Feeding behaviour of tsetse flies infected with salivarian trypanosomes

Abstract

Although much is known about factors which determine infection rates of salivarian trypanosomes (subgenera Nannomonas, Duttonella and Tryanozoon) in the tsetse fly Glossina, it is not clear why infection rates of Trypanozoon are high in mammalian hosts but low in wild-caught Glossina and why trypanosomiasis occurs where Glossina is not readily detectable. We report here that the feeding behaviour of trypanosome-infected Glossina differed from that of uninfected control flies. Infected flies probed more frequently and fed more voraciously. We describe a specific relationship between trypanosomes and the mechanoreceptors responsible for detecting the rate of blood flow, and show how infection affects that rate in the labrum. We suggest that the observed differences in feeding behaviour result from impaired function of the labral mechanoreceptors in infected Glossina.

The malaria parasite, Plasmodium falciparum, increases the frequency of multiple feeding of its mosquito vector, Anopheles gambiae

“…The plague bacterium Yersinia pestis, transmitted by the tropical rat £ea Xenopsylla cheopis, blocks the proventriculus of the £ea and causes regurgitation when the £ea is blood feeding (Bacot & Martin 1914). Trypanosomes can a¡ect the mechanoreceptive sensilla of their tsetse £y hosts, so that infected £ies probe more frequently than uninfected £ies (Jenni et al 1980;Roberts 1981). As parasites are frequently transmitted during probing, transmission is likely to be increased.…”

Parasitogenic alterations of vector behaviour

“…Whereas in some investigations infected flies probed three times more often than non-infected flies and needed more time for blood ingestion (e.g. Jenni et al, 1980), these effects could not be observed in other investigations (Makumi and Moloo, 1991). Strong effects have been observed in another trypanosomatid group, the Leishmania.…”

“…Some salivarian trypanosomatids develop carpets of flagellates in the foregut. Since the capacity of the cibarial pump cannot be increased indefinitely, this might reduce the blood speed (Jenni et al, 1980). Much stronger reductions of the diameter are known for Leishmania-infected phlebotomines and Yersinia pestis-infected rat fleas.…”

“…Some of them remain and multiply in the anterior region of the gut and are transmitted to the next host during probing or through regurgitation. Examples are the aetiologic agents of plague, the bacterium Y. pestis, in the flea and T. vivax in tsetse flies (Holdenried, 1952;Bibikova, 1977;Jenni et al, 1980). Leishmania are also transmitted in this way by sandflies, but after ingestion they first multiply in the abdominal midgut and attach by their flagella to the microvillar border, followed by a forward migration to the thoracic midgut and in some cases to the foregut, including pharynx, cibarium, and proboscis (Pimenta et al, 1992;Ilg et al, 1999;Sacks, 2001).…”

Host–parasite molecular cross-talk during the manipulative process of a host by its parasite

“…In tsetse-fly-trypanosome associations, many studies have now demonstrated that infected flies increase the probing rate and feed more voraciously than uninfected flies (e.g. Hurd, 2003;Jenni et al, 1980;Lefèvre and Thomas, 2008;Molyneux and Jefferies, 1986;Roberts, 1981). Two parasito-proteomics studies were done on two insect-vector-parasite associations to improve understanding of the proximate cause(s) leading to the alteration of the insect vector behaviour: (1) the mosquito Anopheles gambiae Giles (Diptera, Culicidae) parasitized by a malaria parasite, Plasmodium berghei (Haemosporida, Plasmodiidae) (Lefèvre et al, 2007a), and (2) the tsetse fly Glossina palpalis gambiensis (Vanderplank) (Diptera, Glossinidae), parasitized by the sleeping sickness parasite, Trypanosoma brucei brucei (Kinetoplastida, Trypanosomatidae) (Lefèvre et al, 2007b).…”