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.

Shedding dynamics of Morogoro virus, an African arenavirus closely related to Lassa virus, in its natural reservoir host Mastomys natalensis.

Arenaviruses can cause mild to severe hemorrhagic fevers. Humans mainly get infected through contact with infected rodents or their excretions, yet little is known about transmission dynamics within rodent populations. Morogoro virus (MORV) is an Old World arenavirus closely related to Lassa virus with which it shares the same host species Mastomys natalensis. We injected MORV in its host, and sampled blood and excretions at frequent intervals. Infection in adults was acute; viral RNA disappeared from blood after 18 days post infection (dpi) and from excretions after 39 dpi. Antibodies were present from 7 dpi and never disappeared. Neonatally infected animals acquired a chronic infection with RNA and antibodies in blood for at least 3 months. The quantified excretion and antibody patterns can be used to inform mathematical transmission models, and are essential for understanding and controlling transmission in the natural rodent host populations.

Spatial distribution patterns of plague hosts: point pattern analysis of the burrows of great gerbils in Kazakhstan.

AIM: The spatial structure of a population can strongly influence the dynamics of infectious diseases, yet rarely is the underlying structure quantified. A case in point is plague, an infectious zoonotic disease caused by the bacterium Yersinia pestis. Plague dynamics within the Central Asian desert plague focus have been extensively modelled in recent years, but always with strong uniformity assumptions about the distribution of its primary reservoir host, the great gerbil (Rhombomys opimus). Yet, while clustering of this species' burrows due to social or ecological processes could have potentially significant effects on model outcomes, there is currently nothing known about the spatial distribution of inhabited burrows. Here, we address this knowledge gap by describing key aspects of the spatial patterns of great gerbil burrows in Kazakhstan. LOCATION: Kazakhstan. METHODS: Burrows were classified as either occupied or empty in 98 squares of four different sizes: 200 m (side length), 250 m, 500 m and 590-1020 m. We used Ripley's K statistic to determine whether and at what scale there was clustering of occupied burrows, and semi-variograms to quantify spatial patterns in occupied burrows at scales of 250 m to 9 km. RESULTS: Significant spatial clustering of occupied burrows occurred in 25% and 75% of squares of 500 m and 590-1020 m, respectively, but not in smaller squares. In clustered squares, the clustering criterion peaked around 250 m. Semi-variograms showed that burrow density was auto-correlated up to a distance of 7 km and occupied density up to 2.5 km. MAIN CONCLUSIONS: These results demonstrate that there is statistically significant spatial clustering of occupied burrows and that the uniformity assumptions of previous plague models should be reconsidered to assess its significance for plague transmission. This field evidence will allow for more realistic approaches to disease ecology models for both this system and for other structured host populations.

Puumala hantavirus infection alters the odour attractiveness of its reservoir host.

The random-mixing assumptions of many parasite-transmission models are challenged if healthy individuals can alter their behaviour to reduce their risk of infection. Some pathogens reduce the attractiveness of their hosts' excretions, for example, potentially altering contact rates and thus the predicted force of infection for pathogens transmissible by contact with excretions. For bank voles (Myodes glareolus), contact with contaminated urine is an important route of transmission for Puumala hantavirus (PUUV); however, it is not known whether PUUV infection changes the voles' urinary odours or their attractiveness. Here, we use a Y-maze to test whether PUUV infection alters the attractiveness of male bank voles' urine. We presented wild-caught PUUV-free male and female bank voles with PUUV-infected conspecific urine, uninfected urine and a water control, and measured the relative and absolute latency to first visit, number of visits, and total time bank voles spent investigating each treatment over 30 min. PUUV infection significantly altered the bank voles' initial response to conspecific urine, with fewer visits and less time spent close to infected urine relative to uninfected urine, and less total time spent near the infected urine than the uninfected urine or control. These strong preferences weakened over the 30-min trial, however, partly due to a general decline in male activity, and there were no absolute differences between the treatments overall. This suggests that PUUV infection does change the attractiveness of bank vole urine to conspecifics, and we discuss the implications of these results for random-mixing assumptions.

Dangerous liaisons: the predation risks of receiving social signals.

Individuals are at risk when communicating because conspicuous signals attract both conspecifics and eavesdropping predators. This predation cost of communicating has typically been attributed to signalling individuals because of their conspicuous role, and is a core concept within sexual selection and communication ecology. But, if predators are attracted to signals, then receivers, both intended or otherwise, may also find themselves at risk of predation. Here, we review the theoretical basis and empirical evidence that receiving also carries a risk of predation. We distinguish between the risks of receiving and responding to signals, and we argue that receivers of signals that are long lived, are highly predictable in time or place and/or cannot be received quickly are likely to be at greater risk of predation compared to receivers of signals without these properties. We review recent empirical evidence from a variety of taxa that supports the hypothesis that receivers (including heterospecific prey) are aware of these risks and that they modify their behaviour to balance the risks against the benefits of receiving under predation threat. We also discuss the wider implications of risky receiving for receiving and signalling behaviour in prey, as well as for the prey's predators.

Predators are attracted to the olfactory signals of prey.

BACKGROUND: Predator attraction to prey social signals can force prey to trade-off the social imperatives to communicate against the profound effect of predation on their future fitness. These tradeoffs underlie theories on the design and evolution of conspecific signalling systems and have received much attention in visual and acoustic signalling modes. Yet while most territorial mammals communicate using olfactory signals and olfactory hunting is widespread in predators, evidence for the attraction of predators to prey olfactory signals under field conditions is lacking. METHODOLOGY/PRINCIPAL FINDINGS: To redress this fundamental issue, we examined the attraction of free-roaming predators to discrete patches of scents collected from groups of two and six adult, male house mice, Mus domesticus, which primarily communicate through olfaction. Olfactorily-hunting predators were rapidly attracted to mouse scent signals, visiting mouse scented locations sooner, and in greater number, than control locations. There were no effects of signal concentration on predator attraction to their prey's signals. CONCLUSIONS/SIGNIFICANCE: This implies that communication will be costly if conspecific receivers and eavesdropping predators are simultaneously attracted to a signal. Significantly, our results also suggest that receivers may be at greater risk of predation when communicating than signallers, as receivers must visit risky patches of scent to perform their half of the communication equation, while signallers need not.

Interacting effects of predation risk and signal patchiness on activity and communication in house mice.

1. Social signalling can be risky when signals are open to exploitation by eavesdropping predators. Unlike other signal modalities, olfactory signals cannot be 'switched off' in the presence of an eavesdropping predator, leaving receivers of scent signals at an increased risk of predation long after the signaller has moved on. Yet individuals of some olfactorily communicating species appear unwilling to forego the receiving of signals under an increased risk of predation. Foraging theory predicts that predation risk can operate at multiple spatial scales, however, such that prey behaviour should be sensitive to the broader olfactory environment beyond the risks of a single point source of odour. 2. Here, we use the house mouse Mus domesticus to test whether the spatial distribution and overall level of receiving activity varies with the spatial distribution of conspecific scent signals and the risks posed by an eavesdropping predator, the cat Felis catus. We assessed the mice's responses to these risks using overall visitation, activity and scent marking rates at conspecific scented locations (in clumped, random or regular distributions) and the surrounding matrix (non-scented) locations with and without a predator cue (cat urine). We then used univariate and bivariate spatial point pattern analyses to assess behavioural responses (activity) to both treatments across a range of spatial scales. 3. Visitation, activity and scent marking rates were not affected by the predator cue or the spatial distribution of scents. But these non-significant results masked a fine scale anti-predatory response. Mouse activity was significantly more clustered at small scales when in the presence of the predator cue; this response held across all spatial distribution treatments. Mice were also sensitive to the predation risks of clumped scents, and dispersed their activity at intermediate scales significantly more when exposed to the predator cue, than in the control scent treatment. 4. These results suggest that olfactorily communicating species use scale-sensitive anti-predatory behavioural changes to compensate for their increased risks of predation when receiving scent signals. We highlight the importance of examining a variety of scales when investigating predator-prey interactions, and discuss the implications of these findings for behaviourally responsive predators and prey.

Receiving behaviour is sensitive to risks from eavesdropping predators.

Conspicuous signals may attract both intended receivers as well as unintended receivers such as predators. However, signalling individuals are not the only ones at risk when communicating, as the intended receiver may encounter eavesdropping predators that are attracted to the same signals. Here, we show that the house mouse (Mus domesticus) behaviourally responds to social signals (scents) as though receiving carries a risk of predation. We presented mice with their own scents (low social benefit to receiving) and those from an unknown "intruder" (high social benefit to receiving) under high (cat urine added) and low (water added) perceived predation risk. Mice traded-off the potential social benefits of receiving a signal against the costs of potential predator encounter. Receiving rates of both social signals (own and intruder) were high under low predation risk. Mice reduced receiving of both social signals when predation risk was increased; however, the effect was greater for their own low value scent than for the high social value intruder scent. Notably, rates of signalling did not vary with the level of perceived predation risk. Our findings suggest that mice traded-off the potential social benefits of receiving a signal (scent mark) against the costs of potential predator encounter. We suggest that, for some species, the costs of communication are borne more by the receivers than the signallers, and that the influence of risks to receivers on the design of communication systems may have been underestimated.