scholarly journals Blood meal analysis of tsetse flies (Glossina pallidipes: Glossinidae) reveals a reduction in host fidelity when feeding on domestic compared to wild hosts

2019 ◽  
Author(s):  
Manun Channumsin ◽  
Marc Ciosi ◽  
Dan Masiga ◽  
Harriet Auty ◽  
C. Michael Turner ◽  
...  

AbstractBackgroundBoth male and female tsetse flies, haematophagous insects, transmit trypanosomes between hosts and are the cyclical vectors for Human African Trypanosomiasis (HAT) and Animal African Trypanosomiasis (AAT). Trypanosomes responsible for AAT can be transmitted by tsetse between wild animals and livestock. However, the degree of connectivity between the sylvatic and domestic cycles is unknown. The objectives of this study were to investigate patterns of host feeding in relationship to trypanosome prevalence among Kenyan populations of G. pallidipes at the livestock-wildlife interface.Methodology/Principal FindingsSources of blood meals of Glossina pallidipes were identified by polymerase chain reaction amplification and sequencing of the mitochondrial cytochrome b gene and compared with previous characterization of trypanosome prevalence from the same flies. In the Nguruman region in southern Kenya, the majority (98%) of the 148 flies for which dominant hosts could be resolved fed on single host species and only a single fly had fed on a domestic host; intriguingly this was the only fly confirmed to have fed on cattle. In contrast, in the Shimba Hills region (South Coast), multiple host feeding was more common: 42% inside a fenced wildlife protected area, where 35% of dominant hosts were domestic animals or humans, compared with 62% from traps set along the border to an adjacent village, which was dominated by domestic hosts (77%). Across sites, 44% of flies tested positive for trypanosomes (28/50 domestic hosts; 78/193 wild hosts). Multiple Correspondence Analysis revealed strong correlations between feeding pattern, host type and site but these were resolved along a different dimension than trypanosome status.Conclusions/SignificanceOur results suggest that host fidelity when feeding on wild hosts in G. pallidipes could reduce risk of transmission of trypanosomes to domestic hosts in interface areas and emphasise the importance of considering vector behaviour when designing management interventions.Author SummaryTsetse flies are the main vectors transmitting trypanosomes, which cause disease in both humans and animals. Since tsetse flies feed on a wide range of vertebrate hosts, there is the potential for transmission between wild and domestic animals in regions where their ranges overlap. In this study, we used molecular methods to determine the hosts fed on by tsetse flies sampled from three sites in Kenya at the wildlife-livestock interface. In areas where wildlife dominated, tsetse tended to feed on single host species, whereas in areas with more domesticated animals, they tended to feed on multiple hosts. These results suggest either that tsetse flies get interrupted more while feeding on domestic hosts or that they prefer to feed on wildlife and so switch hosts more often when feeding on less desirable hosts. Using data from a previous study on the same samples, we found that trypanosome prevalence was not correlated with the type or number of hosts fed on. These results have important implications for understanding the risk of transmission between wildlife and livestock in regions bordering protected areas but the high host fidelity for wild hosts suggests that tsetse feeding preferences could reduce risks of disease transmission to livestock.

2021 ◽  
Vol 6 ◽  
pp. 213
Author(s):  
Manun Channumsin ◽  
Marc Ciosi ◽  
Dan Masiga ◽  
Harriet Auty ◽  
C. Michael Turner ◽  
...  

Background: Changes in climate and land use can alter risk of transmission of parasites between domestic hosts and wildlife, particularly when mediated by vectors that can travel between populations. Here we focused on tsetse flies (genus Glossina), the cyclical vectors for both Human African Trypanosomiasis (HAT) and Animal African Trypanosomiasis (AAT). The aims of this study were to investigate three issues related to G. palldipes from Kenya: 1) the diversity of vertebrate hosts that flies fed on; 2) whether host feeding patterns varied in relation to type of hosts, tsetse feeding behaviour, site or tsetse age and sex; and 3) if there was a relationship between trypanosome detection and host feeding behaviours or host types. Methods: Sources of blood meals of Glossina pallidipes were identified by sequencing of the mitochondrial cytochrome b gene and analyzed in relationship with previously determined trypanosome detection in the same flies. Results: In an area dominated by wildlife but with seasonal presence of livestock (Nguruman), 98% of tsetse fed on single wild host species, whereas in an area including a mixture of resident domesticated animals, humans and wildlife (Shimba Hills), 52% of flies fed on more than one host species. Multiple Correspondence Analysis revealed strong correlations between feeding pattern, host type and site but these were resolved along a different dimension than trypanosome status, sex and age of the flies. Conclusions: Our results suggest that individual G. pallidipes in interface areas may show higher feeding success on wild hosts when available but often feed on both wild and domesticated hosts. This illustrates the importance of G. pallidipes as a vector connecting the sylvatic and domestic cycles of African trypanosomes.


2021 ◽  
Vol 15 (1) ◽  
pp. e0008267
Author(s):  
Edward Edmond Makhulu ◽  
Jandouwe Villinger ◽  
Vincent Owino Adunga ◽  
Maamun M. Jeneby ◽  
Edwin Murungi Kimathi ◽  
...  

African trypanosomiasis (AT) is a neglected disease of both humans and animals caused by Trypanosoma parasites, which are transmitted by obligate hematophagous tsetse flies (Glossina spp.). Knowledge on tsetse fly vertebrate hosts and the influence of tsetse endosymbionts on trypanosome presence, especially in wildlife-human-livestock interfaces, is limited. We identified tsetse species, their blood-meal sources, and correlations between endosymbionts and trypanosome presence in tsetse flies from the trypanosome-endemic Maasai Mara National Reserve (MMNR) in Kenya. Among 1167 tsetse flies (1136 Glossina pallidipes, 31 Glossina swynnertoni) collected from 10 sampling sites, 28 (2.4%) were positive by PCR for trypanosome DNA, most (17/28) being of Trypanosoma vivax species. Blood-meal analyses based on high-resolution melting analysis of vertebrate cytochrome c oxidase 1 and cytochrome b gene PCR products (n = 354) identified humans as the most common vertebrate host (37%), followed by hippopotamus (29.1%), African buffalo (26.3%), elephant (3.39%), and giraffe (0.84%). Flies positive for trypanosome DNA had fed on hippopotamus and buffalo. Tsetse flies were more likely to be positive for trypanosomes if they had the Sodalis glossinidius endosymbiont (P = 0.0002). These findings point to complex interactions of tsetse flies with trypanosomes, endosymbionts, and diverse vertebrate hosts in wildlife ecosystems such as in the MMNR, which should be considered in control programs. These interactions may contribute to the maintenance of tsetse populations and/or persistent circulation of African trypanosomes. Although the African buffalo is a key reservoir of AT, the higher proportion of hippopotamus blood-meals in flies with trypanosome DNA indicates that other wildlife species may be important in AT transmission. No trypanosomes associated with human disease were identified, but the high proportion of human blood-meals identified are indicative of human African trypanosomiasis risk. Our results add to existing data suggesting that Sodalis endosymbionts are associated with increased trypanosome presence in tsetse flies.


Author(s):  
Merid N. Getahun ◽  
Jandouwe Villinger ◽  
Joel L. Bargul ◽  
Abel Orone ◽  
John Ngiela ◽  
...  

AbstractBackgroundAfrican animal trypanosomosis is becoming prevalent beyond its traditionally defined geographical boundaries and is a threat to animals beyond the tsetse belts in and outside Africa. However, knowledge of infections with clinically important trypanosome species and their diversity among field-collected hematophagous biting flies and domestic animals is limited mainly to tsetse and their mammalian hosts in tsetse-infested areas. This study aimed to examine the presence of trypanosomes in both biting flies and domestic animals outside the tsetse belt in northern Kenya, potential mechanical vector species, and their host-feeding profiles.MethodsWe screened for pathogenic African trypanosomes in blood samples from domestic animals and field-trapped flies by microscopy and sequencing of internal transcribed spacer (ITS1) gene PCR products. We sequenced kinetoplast maxicircle genes to confirm Trypanosoma brucei detection and the RoTat 1.2 and kinetoplast minicircle genes to differentiate type-A and type-B Trypanosoma evansi, respectively. Further, we identified the hosts that field-trapped flies fed on by PCR-HRM and sequencing of 16S rRNA genes.ResultsHippobosca camelina, Stomoxys calcitrans, Tabanus spp., and Pangonia rueppellii are potential vectors of trypanosomes outside the tsetse belt in Marsabit County, northern Kenya. We identified Trypanosoma spp., including Trypanosoma vivax, T. evansi, T. brucei, and T. congolense in these biting flies as well as in camels (Camelus dromedarius). Trypanosomes detected varied from single up to three trypanosome species in H. camelina and camels in areas where no tsetse flies were trapped. Similar trypanosomes were detected in Glossina pallidipes collected from a tsetse-infested area in Shimba Hills, coastal Kenya, showing the wide geographic distribution of trypanosomes. Furthermore, we show that these biting flies acquired blood meals from camels, cattle, goats, and sheep. Phylogenetic analysis revealed diverse Trypanosoma spp. associated with variations in virulence and epidemiology in camels, which suggests that camel trypanosomosis may be due to mixed trypanosome infections rather than only surra (T. evansi), as previously thought.


2019 ◽  
Author(s):  
Lucas J. Cunningham ◽  
Jessica K. Lingley ◽  
Iñaki Tirados ◽  
Johan Esterhuizen ◽  
Mercy A. Opiyo ◽  
...  

AbstractBackgroundLarge-scale control of sleeping sickness has led to a decline in the number of cases of Gambian human African trypanosomiasis (g-HAT) to <2000/year. However, achieving complete and lasting interruption of transmission may be difficult because animals may act as reservoir hosts for T. b. gambiense. Our study aims to update our understanding of T. b. gambiense in local vectors and domestic animals of N.W. Uganda.MethodsWe collected blood from 2896 cattle and 400 pigs and In addition, 6664 tsetse underwent microscopical examination for the presence of trypanosomes. Trypanosoma species were identified in tsetse from a subsample of 2184 using PCR. Primers specific for T. brucei s.l. and for T. brucei sub-species were used to screen cattle, pig and tsetse samples.ResultsIn total, 39/2,088 (1.9%; 95% CI=1.9-2.5) cattle, 25/400 (6.3%; 95% CI=4.1-9.1) pigs and 40/2,184 (1.8%; 95% CI=1.3-2.5) tsetse, were positive for T. brucei s.l.. Of these samples 24 cattle (61.5%), 15 pig (60%) and 25 tsetse (62.5%) samples had sufficient DNA to be screened using the T. brucei sub-species PCR. Further analysis found no cattle or pigs positive for T. b. gambiense, however, 17/40 of the tsetse samples produced a band suggestive of T. b. gambiense. When three of these 17 PCR products were sequenced the sequences were markedly different to T. b. gambiense, indicating that these flies were not infected with T. b. gambiense.ConclusionThe absence of T. b. gambiense in cattle, pigs and tsetse accords with the low prevalence of g-HAT in the human population. We found no evidence that livestock are acting as reservoir hosts. However, this study highlights the limitations of current methods of detecting and identifying T. b. gambiense which relies on a single copy-gene to discriminate between the different sub-species of T. brucei s.l.Author SummaryThe decline of annual cases of West-African sleeping sickness in Uganda raises the prospect that elimination of the disease is achievable for the country. However, with the decrease in incidence and the likely subsequent change in priorities there is a need to confirm that the disease is truly eliminated. One unanswered question is the role that domestic animals play in maintaining transmission of the disease. The potential of cryptic-animal reservoirs is a serious threat to successful and sustained elimination of the disease. It is with the intent of resolving this question that we have carried out this study whereby we examined 2088 cattle, 400 pigs and 2184 tsetse for Trypanosoma brucei gambiense, the parasite responsible for the disease. Our study found T. brucei s.l. in local cattle, pigs and tsetse flies, with their respective prevalences as follows, 1.9%, 6.3% and 1.8%. Further analysis to establish identity of these positives to the sub-species level found that no cattle, pigs or tsetse were carrying the pathogen responsible for Gambian sleeping sickness. Our work highlights the difficulty of establishing the absence of a disease, especially in an extremely low endemic setting, and the limitations of some of the most commonly used methods.


2020 ◽  
Vol 14 (12) ◽  
pp. e0008867
Author(s):  
José Guillermo Estrada-Franco ◽  
Nadia A. Fernández-Santos ◽  
Adeniran A. Adebiyi ◽  
María de J. López-López ◽  
Jesús A. Aguilar-Durán ◽  
...  

Background Aedes aegypti mosquito-borne viruses including Zika (ZIKV), dengue (DENV), yellow fever (YFV), and chikungunya (CHIKV) have emerged and re-emerged globally, resulting in an elevated burden of human disease. Aedes aegypti is found worldwide in tropical, sub-tropical, and temperate areas. The characterization of mosquito blood meals is essential to understand the transmission dynamics of mosquito-vectored pathogens. Methodology/principal findings Here, we report Ae. aegypti and Culex quinquefasciatus host feeding patterns and arbovirus transmission in Northern Mexico using a metabarcoding-like approach with next-generation deep sequencing technology. A total of 145 Ae. aegypti yielded a blood meal analysis result with 107 (73.8%) for a single vertebrate species and 38 (26.2%) for two or more. Among the single host blood meals for Ae. aegypti, 28.0% were from humans, 54.2% from dogs, 16.8% from cats, and 1.0% from tortoises. Among those with more than one species present, 65.9% were from humans and dogs. For Cx. quinquefasciatus, 388 individuals yielded information with 326 (84%) being from a single host and 63 (16.2%) being from two or more hosts. Of the single species blood meals, 77.9% were from dogs, 6.1% from chickens, 3.1% from house sparrows, 2.4% from humans, while the remaining 10.5% derived from other 12 host species. Among those which had fed on more than one species, 11% were from dogs and humans, and 89% of other host species combinations. Forage ratio analysis revealed dog as the most over-utilized host by Ae. aegypti (= 4.3) and Cx. quinquefasciatus (= 5.6) and the human blood index at 39% and 4%, respectively. A total of 2,941 host-seeking female Ae. aegypti and 3,536 Cx. quinquefasciatus mosquitoes were collected in the surveyed area. Of these, 118 Ae. aegypti pools and 37 Cx. quinquefasciatus pools were screened for seven arboviruses (ZIKV, DENV 1–4, CHIKV, and West Nile virus (WNV)) using qRT-PCR and none were positive (point prevalence = 0%). The 95%-exact upper limit confidence interval was 0.07% and 0.17% for Ae. aegypti and Cx. quinquefasciatus, respectively Conclusions/significance The low human blood feeding rate in Ae. aegypti, high rate of feeding on mammals by Cx. quinquefasciatus, and the potential risk to transmission dynamics of arboviruses in highly urbanized areas of Northern Mexico is discussed.


2011 ◽  
Vol 77 (23) ◽  
pp. 8400-8408 ◽  
Author(s):  
Rebecca E. Symula ◽  
Ian Marpuri ◽  
Robert D. Bjornson ◽  
Loyce Okedi ◽  
Jon Beadell ◽  
...  

ABSTRACTVertical transmission of obligate symbionts generates a predictable evolutionary history of symbionts that reflects that of their hosts. In insects, evolutionary associations between symbionts and their hosts have been investigated primarily among species, leaving population-level processes largely unknown. In this study, we investigated the tsetse (Diptera: Glossinidae) bacterial symbiont,Wigglesworthia glossinidia, to determine whether observed codiversification of symbiont and tsetse host species extends to a single host species (Glossina fuscipes fuscipes) in Uganda. To explore symbiont genetic variation inG. f. fuscipespopulations, we screened two variable loci (lonandlepA) from theWigglesworthia glossinidiabacterium in the host speciesGlossina fuscipes fuscipes(W. g. fuscipes) and examined phylogeographic and demographic characteristics in multiple host populations. Symbiont genetic variation was apparent within and among populations. We identified two distinct symbiont lineages, in northern and southern Uganda. Incongruence length difference (ILD) tests indicated that the two lineages corresponded exactly to northern and southernG. f. fuscipesmitochondrial DNA (mtDNA) haplogroups (P= 1.0). Analysis of molecular variance (AMOVA) confirmed that most variation was partitioned between the northern and southern lineages defined by host mtDNA (85.44%). However, ILD tests rejected finer-scale congruence within the northern and southern populations (P= 0.009). This incongruence was potentially due to incomplete lineage sorting that resulted in novel combinations of symbiont genetic variants and host background. Identifying these novel combinations may have public health significance, since tsetse is the sole vector of sleeping sickness andWigglesworthiais known to influence host vector competence. Thus, understanding the adaptive value of these host-symbiont combinations may afford opportunities to develop vector control methods.


Author(s):  
Edward Edmond Makhulu ◽  
Jandouwe Villinger ◽  
Vincent Owino Adunga ◽  
Maamun M. Jeneby ◽  
Edwin Murungi Kimathi ◽  
...  

AbstractBackgroundAfrican trypanosomiasis (AT) is a neglected disease of both humans and animals caused by Trypanosoma parasites, which are transmitted by obligate hematophagous tsetse flies (Glossina spp.). Understanding of AT transmission is hampered by limited knowledge on interactions of tsetse flies with their vertebrate hosts and the influence of endosymbionts on vector competence, especially in wildlife-human-livestock interfaces. We identified the tsetse species, their blood-meal sources, and the correlation between endosymbiont and trypanosome infection status in the trypanosome-endemic Maasai Mara National Reserve (MMNR) of Kenya.Methodology/Principal FindingsAmong 1167 tsetse flies (1136 Glossina pallidipes, 31 Glossina swynnertoni) collected from 10 sampling sites, 28 (2.4%) were positive by PCR for trypanosomes, majority (17/28) being Trypanosoma vivax. Blood-meal analyses based on high-resolution melting analysis of mitochondrial cytochrome c oxidase 1 and cytochrome b gene PCR products (n = 345) identified humans as the most common vertebrate host (37%), followed by hippopotamus (29.1%), African buffalo (26.3%), elephant (3.39%), and giraffe (0.84%). Trypanosome-infected flies had fed on hippopotamus and buffalo. Additionally, PCR analysis revealed that tsetse flies were more likely to be infected with trypanosomes if they were infected with the Sodalis glossinidius endosymbiont (P = 0.0022 Fisher’s exact test).Conclusions/SignificanceDiverse species of wildlife hosts may contribute to the maintenance of tsetse populations and/or persistent circulation of African trypanosomes in the MMNR. Although the African buffalo is known to be a key reservoir of AT, the higher proportion of hippopotamus blood-meals in trypanosomes-infected flies identified here indicates that other wildlife species may also be important to transmission cycles. No trypanosomes associated with human disease were identified, but the high proportion of human blood-meals identified are indicative of human African trypanosomiasis transmission risk. Furthermore, this work provides data showing that Sodalis endosymbionts can is associated with increased trypanosome infection rates in endemic ecologies.Author summaryHuman and animal African trypanosomiasis are neglected tropical diseases with potential to spread to new areas. Wild animals are important reservoirs for African trypanosomes and crucial in the emergence and re-emergence of AT. Vertebrate host-vector-parasite interactions are integral to trypanosome transmission. We investigated the vertebrate blood-meals and trypanosomes-endosymbionts co-infections in tsetse flies, which have been associated with reservoirs and vector competence, respectively, on AT transmission in Kenya’s Maasai Mara National Reserve. We identified tsetse fly diversity, trypanosome and endosymbiont infection status, and vertebrate blood-meal hosts to infer potential transmission dynamics. We found that Glossina pallidipes was the major tsetse fly vector and that Trypanosoma vivax was the main trypanosome species circulating in the region. Humans, hippopotamus, and buffalo were the most frequented for blood-meals. Buffalo and hippopotamus blood-meals were identified in trypanosome infected flies. Feeding of the flies on both humans and wildlife may potentiate the risk of the human trypanosomiasis in this ecology. Additionally, we found that the endosymbiont Sodalis glossinidius is associated with higher trypanosome infection rates in wild tsetse flies. These findings emphasize the importance of understanding the interaction of tsetse flies with vertebrate blood-meal sources and their endosymbionts in the transmission and control of AT.


2021 ◽  
Vol 14 (1) ◽  
Author(s):  
Richard S. Gashururu ◽  
Samuel M. Githigia ◽  
Methode N. Gasana ◽  
Richard Habimana ◽  
Ndichu Maingi ◽  
...  

Abstract Background Glossina (tsetse flies) biologically transmit trypanosomes that infect both humans and animals. Knowledge of their distribution patterns is a key element to better understand the transmission dynamics of trypanosomosis. Tsetse distribution in Rwanda has not been well enough documented, and little is known on their current distribution. This study determined the current spatial distribution, abundance, diversity, and seasonal variations of tsetse flies in and around the Akagera National Park. Methods A longitudinal stratified sampling following the seasons was used. Biconical traps were deployed in 55 sites for 6 consecutive days of each study month from May 2018 to June 2019 and emptied every 48 h. Flies were identified using FAO keys, and the number of flies per trap day (FTD) was used to determine the apparent density. Pearson chi-square (χ2) and parametrical tests (t-test and ANOVA) were used to determine the variations between the variables. The significance (p < 0.05) at 95% confidence interval was considered. Logistic regression was used to determine the association between tsetse occurrence and the associated predictors. Results A total of 39,516 tsetse flies were collected, of which 73.4 and 26.6% were from inside Akagera NP and the interface area, respectively. Female flies accounted for 61.3 while 38.7% were males. Two species were identified, i.e. G. pallidipes [n = 29,121, 7.4 flies/trap/day (FTD)] and G. morsitans centralis (n = 10,395; 2.6 FTD). The statistical difference in numbers was significant between the two species (p = 0.000). The flies were more abundant during the wet season (15.8 FTD) than the dry season (4.2 FTD). Large numbers of flies were trapped around the swamp areas (69.1 FTD) inside the park and in Nyagatare District (11.2 FTD) at the interface. Glossina morsitans was 0.218 times less likely to occur outside the park. The chance of co-existing between the two species reduced outside the protected area (0.021 times). Conclusions The occurrence of Glossina seems to be limited to the protected Akagera NP and a narrow band of its surrounding areas. This finding will be crucial to design appropriate control strategies. Glossina pallidipes was found in higher numbers and therefore is conceivably the most important vector of trypanosomosis. Regional coordinated control and regular monitoring of Glossina distribution are recommended. Graphic Abstract


2011 ◽  
Vol 139 (10) ◽  
pp. 1626-1630 ◽  
Author(s):  
E. SERRANO ◽  
P. C. CROSS ◽  
M. BENERIA ◽  
A. FICAPAL ◽  
J. CURIA ◽  
...  

SUMMARYWhen a pathogen infects a number of different hosts, the process of determining the relative importance of each host species to the persistence of the pathogen is often complex. Removal of a host species is a potential but rarely possible way of discovering the importance of that species to the dynamics of the disease. This study presents the results of a 12-year programme aimed at controlling brucellosis in cattle, sheep and goats and the cascading impacts on brucellosis in a sympatric population of red deer (Cervus elaphus) in the Boumort National Game Reserve (BNGR; NE Spain). From February 1998 to December 2009, local veterinary agencies tested over 36 180 individual blood samples from cattle, 296 482 from sheep and goats and 1047 from red deer in the study area. All seropositive livestock were removed annually. From 2006 to 2009 brucellosis was not detected in cattle and in 2009 only one of 97 red deer tested was found to be positive. The surveillance and removal of positive domestic animals coincided with a significant decrease in the prevalence of brucellosis in red deer. Our results suggest that red deer may not be able to maintain brucellosis in this region independently of cattle, sheep or goats, and that continued efforts to control disease in livestock may lead to the eventual eradication of brucellosis in red deer in the area.


2008 ◽  
Vol 8 (4) ◽  
pp. 565-574 ◽  
Author(s):  
Satoru Konnai ◽  
Hirohisa Mekata ◽  
Raadan Odbileg ◽  
Martin Simuunza ◽  
Mwelwa Chembensof ◽  
...  
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