Flea infestation of rodent and their community structure in frequent and non-frequent plague outbreak areas in Mbulu district, northern Tanzania.

Understanding rodent-ectoparasite interactions and the factors driving them is important in understanding the epidemiology of diseases involving an arthropod vector. Fleas are the primary vector for Yersinia pestis, the bacteria that causes plague and monitoring of flea population is essential for planning the potential mitigation measures to prevent the disease outbreak. In this study, we investigated flea abundance, community structure and the potential factors driving flea infestation in areas with frequent (persistent) and non-frequent plague (non-persistent) outbreaks. We collected fleas from captured rodents in two villages with both forest and farm habitats. We found 352 fleas belonging to 5 species with Dinopsyllus lypusus the most abundant overall (57.10%) and Ctenophthalmus spp. the lowest (1.70%). There were no significant differences of flea abundance between study localities, habitats and seasons (p > 0.05) but, flea infestation was significantly positively associated with the persistent locality and with the short rain season (p < 0.05). Further, flea abundance increased significantly with rodent body weight (p < 0.05). Furthermore, we found fleas broadly structured into two communities varying between the dry, long rain and short rain seasons. These findings have important implications for public health, as they may be used to assess and control the risks of plague transmission and other flea borne diseases in the foci.

Twenty-nine years of continuous monthly capture-mark-recapture data of multimammate mice (Mastomys natalensis) in Morogoro, Tanzania.

The multimammate mice (Mastomys natalensis) is the most-studied rodent species in sub-Saharan Africa, where it is an important pest species in agriculture and carrier of zoonotic diseases (e.g. Lassa virus). Here, we provide a unique dataset that consists of twenty-nine years of continuous monthly capture-mark-recapture entries on one 3 ha mosaic field (MOSA) in Morogoro, Tanzania. It is one of the most accurate and long-running capture-recapture time series on a small mammal species worldwide and unique to Africa. The database can be used by ecologists to test hypotheses on the population dynamics of small mammals (e.g. to test the effect of climate change), or to validate new algorithms on real long-term field data (e.g. new survival analyses techniques). It is also useful for both scientists and decision-makers who want to optimize rodent control strategies and predict outbreaks of multimammate mice.

Impact of contraceptive hormones on the reproductive potential of male and female commensal black rats (Rattus rattus).

The black rat is considered one of the world's top pests. With increased restrictions on rodenticides, new alternatives to manage rats are urgently needed. Research on the use of contraceptive hormones, levonorgestrel (LE), and quinestrol (QU), have been evaluated against some rodent species, and this research is the first study to assess these on black rats. Hormones were incorporated into rodent bait at 10 and 50 ppm concentrations singly and in combination (EP-1). Groups of 10 animals of each sex were fed the baits over 7 days. Lower bait consumption was observed with slight body mass reductions. On dissection, it was observed that the uterus was in a state of edema and male reproductive organs weighed less with reduced sperm counts/motility. The 2 most promising baits, 50 ppm QU and EP-1, were used to assess impact on pregnancy and litter size. Pregnancy was reduced from 70% success when both males and females consumed untreated bait, down to 30% when males had consumed contraceptive bait but females had not, and down to 0% when females had consumed contraceptive bait, regardless of whether they had paired with a treated or untreated male. Litter size in the untreated pairs was 8 pups, but only 4 pups in those cases where the male only had consumed the contraceptive. Further studies should investigate how long the effect lasts and its reversibility. Field studies at the population level may also shed light on the practicality of using contraceptive baits for black rats in different habitats.

Leptospira Seropositivity in Humans, Livestock and Wild Animals in a Semi-Arid Area of Tanzania.

BACKGROUND: Leptospirosis is among the major neglected zoonoses in developing countries. The prevalence of leptospirosis remains underestimated in many African countries because of limited diagnostic facilities. We studied Leptospira seropositivity prevalence in humans, sheep, goats and rodents in a semi-arid region of central Tanzania and compared findings with reports from humid tropical areas. The aims were to establish the disease burden in different settings; understand circulating Leptospira serovars and potential major reservoirs for establishing appropriate control measures. METHODS: Humans, sheep, goats, rodents and shrews (insectivores) were sampled from Bahi district, a semi-arid area in central Tanzania. Samples were tested for leptospiral antibodies using microscopic agglutination test (MAT) consisting of Leptospira serovars mainly reported in Tanzania and reference strains. Findings were compared with previous data to determine the disease epidemiological patterns. RESULTS AND CONCLUSION: Semi-arid area showed high Leptospira seropositivity prevalence in humans and domestic animals due to intensive human-animal interactions at scarce water points and by flash flooding which occur in the area. Rodent population in the semi-arid areas was relatively low due to flooding. Leptospira seropositivity in rodents was also slightly lower, and the rodents appeared to be prolific breeders, probably as a means to compensate for the lost population during extreme drought as well as during short spells of floods. Intensive human-animal interaction in the semi-arid areas especially, in water sources in valleys where human and animals often meet, likely increased the risk of leptospirosis transmission to rice farmers in the area. Goats and sheep which are kept around homesteads had higher leptospiral antibodies prevalence (62%), nearly double of the 38% reported in same species in humid tropical regions of Tanzania. Livestock, especially goats and sheep, could be the major source of leptospirosis transmission to humans. Vaccination of livestock with vaccines against local Leptospira strains should be encouraged, and rodent control emphasized, as part of a management strategy against leptospirosis. Public awareness of leptospirosis must also be raised and supported by availability of rapid test kits in clinics for preliminary testing of leptospirosis in people with fevers of unknown origin.

The effects of personality on survival and trappability in a wild mouse during a population cycle.

The pace-of-life syndrome (POLS) theory provides an evolutionary explanation for the existence of consistent among-individual variation in behaviour, or animal personality. Herein, individuals with a fast lifestyle are considered to be bolder and should take more risks resulting in a lower life expectancy compared to shyer individuals with a slower lifestyle. However, this assumption depends on the levels of intra-specific competition that the individuals experience which has rarely been tested in species that experience large changes in competition on a very short time scale. We used the multimammate mice (Mastomys natalensis) as a model system to study the POLS assumption by investigating the effects of two personality traits (exploration and stress-sensitivity) on survival, maturation (a proxy for reproductive investment) and recapture probability during one population cycle (Nindividuals = 201). Such a cycle consists of two phases in which the levels of intra-specific competition vary drastically. We found that only one personality trait, namely stress-sensitivity, had a negative effect on both survival and recapture probability but none of them affected maturation. This suggests that less stress-sensitive individuals take more risks in the wild and have a higher survival probability compared to high stress-sensitive individuals. However, the effect of personality on survival was only present during the population decrease phase, when the levels of intra-specific competition are high due to a scarcity of food. This suggests that seasonal changes in competition might be important in the evolution and maintenance of animal personalities in species whose population dynamics have a clear seasonal component.

Effects of forest disturbance on the fitness of an endemic rodent in a biodiversity hotspot.

Praomys delectorum occurs abundantly in both disturbed and intact forests in the Ukaguru Mountains within the Eastern Arc Mountains (EAM), Morogoro, Tanzania. While previous studies have reported that anthropogenic disturbances such as grazing, wood cutting, and harvesting have a positive effect on the population density of P. delectorum, the impact of habitat disturbance on its demographic traits is still unknown. We performed a capture-mark-recapture study in both disturbed and intact forests from June 2018 to February 2020 in order to investigate the effects of habitat disturbance on abundance and two demographic traits: survival and maturation of P. delectorum in the Ukaguru Mountains. We found no variation in abundance or maturation between intact and disturbed forests, but habitat type did affect survival. However, this effect was sex-dependent since female survival was higher in disturbed forests, while male survival remained similar across the two forest types potentially due to differences in predation pressure or food availability between the two habitats. Continuous demographic monitoring of P. delectorum in EAM is necessary given that the increasing human population surrounding the landscape is leading to higher deforestation rates and expansion of the pine plantation in the forest reserve.

Comparative assessment on rodent impacts and cultural perceptions of ecologically based rodent management in 3 Afro-Malagasy farming regions.

Rodents generate negative consequences for smallholder farmers in Africa that directly impact household and livestock damage, food security, and public health. Ecologically Based Rodent Management (EBRM) seeks sustainable solutions for the mitigation of rodent damage through assessments of rodent population dynamics, agro-ecosystems, and socio-cultural contexts. We adopt a comparative approach across 3 rural Afro-Malagasy smallholder farming regions in South Africa, Tanzania, and Madagascar to assess the household impacts of rodent pests and current perceptions and preferences associated with several rodent control measures. We conducted focus group questionnaires and interviews in different study site locations. Rodents assert multiple impacts on Afro-Malagasy farmers demonstrating recurrent and emerging agricultural and household costs, and public health impacts. We identify a significant knowledge gap in educating communities about the application of different EBRM approaches in favor of acute poisons that are perceived to be more effective. Cultural issues and taboos also have a significant impact on the social acceptance of rodent hunting as well as biological control using indigenous predators. We advocate for an enhanced investigation of the socio-cultural beliefs associated with different rodent practices to understand the factors underlying social acceptance. A collaborative approach that integrates the perspectives of target communities to inform the design of EBRM initiatives according to the specific agro-ecosystem and socio-cultural context is necessary to ensure programmatic success.

Density dependence and persistence of Morogoro arenavirus transmission in a fluctuating population of its reservoir host.

A key aim in wildlife disease ecology is to understand how host and parasite characteristics influence parasite transmission and persistence. Variation in host population density can have strong impacts on transmission and outbreaks, and theory predicts particular transmission-density patterns depending on how parasites are transmitted between individuals. Here, we present the results of a study on the dynamics of Morogoro arenavirus in a population of multimammate mice (Mastomys natalensis). This widespread African rodent, which is also the reservoir host of Lassa arenavirus in West Africa, is known for its strong seasonal density fluctuations driven by food availability. We investigated to what degree virus transmission changes with host population density and how the virus might be able to persist during periods of low host density. A seven-year capture-mark-recapture study was conducted in Tanzania where rodents were trapped monthly and screened for the presence of antibodies against Morogoro virus. Observed seasonal seroprevalence patterns were compared with those generated by mathematical transmission models to test different hypotheses regarding the degree of density dependence and the role of chronically infected individuals. We observed that Morogoro virus seroprevalence correlates positively with host density with a lag of 1-4 months. Model results suggest that the observed seasonal seroprevalence dynamics can be best explained by a combination of vertical and horizontal transmission and that a small number of animals need to be infected chronically to ensure viral persistence. Transmission dynamics and viral persistence were best explained by the existence of both acutely and chronically infected individuals and by seasonally changing transmission rates. Due to the presence of chronically infected rodents, rodent control is unlikely to be a feasible approach for eliminating arenaviruses such as Lassa virus from Mastomys populations.

Relationship between population density and viral infection: A role for personality?

Conspecific density and animal personality (consistent among-individual differences in behavior) may both play an important role in disease ecology. Nevertheless, both factors have rarely been studied together but may provide insightful information in understanding pathogen transmission dynamics. In this study, we investigated how both personality and density affect viral infections both direct and indirectly, using the multimammate mice (Mastomys natalensis) and Morogoro arenavirus (MORV) as a model system. Using a replicated semi-natural experiment, we found a positive correlation between MORV antibody presence and density, suggesting that MORV infection is density-dependent. Surprisingly, slower explorers were more likely to have antibodies against MORV compared to highly explorative individuals. However, exploration was positively correlated with density which may suggest a negative, indirect effect of density on MORV infection. We have shown here that in order to better understand disease ecology, both personality and density should be taken into account.

Species composition and community structure of small pest rodents (Muridae) in cultivated and fallow fields in maize-growing areas in Mayuge district, Eastern Uganda.

Pest rodents remain key biotic constraints to cereal crops production in the East African region where they occur, especially in seasons of outbreaks. Despite that, Uganda has scant information on rodents as crop pests to guide effective management strategies.A capture-mark-recapture (CMR) technique was employed to study the ecology of small rodents, specifically to establish the species composition and community structure in a maize-based agro ecosystem. Trapping of small rodents was conducted in permanent fallow land and cultivated fields, with each category replicated twice making four study grids. At each field, a 60 × 60 m grid was measured and marked with permanent trapping points spaced at 10 × 10 m, making a total of 49 trapping points/grids. Trapping was conducted monthly at 4-week interval for three consecutive days for two and half years using Sherman live traps.Eleven identified small rodent species and one insectivorous small mammal were recorded with Mastomys natalensis being the most dominant species (over 60.7%). Other species were Mus triton (16.1%), Aethomys hendei (6.7%), Lemniscomys zebra (5.2%), Lophuromys sikapusi (4.8%), Arvicanthis niloticus (0.9%), Gerbilliscus kempi (0.1%), Graphiurus murinus (0.1%), Steatomys parvus (0.1%), Dasymys incomtus (0.1%), and Grammomys dolichurus (0.1%). Spatially, species richness differed significantly (p = 0.0001) between the studied field habitats with significantly higher richness in fallow land compared with cultivated fields.Temporally, total species richness and abundance showed a significant interaction effect over the months, years, and fields of trapping with significantly (p = 0.001) higher abundances during months of wet seasons and in the first and third year of trapping. In terms of community structure, higher species diversity associated more with fallow field habitats but also with certain rare species found only in cultivated fields.Synthesis and applications. Based on these findings, management strategies can be designed to target the key pest species and the most vulnerable habitats thus reducing the impact they can inflict on field crops.

Does exploratory behavior or activity in a wild mouse explain susceptibility to virus infection?

Exploration and activity are often described as trade-offs between the fitness benefits of gathering information and resources, and the potential costs of increasing exposure to predators and parasites. More exploratory individuals are predicted to have higher rates of parasitism, but this relationship has rarely been examined for virus infections in wild populations. Here, we used the multimammate mouse Mastomys natalensis to investigate the relationship between exploration, activity, and infection with Morogoro virus (MORV). We characterized individual exploratory behavior (open field and novel object tests) and activity (trap diversity), and quantified the relationship between these traits and infection status using linear regression. We found that M. natalensis expresses consistent individual differences, or personality types, in exploratory behavior (repeatability of 0.30, 95% CI: 0.21-0.36). In addition, we found a significant contrasting effect of age on exploration and activity where juveniles display higher exploration levels than adults, but lower field-activity. There was however no statistical evidence for a behavioral syndrome between these 2 traits. Contrary to our expectations, we found no correlation between MORV infection status and exploratory behavior or activity, which suggests that these behaviors may not increase exposure probability to MORV infection. This would further imply that variation in viral infection between individuals is not affected by between-individual variation in exploration and activity.

Arenavirus infection correlates with lower survival of its natural rodent host in a long-term capture-mark-recapture study.

BACKGROUND: Parasite evolution is hypothesized to select for levels of parasite virulence that maximise transmission success. When host population densities fluctuate, low levels of virulence with limited impact on the host are expected, as this should increase the likelihood of surviving periods of low host density. We examined the effects of Morogoro arenavirus on the survival and recapture probability of multimammate mice (Mastomys natalensis) using a seven-year capture-mark-recapture time series. Mastomys natalensis is the natural host of Morogoro virus and is known for its strong seasonal density fluctuations. RESULTS: Antibody presence was negatively correlated with survival probability (effect size: 5-8% per month depending on season) but positively with recapture probability (effect size: 8%). CONCLUSIONS: The small negative correlation between host survival probability and antibody presence suggests that either the virus has a negative effect on host condition, or that hosts with lower survival probability are more likely to obtain Morogoro virus infection, for example due to particular behavioural or immunological traits. The latter hypothesis is supported by the positive correlation between antibody status and recapture probability which suggests that risky behaviour might increase the probability of becoming infected.

Effect of synthetic hormones on reproduction in Mastomys natalensis.

Rodent pest management traditionally relies on some form of lethal control. Developing effective fertility control for pest rodent species could be a major breakthrough particularly in the context of managing rodent population outbreaks. This laboratory-based study is the first to report on the effects of using fertility compounds on an outbreaking rodent pest species found throughout sub-Saharan Africa. Mastomys natalensis were fed bait containing the synthetic steroid hormones quinestrol and levonorgestrel, both singly and in combination, at three concentrations (10, 50, 100 ppm) for 7 days. Consumption of the bait and animal body mass was mostly the same between treatments when analysed by sex, day and treatment. However, a repeated measures ANOVA indicated that quinestrol and quinestrol + levonorgestrel treatments reduced consumption by up to 45%, particularly at the higher concentrations of 50 and 100 ppm. Although there was no clear concentration effect on animal body mass, quinestrol and quinestrol + levonorgestrel lowered body mass by up to 20% compared to the untreated and levonorgestrel treatments. Quinestrol and quinestrol + levonorgestrel reduced the weight of male rat testes, epididymis and seminal vesicles by 60-80%, and sperm concentration and motility were reduced by more than 95%. No weight changes were observed to uterine and ovarian tissue; however, high uterine oedema was observed among all female rats consuming treated bait at 8 and 40 days from trial start. Trials with mate pairing showed there were significant differences in the pregnancy rate with all treatments when compared to the untreated control group of rodents.

Arenavirus Dynamics in Experimentally and Naturally Infected Rodents.

Infectious diseases of wildlife are typically studied using data on antibody and pathogen levels. In order to interpret these data, it is necessary to know the course of antibodies and pathogen levels after infection. Such data are typically collected using experimental infection studies in which host individuals are inoculated in the laboratory and sampled over an extended period, but because laboratory conditions are controlled and much less variable than natural conditions, the immune response and pathogen dynamics may differ. Here, we compared Morogoro arenavirus infection patterns between naturally and experimentally infected multimammate mice (Mastomys natalensis). Longitudinal samples were collected during three months of bi-weekly trapping in Morogoro, Tanzania, and antibody titer and viral RNA presence were determined. The time of infection was estimated from these data using a recently developed Bayesian approach, which allowed us to assess whether the natural temporal patterns match the previously observed patterns in the laboratory. A good match was found for 52% of naturally infected individuals, while most of the mismatches can be explained by the presence of chronically infected individuals (35%), maternal antibodies (10%), and an antibody detection limit (25%). These results suggest that while laboratory data are useful for interpreting field samples, there can still be differences due to conditions that were not tested in the laboratory.

Correction: A systematic review of rodent pest research in Afro-Malagasy small-holder farming systems: Are we asking the right questions?

[This corrects the article DOI: 10.1371/journal.pone.0174554.].

A systematic review of rodent pest research in Afro-Malagasy small-holder farming systems: Are we asking the right questions?

Rodent pests are especially problematic in terms of agriculture and public health since they can inflict considerable economic damage associated with their abundance, diversity, generalist feeding habits and high reproductive rates. To quantify rodent pest impacts and identify trends in rodent pest research impacting on small-holder agriculture in the Afro-Malagasy region we did a systematic review of research outputs from 1910 to 2015, by developing an a priori defined set of criteria to allow for replication of the review process. We followed the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines. We reviewed 162 publications, and while rodent pest research was spatially distributed across Africa (32 countries, including Madagascar), there was a disparity in number of studies per country with research biased towards four countries (Tanzania [25%], Nigeria [9%], Ethiopia [9%], Kenya [8%]) accounting for 51% of all rodent pest research in the Afro-Malagasy region. There was a disparity in the research themes addressed by Tanzanian publications compared to publications from the rest of the Afro-Malagasy region where research in Tanzania had a much more applied focus (50%) compared to a more basic research approach (92%) in the rest of the Afro-Malagasy region. We found that pest rodents have a significant negative effect on the Afro-Malagasy small-holder farming communities. Crop losses varied between cropping stages, storage and crops and the highest losses occurred during early cropping stages (46% median loss during seedling stage) and the mature stage (15% median loss). There was a scarcity of studies investigating the effectiveness of various management actions on rodent pest damage and population abundance. Our analysis highlights that there are inadequate empirical studies focused on developing sustainable control methods for rodent pests and rodent pests in the Africa-Malagasy context is generally ignored as a research topic.

Soil type limits population abundance of rodents in crop fields: case study of the multimammate rat Mastomys natalensis Smith, 1834 in Tanzania.

Studies of populations of the multimammate rat Mastomys natalensis in Morogoro, Tanzania, show that soil texture appears to influence the population abundance and distribution of these rats in agricultural fields. The lowest rodent population abundance was found on sandy clay soils (F((2, 5)) = 8.42; P= 0.025). The population abundances of M. natalensis on sandy clay loam and sandy loam soils did not differ significantly (P≤ 0.05), possibly because these soils have a very similar texture. The results of this study suggest that M. natalensis prefers loam-textured soils with a high percentage of sand, which are probably better than clay soils for burrowing and nesting, particularly in the rainy season. The lower preference for clay soils is probably related to the poor aeration in these soils and the waterlogging that occurs during the wet season.

Relationship between sampling intensity and precision for estimating damage to maize caused by rodents.

In this study we aimed to determine the relationship between sampling intensity and precision for estimating rodent damage. We used the systematic row sampling technique to provide data to achieve precision and accuracy in estimations of rodent damage in maize fields at the planting and seedling stages. The actual rodent damage to maize in 15 fields, each 0.5 ha in size, in Morogoro, Tanzania, was established at the seedling stage. These data were used to simulate the sampling intensities that would provide precision and accuracy. The variations between estimates were plotted against the sampling intervals. The results of this study show that the relationship between average standardized variances and sampling intervals is linear. The heterogeneous distribution of damage in some plots caused variations in the accuracy of the estimates between plots, but a sampling interval of five rows consistently produced estimates with a variance of less than 10%. We provide a standard curve that will allow a decision to be made on the sampling intensity as a function of required precision using the systematic row sampling technique in maize fields.

Reproduction and population dynamics of Mastomys natalensis Smith, 1834 in an agricultural landscape in the Western Usambara Mountains, Tanzania.

The multimammate rat, Mastomys natalensis Smith 1834, is a dominant species in agro-ecosystems in Sub-Saharan Africa, but adapts quickly to changes in non-agricultural landscape, particularly woodlands and forests. In this study we report on reproduction and population dynamics of M. natalensis in deforested high elevation localities in the Usambara Mountains, north-east Tanzania. We conducted Capture-Mark-Recapture studies in 2002-2004, and established that reproduction of M. natalensis takes place in the extended wet season between February and June, and the population density peaks in June-August. Reproduction cease in July to January and population density drops from July onwards. Reproduction and population density fluctuations are linked to the duration and amount of rainfall. In years when rainfall was below average and the wet season was short, the population density was significantly lower (below 10 animals/ha and 60 animals/ha in 2003 and 2004 respectively, compared to >100 animals/ha in 2002 when rainfall was above the seasonal average) (F(df 2,13)= 9.092, p < 0.01 for in between years variations and F(df 12,15)= 5.389, p < 0.01 for effect of cumulative annual rainfall on population density). These densities were much lower than in the lowland savannah habitats in central and southwest Tanzania. A comparison between the farmland/fallow mosaic fields and agro-forestry areas showed higher population densities in the former, which have similarities to the preferred habitats in the lowland savannahs. The increasing abundance of M. natalensis in the Usambara could have some consequences: M. natalensis is major pest and is involved in the plague cycle in the western Usambara Mountains. Mastomys natalensis is also a strong competitor and the impact on endemic rodent species, e.g. Lophuromys flavopunctatus and Praomys delectorum is unknown.