. A Swedish army officer who Chief Counsel to the House Armed Services Committee
was present blamed the plague outbreak on the contami- during a hearing. The basis for his assertion is not given.174
nated water, but that is highly unlikely.170 Similarly, it does not appear that anyone has researched the
What is clear, however, is that the claim that the Russians validity of allegations, circulating in Canada in 1865, that
catapulted dead bodies into the city is completely wrong. the United States tried to infect British-allied Indians with
All these accounts appear to have originated with a report smallpox during the War of 1812.175,176
issued by a Swedish defense agency. There has been a A French source (not located for this survey) apparently
considerable amount of work done on the plague outbreaks reported that in 1785 a Tunisian army sent clothes con-
that occurred at that time in Eastern Europe and the Baltic taminated with plague to their enemy.4,177 This may be a
area, including some studies focused specifically on Reval. misrepresentation of what actually happened. There was a
Unfortunately, most of those accounts are in German or major plague epidemic in Tunis during 1784-85, causing
Estonian, so they have not been consulted for this study. much loss of life. The small European community isolated
Wheelis, who examined the evidence he could find, found itself from the rest of the city and suffered far less. Ac-
the allegation dubious.20 cording to one account, ‘‘By burying their dead near the
Another dubious allegation asserts that Napoleon Bo- walls and throwing rags dipped in suppurating buboes over
naparte tried to use malaria to break the resistance during the walls, the Muslims tried to introduce the disease among
the siege of an Austrian army at Mantua in 1797.16 the Christians, indicating their belief in contagion and their
However, campaign histories do not support the claim. If resentment of the European presence.’’178(p30)
anything, the risk of malaria posed as much of a danger to We have considerably more information about plots and
the besieging French as to the Austrians. The Austrians suspicions of plots during the American Civil War. The
surrendered in February 1797 after an 8-month siege. first effort to review this topic was Paul Steiner’s Disease in
During the final months of the siege, typhus, dysentery, the Civil War: Natural Biological Warfare in 1861-1865, a
scurvy, and starvation were the main causes of illness.171 medical history.179 On several occasions, Southern officers
More plausible are allegations that Napoleon ordered his believed that Northerners tried to spread smallpox among
commanders to break dikes in the Netherlands in 1810 to their forces, although there is no confirmation.179 Some
promote the spread of malaria among British troops, al- Southerners also believed that the North deliberately in-
though it is unclear how much of the resulting illness re- oculated Southern prisoners of war with smallpox vaccine
sulted from preexisting conditions and how much from the contaminated in some fashion with syphilis. That particular
claimed French actions.172 It is possible, however, that the claim was investigated by the US Army, which denied that
dikes were destroyed to obstruct the movement of enemy it occurred but suspected that there may have been side
armies, not to create conditions conducive to the spread of effects resulting from the poor health of the prisoners.180
Steiner, for one, was confident that no one considered BW starting with early civilizations and continuing through
during the Civil War: ‘‘no evidence is found for the de- the medieval era. In some cases, we know that more
liberate use of disease as an offensive weapon by either can be learned. In other cases, it is unclear whether the
side.’’179(p43) absence of information results from lack of research or
In fact, there was a plot to employ BW. Although the from the lack of material to be researched.
episode received considerable attention at the time, it was 5. The growth of the taboo against poisons in civilized
largely forgotten until uncovered by historians researching societies, especially the evident decline in the use of
related topics. Thus, Nancy Disher Baird, an archivist, poisonous substances in warfare: It is widely argued
uncovered reports about this plot while writing a biography that norms developed against the use of poisons in
of Luke Pryor Blackburn, who was a governor of Ken- war. However, we know little about the use of poi-
tucky.181,182 Additional details were uncovered by a stu- sons or about attitudes toward them in the transition
dent of the Lincoln assassination, Edward Steers, who from primitive to more modern societies. Accord-
mentioned the incident in his pioneering research.183,184 ingly, it is difficult to understand how and when such
Jane Singer provides probably the best single account of the a shift may have occurred.
story in her works on Confederate covert operations, but 6. Threatened use of pathogens against or by Native
she adds nothing to what was already known.185,186 Americans: It is possible that there is little more
Northern officials collected considerable evidence to useful to be said about this topic, but it would be
support allegations that Blackburn had collected clothing worth the effort to ensure that was the case. Where
and bedding from yellow fever victims, intending to use it did the British come up with the idea of dissemi-
to cause outbreaks in Northern cities and among Union nating smallpox-contaminated materials? Is there a
forces. At the time, many physicians and sanitarians be- possible linkage between the incident at Fort Pitt and
lieved that yellow fever could be spread by fomites, but we the alleged use in Australia? Is it possible to say more
now know it could never have worked. More plausibly, about the incident described by Isaac McCoy?
Blackburn also hoped to infect Abraham Lincoln with 7. Attempts to employ biological agents during the
smallpox, but we now know that Lincoln probably had a American Civil War.
mild case of smallpox in late 1863 and so would have had
immunity.187
The Emergence of Scientific BW:
1880-1945
A Research Agenda
The following is a list of topics from the period before the It is sometimes assumed that the dramatic advances in
development of germ theory that could benefit from ad- microbiology during the late 19th century and first years of
ditional research. the 20th century opened the way for BW. Certainly, bi-
ologists understood that microorganisms could cause dis-
1. A global perspective on arrow poisons: There has ease in humans, animals, and plants. Bacteria and rickettsia
never been a comprehensive, global study of arrow were known at the time, although knowledge of viruses
poisons in English. The last such survey of arrow lagged. Yet, it is misleading to say, ‘‘Modes of transmission
poisons is now approaching a century old, so it is were well understood for many agents.’’188(p35) In reality,
perhaps time for an updated study to supplant the the understanding of disease transmission was hampered by
studies of Lewin and Perrot. the prevailing view, certainly held by most scientists and
2. The cultural and scientific context of biological agent health professionals in the Anglo-American world, that
use by primitive societies: Most studies of poison use infectious diseases were transmitted primarily through
by primitive societies focus on what they did, rather contact exposure, and that the airborne route was of ‘‘minor
than on why they chose to use poisons or the moral importance.’’189 This perspective on the issue of disease
implications of such use. There is opportunity for transmission through the air is reflected in the writings of
studies from an anthropological perspective. an icon of American public health, Alexander Langmuir.
3. An assessment of the contaminants used by tribal According to his accounts, only a 1934 study by William F.
societies allegedly capable of causing infection: There Wells began to erode this dogma.190-193
are widespread claims that indigenous peoples cre- Studies conducted by the World War II biological
ated arrow poisons, apparently for warfare, intended weapons programs of the United States and Great Britain
to cause infection. This topic would benefit from definitively demonstrated the importance of the airborne
both a comprehensive survey of such reports and an route and, even more significantly, the importance of bio-
assessment of their scientific plausibility. logical aerosols. Most of this knowledge, however, was
4. Exploring possible use of toxins among early civiliza- gained too late and affected the conduct of BW programs
tions, especially non-Western: There has been little or only during the early Cold War. When it was assimilated,
no exploration of possible use of toxins by armies, the result was a ‘‘theory of biological warfare,’’ to use
Langmuir’s phrase,190 that changed the potential impact of more to be said about these matters is unknown, but it is
a BW attack as much as the invention of the atomic bomb also a topic that has never attracted the attention of
changed the potential effect of explosive devices. From this someone potentially familiar with the appropriate source
perspective, the BW threat was far more limited before material.
1945 than is commonly realized. Of particular interest for this essay is another topic that
It is unclear to what extent this perspective was shared until recently received little scholarly attention: the criminal
elsewhere. Anglo-American researchers appeared largely use of pathogens and bacterial toxins as weapons. There
unaware of the research performed by André Trillat, a were a number of rather dramatic cases during the first years
French military scientist who did pioneering work on air- of the 20th century, including incidents in Germany,
borne transmission of disease during the 1920s and 1930s France, and possibly the United States. Equally significant
that anticipated the later work done in British and Amer- was a Russian incident involving the use of diphtheria
ican laboratories.194 To what extent Trillat understood the toxin, making use of the new discoveries in microbiology to
physics and biology of aerosol infection, as opposed to access a toxin previously unavailable. These incidents are
droplet transmission, is unclear from the secondary litera- reviewed in a survey of terrorism and criminal cases ex-
ture, so his publications merit further investigation by amined by me, relying almost exclusively on English lan-
someone with expertise in aerobiology. There is little evi- guage sources.203 Such incidents appear to have been rare,
dence to demonstrate that other BW programs were equally but, given the lack of serious attention to the topic of
sophisticated. Neither the German, Japanese, nor Soviet biocrimes, it is impossible to determine how rare they were.
programs seem to have fully understood the implications of It deserves more attention by scholars able to work with
pathogen aerosolization prior to World War II. According non–English language sources.
to Zilinskas and Leitenberg, the Soviets began to under- One additional episode may merit attention. In 1901
stand the role of aerosols only after studying the tularemia and 1902, rumors suggested that the Boers had infected
outbreaks during the siege of Stalingrad.24 The only effort horses, purchased in the United States by the British for
to undertake a cross-country analysis of this topic is a shipment to South Africa, with the pathogens causing
monograph by Neil Davison.195 It is a subject that merits glanders and anthrax. It is not known what steps, if any,
additional research. were taken to investigate these allegations.204-206 While it
seems highly unlikely that the Boers actually used biological
agents, the persistence of such rumors is intriguing. As with
Before 1914 many such allegations, the subject has not been scrutinized
The use of toxins for assassinations and criminal activities in the secondary literature.
has a long, if not well documented, history. Unfortunately,
most studies tend to be sensationalistic. It is a topic worthy
of more serious study, including, perhaps, an exploration World War I
into the reasons why it appears that the poisons of choice The German military was the first to rely on biology to create
transitioned over time from toxins to metallic poisons. a new form of warfare. During World War I, the German
Some 19th century anarchist theoreticians, such as Karl general staff mounted a substantial effort to use biological
Heinzen and Johann Most, expressed interest in biological agents against the Allies, targeting mostly horses and live-
agents, although they clearly had no understanding of the stock. The French reciprocated, but on a much smaller scale.
science.196-199 These ideas never found an audience, although The best summary of these activities appears in another essay
we do not know why. However, a British journal claimed that by Mark Wheelis, ‘‘Biological Sabotage in World War I.’’188
some anarchists did resort to bioterrorism. In 1894, Tit-Bits His account superseded early studies,207,208 and has not been
(a popular British magazine of the era) reported that anar- overtaken by more recent histories. It has been supplemented
chists imported yellow fever–contaminated materials into by a biography of one of the German saboteurs, Anton
England in the early 1890s, killing several customs offi- Dilger, which provides much new information about his
cials.200,201 Since we know that fever is not transmitted operations in the United States. Unfortunately, as with other
through fomites, the story cannot possibly be true. We are recent books describing German BW in the United States, it
also told that Johann Most contemplated spreading cholera is a journalistic account without a standard scholarly appa-
and yellow fever ‘‘for the purpose of exterminating mankind, ratus. All we are given is a list of sources for each chapter.209
rather than suffer the present condition of society to perpet- This same weakness mars another recent account of these
uate itself,’’ certainly another canard.202(p244) activities, told from the perspective of the New York Police
We thus find 2 interesting developments. Terrorist the- Department detective who played a central role in uncovering
oreticians discussed the use of pathogens for bioterrorism, the German activities in the United States.210
but their views generated little or no interest in terrorist Efforts to reconstruct what happened have been limited
practitioners. At the same time, some members of the press, by the destruction of relevant German archives. It is clear
drafted into the cause of combating anarchism, found it that the German military organized and implemented a
useful to raise accusations of bioterrorism. Whether there is global campaign to spread infectious diseases in animals,
relying on anthrax and glanders, operating in Finland, the ever investigated or if they were scrutinized and dismissed
United States, Spain, Argentina, Romania, and elsewhere. because there was no corroborating evidence. Irrespective of
The best-documented parts of the German program are the merits of the allegations, this apparent widespread fear of
their operations in the United States and Romania. The US German BW merits more attention by today’s researchers.
government collected a considerable amount of material to That there is more to learn about German activities is
support its claims against Germany for its violations of US evident from the research of Jamie Bisher, who located ad-
neutrality. In addition, the United States was involved in ditional material about the activities of Baron Otto Carl
the seizure of sabotage supplies from the grounds of the Robert von Rosen, a Swedish national working for German
former German embassy in Bucharest, which included vials intelligence in Finland, using Norway as a base of operations.
containing cultures of Bacillus anthracis.188 At the time, Finland was part of Russia, but many Finns
The Germans, we are told, had no interest in causing sought independence and worked for the Germans during
human casualties. Rather, their efforts were directed against the war. Relying on material found in the US National Ar-
horses and mules supporting the Allied war effort. World chives and in extracts from a Norwegian police officer’s
War I armies depended largely on horses to move equip- autobiography, Bisher found that the primary target of the
ment and supplies, and the rigors of war meant that they anthrax was not reindeer, as commonly reported, but horses
needed a steady supply of new animals to replace those lost used by Russian army units. In addition, Baron von Rosen’s
in combat. Operations in the United States, Spain, and diary mentioned providing Finnish separatists with patho-
Argentina apparently focused on horses and mules pur- gens that caused both anthrax and typhus (the Germans also
chased by the Allies. The pathogens causing anthrax and relied on locals to spread disease among horses in the United
glanders were the agents of choice, usually shipped clan- States). When the baron was arrested in early 1917, the
destinely from Germany, although small labs were estab- Norwegians found boxes in his belongings filled with sugar
lished in Spain and the United States as well.188 cubes, each containing a small glass vial filled with B. an-
There remain a number of unanswered questions about thracis, and a glass jar with ‘‘toxic bacteria bullion.’’ Re-
German BW activities in the United States. One of the more portedly, the Smithsonian Institution possessed some of
interesting arises from a reference in an early account, Henry those vials but destroyed them in the 1960s.213,214 It remains
Landau’s The Enemy Within. According to Landau, papers an interesting question as to how those vials ended up in
found in the possession of a German embassy official included Washington. In any case, someone able to read German,
reference to the expenditure, through November 30, 1915, of Norwegian, Swedish, and Finnish probably could undertake
$82,109.08 to acquire tetanus germs.208 To this must be research that would reveal more about this episode.
added 2 other interesting facts. First, Dilger had some famil- German BW during World War I presents a final conun-
iarity with tetanus from his work as a military surgeon during drum. According to Wheelis, German officials associated with
the Second Balkan War.209 Second, public health laboratories the program certainly believed it was effective, but he could
in 1917 found court plaster, a predecessor to the adhesive find limited evidence to support that view. It is an interesting
bandage, contaminated with Clostridium tetani. US officials question whether the Germans deluded themselves, which is
doubted that the contamination was intentional, but it is not the prevailing consensus, or if the Allies were unaware of the
clear that they had any basis for reaching such a conclusion.211 consequences of the BW operations.188 Martin Furmanski
It is possible, perhaps likely, that the skepticism was warranted. researched British veterinary records and presented his con-
However, the matter deserves more attention. clusions at a 2004 conference. Based on these records, he
It is generally believed that the Germans stopped using concluded that the impact ‘‘was militarily insignificant.’’215
biological weapons in the United States after the US dec- Unfortunately, Furmanski has not published his research.216
laration of war. This conclusion may be an artifact of the France was the only other country that dabbled in BW
peculiar nature of the primary records used to research during World War I, according to Wheelis. Thus, the
German BW activities in the United States. Most re- French reportedly infected horses in Switzerland that were
searchers have relied heavily on the records of the Mixed being shipped to Germany with Burkholderia mallei and
Claims Commission, which was established to litigate US may have provided unidentified pathogens to prisoners of
claims that Germany violated its neutrality. The commis- war inside Germany to employ in sabotage operations.
sion had no interest in German activities that occurred However, he suggests that additional research needs to be
while the 2 countries were at war. done in French archives to understand the scope of those
In any case, there was widespread popular suspicion that activities.188
the Germans were responsible for anthrax outbreaks on
ranches and in dairies throughout the United States and its
territories. There is no evidence to link any of these outbreaks Between the Two Wars
to German saboteurs, but the epidemiology of some of the In November 1920, the British raided an Irish Republican
incidents led responsible government officials to suspect hu- Army safe house and captured a trove of documents, in-
man involvement.212 The existing histories make little or no cluding one attributed to Michael Collins, the IRA’s com-
mention of these allegations, so we do not know if they were mander-in-chief, proposing use of biological weapons.217
While supporters of the IRA claimed that it was either a extremely poor science. Given the controversies surround-
forgery or a plant, historians generally accept the British ing the Armenian genocide, and the intense emotions it
government claims.218 If real, this memorandum is unique: engenders, a cautious approach must be taken to accepting
It appears to be one of the few discussions of biological agent or rejecting the possibility of intent to deliberately spread
use written by someone in a position of responsibility in a typhus. Some authors have called into question the quality
terrorist or guerilla organization. Unfortunately, there has of Dadrian’s research, suggesting that he made selective use
been no satisfactory history written of this incident, so we do of material and quoted original sources out of con-
not fully understand its provenance, the context in which text.223,224 Such criticisms were not aimed specifically at
the plan was written, or its broader significance. The Ger- this allegation, so they are not a reason to reject Dadrian’s
mans recruited agents of Irish origin during their activities research out of hand. In any case, it would be useful to have
in the United States, and it would be interesting to know if the technical documents associated with the incident re-
the IRA’s leadership knew of that experience.188 viewed by someone with appropriate scientific training.
Vahakn Dadrian, a respected historian of the Armenian Lévi-Strauss, who heard reports of smallpox virus dis-
genocide, has reported allegations that some Turks delib- semination in colonial Brazil by the Portuguese, also re-
erately inoculated Armenians with ‘‘typhus.’’ He describes 2 ported hearing of similar tales in the modern era. Indeed, he
separate incidents in which Turkish physicians injected seems to claim that similar methods were used between
Armenians with blood from ‘‘typhus’’ patients under the 1918 and 1935 by Brazilian landowners to eliminate the
guise of developing or providing prophylactic protection. Indian population of the Brazilian state of São Paolo. He
For one of these episodes, he draws primarily from the describes what happened as follows:
outraged descriptions provided by Turkish physicians not
complicit in the alleged events, while the other relied on the Their favourite pastime [referring to the Brazilian upper
observations of an Armenian physician.219 class] had been to call at the hospital for the clothes left
Typhus epidemics had a tremendous impact on the behind by those who had died of small-pox: these they
conduct of World War I. At the time, the only treatment would then strew, together with other presents, along the
lanes still used by the natives. This brought about the fol-
available for typhus patients was supportive therapy, al-
lowing brilliant result: that whereas in 1918 two-thirds of
though there was hope of developing both a vaccine and a
the State of Sao Paulo (as big as France, by the way) was
‘‘serum-therapy,’’ presumably meaning antibodies obtained marked on the map as ‘unexplored territory, inhabited only
from the blood of an infected animal.220 This was the ap- by Indians’, not one single native was left by the time of my
proach successfully used to treat other infectious diseases arrival in 1935—with the exception of a few isolated
at the time, such as anthrax.221 There is one difficulty families on the coast who sold ‘curiosities’ every Sunday on
with this account that requires some further exploration. the beaches of Santos.146(p51)
Furmanski notes that during this period the Germans, and
those trained by the Germans, used the term ‘‘typhus’’ to I have done a thorough review of criminal use of pathogens
refer to the disease now called typhoid. The Germans re- during this period, identifying a number of cases in the
ferred to what is now called typhus as ‘‘exanthemous ty- United States, Japan, and India.203 The Japanese cases re-
phus’’ or ‘‘spotted fever.’’216 Hence, it is unclear if this ceived additional attention by a Japanese researcher, Ma-
account is about the disease caused by Salmonella typhi or saaki Sugishima.225 However, I have also mentioned other
the one caused by Rickettsia prowazekii. cases, listed as ‘‘probable or possible,’’ in Hungary (alleged
Another author suggested that this incident constituted pathogen involvement) and Germany (involving a toxin),
‘‘the initial, scientifically-informed use of biological but was unable to further investigate them.203 The use of
agents.’’222(p222) Such a claim is clearly not sustainable, even pathogens as a murder weapon appears rare, but it is un-
if the incidents involved deliberate attempts to spread dis- clear whether more such cases would emerge from explo-
ease. The author was unaware of the well-documented use ration of materials in languages other than English.
of biological agents by the Germans during World War I. According to documents uncovered by an Italian re-
The episodes described by Dadrian merit further re- searcher, Alberto Sbacchi, Benito Mussolini suggested in
search, and his account suggests that there is additional February 1936 that his troops employ bacteriological
information available about both incidents. He indicates weapons in Ethiopia, but that one of his field commanders,
that records associated with one of the incidents were Marshall Pietro Badoglio, objected for political reasons.
believed to exist in an archive in Soviet Armenia (Dadrian According to the documents reviewed by Sbacchi, the
wrote his account before the collapse of the Soviet marshall worried that the main victims would be pro-
Union). The physician involved in the other incident Italian Tigreans and that any operational benefit would be
published a medical journal article about his work, which outweighed by negative international reaction. Sbacchi also
Dadrian apparently did not locate, but which should be suggests that the Italians would have used BW if their
obtainable. chemical weapons had proven less effective earlier in the
That these activities were documented suggests they war, although it is unclear if this is his personal opinion or if
might have been highly unethical research coupled with the documents state this directly.226
Japanese BW During World War II In any case, the literature suggests that the scope of Japanese
operations declined after 1942 for unexplained reasons.
Japan’s use of biological weapons constitutes the single Examples of what can be accomplished using the available
most important instance of BW and represents the only sources is illustrated by 2 important studies. A chapter in a
known concerted effort to employ biological agents in book by R. Keith Schoppa provides an account of the impact
the context of combat operations during a war. Appro- of the 1940 biological attacks on 2 Chinese cities, Quzhou
priately, the Japanese program has been the subject of and Ningbo, focusing on the nature of the responses by the
numerous accounts of uneven quality. Most authors focus local governments. He demonstrates that the consequences
on the horrors of Japan’s use of human subjects to study were far more severe in Quzhou due to the inefficiency of the
the clinical effects of infectious diseases. Thousands local government. While Quzhou ultimately suffered 2,000
of people were murdered in these experiments, perhaps deaths, the government and people of Ningbo organized a
as many as 10,000 according to some accounts, which highly effective response and managed to limit the number of
equaled or even exceeded the horrors of German con- fatalities to 107. According to Schoppa’s research, many of
centration camp medical experimentation.227-234 Much the victims died as the disease spread because of the move-
less attention has been devoted to Japanese military use of ment of those originally infected to apparently unaffected
biological weapons. areas.237 The richness and detail that Schoppa provides,
The English language literature on Japan’s use of bio- drawing heavily on local newspapers, is strongly suggestive
logical weapons is unsatisfactory. Despite its importance, that it should be possible to better document other attacks.
historians and others have focused far more attention on the Martin Furmanski wrote an interesting study of Japan’s
program itself, and especially on the medical experimen- 1942 Zhejiang BW operations. The Zhejiang campaign
tation. Sheldon Harris wrote a chapter in the volume edited was mounted in response to the Doolittle raid on the
by Geissler and Moon that provided an excellent English Japanese homeland, because of a false belief that the
language summary of the military operations235—better bombers had operated from Chinese territory. Furmanski
than the one that appears in his book-length study of the argues that the BW attacks were part of a larger operation
Japanese program.233 However, it is not free of flaws, such intended to prevent future aircraft raids from that area.238
as the unsubstantiated claim that the Japanese biological He believes that this may have been the most important
attacks killed ‘‘several hundred thousand’’ Chinese.235 BW campaign ever conducted, because it was undertaken
Much of the literature on the Japanese BW program is to achieve strategic and operational objectives.216
from Japan and China. There is a substantial Japanese lit- A different kind of study by John Walker reviews what
erature on their BW program, based on a cursory review of was known by one country (the United Kingdom) about a
books held by the Library of Congress. Its catalog reports specific instance of claimed Japanese BW employment in
holdings of 26 Japanese-language books catalogued under November 1941.239 It also usefully highlights the com-
the subject ‘‘Sino-Japanese War, 1937-1945—Biological plexities of bioattribution.
warfare,’’ published between 1981 and 2009. The Library Despite the clear importance of some of the translated
also catalogs 26 Chinese-language publications with the Chinese writings to an understanding of Japan’s employ-
same subject heading, published between 1989 and 2011. ment of BW, they also pose a problem for the serious stu-
These studies were not reviewed for this survey. Their dent of biological warfare. Consider, for example, the study
quality is unknown, although review of some translated by James Yin, The Rape of Biological Warfare, produced with
materials suggests that at least some of it is very good. the assistance of the ‘‘Japanese Biological Warfare Crimes
An essay by Tsuneishi Keiichi, translated from the Jap- Investigation Committee.’’228 The author and his collab-
anese, gives a more recent survey of the program and its orators took advantage of surviving material to present a
employment of biological weapons and deserves greater book-length account that provides extensive information
attention.236 Considerably more detail appears in a number on what the Japanese did with their biological weapons.
of Chinese publications providing English translations of This is a welcome contrast to most Western writers
some or all of their text.228,231,232 This Chinese literature who focus largely on Japanese biological weapons research
provides a rich lode of original material, based on surviving facilities. While the production value of Yin’s book is
documents, interviews with survivors of attacks and their poor—it is filled with misspellings and what are clearly
perpetrators, and physical evidence collected by partici- poor translations—the more significant problem is the
pants and researchers. inadequate analytic rigor. It is unclear to what extent the
A cursory review of this literature suggests that it may author and his collaborators really understood the science
now be possible to piece together a more detailed view of and technology of BW or the epidemiology of disease spread.
Japan’s wartime employment of BW, even if significant Yin convincingly documents that the Japanese resorted
gaps remain. One Chinese researcher has identified 161 to BW far more extensively than generally believed, but he
different incidents involving the use of biological agents.228 fails to make a convincing case for the magnitude of the
In contrast, Harris lists only 7 major operations through impact. He claims that nearly 750,000 deaths resulted from
1942, presumably excluding the many smaller attacks.235 the attacks. This includes nearly 110,000 people who died
after the war from outbreaks that he associates with the causing typhoid fever, it is unclear whether the perpetrator
earlier Japanese BW operations. His totals derive from a was acting alone, as part of an independent partisan group,
tabulation of the deaths associated with around 130 attacks, as an agent for the Soviet Union, or as an agent of some
as well as those murdered in the research facilities. This is other government. However, the Germans claimed to have
several times more than the highest estimate for the number found at least one Soviet document ordering partisans to
of deaths from the atomic bombings of Hiroshima and use biological agents against the Germans.243 This last al-
Nagasaki. legation comes from the writings of David Irving, whose
Are such allegations credible? An old adage suggests that known Nazi sympathies make many skeptical of his re-
an extraordinary claim requires extraordinary proof. While search. He also provides no references for this particular
Yin makes extraordinary claims, he does not provide ex- assertion, although checking his claims should be easy,
traordinary proof. Given that some of the diseases em- because his account is based on captured German docu-
ployed by the Japanese often appear in war zones or socially ments.244 Although both of Geissler’s essays seem to treat
disrupted areas, the causal linkage between alleged attacks all the attacks identified by the Germans as related, the
and claimed outbreaks requires careful scrutiny. Yin re- political differences between the Soviet Union and the
ports, for example, evidence that the Japanese spread Poles make any connection unlikely.
cholera in August 1943 in western Shandong, and that There are enough hints about the Polish activities to
200,000 people died as a result. This is documented in 1 warrant further exploration. Geissler and Moon included
page of text and 6 pages of supporting graphics and men- an essay on Poland in their volume, which unfortunately
tions only 2 sources. There simply is not enough evidence ignores these allegations. However, there are multiple
to justify the claim. sources that confirm Polish biological agent use. The
Martin Furmanski, who has looked carefully into these Germans believed that the Poles were engaged in bio-
accounts, is unwilling to accept such expansive claims and terrorism, investigating many such incidents. Indeed, the
concluded that ‘‘the Japanese BW program caused a few Germans reported finding a makeshift microbiology lab to
tens of thousands of deaths overall, almost all Chinese ci- support such operations. The Polish resistance also told the
vilians (if you don’t count whatever ‘blowback’ casualties British that they were using biological agents against the
occurred among Japanese troops).’’240 Germans. The Polish account reports that the German
These criticisms are not meant to denigrate the hard casualties resulted from ‘‘typhoid fever microbes and ty-
work that activists have undertaken to document an often- phoid fever lice,’’ presumably referring to the causative
ignored history. Yin correctly identifies an issue most agents of typhoid and typhus.244,245 This terminology,
researchers ignore (although the leaders of the US BW which is confusing to those schooled in modern microbi-
program understood it well).241 Biological warfare can ology, apparently reflects German usage of the era.216
cause new enzootic reservoirs and thus cause outbreaks We even have an account of one incident described by
long after an attack. Clearly, the victims of such epidemics Jan Nowak, a prominent member of the Polish under-
are as much BW casualties as those infected in the original ground, who claimed to have heard it from the perpetra-
attack, but only if the subsequent outbreaks would not tors. According to Nowak, the Polish resistance, alarmed
have occurred except for the original biological attack. that fellow Poles were taking vengeance on other Poles by
Nevertheless, the problem remains that we need much making accusations in letters sent to the Gestapo, decided
better accounts of what happened in China. to end the practice by contaminating letters with Bacillus
anthracis. The result was an outbreak of cutaneous anthrax
that caused the Gestapo to stop opening such letters.246
Geissler, who has studied the German records closely, ac-
World War II Resistance Movements cepts that the Poles used biological agents against the
and BW Germans on numerous occasions, but unfortunately pro-
The Germans believed, apparently correctly, that operatives vides few details.242,243
associated with the Soviets and Poles employed biological It is disappointing that we know so little about these
agents against their personnel. These allegations are dis- operations. If the reported German assessments are correct,
cussed in Geissler’s essay on the German BW program as they represent one of history’s most significant uses of BW,
well as in another essay on the Soviet BW program in the affecting thousands of people. It also makes the German
same volume co-authored by Geissler.242 During 1943, the lack of interest in BW even more puzzling. In the chemical
Germans apparently identified 25 incidents. In one inci- arena, Germany’s leadership felt the need for a sophisticated
dent, more than 3,800 people were infected with ty- retaliatory capability and invested considerable resources to
phus.242,243 Unfortunately, neither article provides much develop what became the world’s most advanced chemical
detail, relying primarily on German documents that report warfare capability.247 The apparent indifference to BW
on the results of their investigations into suspected bio- despite their belief that they were being attacked suggests
logical attacks. In some cases, as with the incident involving the potential value of a comparative study of Hitler’s atti-
a Czech who contaminated coffee with the organism tudes toward chemical and biological weapons, perhaps
drawing on some of the excellent studies of chemical BW program, although some BW-related research was
weapons in that period.248 conducted. There are book-length German-language ac-
counts of the BW activities of the Germans after World
War I,261-263 which this author has not reviewed. The only
Non-Use and Allegations of BW serious account available in English is an essay by Erhard
Although other countries researched biological weapons, Geissler.242 Even though the Germans pioneered the use of
including Canada, France, Germany, Great Britain, the BW, Geissler persuasively argues that Hitler refused to
Soviet Union, and the United States, it was only the Jap- support an offensive program, even for retaliatory strikes,
anese military that used them.24,194,242,243,249-252 There are and limited research to biological defense. The reasons for
numerous allegations of BW use, but most of them are Hitler’s opposition are not known. BW advocates in Ger-
unverified and are probably not true. Some of these alle- many conducted research on offensive capabilities by pre-
gations are reviewed here. tending it was permitted defensive research. Geissler
Ken Alibek, who had senior management positions in the believes, however, that it was disorganized and of uneven
former Soviet biological weapons program, claimed that the quality and that there is no evidence that the Germans ever
Soviet Union may have used BW during World War II. Ac- used even the limited capabilities at their disposal.
cording to Alibek, a major tularemia outbreak near Stalingrad Nevertheless, the British worried that the Germans were
resulted from the deliberate dissemination of Francisella tu- continuing their BW activities before the outbreak of World
larensis.253 His arguments have not convinced Western experts. War II, as documented in an important study by Martin
The German military clearly did not believe that they had been Hugh-Jones. According to a British journalist, Wickham
attacked at the time with biological agents, attributing the Steed, the Germans performed tests using biological surro-
outbreak of tularemia among their forces during the battle of gates of biological attacks, including in the Paris subway.
Stalingrad to transmission from Russian civilians.24,254,255 The accuracy of those claims is doubtful.242,264
Robert Harris and Jeremy Paxman report, apparently Frank Snowden, a historian with expertise in Italian history
relying on American reports based on interrogations of and the history of medicine, has claimed that in 1943 the
former members of the Japanese BW program, that Japa- Germans deliberately flooded the Pontine Marshes near Rome
nese police captured 5 Russian spies in 1935 and found that to spread malaria in a desperate attempt to stop the advancing
they were carrying the organisms responsible for anthrax, Allied armies.265-267 Although this allegation has appeared in
cholera, and typhoid. Allegedly, 6,000 Japanese soldiers subsequent accounts of the Italian campaign, Geissler and
died of cholera and 2,000 horses died of anthrax from Guillemin examined the evidence and found it unconvinc-
infections.245 This story cannot be taken seriously, if only ing.268 An Italian author, Annibale Folchi, an expert on the
because of the source. It is just as likely that the story was Pontine Marshes, also reached a similar conclusion after in-
invented to justify Japanese BW activities. Harris and vestigating Snowden’s allegations.269 Unfortunately, her study
Paxman claim that Ishii used the story to gain support for appears to be unavailable in the United States and was not
his activities, but it is unclear if there was any substantiation examined by this reviewer. However, her conclusions have been
for that assertion either. Without additional evidence, this summarized in a more accessible Italian language article.270
allegation cannot be accepted.
Harris and Paxman also are responsible for a widely cited
claim that the British gave weapons contaminated with A Research Agenda
botulinum toxin to Czech resistance fighters for use in the The following is a list of topics from 1914 to 1945 that
assassination of Reinhard Heydrich. There is no docu- merit additional research.
mentation to support this allegation, which apparently is
based solely on the recollections of scientists who heard the 1. Japanese use of biological weapons in China and
story from Paul Fildes, the microbiologist who directed Manchuria: The most significant gap in our under-
British BW research during World War II.245 Several BW standing of BW is the absence of a comprehensive
experts have cast doubt on the accuracy of the account. For study of Japanese use of biological agents against the
example, G. B. Carter points out that not only is there no Soviets in Manchuria and against the Chinese. There is
documentation to support the claim, but that the British considerable material in Japanese and Chinese that has
only initiated their research program in botulinum toxin not been exploited, suggesting that a serious effort to
after the assassination.256-258 More recently, Czech re- study Japanese BW operations will require one or more
searchers have discovered the autopsy report performed on people with knowledge of both Chinese and Japanese
Heydrich. There were no indications of botulinum toxin and an understanding of the technical aspects of BW.
intoxication, and the available evidence suggests that 2. German non-use of BW in World War II: How do
Heydrich almost certainly died of sepsis.259,260 we explain the contrast between Germany’s activities
Despite Germany’s use of biological weapons in World in the 2 world wars? Wilhelmian Germany had an
War I, it did not do so during World War II. Indeed, it organized BW program in World War I, directed by
appears that the Nazi regime never authorized an offensive its general staff and involving operations on at least 3
continents. In contrast, Nazi Germany did not en- descriptions of particular incidents or allegations, due in
gage in BW, and Adolph Hitler appears to have re- part to the continued classification of official documents.
jected attempts to even develop a capability for Original documentation often is unavailable, and even
retaliatory reasons. Understanding this contrast when some material becomes available it rarely tells the
might provide important insights into the motiva- whole story. Thus, the Chinese and North Koreans have
tions that lead states to pursue or reject BW. It is not released documents related to their allegations of US
unclear if there is more to say than is evident from BW during the Korean War, only a handful of Soviet
Geissler’s study, but he clearly did not feel he had documents have surfaced, and some extant American ma-
answered this important question. terial remains classified.271,272
3. Use of biological agents against the Germans by the Nowhere is the problem more evident than in trying to
Polish resistance: The evidence for terrorist attacks by document the history of the programs. Since the end of the
the Polish resistance seems strong, but little is known Cold War, the full scope and sophistication of the Soviet
about it. Researching this episode would require biological weapons program has become increasingly evi-
someone with fluency in Polish and German. dent. Of special importance is a book by Milton Leitenberg
4. Use of biological agents by Soviet-associated parti- and Raymond Zilinskas, The Soviet Biological Weapons
sans: There seem to be credible claims that partisans Program.24 This volume is the most comprehensive effort
associated with the Soviet Union used biological to study the history of the Soviet efforts to develop bio-
agents. However, only one scholar has looked into logical weapons capabilities, and it is an indispensable re-
them, and there is little in English about them. source for anyone interested in BW. Two books,
5. The Italian biological weapons program and the coauthored by former participants in the program, Ken
Abyssinia War: What were the bacteriological weapons Alibek and Igor Domaradskiı̆, provide personal perspec-
discussed by Mussolini and Badoglio in 1936? Is there tives.253,273 Although Leitenberg and Zilinskas have re-
more to be learned about this instance of non-use of searched and written an impressive history, by their own
BW? admission it tells only part of the story. The secrecy that
6. Alleged Irish Republican Army interest in BW: Al- continues to surround Soviet activity explains why they had
though no BW is associated with this incident, it is to largely ignore the roles of the Ministry of Agriculture, the
important simply because it is the only concept of use Ministry of Health, the intelligence services, and offensive
originating with a nonstate actor known to exist. It also activities of the Ministry of Defense.
would be worth knowing if there were linkages back to While there is much more information available on the
the German World War I activities, which certainly former US biological weapons program, some portion of
involved Irish-origin longshoremen in the United States. the information remains classified and a substantial amount
7. The emergence of biocrimes in the early 20th century: of material was destroyed. Thus, the CIA had destroyed the
The story of biocrimes in the first half of the 20th documents related to its clandestine program for develop-
century remains largely unwritten. The only accounts ing biological agents, as documented by the Church
draw primarily on English and Japanese language Committee in the 1970s, while the US Army also destroyed
sources. It seems clear that research by scholars fa- many of its most sensitive documents. A significant amount
miliar with other languages will uncover additional of material remains classified, or unclassified but releasable
examples. Ultimately, it would be useful to get a ho- only within the government, due to concerns that the re-
listic sense as to why biocrimes emerged, apparently lease of technical details related to biological weapons de-
largely disappearing in the years after World War II. velopment might be useful to others trying to create an
8. Anarchist reactions to ideas of BW: This is a ‘‘dog that offensive BW program.274
didn’t bark’’ story, given that there was interest in BW What is clear, however, is that scientific and technical
by 19th century anarchists, but no use. It would be advances made by the United States and the Soviet Union
helpful to understand better why the idea of biological revolutionized BW. Although the foundations of this work
terrorism would interest anarchist theoreticians, and were laid during the early 1940s, it was not until the 1950s
why those ideas apparently had no practical impact. and 1960s that the theoretical potential of BW became a
frightening reality. As the United States demonstrated in its
Large Area Coverage (LAC) exercises, biological agents
The Late 20th and Early 21st Centuries properly prepared and disseminated could have effects that
(1946-2014) matched or exceeded those of thermonuclear weapons.
Small amounts of lethal agent could cover thousands of
Writing histories of post–World War II BW is problematic. square kilometers with overwhelming doses.241,275
First, there has been relatively little use of biological Yet, the period since 1945 has seen no verified use of
weapons: a few by governments, some instances of bio- biological agents during an inter-state war. In contrast, they
terrorism, and a number of attempted and successful have been used primarily by nonstate actors, but only in
criminal cases. Second, it is often difficult to obtain detailed ways akin to the German WWI biological sabotage
operations. Despite its theoretical capabilities, or perhaps lacked the requisite scientific expertise, and that unnamed
because of them, no country has attempted large-scale BW, outside forces (the United States?) may have provided the
just as no country has employed nuclear weapons since South Africans with the biological agents to test them. In the
1945. Rather, the period 1946 to present has seen false end, however, he had to admit that he had no concrete
accusations, a few credible clandestine operations by state evidence for any of his allegations.293
intelligence services, minor cases of bioterrorism, and a A 2007 doctoral thesis on the Rhodesian BW program
spate of biocrimes. written by Glenn Cross was never released publicly.294
Since then, Cross has obtained new material and hopes to
publish a book on the topic in 2016. This promises to
State Use of BW provide considerable new information on Rhodesian ac-
There are several documented instances of BW use by tivities and to clarify many of the remaining uncertainties.
states, although none employed the new technology de- The South Africans also are known to have employed
veloped by the United States and the Soviet Union. In fact, biological agents during the apartheid period. There are
all used techniques not dissimilar from those that were several good accounts of the South African effort to develop
available at the beginning of the 20th century. biological weapons, but accounts of actual use of such
The Rhodesian military employed chemical and bio- weapons are less useful. A South African researcher,
logical agents during the war that country’s white minority Chandré Gould, has authored or co-authored the best of
fought to maintain control over what is now Zimbabwe. these studies,278,295-297 which are more carefully researched
The use of chemicals, primarily organophosphate pesti- than those by other authors.292,298,299 Unfortunately, we
cides, to contaminate clothing that was given to guerrillas is know relatively little about the actual employment of their
well documented.276,277 Less well documented is the use of biological agents. These are reviewed in the book by Gould
biological agents. It seems widely agreed that the Rhode- and Peter Folb, which lists the reported agents stocked by
sians dispensed V. cholerae on at least 2 occasions into rivers the South Africans (Bacillus anthracis, botulinum toxin,
near guerilla camps, ‘‘attacks’’ that were unlikely to have Salmonella typhimurium, Vibrio cholerae, and Brucella me-
caused any harm. These operations are discussed in several litensis) and what little is known of their use. Reportedly,
accounts, but a complete summary of the available infor- the South Africans used 1 of 32 containers of V. cholerae to
mation appears in a study of the South African chemical infect the water supply of a guerrilla camp, but to no avail
and biological weapons program authored by Chandré because chlorination killed the microbes. Sugar contami-
Gould and Peter Folb.278 nated with S. typhimurium was provided to an ANC
Of more consequence, the Rhodesians have been accused meeting, which may or may not have caused illness among
of causing a well-documented outbreak of anthrax, which the participants. Unfortunately, the South African gov-
started among cattle belonging to blacks and then spread to ernment has refused to clarify this past use, even to the
the human population starting in November 1978 and extent of falsely reporting that their country never had an
continuing through at least October 1980.279-288 According offensive biological weapons programs.278 Yet, if they only
to an account by Meryl Nass, drawing on official Rhodesian used biological agents on these 2 occasions with little to no
statistics, around 10,000 people were affected and 189 died, consequence, their effort would have constituted one of the
making it the world’s largest recorded anthrax outbreak. least cost-effective BW programs in modern history. Some
Nass, who was the first to argue that it was intentionally as yet unsubstantiated claims contend that surplus Rho-
caused, outlined evidence supporting her views in 2 articles, desian materials—largely organophosphate-contaminated
both heavily researched but neither published in a peer- clothing and poisoned foodstuffs—were used by South
reviewed scientific publication.289,290 Other accounts African units against SWAPO in Namibia.
largely repeat what Nass described, although Tom Mangold Avner Cohen, best known for his studies of the Israeli
and Jeff Goldberg did add a few additional details in a nuclear weapons program, convincingly shows that the
chapter of their book, Plague Wars.291,292 Israeli military used biological agents during the 1948
Nass offered several sensible suggestions for follow-on Arab-Israeli War. Less clear is the impact of the attacks, as
studies that might prove or disprove her thesis. It is unclear there is no evidence that BW operations, which focused on
why the government of Zimbabwe chose not to investigate water contamination, caused any disease outbreaks.300,301
her claims. Dr. Timothy Stamps, while serving as that According to a declassified 1949 CIA report, Quarterly
country’s Minister of Health, claimed to have launched an Review of Biological Warfare Intelligence, ‘‘There is some
investigation into the incident, but it does not appear that evidence that deliberate contamination by Jewish forces of
any report was issued. This being the case, it cannot be the water supply at Acre, Palestine, was responsible for the
determined if his investigators followed any of Nass’s advice. typhoid fever epidemic among British Troops during
Dr. Stamps also linked outbreaks from Ebola virus, Mar- April-May, 1948.’’302(pp3-4)
burg virus, and Y. pestis in Zimbabwe to intentional intro- A number of countries allegedly employed or tried to
ductions. He also claimed that South Africa must have been employ pathogens or toxins in assassinations, including
responsible for those outbreaks, because the Rhodesians Israel, Rhodesia, Russia, South Africa, the Soviet Union,
and the United States. Generally, such assassinations relied Minnesota Patriots Council describe real incidents that did
on chemicals, but poisons of biological origin also have been not amount to very much.314,315 Jessica Stern has provided
used. Only on occasion have pathogens been employed. what is probably the definitive account of the antics of Larry
Shlomo Shpiro attempted to comprehensively review the Wayne Harris, the white supremacist fascinated by bio-
use of biological and chemical agents by intelligence orga- logical weapons.316 John Parachini convincingly de-
nizations, but he relies totally on a selective use of secondary molishes claims that the Weather Underground, a left-wing
sources and, as a result, sometimes gives inaccurate accounts radical group, was interested in BW.317
of particular incidents.303 The Soviet Union often employed The only essay superseded by subsequent scholarship is on
poisons but also used or considered use of pathogens. Ac- Aum Shinrikyo.318 Milton Leitenberg argued that the whole
cording to a report translated by the Wilson Center’s Cold matter was overblown and distorted,319 while Richard Dan-
War International History Project, in 1953 the Soviets zig and his coauthors more recently provide a nuanced study
planned to assassinate Tito through the dissemination of that demonstrates both the grand ambitions and the con-
Yersinia pestis. The plot was cancelled after Stalin’s death.304 siderable incompetence of those responsible for the cult’s
The most famous incident was the murder of the Bul- biological weapons program.320 The Danzig et al essay is
garian Georgi Markov. Although it is often asserted that particularly valuable because of its analytic framework, pro-
ricin was used, the forensics examination could not identify viding some convincing insights into the organizational and
the poison used. Rather, the pathologists guessed that the cultural obstacles facing terrorist organizations, even when
poison involved was ricin, based on clinical symptoms.305 well-funded, that seek to develop biological weapons. It
Most recently, a Bulgarian journalist has obtained access to would be interesting to see if those insights might apply to
archives of the Communist-era Bulgarian State Security other groups, especially the Rajneeshees and al Qaida.
Service and published 2 books based on that information. At least 2 of the subjects of essays in the Tucker volume
Unfortunately, it appears that key operational documents merit additional attention, if only because they illustrate the
were destroyed, so we know little more about how the op- problems confronting those trying to write contemporary
eration was conducted than before.306,307 This suggests that history. Terence Taylor and Tim Trevan, both respected BW
aspects of this case, and others like it, may never be known. experts, failed to definitively demolish claims that French
One of the most disturbing allegations of the modern era is authorities discovered that the Red Army Faction was trying
a report that Brazilian officials with its Indian Protection to produce botulinum toxin during a 1980 raid on a Red
Service deliberately infected Amazonian tribes with the Army Faction safe house. The authors mention that a Ger-
pathogens causing smallpox, influenza, tuberculosis, and man prosecutor publicly supported the allegation at the time,
measles.308-310 Little has been written about the subject, but they never explain why he did so if the allegation was
perhaps because the Brazilian government deliberately sup- false.321 However, it turns out that all of the alleged perpe-
pressed a report documenting these allegations.311 Wheelis trators appear to have broken with the Red Army Faction in
and Sugishima correctly argue that this case is ‘‘of consider- 1980 and were living in East Germany under the protection
able importance,’’ but that it ‘‘has yet to receive the scholarly of the Stasi. All currently live in Germany, and one would
study that it deserves.’’312(p286) Although they categorize this assume they could be interviewed about the supposed plot.322
incident as terrorism, the actions were undertaken by or with Because the claimed incident occurred in Paris, there should
the direct connivance of Brazilian government officials. be some French government records related to the incident if
However, not enough is known about what happened to it really happened. In the end, Taylor and Trevan almost
clearly identify the responsible parties. certainly are right to discredit the story and to conclude that
there was no reason to believe that the Red Army Faction had
any interest in acquiring a toxin weapon. Nonetheless, the
Nonstate Use whole story still raises interesting questions about the possible
There is an enormous literature covering almost all aspects deliberate fabrication of stories intended to denigrate or raise
of bioterrorism during the period since 1945, but little is fears about terrorist groups.
focused on its history and even less makes original contri- A new study of the Rajneeshees also is needed. This is
butions. This reflects the reality that there have been few one of the few confirmed bioterrorism incidents and the
documented instances of terrorist interest in biological one that caused the most casualties. The account in my
agents and even fewer documented cases of bioterrorism. chapter in Tucker’s book Toxic Terror was derived from
The first serious studies of actual cases of bioterrorism official documents and interviews with government officials
were the articles that appeared in Toxic Terror, edited by the and journalists.323 It should be supplemented by the
late Jonathan Tucker, which examined allegations con- chapter in Germs, coauthored by Judith Miller, Stephen
cerning the activities of 7 BW incidents.313 Several of the Engelberg, and William Broad, which provides additional
case studies cast doubt on the reality of some of the alle- details.324 Both accounts are solid but not definitive. There
gations, while other studies demonstrate the reality of is certainly additional detail in FBI files. Moreover, none of
others. As a result, this is an essential resource for anyone the authors actually interviewed any of the perpetrators.
interested in BW history. The essays on R.I.S.E. and the Finally, as mentioned above, it would be useful to
reexamine the case using the template offered by the Danzig from Bioterrorism and Biocrimes, the working paper written
et al study of Aum Shinrikyo. by this author.203
Toxic Terror also did not address a number of alleged The Mau Mau apparently poisoned cattle at a mission
bioterrorism incidents. One of the more interesting is re- station with latex from either Synadenium grantii or another
lated to claims that Jewish resistance fighters who survived plant in the same family. There apparently were other similar
World War II sought biological agents to use against incidents. Some involved use of arsenic, but in other instances
German cities.325,326 The only serious look into the activ- the poison could not be identified, and it was suspected that a
ities of one of these groups, a book chapter by terrorism plant toxin was used.347 There should be evidence of this
expert Ehud Sprinzak and a colleague about a group known conclusion in archival documents held by the National Ar-
as DIN (the Hebrew acronym for Avenging Israel’s Blood), chives in Kew, Richmond, Surrey, near London.
discounts those claims.327 However, this author found My working paper mentions numerous ricin incidents, and
Sprinzak’s arguments unconvincing.203 According to Co- there have been other cases as well. A collective account of ricin
hen’s study of the Israeli chemical and biological weapons incidents might be useful. Perhaps more significant is a case
programs, at least 2 of the Israeli scientists contacted by that I also mention: ‘‘Egyptian gangsters’’ infected people with
DIN were involved in that country’s nascent biological typhoid bacteria to obtain their life insurance. Unfortunately, I
weapons program, a fact not mentioned by Sprinzak.300 was unable to follow up on the story, because the original
Given Israel’s subsequent use of BW, this interaction merits source was an Arabic-language newspaper. This is another
more attention. instance where access to a foreign language might identify (or
The most lethal use of biological agents by a nonstate actor perhaps debunk) another intentional use of a pathogen.203
since 1945 occurred after the publication of Toxic Terror. Since 9/11, US law enforcement authorities have arrested
This was the mailing of envelopes containing Bacillus an- numerous individuals for possessing or attempting to ac-
thracis spores to journalists and government officials in the quire toxins, usually ricin. In some instances, the ricin was
United States in late 2001. The Amerithrax case, the FBI found in letters mailed to intended victims. These incidents
name for its investigation, is without doubt the most thor- have received considerable press coverage but much less
oughly reported incident of illicit biological agent employ- attention in the analytic literature. The best survey of these
ment. Attributed by government officials to a biodefense incidents, putting them into context, may be a polemical
researcher, Dr. Bruce Ivins, it remains controversial. The best article by George Smith that discounts the significance of
single account is probably American Anthrax, written by ricin as a biological threat.348 His work is usefully supple-
Jeanne Guillemin, which reflects both an understanding of mented by a Congressional Research Service report and by
the science and the importance of technical aspects of the case some thoughtful scientific articles.349-351 At least one in-
ignored by others.328 Typical is the discussion of the impact dividual attempted to create a business selling toxins, and
on American officials of the Canadian chamber tests those poisons were employed in at least one murder plot.352
demonstrating the extent to which B. anthracis spores in
envelopes could aerosolize. It clearly goes well beyond
earlier accounts.329-334 Investigators issued an extensive False Allegations
official report of their findings, which laid out the basis for A considerable body of BW research during the post-1945
their identification of Ivins as the perpetrator.335 The era has focused on 2 episodes of alleged use that almost
Amerithrax literature is extensive and encompasses scores certainly never happened: Communist bloc claims that the
of technical articles, including clinical descriptions,336-338 United States employed BW in the Korean War and the US
epidemiologic studies,339-341 and scientific analyses.342,343 allegation that the Soviet allies used biological agents in
The forensic evidence used in the Amerithrax case has Southeast Asia in the late 1970s (‘‘yellow rain’’). These are
received considerable attention, due in part to the emphasis not the only such allegations, only the best known.
given it by the investigators. To support their claims, the FBI The Soviet Union and its allies made numerous claims
commissioned a National Research Council review of their that the United States has engaged in biological warfare.
microbial forensics. Although generally complimentary, the Leitenberg reviews Soviet allegations of US employment of
study did not support FBI assertions that the Amerithrax BW in The Soviet Biological Weapons Program. As he
perpetrator had to have used a specific B. anthracis culture demonstrates, the Soviet Union and its allies have made
prepared by Ivins.344 A subsequent US General Account- palpably false claims of US BW since the late 1940s.24
ability Office review concurred.345 In contrast, a court-au- A Soviet bloc campaign to link the United States with
thorized Expert Analysis Panel, which analyzed Ivins’s mental the origin of HIV has been the subject of several articles.
health records, strongly supported the FBI’s conclusions.346 Thomas Boghardt attributes the HIV campaign largely to
Ultimately, the FBI and Justice Department have not con- the East German secret police, the Stasi. In contrast, Erhard
vinced skeptics that they correctly identified the perpetrator. Geissler examined Stasi records and discounts the impor-
There are numerous other claimed uses or plans to em- tance of the East German role. Both agree that there was a
ploy biological agents by terrorists and criminals, some disinformation campaign, but they disagree about its ef-
more serious than others. The following examples are taken fectiveness.353,354
The Cubans charged that the United States attacked some kind of chemical or biological warfare attacks took
Cuba with biological agents on multiple occasions; these place, the evidence does not support any conclusion about the
claims were reviewed and refuted by Raymond Zilinskas agent employed.375-377 An article by a former CIA operations
and Milton Leitenberg.355-357 Charles Calisher gave a first- officer gives a highly skeptical view of the whole matter from
hand account of a Cuban claim that the United States the perspective of someone involved in the search for intel-
deliberately introduced the dengue virus into Cuba, putting ligence supporting the ‘‘yellow rain’’ allegations,378 as does
it into a broader perspective.358 Martin Furmanski and the account of a former Australian intelligence official.379
Mark Wheelis take a skeptical view of the Cuban claims in a False allegations were not just the product of the Cold
book chapter reviewing allegations of biological weapons War. For example, the Libyan government claimed foreign
use, but they believe that the Cubans may have had plau- medical workers (mostly Bulgarians) deliberately caused an
sible reasons to suspect that the United States was respon- HIV outbreak at a pediatric hospital, causing some 400
sible for at least 2 animal epidemics.359 cases.380,381 The allegation became a cause célèbre in the
During the Korean War, the Communist bloc countries international scientific community, especially after the
claimed that the United States employed biological agents Libyans chose to ignore scientific evidence that contra-
against North Korea and China. To prove their claims, the dicted their desire to divert blame from the incompetence
Chinese supported an investigation by sympathetic foreign of their own medical system.382-385
experts, the International Scientific Commission for the Given the numerous allegations of BW, and the extent to
Investigation of the Facts Concerning Bacterial Warfare in which many of them have been proven false—either fab-
Korea and China. Chaired by the noted scholar of Chinese ricated out of whole cloth or based on scientifically un-
technology, Joseph Needham, the Commission not sur- tenable evidence—the topic merits greater attention. The
prisingly fully supported the allegations. These allegations best study to date is the book chapter by Furmanski and
were reviewed in several SIPRI volumes.2,360,361 Wheelis already mentioned, which reviews the Korean
Some authors continue to take these allegations seri- War, yellow rain, and the Cuban allegations.359
ously; the main Western proponent is Stephen End-
icott.227,362 Others who have studied the incident,
including Leitenberg and Moon, believe that the Chinese A Research Agenda
and North Koreans fabricated the allegations.363-366 The The following is a list of topics for the period since 1945
first major new development was the release of about a that would benefit from additional research.
dozen documents from Russian archives showing that the
Soviets believed the accusations to be false.272 Furmanski 1. Plots to use BW to retaliate against the Germans by
and Wheelis argue that the allegations coming from the Jewish survivors of the Holocaust: There is clearly more
North Koreans were scientifically implausible, but that at to the story of the Avengers, and it would be helpful for
least one set of allegations from the Chinese, involving cases someone to dissect the available sources to give an ac-
of anthrax, were scientifically valid, even if it is doubtful count of what was planned and why it was disrupted.
that the United States was responsible.359 2. Israeli (and pre-independence Haganah) use of biolog-
Some Sinologists continue to accept the possibility that ical agents in 1948: It is unclear how much more can be
the allegations may be true,271,367,368 although they tend added to the research of Avner Cohen, but as one of the
to distance themselves from the writings of Endicott and few examples of BW, it merits at least some attention.
Hagerman.362 Similarly, some scientists writing about 3. The covert BW capabilities of the United States, as
BW, such as Jeffrey Lockwood in his study of insects as developed by the CIA for clandestine operations and
weapons, are remarkably uncritical in reviewing the whole the special forces for covert military operations: The
matter.25 In contrast, Reid Kirby, a student of the US destruction of documents in the 1970s may make it
chemical and biological warfare programs, argues that the impossible to adequately research this topic.
US military arthropod effort began only after the Korean 4. Soviet bloc allegations of Western (and especially US)
War.369 Recently, a Chinese historical journal published a use of BW: As suggested by recent scholarly writing,
short account by Wu Zhili, Director of the Chinese there is more that can be said about Soviet bloc al-
People’s Volunteer Army Health Division at the time, legations during the Cold War. Geissler’s exploitation
claiming that the Chinese never had evidence of US bio- of East German archives suggests that there may be
logical weapons use.370 more information in Warsaw Pact country intelli-
During the Reagan Administration, the United States ac- gence archives that are now available to researchers.
cused the Soviet Union of employing mycotoxins (popularly 5. History of Rhodesian BW: A definitive review of the
called ‘‘yellow rain’’) in Southeast Asia and Afghanistan. Most available evidence would be extremely helpful in
BW experts, including Elisa Harris, Matthew Meselson, and clarifying this obscure aspect of the history of BW.
Julian Perry Robinson, either reject the allegation359,371-373 or 6. Additional studies of false allegations of BW: Much
find it open to dispute.374 Rebecca Katz argues that while more could be said about the many false claims of
formerly classified documents support the hypothesis that biological weapons use since the end of World War II.
7. Ricin incidents: There have been many instances, recurs through time and across cultures.’’392(p38) As should
especially since the 1990s, of attempted or plotted be evident from the discussion of the role of poisons in
use of ricin, although it is unclear whether they were primitive societies, this proposition is certainly debatable.
successful. Nevertheless, his effort to make use of the insights offered
by evolutionary social sciences hints at the possibilities for a
richer set of studies.
Topical Areas Third, relatively little has been written on the evolving
role of BW science and technology. Malcolm Dando wrote
Some of the most interesting BW histories address relatively an article that hints at the possibilities for research in this
narrow topics. Several topics that merit additional work are arena.393 Dando’s study apparently inspired Neil Davison
highlighted here, although there clearly are others that to look into how science and technology shaped the first
could be added to the list. modern BW programs in the 20th century.195 While these
First, fears of intentional disease existed in many primitive studies mainly help understand the structure of offensive
societies and recur in more modern societies as well.101,386 biological weapons programs, they also contribute to an
This topic merits additional attention, because it might help appreciation of the conduct of BW. Given the hyperbolic
policymakers understand how we should think about con- language often employed when describing capabilities to
temporary bioterrorism concerns. Only a few studies look employ BW, these studies help put into context the
into fears of intentional biological agent use. Samuel K. strengths and weaknesses of capabilities.
Cohn reviewed reactions to the arrival of the Black Death in Fourth, more could be done by exploring in depth spe-
14th century Europe and highlighted the pathological sca- cific forms of BW. The potential value of such accounts is
pegoating that resulted.387 Similarly, Fenn’s studies of evident in the survey of agricultural terrorism undertaken
smallpox outbreaks in pre-Revolutionary and Revolutionary by Haralampos Keremidis and his colleagues.394 Such re-
America highlight the fears that the British were trying views highlight the need for more focused studies of par-
to deliberately spread smallpox virus into the Continental ticular topics. Keremidis et al identified only 4 instances of
Army and pro-rebel communities.149,150 However, such agricultural bioterrorism; in several of those cases, it should
fears are not inevitable. Cohn also has shown that reactions be possible to obtain more information about what hap-
to epidemics can vary widely and do not inevitably pened and why.
lead communities to seek scapegoats to explain natural Finally, the reasons for the relatively limited resort to BW
outbreaks.388 deserve a serious historical review. Although the technical
The utility of such studies is indicated by the research of obstacles to the use of biological agents are not trivial, it is
Furmanski, who has examined fears of hostile BW and doubtful that these obstacles alone have prevented resort to
shown how unwarranted concerns have led to investments BW. Other factors, and not just moral and ethical consid-
in both biological defenses and offensive biological warfare erations, undoubtedly were important in decisions to de-
capabilities.389 velop biological weapons, and then employ them, or the
Second, many scholars of BW argue that there is a widely reverse, deliberately deciding not to use them. Putting these
accepted taboo against causing intentional disease. Sur- decisions into a historical perspective might be difficult,
prisingly, given how often the existence of such a norm is given the gaps in our existing knowledge, but would con-
mentioned, the topic has received relatively little serious tribute to an understanding of the real dangers posed by BW.
academic attention. Cole provocatively put the issue in the
context of evolutionary biology.54 Moon examined the
emergence of the taboo against poison through multiple A Research Agenda
prisms, including references in Western literature and op- What follows are some suggested topics that merit addi-
position to food contamination and environmental pollu- tional research.
tion.390 Jessica Stern, focusing on risk assessment,
introduced the concept of biological agents as a ‘‘dreaded 1. Fears of intentional disease: There is a long history in the
risk.’’391 Erica Charters has examined the ethical implica- United States of intentional spread of biological agents,
tions of the deliberate spread of smallpox to Native dating to at least the time of the American Revolution.
Americans during the Seven Years War, arguing that British Such fears arose episodically in both the Native Ameri-
commanders knew that their actions transgressed accept- can and European populations. While it seems doubtful
able moral boundaries, even when fighting ‘‘savages.’’154 that such fears were limited to North Americans, there
Michael Mandelbaum, in a book otherwise devoted to are no studies for other parts of the world.
nuclear issues, offered some interesting thoughts on atti- 2. Development of norms against BW: Given the
tudes toward poisons, including an attempt to explore the widespread belief that a taboo against intentional
issue through the lens of E. O. Wilson’s sociobiology. infection is a major barrier against the use of bio-
Unfortunately, like many who have written on the poison logical weapons, it would be helpful to obtain a
taboo, Mandelbaum incorrectly argues, ‘‘The poison taboo better understanding of the emergence of such views.
In some ways, this would be a complementary study the gaps in our knowledge highlighted above, however, it
to one focusing on fears of intentional disease. probably is premature for anyone to write one.
3. The role of science and technology in the evolution
of BW: The potentialities of BW are defined by
scientific and technological possibilities. The uses Acknowledgments
and failed uses of BW require some understanding of
those possibilities. The author is indebted to the anonymous reviewers who
4. Reasons for the use or nonuse of biological weapons: commented on an earlier draft of this article. In addition,
It is striking how relatively little BW there has been, he would like to thank John van Courtland Moon and the
despite the growing mastery of biological sciences other participants of a not-for-attribution session on gaps in
that have made biological weapons increasingly ac- the history of biological warfare at the Chemical and Bio-
cessible. Yet, some people have sought to employ logical Warfare workshop, held November 7, 2013, in
them. Getting a better understanding of the condi- memory of Jonathan Tucker and cosponsored by the James
tions under which barriers to BW can erode would be Martin Center for Nonproliferation Studies (CNS) of the
useful in strengthening norms against BW. Monterey Institute of International Studies and the Na-
tional Defense University’s Center for the Study of
Weapons of Mass Destruction. John Moon, Milton Lei-
Conclusions tenberg, Martin Furmanski, Glenn Cross, Lou Elin Dwyer,
Amanda Moodie, and Raymond Zilinskas provided ex-
Thanks to the efforts of scholars and journalists during the tensive comments on earlier drafts of this article. The views
past 45 years, we know a great deal more about BW today expressed in this article are the author’s and do not neces-
than when Leitenberg undertook his survey in 1969. BW sarily reflect those of the National Defense University or the
has occurred, although few of the allegations are provable Department of Defense.
using Rosebury’s high standard of evidence. In most in-
stances, the evidence is sufficiently compelling to satisfy the
more reasonable standard of ‘‘beyond a reasonable doubt.’’
Two problems hamper our understanding of BW’s his-
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