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Wildlife Research Wildlife Research Society
Ecology, management and conservation in natural and modified habitats
RESEARCH ARTICLE

We are connected: flea–host association networks in the plague outbreak focus in the Rift Valley, northern Tanzania

Rhodes H. Makundi A D , Apia W. Massawe A , Benny Borremans B , Anne Laudisoit B C and Abdul Katakweba A
+ Author Affiliations
- Author Affiliations

A Pest Management Centre, Sokoine University of Agriculture, PO Box 3110, Morogoro, 0505 TZ.MO.MU, Tanzania.

B Evolutionary Ecology Group, University of Antwerp,B-2020 Antwerpen, Belgium.

C Institute of Integrative Biology, University of Liverpool, Liverpool, L69 7ZB, UK.

D Corresponding author. Email: rmakundi@yahoo.com

Wildlife Research 42(2) 196-206 https://doi.org/10.1071/WR14254
Submitted: 12 December 2014  Accepted: 10 May 2015   Published: 12 June 2015

Abstract

Context: Plague is a serious health problem in northern Tanzania, with outbreaks since 2008 in two districts located in Rift Valley. There is dearth of knowledge on diversity of small mammal and flea fauna occurring in this plague focus. Knowledge on interactions between fleas and rodent species that harbour the plague bacterium, Yersinia pestis, is important for developing strategies for control and prevention of plague.

Aims: This study aims to show how rodents and fleas are associated with each other in the plague focus.

Methods: Animals were trapped bimonthly from 2009 to 2012 in different habitats. The fur of animals was brushed to collect fleas, which were identified and quantified. Network analysis methods, randomisation and rarefaction curves were used to show how hosts and fleas are associated.

Key results: Thirteen species of rodents were associated with 26 species of fleas of which Dinopsyllus lypusus, Xenopsylla brasiliensis and X. cheopis are confirmed efficient vectors of Y. pestis. Randomisation and rarefaction curves established that Lophuromys flavopunctatus had significantly higher flea species richness (n = 9) than did all other hosts, whereas Xenopsylla cheopis and Dinopsyllus spp. showed greater host species richness than did other species of fleas. There was no significant correlation between host sex and flea abundance (χ2 = 0.8, d.f. = 6, P = 0.371), but significant differences between reproductive states (adults had more fleas than did subadults) were observed, which probably reflected typical positive correlation between size and flea abundance (χ2 = 4.1955, d.f. = 1, P = 0.040).

Conclusions: The plague outbreak focus in northern Tanzania has a diverse fauna of rodents and fleas with multiple patterns of association and connectivity.

Implications: Existence of diverse populations of rodents associated with a large number of flea species, some of which are efficient plague vectors, increases the potential for persistence and transmission of plague to humans in northern Tanzania.

Additional keywords: Karatu, Mbulu, rodents, Yersinia pestis.


References

Amatre, G., Babi, N., Enscore, R. E., Ogen-Odoi, A., Atiku, L. A., Akol, A., Gage, K. L., and Eisen, R. J. (2009). Flea diversity and infestation prevalence on rodents in a plague-endemic region of Uganda. The American Journal of Tropical Medicine and Hygiene 81, 718–724.
Flea diversity and infestation prevalence on rodents in a plague-endemic region of Uganda.Crossref | GoogleScholarGoogle Scholar | 19815894PubMed |

Bearden, S. W., and Brubaker, R. R. (2010). Recent findings regarding maintenance of enzootic variants of Yersinia pestis in sylvatic reservoirs and their significance in the evolution of epidemic plague. Vector Borne and Zoonotic Diseases 10, 85–92.
Recent findings regarding maintenance of enzootic variants of Yersinia pestis in sylvatic reservoirs and their significance in the evolution of epidemic plague.Crossref | GoogleScholarGoogle Scholar | 20158336PubMed |

Bevins, S. N., Baroch, J. A., Nolte, D. L., Zhang, M., and Hongxuan, H. E. (2012). Yersinia pestis: examining wildlife plague surveillance in China and USA. Integrative Zoology 7, 99–109.
Yersinia pestis: examining wildlife plague surveillance in China and USA.Crossref | GoogleScholarGoogle Scholar | 22405453PubMed |

Carter, T. B., Handcock, M. S., and Hunter, D. R. (2014a). ‘Network: Classes for Relational Data. R Package Version 1.9.0.’ (University of Washington: Irvine, CA.) Available at http://statnet.org/ [accessed 10 October 2014]

Carter, T. B., Handcock, M. S., and Hunter, D. R. (2014b). ‘Network: Classes for Relational Analysis. R Package Version 2.3-2’. Available at http://CRAN.R-project.org/package=sna [accessed 10 October 2014]

Davis, R. M., Smith, R. T., Madon, M. B., and Sitko-Cleugh, E. (2002). Fleas, rodents and plague ecology at Chuchupate Campground, Ventura County, California. Journal of Vector Ecology 27, 107–127.
| 12125863PubMed |

Davis, S., Makundi, R. H., Machangu, R. S., and Leirs, H. (2006). Demographic and spatio-temporal variation in human plague at a persistent focus in Tanzania. Acta Tropica 100, 133–141.
Demographic and spatio-temporal variation in human plague at a persistent focus in Tanzania.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28jgt1CjtA%3D%3D&md5=3bb209389923ba50155156e022337cd1CAS | 17113555PubMed |

Drewe, J. A. (2010). Who infects whom? Social networks and tuberculosis transmission in wild meerkats. Proceedings Royal Society London B. Biology 277, 633–642.

Durden, L. A., and Hinckle, N. C. (2009). Fleas (Siphonaptera) In ‘Medical and Veterinary Entomology’. 2nd edn. (Eds G. R. Mullen and L. A. Durden.) pp. 115–135. (Academic Press: New York.)

Eames, K. T. D., and Keeling, M. J. (2002). Modelling dynamics and network heterogeneities in the spread of sexually transmitted diseases. Proceedings of the National Academy of Sciences, USA 99, 13330–13335.
Modelling dynamics and network heterogeneities in the spread of sexually transmitted diseases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnvFGgsL0%3D&md5=b6211239ff3676fcde07c72dec9fce31CAS |

Eisen, R. J., Borchert, J. N., Mpanga, J. T., Atiku, L. A., MacMillan, K., Boegler, K. A., Montenieri, J. A., Monaghan, A., and Gage, K. L. (2012). Flea diversity as an element for persistence of plague bacteria in an East African plague focus. PLoS One 7, e35598.
Flea diversity as an element for persistence of plague bacteria in an East African plague focus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmsVGhtr4%3D&md5=82bd8a569923574f173b70b9b124a09bCAS | 22530057PubMed |

Foley, P., and Foley, J. (2010). Modeling susceptible infective recovered dynamics and plague persistence in California rodent–flea communities. Vector-Borne and Zoonotic Diseases 10, 59–67.
Modeling susceptible infective recovered dynamics and plague persistence in California rodent–flea communities.Crossref | GoogleScholarGoogle Scholar | 20158333PubMed |

Gage, K. L., and Kosoy, M. Y. (2005). Natural history of plague: perspectives from more than a century of research. Annual Review of Entomology 50, 505–528.
Natural history of plague: perspectives from more than a century of research.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFOqtb8%3D&md5=d19f521be871d93f8c1f975361b639b6CAS | 15471529PubMed |

Haule, M., Lyamuya, E. E., Hang’ombe, B. M., Kilonzo, B. S., and Matee, M. I. (2013). Investigations of fleas as vectors in the transmission of plague during quiescent period in north-eastern Tanzania. Journal of Entomology and Nematology 5, 88–93.
Investigations of fleas as vectors in the transmission of plague during quiescent period in north-eastern Tanzania.Crossref | GoogleScholarGoogle Scholar |

Kilonzo, B. S. (1976). A survey of rodents and their flea ectoparasites in north-eastern Tanzania. East African Journal of Medical Research 3, 117–126.

Kilonzo, B. S., and Mtoi, R. S. (1983). Entomological, bacteriological and serological observations after the 1977 plague outbreak in Mbulu District, Tanzania. East African Medical Journal 60, 91–97.
| 1:STN:280:DyaL2c%2FgsVWjtg%3D%3D&md5=2f161e0344679edddc33932eda986b82CAS | 6617551PubMed |

Kilonzo, B. S., and Mhina, J. I. K. (1983). Observations on the current status of plague endemicity in the Western Usambara mountains, north-east Tanzania. Acta Tropica 40, 365–373.
| 1:STN:280:DyaL2c7ltVarsQ%3D%3D&md5=5f20844befa2017b1573aeb3814ef6c9CAS | 6142635PubMed |

Kilonzo, B. S., Julius, M., Sabuni, C., and Mgode, G. (2005). The role of rodents and small carnivores in plague endemicity in Tanzania. Belgian Journal of Zoology 135, 119–125.

Kingdon, J. (1974). ‘The Kingdon Field Guide of African Mammals.’ (A&C Black Publishers.)

Krasnov, B., Shenbrot, G. I., Medvedev, S., Vatschenok, V., and Khokhlova, I. (1997). Host–habitat relations as an important determinant of flea assemblages (Siphonaptera) on rodents in the Negev desert. Parasitology 114, 159–173.
Host–habitat relations as an important determinant of flea assemblages (Siphonaptera) on rodents in the Negev desert.Crossref | GoogleScholarGoogle Scholar | 9051922PubMed |

Krasnov, B., Shenbrot, G., Khokhlova, I., Medvedev, S., and Vatschenok, V. (1998). Habitat dependence of a parasite–host relationship: flea (Siphonaptera) assemblages in two gerbil species of the Negev desert. Journal of Medical Entomology 35, 303–313.
Habitat dependence of a parasite–host relationship: flea (Siphonaptera) assemblages in two gerbil species of the Negev desert.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c3nslOrtg%3D%3D&md5=e2040180ad8069acdbb17dff746b5f12CAS | 9615550PubMed |

Krasnov, B. R., and Khokhlova, I. S. (2001). The effect of behavioural interactions on the transfer of fleas (Siphonaptera) between two rodent species. Journal of Vector Ecology 26, 181–190.
| 1:STN:280:DC%2BD38%2Fos1Ghuw%3D%3D&md5=a21690ba5001f5dffc97afa35d86926cCAS | 11813655PubMed |

Krebs, C. J. (2009). ‘Programs for Ecological Methodology. Version 7.1.’ (Exeter Software: Setauket, NY.)

Laudisoit, A., Neerinckx, S., Makundi, R. H., Leirs, H., and Krasnov, B. R. (2009a). Are local plague endemicity and ecological characteristics of vectors and reservoirs related? A case study in north-east Tanzania. Current Zoology 55, 200–211.

Laudisoit, A., Leirs, H., Makundi, R. H., and Krasnov, B. R. (2009b). Seasonal and habitat dependence of species composition of flea assemblages parasitic on small mammals in Tanzania. Integrative Zoology 4, 196–212.
Seasonal and habitat dependence of species composition of flea assemblages parasitic on small mammals in Tanzania.Crossref | GoogleScholarGoogle Scholar | 21392290PubMed |

Laudisoit, A., Neerinckx, S., Makundi, R. H., Leirs, H., and Krasnov, B. (2010). Plague in Tanzania: from a host and vector perspective. Vector Borne and Zoonotic Diseases 10, 101.

Leirs, H., Neerinckx, S., Laudisoit, A., and Makundi, R. H. (2010). Emergence and growth of plague foci in Africa. Vector Borne and Zoonotic Diseases (Larchmont, N.Y.) 10, 97.

Lemon, J. (2006). Plotrix: a package in the red light district of R. R-News 6, 8–12.

Makundi, R. H., and Kilonzo, B. S. (1994). Seasonal dynamics of rodent fleas and its implication on control strategies in Lushoto district, Tanzania. Journal of Applied Entomology 118, 165–171.
Seasonal dynamics of rodent fleas and its implication on control strategies in Lushoto district, Tanzania.Crossref | GoogleScholarGoogle Scholar |

Makundi, R. H., Kilonzo, B. S., and Massawe, A. W. (2003). Interaction between rodent species in agro-forestry habitats in the western Usambara mountains, northeast Tanzania, and its potential for plague transmission to humans. In ‘Rats, Mice and People. Rodent Biology and Management’. (Eds G. R. Singleton, L. A. Hinds, C. J. Krebs and D. M. Spratt.) pp. 20–24. (Australian Centre for International Agricultural Research: Canberra.)

Makundi, R. H., Massawe, A. W., and Mulungu, L. S. (2005). Rodent population fluctuations in three ecologically heterogeneous locations in north-east, central and south-west Tanzania. Belgian Journal of Zoology 135, 159–165.

Makundi, R. H., Massawe, A. W., Mulungu, L. S., Katakweba, A. S., Mbise, T. J., and Mgode, G. F. (2008). Potential mammalian reservoirs in a bubonic plague outbreak focus in Mbulu District, northern Tanzania, in 2007. Mammalia 72, 253–257.
Potential mammalian reservoirs in a bubonic plague outbreak focus in Mbulu District, northern Tanzania, in 2007.Crossref | GoogleScholarGoogle Scholar |

Makundi, R. H., Massawe, A. W., Mulungu, L. S., and Katakweba, A. S. (2009). Diversity and population dynamics of rodents in farm-fallow mosaic fields in Central Tanzania. African Journal of Ecology 48, 313–320.
Diversity and population dynamics of rodents in farm-fallow mosaic fields in Central Tanzania.Crossref | GoogleScholarGoogle Scholar |

Marshall, A. G. (1981). ‘The Ecology of Ectoparasitic Insects.’ (Academic Press: London.)

McCauley, D. J., Salkeld, D. J., Young, H. S., Makundi, R. H., Dirzo, R., Eckerlin, R. P., Lambin, E. F., Gaffikin, L., Barry, M., and Helgen, K. M. (2015). Effects of land use on plague (Yersinia pestis) activity in rodents in Tanzania. The American Journal of Tropical Medicine and Hygiene , .
Effects of land use on plague (Yersinia pestis) activity in rodents in Tanzania.Crossref | GoogleScholarGoogle Scholar | 25711606PubMed |

Msangi, A. S. (1969). Entomological observations after the 1968 plague outbreak in Mbulu District, Tanzania. East African Medical Journal 46, 465–470.
| 1:STN:280:DyaE3c%2Fjslertg%3D%3D&md5=29062cf9ffa43237490339e279741322CAS |

Poulin, R. (2010). Network analysis shining light on parasite ecology and diversity. Trends in Parasitology 26, 492–498.
Network analysis shining light on parasite ecology and diversity.Crossref | GoogleScholarGoogle Scholar | 20561821PubMed |

R CORE TEAM (2013). ‘R: a Language and Environment for Statistical Computing.’ (R Foundation for Statistical Computing: Vienna.) Available at http://www.R-project.org/. [Accessed April 2013]

Rahelinirina, S., Duplantier, J. M., Ratovonjato, J., Ramilijaona, O., Ratsimba, M., and Rahalison, L. (2010). Study on the movement of Rattus rattus and evalauation of the plague dispersion in Madagascar. Vector Borne and Zoonotic Diseases 10, 77–84.
Study on the movement of Rattus rattus and evalauation of the plague dispersion in Madagascar.Crossref | GoogleScholarGoogle Scholar | 20158335PubMed |

Thiagarajan, B., Cully, J. F., Loughin, T. M., Montenieri, J. A., and Gage, K. L. (2008). Geographic variation in rodent-flea relationships in the presence of black-tailed prairie dog colonies. Journal of Vector Ecology 33, 178–190.
Geographic variation in rodent-flea relationships in the presence of black-tailed prairie dog colonies.Crossref | GoogleScholarGoogle Scholar | 18697322PubMed |

Thomas, R. E. (1996). Fleas and the agents they transmit. In ‘The Biology of Disease Vectors’. (Eds B. J. Beaty and W. C. Marquardt.) pp. 146–159. (University Press of Colorado: Niwot, CO.)

Wimsatt, J., and Biggins, D. E. (2009). A review of plague persistence with special emphasis on fleas. Journal of Vector Borne Diseases 46, 85–99.
| 19502688PubMed |

Winter, L. (2014). ‘Bubonic Plague Spread in Madagascar.’ (IFLScience.) Available at http://www.iflscience.com/health-and-medicine/bubonic-plague-outbreak-spreads-madagascar. [Accessed 23 March 2015]

Ziwa, M. H., Matee, M. I., Kilonzo, B. S., and Hang’ombe, B. M. (2013). Evidence of Yersinia pestis DNA in rodents in plague outbreak foci in Mbulu and Karatu Districts, northern Tanzania. Tanzania Journal of Health Research 15, 1–8.
Evidence of Yersinia pestis DNA in rodents in plague outbreak foci in Mbulu and Karatu Districts, northern Tanzania.Crossref | GoogleScholarGoogle Scholar |