The Black Death: was it caused by rats or viruses?

What caused the Black Death, the terrible plague that may have killed as many as half of all Europeans in the 14th century? It has been assumed by most people, this reviewer included, that it was caused by the bacterium Yersinia pestis , the causative factor of bubonic plague. This fascinating and provocative book, however, suggests otherwise.

Bubonic plague is a disease of rodents that lurks in isolated parts of central Asia and northern Africa. It has recently become established in wild rodent populations of North America. As recently as the early 20th century, plague broke out repeatedly from these refuges into the human populations of southern Asia and India. Before the availability of antibiotics, it caused millions of deaths.

The bubonic form of plague, marked by the grossly swollen lymph nodes in the groin and neck known as buboes, is spread by rat fleas. When the guts of the fleas are blocked by bacterial growth, they will bite humans. In the pneumonic form, the lungs haemorrhage and the patient breathes out clouds of bacteria, spreading the plague directly from one human to another.

All this has been well established through the investigations of modern medicine. What is not well established is the nature of the plagues of earlier centuries. Some of these had the typical symptoms of bubonic plague, and some did not. The Black Death is particularly puzzling, for it spread in a pattern very unlike that of present-day bubonic plague. Notably, it spread to new regions even in winter. This is strange, for in the Middle Ages the only rats that we have evidence of in Europe were tropical black rats. In winter, these rats must have huddled in the warmth of houses, seldom travelling.

These discrepancies have led a number of authors to suggest that the plague was indeed bubonic but that it spread primarily in the pneumonic form. But death from this form is so swift that it is hard to see how it could have been transmitted over substantial distances. Others have suggested that the Black Death was caused by some other agent, though they tend to be vague about what that might have been.

Susan Scott and Christopher Duncan go even further. They suggest that except for isolated outbreaks near the Mediterranean, few if any of the plague outbreaks of Europe were bubonic or pneumonic. They marshal a great deal of epidemiological evidence supporting their view that the big plagues, from that of Justinian in the 6th century to the great plague of London in 1665, were caused by something else.

Perhaps, they suggest, these plagues were haemorrhagic fevers caused by viruses, possibly filoviruses allied to Marburg or Ebola - but they are careful to point out that the viruses were unlikely to have been either of these. Marburg and Ebola have relatively short incubation times and are rarely transmitted from one human to another. Neither do these viruses produce the buboes that figure so strongly in many medieval descriptions of plagues. Buboes are characteristic of severe bacterial infections, the result of engorgement of the lymph nodes with bacteria killed by the immune system and with phagocytes that are frantically trying to engulf them all. They are not found in viral diseases. Such diseases tend to produce much smaller swellings of the lymph nodes, a point that the authors neglect to mention.

Do the authors make their case? I do not think so, though they raise many challenging issues. Bubonic plague was certainly not the only disease to devastate Europe in those ghastly centuries. Some, such as the sweating sickness that swept through England at the end of the 15th century, were seemingly different from any present-day diseases. But the buboes, and the occasional accounts of massive die-offs of animals, suggest that bubonic and perhaps pneumonic plague were widespread. There is also tantalising evidence from molecular biology. Traces of the DNA of Yersinia pestis have been found in human remains from 14th-century Provence and from the 18th-century outbreak in Marseilles. However, there is no evidence as yet of the presence (or absence) of this bacterium from medieval cemeteries farther from the Mediterranean.

The strongest part of the authors' case is that neither bubonic nor pneumonic plague was likely to have spread in the patterns that were recorded by contemporary chronicles. The Yersinia camp is forced to propose that brown rats may have been present in medieval times, or that black rats were more mobile than we suppose. Rats are resourceful creatures. A few years ago, I caught a faint glimpse of what life might have been like in medieval times as I watched rats scuttle among people sleeping on the pavements of Bombay. As we await direct DNA evidence from northern Europe, or some other break in the case, we must always remember how difficult it is to construct the world of previous centuries. Although the authors of this challenging book are to be commended for bringing together much fascinating information about plagues, the argument over the nature of the Black Death is far from settled.

Christopher Wills is professor of biology, University of California, San Diego, United States.