Category Archives: Black Death

Rivers in European Plague Outbreak Patterns, 1347-1760

by Michelle Ziegler

The era of big data is coming to historic epidemiology. A new study published this month in Scientific Reports took a database of 5559 European outbreak reports (81.9% from UK, France and Germany) between 1347 and 1760 to analyze the role of rivers in the incidence and spread of plague. Their hypothesis was that river trade played a similar role as maritime trade in disseminating the plague but that the correlation would grow weaker over time as movement of goods over land became less expensive. In the 14th century, water transport was approximately ten times cheaper than land transport; the cost ratio diminishes to two to four times as expensive by the 18th century.  While it is not surprising that rivers had a role in disseminating the plague, the high correlation Yue, Lee, and Wu (2016) found between not only the proximity of the river but also its size and elevation is striking. Over 95% of the outbreaks occurred within 10 km of a ‘navigable’ river, defined as 5 m or greater in modern width and to differentiate maritime from riverine trade, excluded outbreak sites within 5 km of the maritime coastline. To ensure that rivers were suitable as trade routes, they only included rivers that linked two cities and excluded rivers that flowed into a lake without an outlet.

“Figure 1. Temporal and spatial distribution of plague outbreak in Europe in AD 1347–1760 (modifed from Büntgen et al 2012).” Yue, Lee, & Wu, 2016.

If we drill down into their results more directly, then we find that 84% of the city centers were less than 1 km from a river with 79.5% of those being on a river at least 20 meters wide. By their calculations, the average river width was 84.6 m. This correlates well with increased traffic and goods following to and through cities on substantial rivers. It is worth nothing here that the specific examples they give in England, Fossdyke, River Great Ouse, and the River Derwent are either canals or fit into an extensive canal system.

Looking at relationships between the outbreak sites and geography also favors high traffic river routes. When they included a “spatial lag in the regression models” they showed that there is a “highly significantly correlation with the spatial lag (p <0.01), indicating that plague outbreaks were spatially dependent upon previous outbreaks in adjacent cities” (Yu, Lee & Wu, p. 2). There was also a negative correlation between elevation and plague incidence, which they attribute to a lack of navigable rivers at higher elevations noting that only 20 incidents were recorded above 1000 m over sea level.  They also tested their results with controls for population density and economic status which did not effect their results for the likelihood of plague incidence or the association between outbreaks and river width. This will have to be evaluated by those with more modeling experience than I have.

There are a few caveats. First, such studies are only as good as their database. Yue, Lee and Wu used the digitized database constructed by Büntgen et al (2012) that was itself based on  a 35 year old archive published in French. I’ll leave its scrutiny to historians. They also do not address potential biases in all such databases, such as the likelihood that urban sites are recorded at a higher frequency than rural sites or that the political climate can effect the survival of records. Indeed, economic records are likely to note pestilence as a factor effecting commerce. While the environmental destruction of an enduring war could increase plague incidence, the high level of records from the ’30 years war’ needs a historians eye to evaluate. They also note that they are using measurements of modern rivers and canals that may have been significantly different in the past, modified by both natural processes such as silting or flooding and man-made changes such as straightening, dredging, or canal development.

They  also assume there were no European reservoirs, which we now know is not true. Ancient DNA studies have indicated that there were at least two strains descended from the Black Death circulating within late medieval Europe (Bos et al, 2016;  Spyrou et al, 2016). The European reservoir(s) have not yet been located. However, relatively few of the incidents reported in the database are likely to be actual zoonotic events linked directly to a local sylvatic (wild) reservoir, plus many known reservoirs outside of Europe are found at high elevation (for example in Tibet or Madagascar) and so are unlikely to be in this particular database given the absence of sites at higher elevations. Once a new outbreak emerges from a high elevation reservoir and comes off the mountain so to speak, then its transmissions by rivers is as likely as a strain entering from outside of Europe. On the other hand, if cities or even river networks are the actual reservoir, it would significantly effect their results.

River and canal networks or large river ports could function as reservoirs. River ports are similar to coastal maritime ports in that they have warfs, warehouses and nearby markets that would support large rodent populations. Barge traffic would specialize in transport of grain and other foodstuffs attractive to rodents.  Yue, Lee and Wu  (2016) state that they did not query their database for the effect of flooding because they could not accurately predict where floods would occur, that flooding is not predictable based solely on river width. Flooding along these river and canal systems is something that needs to be investigated because it would force rodents out of their normal shelter and could be related to human outbreaks (as the plague of 589 in Rome probably was). Floods could also carry infected rodents or fleas downstream on floating debris.

This study is a interesting jumping off point for future work. The database needs to be evaluated by historians and perhaps subdivided into smaller time periods. Division of the database into regional studies would also allow local archaeology and ecology to be more informative on precise outbreaks. I’m looking forward to all of questions big data studies like this one open up!


Yue, R. P. H., Lee, H. F., & Wu, C. Y. H. (2016). Navigable rivers facilitated the spread and recurrence of plague in pre-industrial Europe. Scientific Reports, 1–8.

Büntgen, U., Ginzler, C., Esperf, J., Tegel, W., & McMichael, A. J. (2012). Digitizing historical plague. Clinical Infectious Diseases, 55(11), 1586–1588.

Bos, K. I., Herbig, A., Sahl, J., Waglechner, N., Fourment, M., Forrest, S. A., et al. (2016). Eighteenth century Yersinia pestis genomes reveal the long-term persistence of an historical plague focus. eLife, 5, 17837.

Spyrou, M. A., Tukhbatova, R. I., Feldman, M., Drath, J., Kacki, S., de Heredia, J. B., et al. (2016). Historical Y. pestis Genomes Reveal the European Black Death as the Source of Ancient and Modern Plague Pandemics. Cell Host and Microbe, 19(6), 874–881.


Plague Dialogues: Monica Green and Boris Schmid on Plague Phylogeny (II)

Monica H. Green (,@MonicaMedHist) is a historian of medieval medicine. An elected Fellow of the Medieval Academy of America, she teaches both global history and the global history of health. She was the editor in 2014 of Pandemic Disease in the Medieval World: Rethinking the Black Death, the inaugural issue of a new journal, The Medieval Globe.

Boris Schmid (@BorisVSchmid) is a theoretical biologist at the University of Oslo, Norway, and specializes in disease ecology and epidemiology. He recently described a link between climate fluctuations in medieval Central Asia and what looks like repeated introductions of plague into Europe’s harbors, a hypothesis that can be tested by the analysis of ancient DNA samples of Y. pestis. He works in a multidisciplinary team of theoreticians, archeologists, microbiologists and historians, led by Nils Chr. Stenseth.


In our previous blog post, Monica and I discussed how different lineages of plague – Yersinia pestis – collected their own genetic signature (SNP profile) as they diversified from a common ancestor. Monica also summarized in broad terms what ancient DNA samples of Y. pestis (extracted from plague victims) are now available from the initial Black Death outbreak and how they are related, using the latest plague studies of Haensch, Bos and Spyrou.

In this blog post Monica will delve into the nitty gritty details of these aDNA plague studies, and give an example of how to transform those details into a new understanding of the past rodent reservoirs and global mobility of plague, one of the deadliest diseases of our collective past. And I close the post by reflecting on the potential of aDNA to connect the fields of history and biology.


Thanks, Boris. It might be important to remind readers that we don’t have any aDNA evidence from past rodent populations yet. All the samples to date have been retrieved from human victims. But the SNP study that Seifert et al. published earlier this year from samples in Brandenburg, an inhumation from the time of the 30 Years War (1618-1648); the whole genome study that Bos and Herbig et al. also published this year, reporting on the samples from 18th-century Marseille; and the sample from Ellwangen included in the new study by Spyrou et al., all document that Branch 1A (see tree in our previous post) “focalized,” that is, it set up shop in some rodent population(s) and happily continued to proliferate for another 400 years. But all that happened, it is clear, separately from what was going on with Branch 1B, what I have taken to call the pestis secunda.

In their most recent study, the Tübingen/Jena team headed by Krause give us further insight into the early stages of Branch 1B. The beginning of Branch 1B was first documented in the 2011 London study, though it was only earlier this year that I realized that London sample 6330 likely dates from the 1360s and does not come from the initial Black Death outbreak. (It comes from a different burial ground, St Mary Graces.) In Bos and Herbig et al. 2016, it was reported that sample 6330 differed from the 1348-50 London Y. pestis genome by two SNPs. In the present study, interestingly, Spyrou et al. report something slightly different. Sample 6330 does indeed differ from the London Black Death genome by two SNPs (p3 and p4), but a third SNP in sample 6330 they are reporting here for the first time (p5) seems to be unique, a ‘G’ to ‘T’ switch at position 4,301,295 not found in any other historic genome or in the reference strain, CO92. (Spyrou et al. did not include London 6330 on their Table 1, so we offer a modified version of it here in fig. 3.)

CORRECTED fig03 for Contagions blog, (a) Spyrou et al 2016 fig02B Y pestis phylogenetic tree (detail of origins of Branches 1A and 1B), (b) Table 1 with 6330 SNPs added (06272016)
Fig. 3: (a) Detail of Spyrou et al. 2016, fig 2B: Yersinia pestis phylogeny – SNPs distinguishing Branches 1A and 1B; (b) Spyrou et al. 2016, Table 1, modified with data on London sample 6330 drawn from Spyrou et al. 2016, Table S4, SNP table. The SNPs unique to London 6330 and Bolgar City are highlighted in yellow.


First of all, we might say that those three SNPs are significant for the time gap they suggest between the Black Death and the 2nd wave of plague to hit London in 1361-63; for the sake of argument, we’ll say “21 years,” to use your formula (3 x 7 years), Boris. But think about the implications of that: plague arrives in London at the end of 1348 as a new disease, and a new strain (with 3 new SNPs) is causing a major new outbreak in 1361-63, which is when this burial seems to date from. 21 years have not passed since the previous outbreak. So what gives? Obviously, the “time-to-SNP” calculus we’re using is an average, not an absolute. But it does make us stop and wonder: did all this really happen so fast? And did it really happen in western Europe?

Which brings us to the Bolgar City sample. It, clearly, is a “descendant” of the same strain as London 6330: it has the two new SNPs, p3 and p4. (It doesn’t have that unique p5 SNP of London 6330, but that may have arisen as little as three days before this person died. We cannot attach any evolutionary significance to it until we see it documented somewhere else.) But note this: the Bolgar City strain has evolved further. It now has the p6 SNP that will define all the rest of Branch 1B and it has its own unique SNP, p7. And again, we have a problem of time compression: the Bolgar City sample (if we can trust the dating of the coins which were said to have been found with the body) may date as early as the late 1360s.

Remember what we need to have an outbreak in humans from a new lineage of Y. pestis: not simply does that new lineage have to arise from a single change in a single cell of Y. pestis, but that new SNP needs to proliferate enough in a reservoir rodent population to cause a new epidemic in humans. So looking over all these SNPs, p1-p7, we can see that they cluster into two “founder effect” phenomena: one that creates the initial Black Death lineage (Branch 1A) and one that creates the pestis secunda lineage (Branch 1B).

Where did those two lineage foundations happen? Let’s go back to Caffa, the “hurling bodies over the walls” scenario. Clearly, if we can believe that story (and remember, we have only one account of it, and that from a non-eye-witness), it tells of an already proliferating plague outbreak. By October 1346, Y. pestis was multiplying by the millions in rats and mice and rodents of whatever kind that lived in and around Caffa.

One, and only one, of those gazillions of Caffese offspring gave rise to Branch 1B. It, too, needed to find a place to set up shop and proliferate to make gazillions of (nearly) identical copies. And where was that place? Was it (as Krause seemed to imply in his April lecture) in London? Maybe it was in or near Bergen op Zoom (NL), where we find a sample with the same SNP profile as the London 6330 sample (Haensch et al. 2010)? Or was it near the same place where Branch 1A had already established its original home, before it reached the Black Sea? Haensch et al. had already proposed in 2010 a “northern” route for the introduction of the pestis secunda strain that reached the Netherlands. I’ll admit, I was skeptical for the longest time. But now I see that this possibility might bear more analysis. At the very least, the question shifts our focus away from western Europe and back to the areas around the Black and Caspian Seas. And that’s exactly where our Bolgar City sample is from, the one that is already showing two SNPs of further evolution beyond London 6330 but might not be a whole lot younger than it. As we said, jetting out of Heathrow wasn’t yet an option in the 14th century. But there was plenty of activity in these central Eurasian areas dominated by the Mongol Golden Horde to connect lots of rodent reservoirs to a bacterium looking for a new place to call home.


Thanks Monica! The amount of information that follows from a few different nucleotides between aDNA samples is quite amazing, and learning how to interpret this data historically is rightly one of the transformative processes now happening in Biology (and if I say so, in Medical History as well).

Monica’s interpretation of plague’s past mobility is based on the same genetic data as the one sketched out in Spyrou 2016, and highlights the challenge of interpreting ancient DNA, given that the ancient DNA sequences of plague are still so sparsely sampled across time and space. One thing that strikes me as especially important is how much the argument of “favor the most simple, parsimonious explanation” changes based on whether you think of plague largely in terms of a human epidemic (which Wagner 2014, and by extension Spyrou 2016 appear to do), or as a disease that spread through human and wildlife both, as Monica and I do. If you include the possibility of new wildlife reservoirs of plague (and plague has created numerous new wildlife reservoirs in time), say near Bolgar City, the logic of how plague moved across Eurasia changes.

As more aDNA data becomes available, it will be very interesting to see the geographic range that a lineage of plague bacteria can spread without collecting changes in its SNP profile. Once we have a good idea of that, and a more complete view of the SNP profiles that existed during the past pandemics, SNP profiles might be used to shed light on the actual source of a historic plague outbreak, and thus offer an independent way of checking the reliability of historic sources that blame particular smugglers, ships, refugees or clothing as the source of a plague outbreak.

Wow, thanks, Monica, for this great discussion. This is an example on how history and biology can intertwine, and while we are all waiting for more revelations from aDNA and historic sources, it seems prudent to start more interactions between historians and biologists. There is an inherent bias to doubt your own data too much, and trust another fields’ data too blindly, leading to mistakes at both sides: we blindly pick some historic report as authoritative, or put too much faith in a report on the (in-) efficiency of plague transmission by different flea species, whilst a single mutation that causes the loss of a gene can have drastic effects on how well the disease transmits (Hinnebusch, 2016). The only practical way to avoid falling into such pitfalls is by investing in cross-talk between scholars of the humanities and natural sciences!


Thank you, Boris. This was great. And very special thanks to Michelle Ziegler, for hosting our discussion on her super blog, Contagions.


Bos, K. I., Herbig, A., Sahl, J., Waglechner, N., Fourment, M., Forrest, S. A., et al. (2016). Eighteenth century Yersinia pestis genomes reveal the long-term persistence of an historical plague focus. eLife, 5, 17837.

Cui, Y., Yu, C., Yan, Y., Li, D., Li, Y., Jombart, T., et al. (2012). Historical variations in mutation rate in an epidemic pathogen, Yersinia pestis. Proceedings of the National Academy of Sciences, 110(2), 577-582.

Haensch, S., Bianucci, R., Signoli, M., Rajerison, M., Schultz, M., Kacki, S., et al. (2010). Distinct Clones of Yersinia pestis Caused the Black Death. PLoS Pathogens, 6(10), e1001134.

Hinnebusch, B. J., Chouikha, I., & Sun, Y.-C. (2016). Ecological Opportunity, Evolution, and the Emergence of Flea-borne Plague. Infection and Immunity, IAI.00188–16–31.

Krause, Johannes (4-12-2016)  Oral Presentation #S577:  Ancient pathogen genomics: what we learn from historic pandemics. European Congress  of Clinical Microbiology and Infectious Diseases

Seifert, L., Wiechmann, I., Harbeck, M., Thomas, A., Grupe, G., Projahn, M., et al. (2016). Genotyping Yersinia pestis in Historical Plague: Evidence for Long-Term Persistence of Y. pestis in Europe from the 14th to the 17th Century. PLoS ONE, 11(1), e0145194-8.

Spyrou, M. A., Tukhbatova, R. I., Feldman, M., Drath, J., Kacki, S., de Heredia, J. B., et al. (2016). Historical Y. pestisGenomes Reveal the European Black Death as the Source of Ancient and Modern Plague Pandemics. Cell Host and Microbe, 19(6), 874–881.

Wagner, D. M., Klunk, J., Harbeck, M., Devault, A., Waglechner, N., Sahl, J. W., et al. (2014). Yersinia pestis and the Plague of Justinian 541–543 AD: a genomic analysis. The Lancet Infectious Diseases, 14(4), 1–8.

Environment, Society and the Black Death in Sweden

Environment, Society and the Black Death: An Interdisciplinary Approach to the Late Medieval Crisis in Sweden. Edited by Per Lagerås. Oxbow Books, 2016. 

9781785700545_1The Black Death is a bit of a phantom in this book. Like the human body casts of Pompeii, the Black Death is perceptible  by the void it left behind — a void in farm occupation, a void in building,  a void in the population/labor but ironically, also a void in mass burials. Without distinctive plague burials, this is how we should expect a scientific investigation of the plague and its  environment context to be. What these sometimes contradictory seeming voids mean is the challenge taken up in this book.  The studies presented in this book used pollen diagrams, dendrochronology, settlement archaeology and human remains to investigate the entire fourteenth century crisis with the clear signature of the Black Death apparent in each type of investigation.

When the Black Death reached Sweden in 1350, the kingdom was in pretty good shape compared to elsewhere in Northern Europe. Sweden seems to have avoided the Great Famine. The population was spread between small villages and isolated homesteads; there were no large urban areas on par with London or Paris. There was still room to expand settlement toward the uplands in the north-west. The relatively thin settlement and lack of large urban areas explains the lack of mass burials. Based on the population distribution and predicted mortality rate (comparable to the rest of northern Europe), they predict that the thin settlement allowed them to keep up with the burials along with some semblance of usual burial customs, such as coffins. The only indicator of plague deaths (or any epidemic) is the incidence of double and triple graves.  So it’s not a matter of discovering the Black Death burials, they have been in plain sight all along.

Staying with the bodies, their osteological sample included 4876 skeletons from 65 medieval churchyards, three execution sites, and two mass military graves spanning the entire medieval period in the region of Lund. Their primary measure of stress was projected height. The only finding of significance was that women were slightly taller (2.5 cm) in the generation after the Black Death. I think they could have made a little more of this considering that the nutrition of young women has a disproportionate effect on fertility, fetal and maternal health. Enough healthy women of reproductive age is a necessity for a population to recover from a mortality crisis. The overall stature of Swedes was on par with elsewhere in Europe and in the 14th century far shorter than modern Swedes. The average height for a man after the Black Death was only 172.5 cm,  (5′ 8″) and women at 162.7 (5’5″). They reached their low point in the 19th century only to sharply rebound to their tallest point in the 20th century.

The isotope data from selected skeletons from Lund, the largest urban district in Sweden, yielded a few surprises. They did find a diet change to include more animal and marine sources, but unlike elsewhere in Northern Europe, the switch occurred in the 12th century, not the 14th century. Could this explain why there is no evidence of the Great Famine in Sweden? Nearly two-thirds of the specimens from Lund had some marine sources in their diet. Zooarchaeological specimens suggest that cod was the primary marine source and that freshwater fish were not major contributors to the diet.  Regardless, there was no 14th century diet change that the isotopes could detect and no correlation between dietary changes and height. Strontium analysis does not indicate many non-natives after the initial establishment phase of Lund. The Black Death period (1350-1370) had the lowest number of non-locals of the medieval to early modern period. They suggest that this means that contact with the non-Swedish world was reduced during this period.

The bulk of this book addresses settlement and land use changes in the mid-fourteenth century. Beginning with dendrochronology, there is a hundred years gap from 1360 to 1460, reflecting the lack of need of new building or expansion after the Black Death. Amazingly, a few of the farm buildings dating to the pre-Black Death period are still standing. Farm abandonment and landscape change unfortunately can’t be as directly measured as dendrochronology.

The pollen data largely reflects the paradox pointed to in Sing Chew’s The Recurring Dark Ages: Ecological Stress, Climate Change and System Transformation (2006), that periods of human crisis allow ecological rejuvenation.  More simply what is bad for humans, is good for the environment. Periods of decreased human environmental exploitation (or resource extraction, if you prefer) allow the environment to recover.  Chew does not address the fourteenth century, which we might call a Dark Age near miss, a time when the Old World tottered on the brink of another possible Dark Age, but the similarities still make a useful comparison (and open up some interesting questions).

In the decades after 1350, the pollen suggests that arable fields decreased, conversion to pasture and increased woodland expansion. The conversion of unused fields to pasture or hay kept those fields from regenerating their woodlands and making it easier to bring them back into arable production. Yet, there was still considerable woodland regeneration.  They note that seedlings that sprouted in the years after the Black Death formed a mature forest that lasted in some areas for 300+ years. A mature forest with 300+ year old trees will seem like a virgin forest, but it is not; it is still an anthropomorphic landscape.

“In summary the late-medieval crisis and in particular the population drop initiated by the Black Death in 1350 did not only result in profound and long-term social changes, but also in environmental and ecological changes. These changes were not only passive consequences of the crisis – they also affected the course of the crisis through different feedback mechanisms, both positive and negative.”(Lagerås, 2016, loc 3603)

They also note that the only previous rejuvenation of woodlands in Europe occurred in the sixth century around the time of the first plague pandemic. I’m encouraged to see their interest in comparing the 14th century environmental context/consequences to the sixth century. It is refreshing to read a book written with such a clear, scientific tone and approach.

They note that the expansion of woodland allowed a rejuvenation of biodiversity mentioned in  a 1376 royal letter that claimed more wolves and bears were damaging humans and livestock. While the abandonment would have decreased hunting pressure, it is also likely that the expansion of the woodland allowed a flourishing of the entire tropic cascade that was capped by predators like wolves and bears. We are more accustomed to thinking of tropic cascades as being suppressed by top down predation (often caused by humans), but the cascade can also bloom bottom up.  While on the topic of biodiversity,  a discussion of small mammals that could play a role in plague transmission during the 1350 epidemic and later epidemics would have been helpful. This ecological flourishing will radically change the landscape and human relationship to it. What effect, if any, did this have on later plague transmission? In this regard, their comparisons to an 18th century plague would have been just about when the post-Black Death ecological changes were giving way to expansion of arable farmland again and the population had rebounded.

The complexity of the ecological and settlement data is a measure of the long-term contextual changes caused by a single massive epidemic and its aftershocks. Populations would have been moving within the country for many years as heirs took possession of better land, and families depleted of heirs dwindled away over time. They note that the post-Black Death period brings about the end of the self-sufficient manor system. Social order evolves into a more specialized and interdependent system. The ecological changes slowly rolled out as fields turned into pastures or were left fallow; forest encroachment and development occurred over many years. This book is a work in progress on the environmental history of Sweden’s anthropomorphic landscape and its people. It should be considered in the context of other environmental studies of the fourteenth century crisis from Scandinavia, Britain and Ireland, Iceland, and the Northern European continent. I look forward to seeing how their work develops in the future.