Is there safety in numbers? The effect of cattle herding on biting risk from tsetse flies

In sub-Saharan Africa, tsetse (Glossina spp.) transmit species of Trypanosoma which threaten 45-50 million cattle with trypanosomiasis. These livestock are subject to various herding practices which may affect biting rates on individual cattle and hence the probability of infection. In Zimbabwe, studies were made of the effect of herd size and composition on individual biting rates by capturing tsetse as they approached and departed from groups of one to 12 cattle. Flies were captured using a ring of electrocuting nets and bloodmeals were analysed using DNA markers to identify which individual cattle were bitten. Increasing the size of a herd from one to 12 adults increased the mean number of tsetse visiting the herd four-fold and the mean feeding probability from 54% to 71%; the increased probability with larger herds was probably a result of fewer flies per host, which, in turn, reduced the hosts' defensive behaviour. For adults and juveniles in groups of four to eight cattle, > 89% of bloodmeals were from the adults, even when these comprised just 13% of the herd. For groups comprising two oxen, four cows/heifers and two calves, a grouping that reflects the typical composition of communal herds in Zimbabwe, approximately 80% of bloodmeals were from the oxen. Simple models of entomological inoculation rates suggest that cattle herding practices may reduce individual trypanosomiasis risk by up to 90%. These results have several epidemiological and practical implications. First, the gregarious nature of hosts needs to be considered in estimating entomological inoculation rates. Secondly, heterogeneities in biting rates on different cattle may help to explain why disease prevalence is frequently lower in younger/smaller cattle. Thirdly, the cost and effectiveness of tsetse control using insecticide-treated cattle may be improved by treating older/larger hosts within a herd. In general, the patterns observed with tsetse appear to apply to other genera of cattle-feeding Diptera (Stomoxys, Anopheles, Tabanidae) and thus may be important for the development of strategies for controlling other diseases affecting livestock.     

Juvenile hormone mimics as effective sterilants for the tsetse fly Glossina morsitans morsitans

The development of puparia of Glossina morsitans morsitans Westwood was disrupted by topical applications of the juvenile hormone mimics S-methoprene (the resolved enantiomer of 11-methoxy-3,7,11-trimethyl-2,4-dodecadienoic acid 1-methyl ester) (Zoecon), S21149 (propionaldoxime-0-4-phenoxyphenoxyethylether) (Sumitomo), or S31183 (2-[1-methyl-2-(4-phenoxyphenoxy)ethoxy]pyridine) (Sumitomo) dissolved in acetone. Puparia so treated during the first 4 days of life suffered developmental abnormalities, the severity of which were dose-dependent. Similarly, puparia produced by adult females treated with these compounds were abnormal. Dose-response data showed that effects were greatest with S31183 and least with S-methoprene. Abnormalities in the form of abdominal lesions and wing crumpling were typical of flies emerging from puparia produced by S-methoprene-treated females. However, arrested development at the red eye and pigmented seta stage within the puparium were typical of offspring of females treated with S21149 and S31183. A dose of 2 micrograms per female of S31183 was sufficient to prevent emergence of offspring produced for the rest of the life of the fly. The same dose resulted in partial recovery of females treated with S21149 some 18 days following treatment. Treatment with 2 micrograms S-methoprene did not suppress completely the production of normal offspring and recovery was complete some 27-35 days after treatment. Exposure of males to 20 micrograms S31183 did not impair their ability to inseminate females; transfer of material during copulation was sufficient to prevent the production of viable offspring by their mates.(ABSTRACT TRUNCATED AT 250 WORDS)     

Multiple host feeding in Glossina palpalis gambiensis and Glossina tachinoides in southeast Mali

Changes in agricultural practices and the resulting extinction of wildlife have led to the reduction or disappearance of savannah tsetse species. Riparian tsetse such as Glossina palpalis gambiensis Vanderplank 1949 and Glossina tachinoides Westwood 1850 (Diptera: Glossinidae) continue to persist in peridomestic sites, transmitting trypanosomiasis. At present, little is known about interspecies differences in feeding behaviour in these two species in southeast Mali, or of the phenomenon of multiple bloodmeals. To study these topics, 279 samples of G. p. gambiensis and G. tachinoides containing host DNA, caught in the Sikasso region between November 2008 and April 2009, were analysed by applying host species‐specific primers and sequencing. Human accounted for > 66% of G. p. gambiensis bloodmeals, whereas G. tachinoides contained in equal parts DNA of human, cattle or both, showing a significantly higher proportion of multiple host use. Further, the trypanosome infection rate was found to be three‐fold higher in G. tachinoides. Logistic regression analysis revealed double‐feeding and infection to be independent of one another, but showed infection to be correlated with engorgement in G. p. gambiensis and female sex in G. tachinoides. Enhanced host‐seeking activities paired with the high trypanosome infection rate found in G. tachinoides would indicate that this species has a higher vectorial capacity than G. p. gambiensis.     

Tsetse: the limits to population growth

Growth rates of tsetse populations were estimated by calculating the dominant eigenvalues of appropriate Leslie matrices. The individual effects of four variables (pre-adult and adult survival probability, interlarval period and pupal duration), have been investigated by varying each one over a wide range of values, while the other three are held constant. R, the log of the growth rate, was found to vary approximately linearly with adult and pre-adult death rate; a 1% change in the adult death rate causes approximately a 10-fold change in R. R varies linearly with the log of fecundity and of the pupal duration. An increase in the pupal duration results in a decrease in the growth rate for populations which have a positive growth rate, but an increase for populations which have a negative growth rate. For a population at equilibrium, a change in the pupal duration has no effect. Small changes in fecundity have less effect on the growth rate than small changes in the death rate; this fact is advanced as an important contributor to the generally very cautious nature of female tsetse, and their aversion to man, particularly as a potential host. A simple linear model is described which relates R to all four variables and their first order interactions. The model is used to produce a set of graphs which encapsulate the relationship between the growth rate and the vital parameters over a wide range of values. It is also used to draw the loci on one side of which tsetse populations grow, and on the other of which they decline. Population resilience is discussed in relation to the problem of tsetse eradication; it is concluded that if one can impose and sustain an added mortality of 4% per day on any female tsetse population then it must go extinct, regardless of the strength of the density dependent processes; and it seems likely that in most field conditions only an added 2-3% is required. It is pointed out that ground and aerial spraying techniques produce much higher daily mortalities than this, but they may often not be sustained for sufficiently long to achieve eradication. When odour-baited targets are used the increased death rate is much smaller, but it can be sustained as required; recent work in Zimbabwe shows that there is a good correspondence between the calculated imposed death rate and the observed rate of decline of tsetse populations.     

Activity of the diastereoisomers of 13,23-dimethylpenta-triacontane, the sex pheromone of Glossina pallidipes, and comparison with the natural pheromone

ABSTRACT. All three synthetic diastereoisomers of 13,23-dimethyl-pentatriacontane, the pheromone of Glossina pallidipes (Austen), have been tested in the G. pallidipes sex pheromone bioassay, together with one of the four diastereoisomers of 13,17-dimethylpentatriacontane, originally proposed as a candidate pheromone of G. pallidipes. Of the three isomers of 13,23-dimethylpentatriacontane only the (13R,23S) isomer was active with an ED-50 of 4.47±1.09/μg (mean±SD). The (13R,17R)-13,17-dimethylpentatriacontane was inactive. The diastereo-isomeric mixtures of 13,17- and 13,23-dimethylpentatriacontane were active with ED-50 values of 17.88±1.25/μg and 8.88±1.15μg respectively. The natural pheromone was active with an ED-50 of 8.07±1.17 μg indicating it to be a diastereoisomeric mixture.     

Cuticular lipid mass and desiccation rates in Glossina pallidipes: interpopulation variation

Abstract.  Tsetse flies, Glossina pallidipes (Diptera: Glossinidae) are said to have strong dispersal tendencies. Gene flow among these populations is estimated to be the theoretical equivalent of no more than one or two reproducing flies per generation, thereby raising the hypothesis of local regimes of natural selection. Flies were sampled from four environmentally diverse locations in Kenya to determine whether populations are homogeneous in desiccation tolerance and cuticular lipids. Cuticular hydrocarbon fractions known to act as sex pheromones do not differ among populations, thereby eliminating sexual selection as an isolating mechanism. Cuticular lipid quantities vary among populations and are not correlated with prevailing temperatures, humidities, and normalized density vegetation indices. Females demonstrate a stronger correlation than males between cuticular lipid mass and body weight. Desiccation rates also vary among populations, but are not correlated with the amounts of cuticular lipid. Chemical analysis of cuticular hydrocarbons by gas chromatography–mass spectroscopy shows that one of the four populations has more 11,15- and 11,21-dimethyl-31 hydrocarbon on females. These results are discussed in the context of population differences and estimates of gene flow.     

Glossina fusca group tsetse as vectors of cattle trypanosomiasis in Gabon and Zaire

1. The significance of Glossina fusca group tsetse flies as vectors of cattle trypanosomiasis was examined using biconical traps to survey tsetse populations at one site in Gabon and two sites in Zaire. 2. Mean trypanosome infection rates in G.tabaniformis Westwood over the study period ranged from a minimum of 8.9% at one site to a maximum of 17.7% at another. The mean infection rate in G.nashi Potts was 6.0%. 3. Up to 49% of bloodmeals of G.tabaniformis were from cattle. Trypanosome prevalence in cattle where G.tabaniformis appeared to be the main vector was 9.5% and 5.4% at the Mushie and OGAPROV ranches, respectively. 4. A highly significant positive correlation was found between tsetse challenge and trypanosome prevalence in N'Dama cattle across sites. Tsetse challenge was defined as the product of tsetse relative densities, trypanosome infection rates in the flies and the proportion of feeds taken by them from cattle. Thus, G.tabaniformis can be an important vector of pathogenic Trypanosoma species in cattle.     

Evidence for a discrete evolutionary lineage within Equatorial Guinea suggests that the tsetse fly Glossina palpalis palpalis exists as a species complex

Tsetse flies of the palpalis group are major vectors of Human African Trypanosomiasis in Africa. Accurate knowledge of species identity is essential for vector control. Here, we combine ribosomal internal transcribed spacer 1 ( ITS1 ), mitochondrial Cytochrome Oxidase 1 ( COI ) and microsatellites to determine the population structure and phylogenetic relations of Glossina p. palpalis in Equatorial Guinea. CO1 sequence data suggest that G. p. palpalis in Equatorial Guinea is a distinct subspecies from previously described G. p. palpalis in West Africa and Democratic Republic of Congo. Glossina p. palpalis in Equatorial Guinea and DRC share a common ancestor which diverged from West African G. p. palpalis around 1.9 Ma. Previous ITS1 length polymorphism data suggested the possible presence of hybrids in Equatorial Guinea. However, ITS1 showed incomplete lineage sorting compared with clearly defined COI groups, and data from 12 unlinked microsatellites provided no evidence of hybridization. Microsatellite data indicated moderate but significant differentiation between the populations analysed (Rio Campo, Mbini and Kogo). Moreover, unlike previous studies of G. p. palpalis , there was no evidence for heterozygote deficiency, presence of migrants or cryptic population structure. Variance effective population size at Rio Campo was estimated at 501–731 assuming eight generations per year. This study of the population genetics of G. p. palpalis in central Africa provides the first estimate of genetic differentiation between geographically separated G. p. palpalis populations.     

The effect of starvation on the susceptibility of teneral and non-teneral tsetse flies to trypanosome infection

Transmission of vector-borne diseases depends largely on the ability of the insect vector to become infected with the parasite. In tsetse flies, newly emerged or teneral flies are considered the most likely to develop a mature, infective trypanosome infection. This was confirmed during experimental infections where laboratory-reared Glossina morsitans morsitans Westwood (Diptera: Glossinidae) were infected with Trypanosoma congolense or T. brucei brucei. The ability of mature adult tsetse flies to become infected with trypanosomes was significantly lower than that of newly emerged flies for both parasites. However, the nutritional status of the tsetse at the time of the infective bloodmeal affected its ability to acquire either a T. congolense or T. b. brucei infection. Indeed, an extreme period of starvation (3-4 days for teneral flies, 7 days for adult flies) lowers the developmental barrier for a trypanosome infection, especially at the midgut level of the tsetse fly. Adult G. m. morsitans became at least as susceptible as newly emerged flies to infection with T. congolense. Moreover, the susceptibility of adult flies, starved for 7 days, to an infection with T. b. brucei was also significantly increased, but only at the level of maturation of an established midgut infection to a salivary gland infection. The outcome of these experimental infections clearly suggests that, under natural conditions, nutritional stress in adult tsetse flies could contribute substantially to the epidemiology of tsetse-transmitted trypanosomiasis.     

Polymorphic microsatellite markers for the tsetse fly Glossina fuscipes fuscipes (Diptera: Glossinidae), a vector of human African trypanosomiasis

Our understanding of Glossina fuscipes fuscipes, a major vector of sleeping sickness, has been severely constrained by a lack of genetic markers for mapping and population genetic studies. Here we present 10 newly developed microsatellite loci for this tsetse species. Heterozygosity levels in Moyo, an Ugandan population, averaged 0.57, with only two loci showing very low heterozygosity. Five loci carried more than six alleles. Together with five recently published microsatellite loci, this brings the number of available microsatellite loci for this species to 15. Their availability will greatly facilitate future studies on the genetics of this important human disease vector.