Sharing space between native and invasive small mammals: Study of commensal communities in Senegal.

Urbanization processes are taking place at a very high rate, especially in Africa. At the same time, a number of small mammal species, be they native or invasive, take advantage of human-induced habitat modifications. They represent commensal communities of organisms that cause a number of inconveniences to humans, including potential reservoirs of zoonotic diseases. We studied via live trapping and habitat characterization such commensal small mammal communities in small villages to large cities of Senegal, to try to understand how the species share this particular space. Seven major species were recorded, with exotic invasive house mice (Mus musculus) and black rats (Rattus rattus) dominating in numbers. The shrew Crocidura olivieri appeared as the main and more widespread native species, while native rodent species (Mastomys natalensis, M. erythroleucus, Arvicanthis niloticus and Praomys daltoni) were less abundant and/or more localized. Habitat preferences, compared between species in terms of room types and characteristics, showed differences among house mice, black rats and M. natalensis especially. Niche (habitat component) breadth and overlap were measured. Among invasive species, the house mouse showed a larger niche breadth than the black rat, and overall, all species displayed high overlap values. Co-occurrence patterns were studied at the global and local scales. The latter show cases of aggregation (between the black rat and native species, for instance) and of segregation (as between the house mouse and the black rat in Tambacounda, or between the black rat and M. natalensis in Kédougou). While updating information on commensal small mammal distribution in Senegal, a country submitted to a dynamic process of invasion by the black rat and the house mouse, we bring original information on how species occupy and share the commensal space, and make predictions on the evolution of these communities in a period of ever-accelerating global changes.

Commensal small mammal trapping data in Southern Senegal, 2012-2015: where invasive species meet native ones.

Describing patterns and testing hypotheses on processes driving biological invasions represent major issues in ecology. Addressing these questions requires building adequate data sets, i.e., covering areas and spanning periods adapted to the invasion processes studied. Rodents include major invasive species, among which the black rat Rattus rattus and the domestic mouse Mus musculus have nearly colonized the entire world, from their native Asian range. To do so, they have benefitted from their ability to cope with human-modified environments and to live in the immediate vicinity of Man, who served as a vector of their dispersal between regions and continents. In Senegal, both R. rattus and M. musculus, initially introduced by early West European colonizers some centuries ago, are currently expanding thanks to road traffic and infrastructure development and rampant urbanization that concerns even remote regions of the country. As part of projects aimed at studying (1) the role of invasive black rat populations in the emergence of zoonotic diseases in southeastern Senegal, and (2) the evolutionary consequences of parasites in R. rattus and M. musculus invasions in Senegal, we conducted a series of field campaigns throughout the southern half of the country, between May 2012 and September 2015. The objectives were to catch commensal small mammals using standard trapping procedures, identify them using morphological or molecular tools, and take samples from them upon autopsy, to look for zoonotic parasites and pathogens. Along with data on individual specimens, information on microhabitats was gathered at each trap position. This resulted in the constitution of a data set of more than 13,000 trapnights, which allowed the capture of more than 3,100 small mammals, all characterized by a series of associated biological, geographical, and environmental data. The small mammals concerned are mainly rodents (10 species), shrews, and hedgehogs. The two invasive rodent species were the most numerous, exceeding in numbers all the other species pooled. This data set makes it possible to study coarse to fine-scaled distribution of species of this commensal community in southern Senegal, as well as the possible determinants of this distribution in terms of habitat preferences and/or interspecific interactions. This data set can be freely used for non-commercial purposes and is licensed under a Creative Commons Attribution 4.0 International License.

Seoul Orthohantavirus in Wild Black Rats, Senegal, 2012-2013.

Hantaviruses cause hemorrhagic fever in humans worldwide. However, few hantavirus surveillance campaigns occur in Africa. We detected Seoul orthohantavirus in black rats in Senegal, although we did not find serologic evidence of this disease in humans. These findings highlight the need for increased surveillance of hantaviruses in this region.

Multihost Transmission of Schistosoma mansoni in Senegal, 2015-2018.

In West Africa, Schistosoma spp. are capable of infecting multiple definitive hosts, a lifecycle feature that may complicate schistosomiasis control. We characterized the evolutionary relationships among multiple Schistosoma mansoni isolates collected from snails (intermediate hosts), humans (definitive hosts), and rodents (definitive hosts) in Senegal. On a local scale, diagnosis of S. mansoni infection ranged 3.8%-44.8% in school-aged children, 1.7%-52.6% in Mastomys huberti mice, and 1.8%-7.1% in Biomphalaria pfeifferi snails. Our phylogenetic framework confirmed the presence of multiple S. mansoni lineages that could infect both humans and rodents; divergence times of these lineages varied (0.13-0.02 million years ago). We propose that extensive movement of persons across West Africa might have contributed to the establishment of these various multihost S. mansoni clades. High S. mansoni prevalence in rodents at transmission sites frequented by humans further highlights the implications that alternative hosts could have on future public health interventions.

Mini-FLOTAC as an alternative, non-invasive diagnostic tool for Schistosoma mansoni and other trematode infections in wildlife reservoirs.

BACKGROUND: Schistosomiasis and food-borne trematodiases are not only of major public health concern, but can also have profound implications for livestock production and wildlife conservation. The zoonotic, multi-host nature of many digenean trematodes is a significant challenge for disease control programmes in endemic areas. However, our understanding of the epidemiological role that animal reservoirs, particularly wild hosts, may play in the transmission of zoonotic trematodiases suffers a dearth of information, with few, if any, standardised, reliable diagnostic tests available. We combined qualitative and quantitative data derived from post-mortem examinations, coprological analyses using the Mini-FLOTAC technique, and molecular tools to assess parasite community composition and the validity of non-invasive methods to detect trematode infections in 89 wild Hubert's multimammate mice (Mastomys huberti) from northern Senegal. RESULTS: Parasites isolated at post-mortem examination were identified as Plagiorchis sp., Anchitrema sp., Echinostoma caproni, Schistosoma mansoni, and a hybrid between Schistosoma haematobium and Schistosoma bovis. The reports of E. caproni and Anchitrema sp. represent the first molecularly confirmed identifications for these trematodes in definitive hosts of sub-Saharan Africa. Comparison of prevalence estimates derived from parasitological analysis at post-mortem examination and Mini-FLOTAC analysis showed non-significant differences indicating comparable results between the two techniques (P = 1.00 for S. mansoni; P = 0.85 for E. caproni; P = 0.83 for Plagiorchis sp.). A Bayesian model, applied to estimate the sensitivities of the two tests for the diagnosis of Schistosoma infections, indicated similar median posterior probabilities of 83.1% for Mini-FLOTAC technique and 82.9% for post-mortem examination (95% Bayesian credible intervals of 64.0-94.6% and 63.7-94.7%, respectively). CONCLUSIONS: Our results showed that the Mini-FLOTAC could be applied as an alternative diagnostic technique for the detection of the zoonotic S. mansoni and other trematodes in rodent reservoirs. The implementation of non-invasive diagnostics in wildlife would offer numerous advantages over lethal sampling methodologies, with potential impact on control strategies of zoonotic helminthiases in endemic areas of sub-Saharan Africa and on fostering a framework of animal use reduction in scientific practice.

Plagiorchis sp. in small mammals of Senegal and the potential emergence of a zoonotic trematodiasis.

Trematodes of the genus Plagiorchis have a wide geographical distribution and can exploit a variety of hosts. The occurrence and zoonotic potential of Plagiorchis spp. have been characterised across several countries in Asia; in contrast, information on Plagiorchis parasites in Africa remains anecdotal. We isolated a previously undescribed Plagiorchis species from the biliary tract and small intestine of 201 out of 427 small mammals collected in the region of Lake Guiers, Senegal, with local prevalence ranging from 38.6% to 77.0%. Conversely, Plagiorchis isolates were not observed in the 244 small mammals sampled in and around the town of Richard Toll, Senegal. Molecular phylogenetics of the internal transcribed spacer region, nuclear ribosomal DNA, and of the cytochrome c oxidase subunit 1 gene, mitochondrial DNA, supported the monophyly and multi-host spectrum of this newly discovered West African Plagiorchis species. Sequencing of individual cercariae shed by Radix natalensis (Gastropoda: Lymnaeidae) suggested that these freshwater snails may act as suitable first intermediate hosts. Phylogenetic analysis yielded a highly resolved topology indicating two different clades, one composed by Plagiorchis spp. infecting rodents, insectivores, and birds, while the other included parasites of bats. Our findings showed the low host specificity and high prevalence of the isolated Plagiorchis sp. in the Lake Guiers region, with Hubert's multimammate mice (Mastomys huberti) appearing to play a primary role in the epidemiology of this parasite. The results raise concern about the zoonotic potential of Plagiorchis sp. in local communities of the Lake Guiers region, and highlight food-borne trematodiases and their link to land-use change as a neglected public health issue in regions of West Africa.

Rodents of Senegal and their role as intermediate hosts of Hydatigera spp. (Cestoda: Taeniidae).

Hydatigera (Cestoda: Taeniidae) is a recently resurrected genus including species seldom investigated in sub-Saharan Africa. We surveyed wild small mammal populations in the areas of Richard Toll and Lake Guiers, Senegal, with the objective to evaluate their potential role as intermediate hosts of larval taeniid stages (i.e. metacestodes). Based on genetic sequences of a segment of the mitochondrial DNA gene cytochrome c oxidase subunit 1 (COI), we identified Hydatigera parva metacestodes in 19 out of 172 (11.0%) Hubert's multimammate mice (Mastomys huberti) and one out of six (16.7%) gerbils (Taterillus sp.) and Hydatigera taeniaeformis sensu stricto metacestodes in one out of 215 (0.5%) Nile rats (Arvicanthis niloticus). This study reports epidemiological and molecular information on H. parva and H. taeniaeformis in West African rodents, further supporting the phylogeographic hypothesis on the African origin of H. parva. Our findings may indicate significant trophic interactions contributing to the local transmission of Hydatigera spp. and other parasites with similar life-cycle mechanisms. We therefore propose that further field investigations of rodent population dynamics and rodent-borne infectious organisms are necessary to improve our understanding of host-parasite associations driving the transmission risks of rodent parasites in West Africa.

Seroprevalence of Toxoplasma gondii in commensal rodents sampled across Senegal, West Africa.

Risks related to Toxoplasma gondii infection in humans remain poorly known in Senegal. Although rodent surveys could help to assess the circulation of T. gondii, they have seldom been set up in sub-Saharan Africa. The aim of this study was to examine Toxoplasma seroprevalence in rodents from villages and towns across Senegal. Rodents were sampled in 40 localities using a standardised trapping protocol. Detection of T. gondii antibodies was performed on 1205 rodents, using a modified agglutination test (MAT) technique. Seroprevalence data were analysed depending on geography, the local rodent community, and individual characteristics of the rodent hosts. We found 44 seropositive rodents from four different species (Mastomys erythroleucus, Mastomys natalensis, Mus musculus domesticus, Rattus rattus). Toxoplasma seroprevalence was low, averaging 4% in the localities. Higher Toxoplasma seroprevalence (up to 24%) was found in northern Senegal, a region known to be the heart of pastoral herding in the country.

TITLE: Séroprévalence de Toxoplasma gondii chez les rongeurs commensaux au Sénégal, Afrique de l'Ouest. ABSTRACT: Les risques liés à l'infection par Toxoplasma gondii chez l'homme restent mal connus au Sénégal. Bien que les rongeurs soient considérés comme des marqueurs pertinents de la circulation de T. gondii, peu d'études ont ciblé ces hôtes en Afrique sub-saharienne. Le but de cette étude était d'étudier la séroprévalence de Toxoplasma chez les rongeurs des villes et des villages du Sénégal. Les rongeurs ont été échantillonnés dans 40 localités avec un protocole de piégeage standardisé. La détection des anticorps contre T. gondii a été faite sur 1205 rongeurs avec un test d'agglutination modifié. Les données de séroprévalence ont été analysées en fonction de la géographie, de la communauté locale de rongeurs et de caractéristiques individuelles du rongeur. Nous avons trouvé 44 individus séropositifs, de quatre espèces différentes (Mastomys erythroleucus, Mastomys natalensis, Mus musculus domesticus, Rattus rattus). La séroprévalence moyenne est faible, de l'ordre de 4 % au sein des localités. Les plus fortes séroprévalences (jusqu'à 24 %) ont été observées dans le Nord du Sénégal, une région connue pour être le cœur de l'élevage pastoral dans le pays.

Leishmania major and Trypanosoma lewisi infection in invasive and native rodents in Senegal.

Bioinvasion is a major public health issue because it can lead to the introduction of pathogens in new areas and favours the emergence of zoonotic diseases. Rodents are prominent invasive species, and act as reservoirs in many zoonotic infectious diseases. The aim of this study was to determine the link between the distribution and spread of two parasite taxa (Leishmania spp. and Trypanosoma lewisi) and the progressive invasion of Senegal by two commensal rodent species (the house mouse Mus musculus domesticus and the black rat Rattus rattus). M. m. domesticus and R. rattus have invaded the northern part and the central/southern part of the country, respectively. Native and invasive rodents were caught in villages and cities along the invasion gradients of both invaders, from coastal localities towards the interior of the land. Molecular diagnosis of the two trypanosomatid infections was performed using spleen specimens. In the north, neither M. m. domesticus nor the native species were carriers of these parasites. Conversely, in the south, 17.5% of R. rattus were infected by L. major and 27.8% by T. lewisi, while very few commensal native rodents were carriers. Prevalence pattern along invasion gradients, together with the knowledge on the geographical distribution of the parasites, suggested that the presence of the two parasites in R. rattus in Senegal is of different origins. Indeed, the invader R. rattus could have been locally infected by the native parasite L. major. Conversely, it could have introduced the exotic parasite T. lewisi in Senegal, the latter appearing to be poorly transmitted to native rodents. Altogether, these data show that R. rattus is a carrier of both parasites and could be responsible for the emergence of new foci of cutaneous leishmaniasis, or for the transmission of atypical human trypanosomiasis in Senegal.

Rodents as Natural Hosts of Zoonotic Schistosoma Species and Hybrids: An Epidemiological and Evolutionary Perspective From West Africa.

The complex multi-host disease dynamics of schistosomiasis and Schistosoma spp., including the emergence of zoonotic parasite hybrids, remain largely unexplored in West Africa. We elucidated the role of wild small mammals as reservoir for zoonotic Schistosoma species and hybrids in endemic areas of Senegal. We identified Schistosoma mansoni, Schistosoma bovis, and a Schistosoma haematobium/S. bovis hybrid, with local prevalence in wild rodents ranging from 1.9% to 28.6%. Our findings indicate that rodents may be an important local reservoir for zoonotic schistosomiasis in endemic areas of West Africa, amplifying transmission to humans and acting as natural definitive hosts of schistosome hybrids.

Ecological and sanitary impacts of bacterial communities associated to biological invasions in African commensal rodent communities.

Changes in host-parasite ecological interactions during biological invasion events may affect both the outcome of invasions and the dynamics of exotic and/or endemic infections. We tested these hypotheses, by investigating ongoing house mouse (Mus musculus domesticus) and black rat (Rattus rattus) invasions in Senegal (West Africa). We used a 16S gene rRNA amplicon sequencing approach to study potentially zoonotic bacterial communities in invasive and native rodents sampled along two well-defined independent invasion routes. We found that individual host factors (body mass and sex) were important drivers of these bacterial infections in rodents. We observed that the bacterial communities varied along invasion routes and differed between invasive and native rodents, with native rodents displaying higher overall bacterial diversity than invasive rodents. Differences in prevalence levels for some bacterial Operational Taxonomic Units (OTUs) provided support for ecological processes connecting parasitism and invasion success. Finally, our results indicated that rodent invasions may lead to the introduction of exotic bacterial genera and/or to changes in the prevalence of endemic ones. This study illustrates the difficulty of predicting the relationship between biodiversity and disease risks, and advocate for public health prevention strategies based on global pathogen surveillance followed by accurate characterization of potential zoonotic agents.

Parasites and invasions: changes in gastrointestinal helminth assemblages in invasive and native rodents in Senegal.

Understanding why some exotic species become widespread and abundant in their colonised range is a fundamental issue that still needs to be addressed. Among many hypotheses, newly established host populations may benefit from a parasite loss ("enemy release" hypothesis) through impoverishment of their original parasite communities or reduced infection levels. Moreover, the fitness of competing native hosts may be negatively affected by the acquisition of exotic taxa from invaders ("parasite spillover") and/or by an increased transmission risk of native parasites due to their amplification by invaders ("parasite spillback"). We focused on gastrointestinal helminth communities to determine whether these predictions could explain the ongoing invasion success of the commensal house mouse (Mus musculus domesticus) and black rat (Rattus rattus), as well as the associated decrease in native Mastomys spp., in Senegal. For both invasive species, our results were consistent with the predictions of the enemy release hypothesis. A decrease in overall gastrointestinal helminth prevalence and infracommunity species richness was observed along the invasion gradients as well as lower specific prevalence/abundance (Aspiculuris tetraptera in Mus musculus domesticus, Hymenolepis diminuta in Rattus rattus) on the invasion fronts. Conversely, we did not find strong evidence of GIH spillover or spillback in invasion fronts, where native and invasive rodents co-occurred. Further experimental research is needed to determine whether and how the loss of gastrointestinal helminths and reduced infection levels along invasion routes may result in any advantageous effects on invader fitness and competitive advantage.

Borrelia infection in small mammals in West Africa and its relationship with tick occurrence inside burrows.

Tick-borne relapsing fever (TBRF) is a zoonotic disease caused by several Borrelia species transmitted to humans by Ornithodoros tick vectors. In West Africa, Borrelia crocidurae is a common cause of disease in many rural populations. Small mammals act as reservoirs of infection. We report here the results of surveys that investigated the occurrence of B. crocidurae infection in rodents and insectivores from eight countries of West and Central Africa. Animals were identified at the species level and tested for Borrelia either by examination of thick blood film, intra-peritoneal inoculation of blood or brain tissues into laboratory mice, or by molecular techniques. A total of 4358 small mammals belonging to 38 species and 7 families were collected, including 3225 specimens collected in areas where the occurrence of Ornithodoros sonrai tick in rodent burrows was documented, and 1133 in areas where this tick was absent. In areas with O. sonrai, Borrelia infection was demonstrated in 287 of 3109 (9.2%) small mammals tested, and none was documented in 1004 animals tested from other areas. There was no relationship between the occurrence of Rhipicephalus, Hyaloma and Argas ticks in burrows and the distribution of Borrelia infection in small mammals. The 287 specimens infected by Borrelia belonged to 15 rodent and shrew species, including three Saharo-Sahelian species - Gerbillus gerbillus, Gerbillus occiduus and Gerbillus tarabuli - identified as reservoirs for TBRF with a distribution restricted to this area. In Sudan and Sudano-Sahelian areas, Arvicanthis niloticus, Mastomys erythroleucus and Mastomys huberti were the main reservoir of infection. Although most small mammals species collected had a large distribution in West and Central Africa, the fact that only animals collected in areas with O. sonrai were found infected suggest that this tick is the only vector of TBRF in rodents and insectivores in this part of Africa.

Detection of Orientia sp. DNA in rodents from Asia, West Africa and Europe.

Orientia bacterium is the agent of the scrub typhus, a seriously neglected life-threatening disease in Asia. Here, we report the detection of DNA of Orientia in rodents from Europe and Africa. These findings have important implications for public health. Surveillance outside Asia, where the disease is not expected by sanitary services, needs to be improved.

Mitochondrial and nuclear genes-based phylogeography of Arvicanthis niloticus (Murinae) and sub-Saharan open habitats pleistocene history.

A phylogeographic study was conducted on the Nile grass rat, Arvicanthis niloticus, a rodent species that is tightly associated with open grasslands from the Sudano-Sahelian regions. Using one mitochondrial (cytochrome b) and one nuclear (intron 7 of Beta Fibrinogen) gene, robust patterns were retrieved that clearly show that (i) the species originated in East Africa concomitantly with expanding grasslands some 2 Ma, and (ii) four parapatric and genetically well-defined lineages differentiated essentially from East to West following Pleistocene bioclimatic cycles. This strongly points towards allopatric genetic divergence within savannah refuges during humid episodes, then dispersal during arid ones; secondary contact zones would have then stabilized around geographic barriers, namely, Niger River and Lake Chad basins. Our results pertinently add to those obtained for several other African rodent as well as non-rodent species that inhabit forests, humid zones, savannahs and deserts, all studies that now allow one to depict a more comprehensive picture of the Pleistocene history of the continent south of the Sahara. In particular, although their precise location remains to be determined, at least three Pleistocene refuges are identified within the West and Central African savannah biome.

Invasion genetics of the introduced black rat (Rattus rattus) in Senegal, West Africa.

An understanding of the evolutionary history and dynamics of invasive species is required for the construction of predictive models of future spread and the design of biological management measures. The black rat (Rattus rattus) is a major vertebrate invader with a worldwide distribution. Despite the severe ecological, economic and health impacts of this species, its evolutionary history has been little studied. We carried out extensive specimen sampling in Senegal, West Africa, and used microsatellite markers to describe the pattern and processes of invasion in this large continental area. The genetic data obtained were combined with historical knowledge concerning the presence of this species in Senegal. Data were analysed by a combination of Bayesian clustering and approximate Bayesian computation methods. The invasion pathways closely paralleled the history of human trade routes in Senegal. In several places, we detected the occurrence of multiple introductions from genetically different sources. Long-distance migration between towns and villages was also observed. Our findings suggest that genetic bottlenecks and admixture have played a major role in shaping the genetics of invasive black rats. These two processes may generate genetic novelty and favour rapid evolution along the invasion pathways.