Category Archives: microbiology

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.




Beyond Germs: Native Depopulation in North America


Beyond Germs: Native Depopulation in North America. Edited by Catherine Cameron, Paul Kelton and Alan Swedlund. University of Arizona Press, 2015.

With the number of emerging infectious diseases climbing and new revelations about plague’s past, this book is a timely caution to the rhetoric surrounding so-called virgin soil epidemics. This book is the publication of an interdisciplinary conference held to discuss the causes of Native American depopulation hosted by the Amerind Foundation. Essays by David Jones, George Milner, Clark Spenser Larsen, Debra Martin, Gerardo Gutiérrez, Alan Swedlund, Catherine Cameron, Paul Kelton, Katheleen Hull, and James Brooks are included. Most of these essays are case studies in depopulation of specific areas.

David Jones opens the book with a discussion of the rhetoric surrounding so-called virgin soil epidemics that are credited with being the primary cause of native depopulation. Admitting the influence of his mentor evolutionary biologist Stephan J Gould, Jones favors social and contingent causes for depopulation over biological determinism. Perhaps the influential role that Gould played in my own formation as a biologist makes me sympathetic to Jones’ argument, but I can certainly live with that. Genetic determinism, in my opinion, is the easy way out to explain what can not be yet understood. His argument against the sweeping rhetoric of ‘virgin soil epidemics’ is, I think, very effective.

Milner’s chapter tackles the tricky problem of the pre-contact population collapse of the Mississippian culture centered at the mid-continent site of Cahokia, near St. Louis. This had been the largest and most (archaeologically) complex native culture in North America but it collapsed so entirely that the mid-continent was still sparsely populated when Europeans arrived a couple of centuries later. Medieval Cahokia had been more populous than  contemporary London. The example of Cahokia must give us pause for assuming that unrecorded demographic collapses that lack signs of massive destruction must be due to epidemics.

Larsen, Martin, Gutiérrez, and Hull cover the effect of the Spanish mission system in Florida, the Pueblo of the Southwest,  Mexico, and California respectively. Structural violence was seen throughout the Spanish mission system from hard, forced labor. Larsen discusses the changed how changed landscapes and lifestyles make natives more susceptible to infection. He sees a dramatic rise in cribra orbitalis/porotic hyperostosis as a sign of iron deficiency when it may actually be malaria. Wet Florida would have been susceptible to endemic malaria and a reservoir for it to spread through the southeast. Martin looks at the bioarchaeological evidence for a ‘creeping genocide’ in the peublos of the south west. Sporatic massacres of pueblo communities was used to enforce compliance by the wider culture. Cultural resilience was also stressed to the breaking point by a prolonged period of drought and environmental deterioration in the southwest that left them with marginal nutritional sufficiency. In this stressed environment, smallpox spread widely among the pueblo communities. Epidemics were part of a set of practices used to destroy or reorient native culture to make it acceptible, and more importantly controllable for the Spanish. Gutiérrez focuses on the methods and effects of identity erasure on demographics. The caste system that developed was very systematic “virtuous cycle”  with the goal of eliminating native identiy and indeed native (and African) ‘blood’ while maximizing Spanish identity and ‘blood’.

Chapters by Swedlund,  Cameron, and Kelton  examine tribes that dealt more closely with the English colonies and early American states. Swedlund looks at the great smallpox epidemic of 1633-34 beyond coastal New England up into the Connecticutt River valley. Cameron reviews the demographic effects of warfare and captive taking had on the Southeast, the northern Pays d’en Haunt (Great Lakes region), and the Southwest tribes. Colonial politics and trade caused more intertribal warfare than warfare directly with European colonists. Kelton writes about the disastrous experiences of the Cherokee with warfare, famine, and disease during the American Revolutionary War.

On of the overarching problems is the difficulty in determining population size before contact and then for the first couple centuries of the colonial period. Problematically, in the past abandoned villages have been assumed to be extinct due to disease rather than simply relocation or the movement of refugees to other tribes. The reality is that many areas that are fertile with Old World methods and domestic livestock were very difficult to make productive with native resources.

Over arching themes that I noticed which point toward other factors than just “germs” causing depopulation:

  1.  Use of starvation as an intentional weapon accomplished by burning fields and disrupting the agricultural cycle.
  2. Selective taking of women of reproductive age as captives/slaves causing a gender imbalance that prevented populations from rebounding.
  3. Selling captives to slavers rather than incorporating them into the tribe as pre-contact tribes often did to bolster their numbers and replace their dead. Sales were often to repay debts for European trade goods, especially weapons and ammunition.
  4.  Use of tribes as proxy militias by European powers to create intertribal warfare and recruitment of tribes by the British during the American revolution and war of 1812. Set up an adversarial relationship with the young American nation.
 In effect, I think the process they are all searching for is a syndemic that combined epidemics, nutritional deficiencies, systemic violence, slavery, and forced assimilation. Unfortunately they didn’t really consult the syndemic literature.

One of the things I took away from this collection is an appreciation for how long it takes to develop a fully agricultural culture. Many Native American groups were still in transition. Lacking domestic animals other than the dog, they were very vulnerable to climate and social disorder disrupting their agricultural cycle and yield. Some tribes adopted domestic animals from Europeans quickly. Colonists were greatly alarmed at how quickly the Cherokee adopted raising hogs and European crops, bringing them nutritional stability. Of course, horses are were adopted so well by natives that its hard for many of us today to even think of Native Americans without them.  The idea that domestic animals were worth the effort may have been what was missing most, rather than a lack of animals capable of being domesticated.

I highly recommend this book for anyone interested the dynamics of depopulation, “dark ages”, and most importantly for comparison to other “virgin soil” epidemic situations. I don’t think it’s a coincidence that other renowned virgin soil epidemics like the first and second plague pandemics occurred in times of ecological and social stress in addition to the epidemic in question. By opening the explanations for Native American depopulation up to other causes than disease,  it also opens up views into colonial life that even contemporaries tried to ignore. Wether their demise to disease was believed by contemporaries to be divine will or by modern historians as biological determinism, it has diverted attention away from the very human causes of depopulation and in some cases genocide.

Grandes Chroniques de France The Death of Saint Louis.

The Schistosoma in the Reliquary

The 800th anniversary of the birth of Saint Louis, King of France, in 2014 provided an opportunity to obtain a sample of his relics for “scientific identification”. With all relics the chain of custody and its backstory are critical for evaluation. Most of Louis’ relics held in the Basilica of Saint-Denis  were destroyed during the religious violence of  sixteenth century Paris. Fortunately the process of preserving and transferring Louis home to France from the site of death on crusade in Tunis, North Africa left bits of him in several locations.  Part of the preservation process used at the time removed his intestines and other internal organs to be embalmed separately while the remainder of the body was boiled to clean the bones to return to Paris. The bones were enshrined in Paris, while the heart and some viscera were enshrined at the abbey of Monreale near Palermo by his brother Charles, King of Sicily, who oversaw the preparation of the body and its transport back to France.

13th century Reliquary of Saint Louis, Basicilla of St. Dominic, Bologna Italy. (Source: Photo of Georges Jansoone, public domain on Wikipedia)

During a stop over at Bologna en route to Lyon and then Paris, some of his viscera were removed and interned in the Basilica of Saint Dominic. In 1297 Louis, who had died on 25 August 1270, was officially canonized as Saint Louis of France.  A portion of these visceral relics were given for the consecration of the cathedral of Turin in 1895, and these were transferred to the cathedral of Versailles in 1985. It is from this visceral relic that the 2 g specimen was obtained for scientific evaluation.

Microscopic Examination

The plan is to do a full “medical and forensic anthropological analysis” of the remains. The first result released by Phillipe Charlier’s team is the discovery of a semicircular parasite viewed by Scanning Electron Microscope (SEM) analysis, identified as a male Schistosoma based on its size and morphology.  Schistomsoma are a sexually dimorphic flat worm, also known as a blood fluke, that inhabit the capillaries of the abdomen (mesentery or bladder plexus depending on species) and release their eggs into either feces or urine. The eggs hatch in fresh water and must pass through a fresh water snail before emerging as larvae that can inhabit a mammalian host. Only about 50% of the eggs produced actually exit the body.  The adult worms and eggs that do not reach the feces or urine can cause extensive inflammation resulting in granulomas and fibrosis (scar tissue) to the abdominal organs (liver, spleen, intestines, bladder) and the blood vessels of the abdomen causing an accumulation of fluid in the peritoneal cavity.  Eggs that do breach into the lumen of the intestine cause chronic blood loss into the lumen producing chronic bloody stools. In the worst cases the blood loss can cause anemia.

Saint Louis
Source: Charlier, Bouchet, Weil & Bonnet, 2015.

Compare to a SEM preparation of a modern (non-mummified) male Schistosoma:

A C-shaped male schistosoma; the smaller female resides in the canal. (Source: David Williams, Illinois State University made public domain, Wikipedia)

King Louis had not been in Tunis long enough for him to contracted schistosomiasis upon his arrival only a month before his death. When and where he contracted the flat worm infestation is open to more speculation.  Schistosoma have been observed in archaeological remains of one individual from 9th century France, but have not yet been commonly observed. Charlier et al. (2015) suggest that Louis’ previous crusade in North Africa between 1250 and 1254, spending some time imprisoned in Damietta, Egypt, is the most likely period for start of the infection. If this is true, then Louis would have had a chronic infection for about 20 years at the time of his death. Charlier’s team do not believe that Schistosomiasis contributed to his death.

So far they have not observed any other parasites in the sample. This is not necessarily surprising considering that they have not yet identified the anatomic source of the specimen. It is not possible to even guess at the anatomic source from the crumbling, blackened specimen pictured in their study (fig. 1). Their analysis is continuing.

Debating Saint Louis’ Cause of Death

As soon as the schistosoma report was published, the debate on the cause of Louis’ death began in the letters of Forensic Science, Medicine and Pathology (where the report was published). So lets begin with the best account of Louis’ death, and go from there.

Beyond skirmishing and entrenching the camp nothing was done, as King Louis was awaiting the arrival of his brother Charles of Anjou (now King of Sicily). Whilst they were waiting encamped, John Tristan fell sick, and died on board one of the ships on August 3rd. A few days later the Legate also died and many other persons, some of fever, some of dysentery. Philip, the King’s eldest son, fell sick with fever; and the King was taken with dysentery (the complaint to which he nearly succumbed in his first Crusade) and died on August 25th. (Guillaume de Nangis account in the Memoirs of Lord Joinville, Book 4, Ch. 4)

Strangely, the plague has traditionally been claimed as Louis’ cause of death. This is completely unfounded since the Black Death will not bring epidemic Yersinia pestis back to the Mediterranean for another 77 years! There is nothing in the account above to suggest plague. This has rightly been dismissed as Louis’ cause of death.

Eric Faure wrote a letter arguing that malaria was a possible cause based on reports of Louis’ history of tertian fevers dating back to the 1242. Faure suggests that Louis went on his first crusade in thanksgiving for surviving “cerebral malaria with a coma” after a relapse in 1244. Cerebral malaria is usually caused by Plasmodium falciparum, which is not a chronic (relapse causing) infection. If Louis suffered relapses of malaria contracted in France then it was most likely Plasmodium vivax, which rarely causes cerebral malaria. Whether or not Louis had cerebral malaria in the 1240s, this doesn’t really inform of his his health in 1270.  Faure also notes that some of the men on Louis’ last crusade had intermittent fevers suggestive of malaria. Faure reaches too far suggesting that the dysentery was a symptom of malaria. Gastrointestinal symptoms are possible but rare in malaria and usually then in children. Philippe Charlier responded with a letter dismissing Faure’s suggestion to look for Plasmodium in the remains, because they would not have caused Louis’ death. Following the report in Lord Joinville’s memoir (quoted above), Charlier reports in his letter that his team is now looking for evidence of bacteria, viruses or amoeba in the embalmed “intestines” that are more likely to be the cause of the “dysenteric syndrome” reported in “Louis and his court”.

I will be watching for the final report, but the idea of a single enteric pathogen being the cause of death may not really represent reality. Based on Joinville’s memoir is appears that the “court” was suffering from a variety of camp diseases found in most medieval armies on prolonged campaigns. In such a situation, co-infection is highly likely particularly with chronic parasites. Indeed, Louis was probably not the only one in camp with schistosomiasis lingering from previous travels.  Although I doubt malaria caused Louis’ dysentery, it is quite possible he was suffering from chronic malaria and that it contributed to weakening his health, making him more susceptible to other pathogens. Indeed co-infection with Schistosoma and Plasmosdium could have made him quite anemic.  It would still be worth knowing if Louis had an active malaria infection, even if Shigella or another enteric pathogen was the primary cause of death.


Charlier, P., Bouchet, F., Weil, R., & Bonnet, B. (Oct. 2015). Schistosomiasis in the mummified viscera of Saint-Louis (1270 AD). Forensic Science, Medicine, and Pathology, 1–2.

Faure, E. (Dec. 2015). The infections of Saint-Louis: possible involvement of malaria.[Letter]  Forensic Science, Medicine, and Pathology, 1–1.

Charlier, P. (2016). Neither plague nor malaria, but dysentery as a cause of death for St. Louis. [Letter]  Forensic Science, Medicine, and Pathology, 1–1.

The Memoirs of Lord Joinvilletranslated by Ethel Wedgwood, E-text. University of Virginia library

Louis IV of France, Wikipedia.

WHO fact sheet: Schistosomiasis

Schistosoma, Wikipedia

Michael Walsh, Schistosomiasis on the Infection Landscapes blog. See this page for the best description of the medical effects of schistosomiasis.