A role for vector-independent transmission in rodent trypanosome infection? A. Smith a, * , S. Telfer a,b , S. Burthe a , M. Bennett b , M. Begon a a Population Biology Research Group, School of Biological Sciences, Bioscience Building, University of Liverpool, Merseyside L69 7ZB, UK b Department of Veterinary Pathology, University of Liverpool, Leahurst, Neston CH64 7TE, UK Received 25 May 2006; received in revised form 17 June 2006; accepted 23 June 2006 Abstract Within host–pathogen systems where vector-borne transmission is the primary route of infection, little or no attention has been paid to the relative importance of secondary or alternative routes of transmission. Here, by contrast, we report the results from a controlled longitudinal field-scale experiment in which the prevalence of fleas (Siphonaptera) was manipulated and the occurrence and distribution of a flea-borne protozoan (Trypanosoma (Herpetosoma) microti) in a natural field vole (Microtus agrestis) population was monitored over a 2-year period. A non-systemic insecticide was applied to individual voles within two treatment grids and the prevalences of fleas and of T. microti were monitored on these and on two control grids. Blood samples were taken from all voles and PCR-based methods used to determine infection status. Insecticidal treatment was highly effective at reducing overall flea prevalence and recaptured animals (treated ca. 4 weeks previously) were very rarely infested (ca. 3%, compared with 50–70+% normally). On the other hand, the probability of try- panosome infection was reduced in treated animals on experimental grids to only around one-third of that normally observed. This sug- gests that direct, as opposed to flea-borne, transmission may not only occur, it may also be of epidemiological importance. The possibility that the importance of such transmission routes may have been underestimated in ‘vector-borne’ infections more generally is discussed. Ó 2006 Australian Society for Parasitology Inc. Published by Elsevier Ltd. All rights reserved. Keywords: Trypanosome prevalence; Field voles; Independent transmission 1. Introduction Fleas (Siphonaptera) are responsible for transmitting many viral, bacterial and protozoan infections to their mammalian hosts, including the stercorarian Trypanosoma (Herpetosoma) species, in which the developmental cycle is completed in the hindgut of the flea and infection occurs primarily by infected flea faeces contaminating superficial wounds or being eaten during grooming (Albright and Alb- right, 1991). Under laboratory conditions, transmission can also occur as a result of direct contact with cultured metacyclic trypomastigote forms, which enter the host’s vascular system via the oral-mucal membranes of the mouth and stomach (Maraghi et al., 1995) and it has been suggested that direct infection may occur as a result of aggressive interactions between infected hosts such as field voles (Microtus agrestis), where wounding is often severe (Molyneux, 1969). However, early attempts to infect M. agrestis directly by feeding them carcasses of infected voles were unsuccessful and it remains unclear whether, or to what extent, direct host-to-host trypanosome transmission occurs under natural conditions. There have been numerous laboratory and captive-ani- mal-based investigations of vector-borne pathogens (des Vignes et al., 2001), which have been used to parameterise models of disease ecology (Tompkins et al., 2002). Howev- er, additional factors such as socially determined behav- ioural interactions, differential contact rates with ectoparasites and condition-dependent susceptibility and expression of virulence are likely to influence disease 0020-7519/$30.00 Ó 2006 Australian Society for Parasitology Inc. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.ijpara.2006.06.014 * Corresponding author. Tel.: +61 8 9937 1318; fax: +61 8 9937 1455. E-mail address: andy23x@gmail.com (A. Smith). www.elsevier.com/locate/ijpara International Journal for Parasitology 36 (2006) 1359–1366