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Tsetse blood-meal sources, endosymbionts and trypanosome-associations in the Maasai Mara National Reserve, a wildlife-human-livestock interface.

ABSTRACT: 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.

SUBMITTER: Makhulu EE

PROVIDER: S-EPMC7822626 | biostudies-literature | 2021 Jan

REPOSITORIES: biostudies-literature

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Tsetse blood-meal sources, endosymbionts and trypanosome-associations in the Maasai Mara National Reserve, a wildlife-human-livestock interface.

Makhulu Edward Edmond EE Villinger Jandouwe J Adunga Vincent Owino VO Jeneby Maamun M MM Kimathi Edwin Murungi EM Mararo Enock E Oundo Joseph Wang'ang'a JW Musa Ali Abdulahi AA Wambua Lillian L

PLoS neglected tropical diseases 20210106 1

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 fro ...[more]

PMID: 33406097

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Project description:The role of questing ticks in the epidemiology of tick-borne diseases in Kenya's Maasai Mara National Reserve (MMNR), an ecosystem with intensified human-wildlife-livestock interactions, remains poorly understood. We surveyed the diversity of questing ticks, their blood-meal hosts, and tick-borne pathogens to understand potential effects on human and livestock health. By flagging and hand-picking from vegetation in 25 localities, we collected 1,465 host-seeking ticks, mostly Rhipicephalus and Amblyomma species identified by morphology and molecular analysis. We used PCR with high-resolution melting (HRM) analysis and sequencing to identify Anaplasma, Babesia, Coxiella, Ehrlichia, Rickettsia, and Theileria pathogens and blood-meal remnants in 231 tick pools. We detected blood-meals from humans, wildebeest, and African buffalo in Rh. appendiculatus, goat in Rh. evertsi, sheep in Am. gemma, and cattle in Am. variegatum. Rickettsia africae was detected in Am. gemma (MIR = 3.10) that had fed on sheep and in Am. variegatum (MIR = 250) that had fed on cattle. We found Rickettsia spp. in Am. gemma (MIR = 9.29) and Rh. evertsi (MIR = 200), Anaplasma ovis in Rh. appendiculatus (MIR = 0.89) and Rh. evertsi (MIR = 200), Anaplasma bovis in Rh. appendiculatus (MIR = 0.89), and Theileria parva in Rh. appendiculatus (MIR = 24). No Babesia, Ehrlichia, or Coxiella pathogens were detected. Unexpectedly, species-specific Coxiella sp. endosymbionts were detected in all tick genera (174/231 pools), which may affect tick physiology and vector competence. These findings show that ticks from the MMNR are infected with zoonotic R. africae and unclassified Rickettsia spp., demonstrating risk of African tick-bite fever and other spotted-fever group rickettsioses to locals and visitors. The protozoan pathogens identified may also pose risk to livestock production. The diverse vertebrate blood-meals of questing ticks in this ecosystem including humans, wildlife, and domestic animals, may amplify transmission of tick-borne zoonoses and livestock diseases.

Project description:Traditional plant use is of tremendous importance in many societies, including most rural African communities. This knowledge is however, rapidly dwindling due to changes towards a more Western lifestyle, and the influence of modern tourism.In case of the Sekenani Maasai, the recent change from a nomadic to a more sedentary lifestyle has not, thus far lead to a dramatic loss of traditional plant knowledge, when compared to other Maasai communities. However, in Sekenani, plants are used much less frequently for manufacturing tools, and for veterinary purposes, than in more remote areas. While the knowledge is still present, overgrazing and over-exploitation of plant resources have already led to a decline of the plant material available.This paper examines the plant use of the Maasai in the Sekenani Valley, North of the Masaai Mara National Reserve. The Maasai pastoralists of Kenya and Tanzania use a large part of the plants in their environment for many uses in daily life. The plant use and knowledge of the Sekenani Maasai is of particular interest, as their clan, the "Il-Purko", was moved from Central Kenya to this region by the British Colonial Administration in 1904.The results of this study indicate that despite their relocation 100 years ago, the local population has an extensive knowledge of the plants in their surroundings, and they ascribe uses to a large percentage of the plants found. One-hundred-fifty-five plant species were collected, identified and their Maa names and traditional uses recorded. Although fifty-one species were reported as of "no use", only eighteen of these had no Maasai name. Thirty-three were recognized by a distinctive Maa name. Thirty-nine species had a medicinal use, and 30 species served as fodder for livestock. Six species could not be identified. Of these plants five were addressed by the Maasai with distinct names. This exemplifies the Sekenani Maasai's in-depth knowledge of the plant resources.Traditionally, the Maasai attribute most illnesses to the effect of pollutants that block or inhibit digestion. These pollutants can include "polluted" food, contact with sick people and witchcraft. In most cases the treatment of illness involves herbal purgatives to cleanse the patient. There are also frequent indications of plant use for common problems like wounds, parasites, body aches and burns.

Project description:BackgroundChanges of land cover modify the characteristics of habitat, host-vector interaction and consequently infection rates of disease causing agents. In this paper, we report variations in tsetse distribution patterns, abundance and infection rates in relation to habitat types and age in the Maasai Steppe of northern Tanzania. In Africa, Tsetse-transmitted trypanosomiasis negatively impacted human life where about 40 million people are at risk of contracting the disease with dramatic socio-economical consequences, for instance, loss of livestock, animal productivity, and manpower.MethodsWe trapped tsetse flies in dry and wet seasons between October 2014 and May 2015 in selected habitats across four villages: Emboreet, Loiborsireet, Kimotorok and Oltukai adjacent to protected areas. Data collected include number and species of tsetse flies caught in baited traps, PCR identification of trypanosome species and extraction of monitored Normalized Difference Vegetation Index (NDVI) data from Moderate Resolution Imaging Spectrometer (MODIS).ResultsOur findings demonstrate the variation of tsetse fly species abundance and infection rates among habitats in surveyed villages in relation to NDVI and host abundance. Results have shown higher tsetse fly abundance in Acacia-swampy ecotone and riverine habitats for Emboreet and other villages, respectively. Tsetse abundance was inconsistent among habitats in different villages. Emboreet was highly infested with Glossina swynnertoni (68%) in ecotone and swampy habitats followed by G. morsitans (28%) and G. pallidipes (4%) in riverine habitat. In the remaining villages, the dominant tsetse fly species by 95% was G. pallidipes in all habitats. Trypanosoma vivax was the most prevalent species in all infected flies (95%) with few observations of co-infections (with T. congolense or T. brucei).ConclusionsThe findings of this study provide a framework to mapping hotspots of tsetse infestation and trypanosomiasis infection and enhance the communities to plan for effective control of trypanosomiasis.

Project description:BackgroundGlossina (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.MethodsA 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.ResultsA 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).ConclusionsThe 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.

Dataset Information

Tsetse blood-meal sources, endosymbionts and trypanosome-associations in the Maasai Mara National Reserve, a wildlife-human-livestock interface.

Publications

Tsetse blood-meal sources, endosymbionts and trypanosome-associations in the Maasai Mara National Reserve, a wildlife-human-livestock interface.

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