Drivers behind co-occurrence patterns between pathogenic bacteria, protozoa, and helminths in populations of the multimammate mouse, Mastomys natalensis.

Advances in experimental and theoretical work increasingly suggest that parasite interactions within a single host can affect the spread and severity of wildlife diseases. Yet empirical data to support predicted co-infection patterns are limited due to the practical challenges of gathering convincing data from animal populations and the stochastic nature of parasite transmission. Here, we investigated co-infection patterns between micro- (bacteria and protozoa) and macroparasites (gastro-intestinal helminths) in natural populations of the multimammate mouse (Mastomys natalensis). Fieldwork was performed in Morogoro (Tanzania), where we trapped 211 M. natalensis and tested their behaviour using a modified open-field arena. All animals were checked for the presence of helminths in their gastro-intestinal tract, three bacteria (Anaplasma, Bartonella, and Borrelia) and two protozoan genera (Babesia and Hepatozoon). Besides the presence of eight different helminth genera (reported earlier), we found that 19% of M. natalensis were positive for Anaplasma, 10% for Bartonella, and 2% for Hepatozoon species. Hierarchical modelling of species communities was used to investigate the effect of the different host-related factors on these parasites' infection probability and community structure. Our results show that the infection probability of Bartonella increased with the host's age, while the infection probability of Anaplasma peaked when individuals reached adulthood. We also observed that less explorative and stress-sensitive individuals had a higher infection probability with Bartonella. Finally, we found limited support for within-host interactions between micro-and macroparasites, as most co-infection patterns could be attributed to host exposure time.

SARS-CoV-2 surveillance in Norway rats (Rattus norvegicus) from Antwerp sewer system, Belgium.

SARS-CoV-2 human-to-animal transmission can lead to the establishment of novel reservoirs and the evolution of new variants with the potential to start new outbreaks in humans. We tested Norway rats inhabiting the sewer system of Antwerp, Belgium, for the presence of SARS-CoV-2 following a local COVID-19 epidemic peak. In addition, we discuss the use and interpretation of SARS-CoV-2 serological tests on non-human samples. Between November and December 2020, Norway rat oral swabs, faeces and tissues from the sewer system of Antwerp were collected to be tested by RT-qPCR for the presence of SARS-CoV-2. Serum samples were screened for the presence of anti-SARS-CoV-2 IgG antibodies using a Luminex microsphere immunoassay (MIA). Samples considered positive were then checked for neutralizing antibodies using a conventional viral neutralization test (cVNT). The serum of 35 rats was tested by MIA showing three potentially positive sera that were later negative by cVNT. All tissue samples of 39 rats analysed tested negative for SARS-CoV-2 RNA. This is the first study that evaluates SARS-CoV-2 infection in urban rats. We can conclude that the sample of rats analysed had never been infected with SARS-CoV-2. However, monitoring activities should continue due to the emergence of new variants prone to infect Muridae rodents.

Linking Behavior, Co-infection Patterns, and Viral Infection Risk With the Whole Gastrointestinal Helminth Community Structure in Mastomys natalensis.

Infection probability, load, and community structure of helminths varies strongly between and within animal populations. This can be ascribed to environmental stochasticity or due to individual characteristics of the host such as their age or sex. Other, but understudied, factors are the hosts' behavior and co-infection patterns. In this study, we used the multimammate mouse (Mastomys natalensis) as a model system to investigate how the hosts' sex, age, exploration behavior, and viral infection history affects their infection risk, parasitic load, and community structure of gastrointestinal helminths. We hypothesized that the hosts' exploration behavior would play a key role in the risk for infection by different gastrointestinal helminths, whereby highly explorative individuals would have a higher infection risk leading to a wider diversity of helminths and a larger load compared to less explorative individuals. Fieldwork was performed in Morogoro, Tanzania, where we trapped a total of 214 individual mice. Their exploratory behavior was characterized using a hole-board test after which we collected the helminths inside their gastrointestinal tract. During our study, we found helminths belonging to eight different genera: Hymenolepis sp., Protospirura muricola, Syphacia sp., Trichuris mastomysi, Gongylonema sp., Pterygodermatites sp., Raillietina sp., and Inermicapsifer sp. and one family: Trichostrongylidae. Hierarchical modeling of species communities (HMSC) was used to investigate the effect of the different host-related factors on the infection probability, parasite load, and community structure of these helminths. Our results show that species richness was higher in adults and in females compared to juveniles and males, respectively. Contrary to our expectations, we found that less explorative individuals had higher infection probability with different helminths resulting in a higher diversity, which could be due to a higher exposure rate to these helminths and/or behavioral modification due to the infection.

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.

Nonlinear maternal effects on personality in a rodent species with fluctuating densities.

Consistent among-individual variation in behavior, or animal personality, is present in a wide variety of species. This behavioral variation is maintained by both genetic and environmental factors. Parental effects are a special case of environmental variation and are expected to evolve in populations experiencing large fluctuations in their environment. They represent a non-genetic pathway by which parents can transmit information to their offspring, by modulating their personality. While it is expected that parental effects contribute to the observed personality variation, this has rarely been studied in wild populations. We used the multimammate mouse Mastomys natalensis as a model system to investigate the potential effects of maternal personality on offspring behavior. We did this by repeatedly recording the behavior of individually housed juveniles which were born and raised in the lab from wild caught females. A linear correlation, between mother and offspring in behavior, would be expected when the personality is only affected by additive genetic variation, while a more complex relationship would suggests the presence of maternal effects. We found that the personality of the mother predicted the behavior of their offspring in a non-linear pattern. Exploration behavior of mother and offspring was positively correlated, but only for slow and average exploring mothers, while this correlation became negative for fast exploring mothers. This may suggests that early maternal effects could affect personality in juvenile M. natalensis, potentially due to density-dependent and negative frequency-dependent mechanisms, and therefore contribute to the maintenance of personality variation.

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.

Population cycles and outbreaks of small rodents: ten essential questions we still need to solve.

Most small rodent populations in the world have fascinating population dynamics. In the northern hemisphere, voles and lemmings tend to show population cycles with regular fluctuations in numbers. In the southern hemisphere, small rodents tend to have large amplitude outbreaks with less regular intervals. In the light of vast research and debate over almost a century, we here discuss the driving forces of these different rodent population dynamics. We highlight ten questions directly related to the various characteristics of relevant populations and ecosystems that still need to be answered. This overview is not intended as a complete list of questions but rather focuses on the most important issues that are essential for understanding the generality of small rodent population dynamics.

Feeding behavior and activity of Phlebotomus pedifer and potential reservoir hosts of Leishmania aethiopica in southwestern Ethiopia.

BACKGROUND: Cutaneous leishmaniasis (CL) is a major public health concern in Ethiopia. However, knowledge about the complex zoonotic transmission cycle is limited, hampering implementation of control strategies. We explored the feeding behavior and activity of the vector (Phlebotomus pedifer) and studied the role of livestock in CL transmission in southwestern Ethiopia. METHODS: Blood meal origins of engorged sand flies were determined by sequencing host DNA. A host choice experiment was performed to assess the feeding preference of P. pedifer when humans and hyraxes are equally accessible. Ear and nose biopsies from livestock were screened for the presence of Leishmania parasites. Sand flies were captured indoor and outdoor with human landing catches and CDC light traps to determine at which time and where P. pedifer is mostly active. PRINCIPAL FINDINGS: A total of 180 P. pedifer sand flies were found to bite hosts of 12 genera. Humans were the predominant blood meal source indoors (65.9%, p < 0.001), while no significant differences were determined outdoors and in caves. In caves, hyraxes were represented in blood meals equally as humans (45.5% and 42.4%, respectively), but the host choice experiment revealed that sand flies have a significant preference for feeding on hyraxes (p = 0.009). Only a single goat nose biopsy from 412 animal samples was found with Leishmania RNA. We found that P. pedifer is predominantly endophagic (p = 0.003), but occurs both indoors and outdoors. A substantial number of sand flies was active in the early evening, which increased over time reaching its maximum around midnight. CONCLUSION: In contrast to earlier suggestions of exclusive zoonotic Leishmania transmission, we propose that there is also human-to-human transmission of CL in southwestern Ethiopia. Livestock does not play a role in CL transmission and combined indoor and outdoor vector control measures at night are required for efficient vector control.

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.

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.