The microbiology of early globalization

Pandemics and imperial entanglement in the 2nd to 8th centuries AD

Updated and translated extract from: Johannes Preiser-Kapeller, Jenseits von Rom und Karl dem Großen. Aspekte der globalen Verflechtung in der langen Spätantike, 300–800 n. Chr. Vienna 2018.

Research is discovering, based on new methods of paleobotany, archeozoology and genetics, an increasing number of "biological transfers" in ancient and early medieval times, the exchange of which intensified with the great empires and their networks. Biology uses the term "hemerochory" for the spread or displacement of species through human culture, including the distribution by domestic animals or species accompanying humans (such as the house rat or house mouse), called "zoochory". A distinction is also made between conscious and unwanted introduction of species. The extent to which these phenomena, which are hotly debated in the modern "globalized" world, affected various ecospheres in antiquity and in the Middle Ages will be the subject of further investigation, but we can assume that even then there were hardly any "untouched" landscapes that were not changed to different degrees by human activity, either intentionally or unknowingly (for example by accompanying "bio-invaders").

Major long-distance trade routes in Afro-Eurasia between AD 500 and 900 (map: J. Preiser-Kapeller, ÖAW, 2020; basemap: google earth)

The “uninvited passengers” of all of these organic transfers definitely included the “microbiomes”, that is, the totality of all microorganisms that colonize a human or other living being. These also included pathogens, some of which first had to adapt to new "living conditions", but which could then have a devastating effect on animals and humans. For example, in his most recent monograph, Kyle Harper speaks for the late ancient Mediterranean region of an “unwanted conspiracy with nature”, through which the Romans in their empire, from the subtropics to the Arctic Circle, “created a disease ecology that would reveal the hidden power of the evolution of pathogens”.

 

Climate change and the "Antonine plague" in the 2nd century AD

A close connection between the large epidemics and the climatic changes of this epoch can be observed. When the "Roman climate optimum" transformed around AD 150 in a much more volatile period, the so-called "Antonine plague" struck the Roman Empire between 165 and 180. According to reports by contemporaries, it had its origins in the looting of the Parthian capital Seleukia-Ctesiphon in what is now Iraq by Roman legionaries; the temple of Apollo was not spared, which had caused the revenge of God. The Roman soldiers were more likely to have been infected with a pathogen introduced into the Mesopotamian commercial center across the Indian Ocean; even before that, there were in ca. 160 AD reports of such an epidemic in today's Yemen. With the returning legionaries, the pathogen came into the Roman Empire and spread over sea and land routes throughout the Mediterranean. The description of the epidemic by contemporaries, including the famous doctor Galen (approx. 129–205), is most likely to suggest a pox disease caused by the orthopoxvirus variola, which is spread by droplet and smear infections and is highly contagious. In large cities like Rome there were thousands of deaths a day, and in total up to 20 percent of the population of the empire probably fell victim to the epidemic (although, there is, as in other cases, a intensive debate on the actual demographic impact of the disease). Lucius Verus (ruled 161–169), son-in-law and co-emperor of Marcus Aurelius Antoninus (ruled 161–180, hence the name “Antonine Plague”), died of it. These (possible) demographic losses may have had a dramatic impact on the economy and society of the empire, which entered a much more troubled period in its history. However, after surviving the disease, the survivors acquired lifelong immunity, so that after a few years the plague probably disappeared around 180 for the time being.

Emperor Marcus Aurelius (161-180) and his adoptive brother and co-emperor Lucius Verus (161-169), who probably both died in different waves of the "Antonine Plague" (https://commons.wikimedia.org/wiki/File:Marcus_Aurelius_and_Lucius_Verus,_British_Museum_(11269159504).jpg)

 

The “Plague of Cyprian” in the 3rd century AD

However, around 249 AD, during the crisis of the 3rd century, which was also accompanied by climatic extremes, the so-called "Plague of Cyprian" broke out, named after the contemporary Christian author Cyprian (approx. 200–258), Bishop of Carthage in what is now Tunisia. According to him and other contemporaries, the plague was introduced into the empire from East Africa and via Egypt and reached Alexandria around 249 and Rome in 251; a second wave broke out around the year 260 and reached today's Romania, then still a Roman province. The various descriptions of the disease have led some researchers to suspect a new outbreak of smallpox, as immunity from previous generations would have been lost again, but this seems unlikely. Another theory targets influenza viruses, whose devastating potential at the end of the First World War illustrated the "Spanish flu" with 50 million deaths worldwide. However, according to Kyle Harper, an even more "promising" candidate is a hemorrhagic fever, which is accompanied by heavy bleeding, for which several pathogens of the families of the Bunya viruses, the arena viruses (including the Lassa virus) and the Filoviruses (including Ebola) can be considered. Rodents and domestic animals such as sheep and goats serve as their natural hosts, and transmission is often carried out by insects such as ticks, sand flies or mosquitoes, but also from person to person for the filoviruses. These viruses would have been less contagious than smallpox, but would have impacted increased mortality (though, again, the actual demographic impact of the epidemic is disputed). In any case, the empire's crisis may have been exacerbated by the disease.

Electron microscope image of Ebola viruses, one of the possible causative agents of hemorrhagic fever (https://de.wikipedia.org/wiki/Ebolafieber#/media/Datei:Ebola_Virus.jpg)

 

The "Justinianic Plague" in the 6th to 8th centuries

From the end of the 3rd century onwards, somewhat more stable climatic conditions followed in the Mediterranean, and there was no further major epidemic outbreak for more than 250 years; but then the so-called " Justinianic Plague" between 540 and 750 changed the late antique world forever. The causative agent of the plague is the bacterium Yersinia pestis, so named due to the discovery by Alexandre Yersin (1863–1943) during an outbreak in Hong Kong in 1894. Its primary host is rodents, the transmission between hosts being carried out by fleas; however, the disease can be passed from rodent populations to humans, and apart from transmission by fleas, it can then spread further between humans, occasionally even via the air. There is a long debate in research as to whether the pathogen identified in 1894 is identical to that of the plague epidemics of the 14th to 17th centuries ("Black Death") and the 6th to 8th centuries ("Justinianic Plague"). However, new results of DNA analyzes of pathogens in the remains of victims of the late medieval and late antique plagues have confirmed this identity. Grave fields in Aschheim and Altenerding in Germany (both in the Munich district) provided valuable information for the authoritative study by David M. Wagner and his colleagues in 2014 for the 6th century. The genetic features reconstructed there refer to a strain of Yersinia that emerged in the area of ​​today's PR China, more precisely probably on the Qinghai-Tibet plateau, between 1000 BC and 500 AD (most recently, Rudolf Pfister also argued for a description of the disease in Chinese medical treatises at least since the 5th century AD).

The particularly damp and cool conditions that prevailed in large parts of Afro-Eurasia after a cold period beginning in 536 (the so-called "Late Antique Little Ice Age", approx. 536-660) favored the transmission of the pathogen, which is endemic among the rodent populations in East Asia, on other rodents or on humans. The plague then spread over the trade routes to the west over the next few years to the Indian Ocean and reached about 540 AD Egypt via the Red Sea, whose neighboring countries such as Aksum (today's Eritrea and Ethiopia) and Himyar (today's Yemen) were also affected, probably in the port of Klysma (today's Suez). In 541 AD, the plague arrived in Pelusion (30 km southeast of today's Port Said) on the Mediterranean. Infected rats and humans traveled from Egypt with the annual grain fleets to supply the imperial capital to Constantinople, where the plague broke out in 542 AD during the reign of Justinian. On the still intact trade and traffic routes, the disease was spread throughout the Middle East, the Mediterranean and beyond to Ireland, with the unintended expansion of the domestic rat in the Roman Empire contributing to the "infrastructure" of the spread.

Map of the possible region of origin and route of diffusion of the plague epidemic of the 6th century AD (map: J. Preiser-Kapeller, ÖAW, 2020)

According to contemporary sources, the plague in Constantinople claimed 250,000 to 300,000 deaths among the 500,000 inhabitants and millions more victims across the Roman empire, in the Persian Empire and in the neighboring states. As the plague returned in regular waves until around 749 AD for the next 200 years, the population of western Afro-Eurasia was permanently decimated; For the eastern Mediterranean, a permanent reduction to half to one third of the population before the pandemic has been assumed before demography could recover from the late 8th century onwards. But was the impact of the "Justinianic Plague" really so devastating? A debate has flared up due to an article published shortly before Christmas 2019 by Lee Mordechai and his team, who call the "Justinianic plague" an "inconsequential pandemic" (see also the earlier critical review of Kyle Harper´s book by John Haldon et al. from 2018). On the basis of a statistical analysis of the frequency of papyri, inscriptions and coins, but also of pollen data (on the intensity of agriculture), they doubt that the plague of the 6th century, like the "Black Death" of the late Middle Ages, accounted for 30 or even 50% population losses - and was more like the East Asian pandemic around 1900, which claimed millions of victims, but by no means depopulated large parts of China. Other researchers are strongly opposed to this scenario (several publication in response are in preparation now; see also Monica H. Green´s contribution on "When Numbers Don't Count: Changing Perspectives on the Justinianic Plague" from November 2019). Even if the lethality of the epidemic was lower than assumed, the social, economic and psychological consequences of the insecurity of the people and the disturbance of normal everyday life should also be taken into account. The latter argument seems understandable given the current situation around the corona virus, considering that the people of the 6th century were completely unclear about the cause and spread of the disease. In any case, the debate on the dimension and impact of the Justinianic Plague will continue.

The bacterium Yersinia pestis under the microscope (from: https://commons.wikimedia.org/wiki/Yersinia_pestis?uselang=de#/media/File:Yersinia.jpg)

 

Epidemics in Late Antique China and Japan, 6th-10th century AD

Overall, the pathogens of the three epidemics in the 2nd, 3rd and 6th centuries, apparently introduced from far outside the Mediterranean via the long-distance trade networks, may have had a far more devastating effect on the "virgin" populations in the Roman Empire and in neighboring regions than in regions near to their "home areas". These may have been exposed to more frequent, but less violent, outbreaks as long as a pathogen did not develop significantly and thus at least partially neutralized existing immunities (the "immunological memory"). For example, information about pandemics comparable to the "Justinianic plague" or "Black Death" are less clear for the Chinese regions much closer to the endemic areas of Yersinia pestis before the great outbreak of the 19th century. An epidemic that may have been identified as plague is recorded in southern China for the year 549 AD, i.e. shortly after the epidemic occurred in the Mediterranean. In addition, however, China was repeatedly hit by (other) epidemics; a disease associated with high fever is said to have claimed millions of victims under Emperor Gaozu (r. 618–626). Another epidemic cost the lives of many people between 636 and 644 AD, and spread between the imperial capitals of Chang'an and Luoyang, each with hundreds of thousands of inhabitants, along the canals that the emperors had been building for hundreds of kilometers since the end of the 6th century in order to connect the north and south of their empire. As in the (post) Roman Mediterranean world, the networks of the imperial infrastructure also offered pathogens new ways of spreading. Until the end of the Tang Dynasty around 907, eighteen other major epidemics, including smallpox, were mentioned; some of the pathogens were apparently brought in from the newly developed subtropical regions of the south, others from the steppes of Central Asia, including animal diseases that decimated the imperial horse population.

The spread of an epidemic in China between 636 and 644 between the imperial capitals along the canal network (map: J. Preiser-Kapeller, ÖAW, 2020)

For comparatively isolated populations, the consequences of contact with new pathogens could be all the more fatal. Between 735 and 737 AD, a devastating smallpox epidemic in Japan, which is said to have been brought in by a ship from the Korean empire of Silla, caused a severe demographic, economic and political crisis, which, among other things, contributed to a stronger focus on Buddhism (also imported from Korea). Here too, both the strengthening of maritime connections and the consolidation of settlements in the form of the new imperial capitals such as Nara (near today's Osaka) had favored the spread of the epidemic. Until around 1200, smallpox returned a total of 28 times every 10 to 20 years on average and permanently inhibited a demographic recovery in the population of Japan.

The copper Buddha statue, over 15 meters high, in the old Japanese capital of Nara, completed in 749 shortly after the first major smallpox epidemic in the country (photo: J. Preiser-Kapeller, 2019)

 

So while monks and princesses smuggled silkworms from China to the west and caliphs had orange trees shipped from India to Iraq, much smaller biological stowaways on board humans and animals turned out to be the most powerful "profiteers" of the global entanglements of late antiquity. One of the unplanned consequences of the exchange between the regions of the world was the “microbiological unification” of Afro-Eurasia, against which even the greatest empires of the time were left powerless.

 

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