Category Archives: environmental history

Looking back on the autumn

fall-2016

This fall was quite the chaotic jumble — not all bad. One project successfully completed. A door closed but I think another better one may be opening. Somehow in the midst of all this I managed to do a little reading, so here is what that stood out for the fall (and early winter).

My publications

Ziegler, M. (2016) Landscapes of DiseaseLandscapes, 17.2. 99-107. An introduction to the concept of ‘landscapes of disease’ and the articles in the issue. (Open access)

Ziegler, M. (2016) Malarial Landscapes in Late Antique Rome and the Tiber Valley  Landscapes, 17.2: 139-155.

Books

  • Yong, Ed. (2016) I Contain Multitudes: The Microbes Within Us and a Grander View of Life. Ecco.  microscope23 (1)microscope23 (1)microscope23 (1)microscope23 (1)microscope23 (1)
  • Holland, John. (2014) Complexity: A Short Introduction. OUP microscope23 (1)microscope23 (1)microscope23 (1)
  • Bronton, Jerry (2004) The Renaissance: A Short Introduction. OUP. microscope23 (1)microscope23 (1)microscope23 (1)
  • Tim Clarkson (2016) Scotland’s Merlin: A Medieval Legend and It’s Dark Age Origins. John Donald/Birlinn.      microscope23 (1)microscope23 (1)microscope23 (1)microscope23 (1)microscope23 (1)
  • Hamerow, Helena. (2012) Rural Settlements and Society in Anglo-Saxon England. OUP. microscope23 (1)microscope23 (1)microscope23 (1)microscope23 (1)

Articles

  • Arnold, E. F. (2017). Rivers of Risk and Redemption in Gregory of Tours’ Writings. Speculum, 92(1), 117–143. http://doi.org/10.1086/689460
  • Arnold, E. F. (2014). Fluid Identities: Poetry and the Navigation of Mixed Ethnicities in Late Antique Gaul. Ecozon@, 1–19.
  • Bahl, J., Pham, T. T., Hill, N. J., Hussein, I. T. M., Ma, E. J., Easterday, B. C., et al. (2016). Ecosystem Interactions Underlie the Spread of Avian Influenza A Viruses with Pandemic Potential. PLoS Pathogens, 12(5), e1005620–20. http://doi.org/10.1371/journal.ppat.1005620
  • Carmichael, A. G., & Silverstein, A. M. (1987). Smallpox in Europe before the seventeenth century: virulent killer or benign disease? Journal of the History of Medicine and Allied Sciences, 42(2), 147–168.

  • Duggan, A. T., Perdomo, M. F., Piombino-Mascali, D., Marciniak, S., Poinar, D., Emery, M. V., et al. (2016). 17th Century Variola Virus Reveals the Recent History of Smallpox. Current Biology, 1–7. http://doi.org/10.1016/j.cub.2016.10.061
  • Fauci, A. S., & Morens, D. M. (2016). Zika virus in the Americas—yet another arbovirus threat. New England Journal of Medicine, 374(7), 601–604.

  • Jones, L. (2016). The Diseased Landscape: Medieval and Early Modern Plaguescapes. Landscapes, 17(2), 108–123. http://doi.org/10.1080/14662035.2016.1251102
  • Marciniak, S., Prowse, T. L., Herring, D. A., Klunk, J., Kuch, M., Duggan, A. T., et al. (2016). Plasmodium falciparum malaria in 1st–2nd century CE southern Italy. Current Biology, 26(23), R1220–R1222. http://doi.org/10.1016/j.cub.2016.10.016
  • Slavin, P. (2016). Epizootic Landscapes: Sheep Scab and Regional Environment in England in 1279–1280. Landscapes, 17(2), 156–170. http://doi.org/10.1080/14662035.2016.1251040
  • Valtuena, A. A., Mittnik, A., Massy, K., Allmae, R., Daubaras, M., Jankauskas, R., et al. (2016). The Stone Age Plague: 1000 years of Persistence in Eurasia. BioRxiv Preprint, 28. http://doi.org/10.1101/094243
  • Walsh, M. G., Amstislavski, P., Greene, A., & Haseeb, M. A. (2016). The Landscape Epidemiology of Seasonal Clustering of Highly Pathogenic Avian Influenza (H5N1) in Domestic Poultry in Africa, Europe and Asia. Transboundary and Emerging Diseases, 1–14. http://doi.org/10.1111/tbed.12537
  • Whittemore, K., Tate, A., Illescas, A., & Saffa, A. (2017). Zika Virus Knowledge among Pregnant Women Who Were in Areas with Active Transmission. Emerging Infectious …. http://doi.org/10.3201/eid2106.150270

  • 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. http://doi.org/10.1038/srep34867

Landscapes of Disease Themed Issue

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For the last couple years, I have been writing about a landscape-based approach to the study of infectious disease in general and historic epidemics in particular. When I first wrote about Lambin et al.’s now classic paper “Pathogenic landscapes” nearly three years ago, I did not know then that it would be so influential in my thinking or that the Medieval Congress sessions would be so successful. In the fall of 2014, Graham Fairclough and I began talking about ways that this first congress session could be represented in the journal he edits, Landscapes. This issue is a departure from their usual approach to landscape studies so I would like to thank Graham Fairclough for entrusting me with a whole issue. It has been a challenge for both of us, and I am proud of our product.

This issue represents the wide variety of studies that can be done all contributing to an understanding of past landscapes of disease. One of the reasons why I like the phrase landscape of disease, rather than simply landscape epidemiology, is that it opens up the array of disciplines that can be involved. In the study of diseases of the past, humanistic approaches can be as valuable as scientific methods. Both are required to build a reasonably coherent reconstruction of the past. Science and the humanities need to act as a check and balance on each other, hopefully in a supportive and collegial way.

The issue was published online a couple days ago. Accessing the journal through your library will register interest in the journal with both your library and the publisher, and would be appreciated. By now the authors should (or will soon) have their codes for their free e-copies if you do not have access otherwise.

Table of Contents

Landscapes of Disease by Michelle Ziegler. An introduction to the concept of ‘landscapes of disease’ and the articles in the issue. (Open access)

The Diseased Landscape: Medieval and Early Modern Plaguescapes by Lori Jones

The Influence of Regional Landscapes on Early Medieval Health (c. 400-1200 A.D.): Evidence from Irish Human Skeletal Remains by Mara Tesorieri

Malarial Landscapes in Late Antique Rome and the Tiber Valley by Michelle Ziegler

Epizootic Landscapes: Sheep Scab and Regional Environment in England in 1279-1280 by Philip Slavin

Plague, Demographic Upheaval and Civilisational Decline: Ibn Khaldūn and Muḥammed al-Shaqūrī on the Black Death in North Africa and Islamic Spain by Russell Hopley

plus seven book reviews. Enjoy!

 


Lambin, E. F., Tran, A., Vanwambeke, S. O., Linard, C., & Soti, V. (2010). Pathogenic landscapes: Interactions between land, people, disease vectors, and their animal hosts. International Journal of Health Geographics, 9(1), 54. http://doi.org/10.1186/1476-072X-9-54

The Promiscuous Human Flea

Female Pulex irritans, the human flea, from the Katja ZSM collection (CC3.0)
Female Pulex irritans, the human flea, from the Katja ZSM collection (CC3.0)

by Michelle Ziegler

The human flea seems like a misnomer today. We are not its current primary host, but that doesn’t mean that it once wasn’t our primary flea.  Pulex irritans  was first described by Carl Linnaeus as the “house flea” in 1758 (Krasnov 2012:4) and it is still found in homes in many parts of the world.

For the most part, the human flea is a nuisance, an irritant as its name implies. Except when it isn’t, when it occasionally transmits Yersinia pestis, the plague, to people. Pulex irritans has been  in homes with human plague cases from Arizona to Madagascar (Archibald & Kunitz, 1971; Ratovonjato et al, 2014). In 2006, Drancourt, Houhamdi, and Raoult argued that either the human flea or louse played a major role in human plague epidemics.

Human fleas have been found in the homes in several areas where plague occurs. P. irritans infected with Y. pestis were found on a dog in a home of a plague victim on Navajo land in Arizona in 1968. They also report knowledge  Y. pestis being isolated from  P. irritans fleas on dogs in the home of an infected child in Kayneta in 1968 (Archibald & Kunitz, 1971).   A recent survey of plague regions in Tanzania found 50% of the fleas in homes were P. irritans (Haule et al, 2013). A recent survey of fleas in Madagascar found that 98% of the fleas found inside control homes  in the control region of the study were Pulex irritans (Miarinjara et al, 2016). The fact that they did not find them in the homes within the area of the plague outbreak a month earlier may be due to extensive spraying of insecticide to end the epidemic. Human fleas are suspected of being the vectors for a variety of zoonotic diseases in Iran today (Rahbari, Nabian, & Nourolahi, 2008).

The human flea, Pulex irritans, has had a very interesting and convoluted history. All of the Pulex fleas are thought to have evolved in South America, perhaps on guinea pigs or piccary . P. irritans is the only member of its genus  that has left the Americas.  It made it to Eurasia long before the “Columbian Exchange”.  So it crossed a land bridge at some point to begin spreading in Eurasia, and it need not have crossed on a human.  Ötzi the 5000 year old ice mummy from the Italian Alps yielded two human fleas from his  artifacts (Schedl, 2000). P. irritans has also been found Egypt from 3500 BC  (Bain 2004) and 1350-1323 BC (Panagiotakopulu, 2001) showing that it does well in warm, dry climates also. So not only where they present for the entire known period of plague but they have been specifically found in warm and cold regions. Pulex irritans has been found in floor debris of uncovered sites from Roman Britain (Kenward, 1998). They were common inhabitants of early medieval Irish homes (O’Sullivan, 2008).  They are fairly common finds in Norse Greenland settlements. Unfortunately flea surveys have not been done on most continental archaeological sites (or at least I haven’t found them).

So why is P. irritans called a promiscuous flea? It has nothing to do with sex! In this case promiscuous means that it will feed off of a wide variety of host species. It has a truly impressive host range beyond humans including pigs, dogs, cats, goats and sheep, cattle, chickens, porcupines, multiple species of foxes, wolves, coyotes,  golden jackel of Iran,  badgers, prairie dogs,  rabbits, wild cats,  and mice. There are undoubtably more species that could be added. It seems to be very common on foxes in North America and Europe. These are, of course, primarily predators of rodents.  Given its wide range of hosts, its distribution and frequency among hosts has probably fluctuated wildly due to environmental and biodiversity changes over the last millennia.

Such a wide host range also makes it a potential bridging vector, one that can move disease between a wild reservoir to a domestic space transmitting it to domestic rodents, pets, and humans. Importantly, bridging vectors work in both directions, meaning that it could be instrumental in developing a wildlife reservoir after a human epidemic in a new region.

fleaslifecycle
General flea life cycle (CDC). Adults are only 5% of flea biomass.

flea-pyramid-1P. irritans has a life cycle that is well suited to thriving in buildings like houses, barns, sheds, and animal nests or dens. Most of their biomass is in the egg stage. Small white eggs are often laid on the host but almost always fall off on to the floor. They do particularly well on the floor of stables and animal sheds where fermenting manure and debris keeps the eggs warm and moist.  They also do well in human homes where it is usually warmer and more humid than outdoors. They breed all year around. The eggs will hatch into larvae that resemble maggots within 4-6 days. The very active larvae will feed on organic debris including feces of the adult flea and other animals. After three molts it will develop a cocooned pupae where it will undergo a metamorphosis to the adult flea. It can remain in the pupa for several months if necessary until the conditions are suitable. So although human fleas are usually not present in stables or sheds during the coldest months the pupa can easily span the winter to emerge as adults in the early spring. This may explain why they are often the most abundant in the spring when all of the pupae from the late fall and winter emerge. It is unclear if the lifecycle pauses inside a heated human home. A well fed adult can live up to 513 days and even starved can last 135 days (Krasnov, 2012: 54). It is unclear how long they live after being infected by Yersinia pestis (or other pathogens). Fleas only feed on blood as adults so this is their only phase that can be infected by Yersinia pestis.

Modern infestations of P. irritans in Greece and Iran can give a few insights into its disease ecology. Sheep and goats are consistently the most heavily infested animals with P. irritans in modern Iran and Greece. In parts of Iran, P. irritans is the most common flea captured from humans or domestic livestock: goats, sheep, cattle and chickens (Moemenbellah-Fard et al, 2014; Rahbari,  Nabian, & Nourolahi, 2008;  Rafinejad et al, 2013). In some modern surveys, P. irritans is over 90% of the fleas collected in rural areas, found on sheep, goats, cattle, humans and chickens — “wherever the animal infestation was high the fleas easily transmitted to humans” (Rahbari et al, 2008:44). In Greece, Christodoulopoulos et al. (2006) made a very important observation:

“fleas accumulated in the goat environment with each successive generation leading to an increase in their number. This conclusion could be corroborated by the observation that the most successful flea control measure was the change of barn location with movement of the goats to another far away new-constructed barn.” (p. 142-143)

So even with modern insecticides, sheep dips, and building techniques available, the infestation of the building could not be controlled. This has implications for human housing. Observations of flea ecology in Iran back this up, albeit without addressing methods of eliminating infestations.

The Iranian reports discuss human flea bites more. Noting that men who worked with animals had a higher bite rate. Bites are primarily around the ankles and lower legs, often multiple bites in a row.  In Iran they noted that human reactions to the flea bites varied from highly allergic to no sensitivity at all (Rahbari, Nabian, & Nourolahi, 2008). This is a difference in human immunology to the fleas and sensitivity is likely to alter the immune response to not only the bite but also bacteria in the bite. There is also likely to be heterogeneity in which humans and animals are bitten.

As we begin to take Pulex irritans more seriously as a plague vector, there is a lot of basic biology that needs to be done yet. How long can they survive infected? How does it effect their feeding behavior? Some studies showed that a small percentage of P. irritans can block, so what effect does that have on transmission in that small percent of fleas?


References

Archibald, W. S., & Kunitz, S. J. (1971). Detection of plague by testing serums of dogs on the Navajo Reservation. HSMHA Health Reports, 86(4), 377–380.

Bain, A. (2004). Irritating intimates: the archaeoentomology of lice, fleas, and bedbugs. Northeast Historical Archaeology, 33(1), 81–90.

Barnes, Jefferey. (22 April 2014)  Human flea, Arthropod Museum Notes, Number 108. University of Arkansas.

Buckland, P. C., & Sadler, J. P. (1989). A biogeography of the human flea, Pulex irritans L.(Siphonaptera: Pulicidae). Journal of Biogeography (UK).

Christodoulopoulos, G., Theodoropoulos, G., Kominakis, A., & Theis, J. H. (2006). Biological, seasonal and environmental factors associated with Pulex irritans infestation of dairy goats in Greece. Veterinary Parasitology, 137(1-2), 137–143. http://doi.org/10.1016/j.vetpar.2005.12.012

Dobler, G., & Pfeffer, M. (2011). Fleas as parasites of the family Canidae. Parasites & Vectors, 4, 139–139. http://doi.org/10.1186/1756-3305-4-139

Drancourt, M., Houhamdi, L., & Raoult, D. (2006). Yersinia pestis as a telluric, human ectoparasite-borne organism. The Lancet Infectious Diseases, 6(4), 234–241. http://doi.org/10.1016/S1473-3099(06)70438-8

Eisen, Rebecca J., David T. Dennis, and Kenneth L. Gage. “The Role of Early-Phase Transmission in the Spread of Yersinia pestis.” Journal of medical entomology 52.6 (2015): 1183-1192.

Haule, M., Lyamuya, E. E., Kilonzo, B. S., Matee, M. I., & Hangombe, B. M. (2013). Investigation of fleas as vectors in the transmission of plague during a quiescent period in North-Eastern, Tanzania. Journal of Entomology and Nematology, 5(7). http://doi.org/10.5897/JEN2013.0083

Hufthammer, Anne Karin, and Lars Walløe. “Rats cannot have been intermediate hosts for Yersinia pestis during medieval plague epidemics in Northern Europe.” Journal of Archaeological Science 40.4 (2013): 1752-1759.

Kenward, H. (1999). Insect remains as indicators of zonation of land use and activity in Roman Carlisle, England. Reports from the Environmental Archaeology Unit (Vol. 99, pp. 1–30).

Kotti, B. K. (2015). Fleas (Siphonaptera) of mammals and birds in the Great Caucasus. Entomological Review, 95(6), 728–738. http://doi.org/10.1134/S0013873815060068

Krasnov, Boris (2012) Functional and Ecological Ecology of Fleas: A Model for Ecological Parasitology. Cambridge University Press.

Laudisoit, A., Leirs, H., Makundi, R. H., Van Dongen, S., Davis, S., Neerinckx, S., et al. (2007). Plague and the human flea, Tanzania. Emerging Infectious Diseases, 13(5), 687–693. http://doi.org/10.3201/eid1305.061084

Miarinjara A, Rogier C, Harimalala M, Ramihangihajason TR, Boyer S. Xenopsylla brasiliensis fleas in plague focus areas, Madagascar. Emerg Infect Dis. 2016 Dec [3 Sept 2016]. http://dx.doi.org/10.3201/eid2212.160318

Moemenbellah-Fard, M. D., Shahriari, B., Azizi, K., Fakoorziba, M. R., Mohammadi, J., & Amin, M. (2014). Faunal distribution of fleas and their blood-feeding preferences using enzyme-linked immunosorbent assays from farm animals and human shelters in a new rural region of southern Iran. Journal of Parasitic Diseases, 40(1), 169–175. http://doi.org/10.1007/s12639-014-0471-1

O’Sullivan, A. (2008). Early medieval houses in Ireland: social identity and dwelling spaces. Peritia, 20, 225–256.

Panagiotakopulu, E. (2001). Fleas from pharaonic Amarna. Antiquity, 75, 499–500.

Pulex irritans, Animal Diversity Web, accessed 18 June 2016.

Rahbari, S., Nabian, S., & Nourolahi, F. (2008). Flea infestation in farm animals and its health implication. Iranian Journal of Parasitology, 3(2), 43–47.

Rafinejad, J., Piazak, N., Dehghan, A., Shemshad, K., & Basseri, H. R. (2013). Affect of some environmental parameters on fleas density in human and animal shelters. American Journal of Research Communication.

Ratovonjato, J., Rajerison, M., Rahelinirina, S., & Boyer, S. (2014). Yersinia pestis in Pulex irritans Fleas during Plague Outbreak, Madagascar. Emerging Infectious Disease, 20(8), 1414–1415. http://doi.org/10.3201/eid1509.090442

Reilly, E. (2003). The contribution of insect remains to an understanding of the environment of Viking-age and medieval Dublin.  pp. 40-61 In: Medieval Dublin IV. Four Courts Press.

Schedl, W. (2000). “Contribution to insect remains from the accompanying equipment of the Iceman”. pp. 151-155 In S. Bortenschlager & K. Oeggl (Eds.), The Iceman and his Natural Environment. Springer.

Yakhchali, M., & Bahramnejad, K. (2015). A survey of Pulex irritans (Linnaeus 1758, Siphonaptera: Pulicidae) infestation in sheep and residential areas in Kurdistan Province, Iran. The Iranian Journal of Veterinary Science and Technology, 7(1), 40–47.