Changing landscapes of Southeast Asia and rodent-borne diseases: decreased diversity but increased transmission risks.

The reduction in biodiversity from land use change due to urbanization and agricultural intensification appears to be linked to major epidemiological changes in many human diseases. Increasing disease risks and the emergence of novel pathogens result from increased contact among wildlife, domesticated animals, and humans. We investigated the relationship between human alteration of the environment and the occurrence of generalist and synanthropic rodent species in relation to the diversity and prevalence of rodent-borne pathogens in Southeast Asia, a hotspot of threatened and endangered species, and a foci of emerging infectious diseases. We used data from an extensive pathogen survey of rodents from seven sites in mainland Southeast Asia in conjunction with past and present land cover analyses. At low spatial resolutions, we found that rodent-borne pathogen richness is negatively associated with increasing urbanization, characterized by increased habitat fragmentation, agriculture cover and deforestation. However, at a finer spatial resolution, we found that some major pathogens are favored by environmental characteristics associated with human alteration including irrigation, habitat fragmentation, and increased agricultural land cover. In addition, synanthropic rodents, many of which are important pathogen reservoirs, were associated with fragmented and human-dominated landscapes, which may ultimately enhance the opportunities for zoonotic transmission and human infection by some pathogens.

Habitat fragmentation alters the properties of a host-parasite network: rodents and their helminths in South-East Asia.

1. While the effects of deforestation and habitat fragmentation on parasite prevalence or richness are well investigated, host-parasite networks are still understudied despite their importance in understanding the mechanisms of these major disturbances. Because fragmentation may negatively impact species occupancy, abundance and co-occurrence, we predict a link between spatiotemporal changes in habitat and the architecture of host-parasite networks. 2. For this, we used an extensive data set on 16 rodent species and 29 helminth species from seven localities of South-East Asia. We analysed the effects of rapid deforestation on connectance and modularity of helminth-parasite networks. We estimated both the degree of fragmentation and the rate of deforestation through the development of land uses and their changes through the last 20 to 30 years in order to take into account the dynamics of habitat fragmentation in our statistical analyses. 3. We found that rapid fragmentation does not affect helminth species richness per se but impacts host-parasite interactions as the rodent-helminth network becomes less connected and more modular. 4. Our results suggest that parasite sharing among host species may become more difficult to maintain with the increase of habitat disturbance.

Helminth parasite species richness in rodents from Southeast Asia: role of host species and habitat.

Southeast Asia is a biodiversity hotspot that harbours many species of rodents, including some that live in close contact with humans. They host helminth parasites, some of which are of zoonotic importance. It is therefore important to understand the factors that influence the richness of the helminths parasitizing rodents. The specific objectives of this study were to evaluate rodent species as a factor determining helminth richness in rodent assemblages, to identify the major rodent helminth reservoir species and to explore the influence of habitat on helminth richness. We estimated helminth species richness using a large dataset of 18 rodent species (1,651 individuals) originating from Southeast Asia and screened for helminth parasites. The use of an unbiased estimator shows that the helminth species richness varies substantially among rodent species and across habitats. We confirmed this pattern by investigating the number of helminth species per individual rodent in all rodent species, and specifically in the two mitochondrial lineages Rattus tanezumi and R. tanezumi R3, which were captured in all habitats.

Is there sex-biased resistance and tolerance in Mediterranean wood mouse (Apodemus sylvaticus) populations facing multiple helminth infections?

Sex-biased parasitism is rarely investigated in relation to host tolerance and resistance, which are two defense strategies hosts can adopt when challenged by parasites. Health or fitness deteriorations in less tolerant individuals with increasing parasite burden would be faster than those in more tolerant ones. Hence, the body condition and reproductive potential of an infected individual host can be considered proxies for tolerance to parasitism. We studied Mediterranean populations of the wood mouse (Apodemus sylvaticus) and its helminth parasites. We assessed their resistance using the phytohemagglutinin test and spleen size, and their tolerance using body condition in males and females and testes mass in males. In order to avoid spurious correlations, we took into account the phylogeographic structure of the Mediterranean wood mouse populations. We used a mixed model adapted from the animal model used in quantitative genetics. While helminth infection did not differ between the two sexes, females and males differed in their measured defenses. Females seem to invest more in immune defense with increasing risk of parasite diversity, but also appear to be potentially more tolerant of parasitic diversity. These results suggest the existence of sexual differences in resistance and tolerance, and that measurements of parasitic loads alone could be insufficient to detect any underlying sexual differences in the two strategies that have evolved in response to multiple parasitic attacks.

Does investment into "expensive" tissue compromise anti-parasitic defence? Testes size, brain size and parasite diversity in rodent hosts.

Species richness of parasite assemblages varies among host species. Earlier studies that searched for host-related determinants of parasite diversity mainly considered host traits that affect the probability of host encounter with parasites, whereas host traits related to defensibility against parasites have rarely been investigated. From the latter perspective, evolutionary investment in "expensive" tissue or organs (like testes or brain) may trade off against energetically costly anti-parasitic defences. If so, richer parasite assemblages are expected in hosts with larger testes and brains. We studied the relationships between testes and brain size and diversity of parasites (fleas, gamasid mites and helminths) in 55 rodent species using a comparative approach and application of two methods, namely the method of independent contrasts and generalized least-squares (GLS) analysis. Both phylogenetically correct methods produced similar results for flea and helminth species richness. Testes size positively correlated with flea and helminth species richness but not gamasid mite species richness. No correlation between brain size and species richness of any parasite group was found by the method of independent contrasts. However, GLS analysis indicated negative correlation between brain size and mite species richness. Our results cast doubt on the validity of the expensive tissue hypothesis, but suggest instead that larger testes are associated with higher parasite diversity via their effect on mobility and/or testosterone-mediated immunosuppression.

Human-dominated habitats and helminth parasitism in Southeast Asian murids.

The effect of habitat anthropization is investigated using a comparative analysis based on a literature survey of the gastrointestinal helminths of murid rodents described in Southeast Asia (SEA). The literature survey gave 30 references on helminth diversity concerning 20 murid rodent species. The diversity of helminths was high with a total of 13 species of cestodes, 15 species of trematodes, 29 species of nematodes and one species of acanthocephalans. The highest helminth species richness was found in Rattus tanezumi, Rattus norvegicus and Rattus argentiventer, all these species were found in more human-dominated habitats (agricultural areas or human settlements). Helminth species richness was positively linked across rodent species to the level of the anthropization of the host environment from forests, agricultural areas to human settlements.

Home range and parasite diversity in mammals.

Parasite diversity among and within host species is not solely the result of random processes; rather, it depends on a suite of physiological or ecological host traits as well as environmental factors. Because most macroparasites exhibit life cycles that include infective stages off the definitive host and that rely on host movements for dissemination, parasite acquisition by a host depends largely on hosts being present in a given area where and when infective stages are present. Consequently, host ranging pattern may have a major influence on parasite diversity. Larger home range size is hypothesized to be associated with higher parasite species richness because hosts living in large home ranges should encounter a greater diversity of habitats and other host individuals, which in turn may favor infection by a great diversity of parasite species. By focusing on helminths in wild mammals, we show that an increase in home range area does not lead to an increase in parasite diversity in ungulates and, moreover, that it is associated with a decrease in parasite species richness in carnivores and in glires (rodents and lagomorphs). We also show that home range size is negatively correlated with host density in mammals after correcting both variables for host body mass. We discuss these results from an epidemiological perspective.

Coevolution between multiple helminth infestations and basal immune investment in mammals: cumulative effects of polyparasitism?

Animals often suffer from multiple parasite attacks in natural conditions (i.e., polyparasitism). The community of these parasites, which simultaneously or sequentially infest given host species, has rarely been investigated as a parasitic pressure per se. From this perspective, and despite the impressive number of immunoecological or comparative studies, the impacts of polyparasitism on immune responses are far from being appreciated. Focusing on helminths across a wide range of mammalian species and using a phylogenetic comparative method, we show, for the first time, that an increase in the number of helminth parasite species is positively correlated with an increase in basal immune investment (estimated by the counts of white blood cells) across mammal species. After discussing inherent limits of this comparative approach, we put this result in the evolutionary perspective of multiple parasitic infestations.

Helminth communities of an introduced hare (Lepus granatensis) and a native hare (Lepus europaeus) in southern France.

We investigated the parasite communities of introduced Iberian hares (Lepus granatensis) and native European hares (Lepus europaeus) in southern France, where Iberian hares were introduced locally 20 yr ago as a game animal. Parasite communities of sympatric populations of the two hare species and of allopatric populations of European hares were compared. Iberian hares in France harbored a depauperate community of parasites relative to the population in its native habitat in Spain. European hares in areas of sympatry also were infected by Nematodiroides zembrae, which normally infects Iberian hares on their native range.

Transmission ecology of rodent-borne diseases: New frontiers.

Rodents are recognized reservoir hosts for many human zoonotic pathogens. The current trends resulting from anthropocene defaunation suggest that in the future they, along with other small mammals, are likely to become the dominant mammals in almost all human-modified environments. Recent intricate studies on bat-borne emerging diseases have highlighted that many gaps exist in our understanding of the zoonotic transmission of rodent-borne pathogens. This has emphasized the need for scientists interested in rodent-borne diseases to integrate rodent ecology into their analysis of rodent-borne pathogen transmission in order to identify in more detail the mechanisms of spillover and chains of transmission. Further studies are required to better understand the true impact of rodent abundance and the importance of pathogen sharing and circulation in multi-host- multi-pathogen communities. We also need to explore in more depth the roles of generalist and abundant species as the potential links between pathogen-sharing, co-infections and disease transmission.

Global parasite and Rattus rodent invasions: The consequences for rodent-borne diseases.

We summarize the current knowledge on parasitism-related invasion processes of the globally invasive Rattus lineages, originating from Asia, and how these invasions have impacted the local epidemiology of rodent-borne diseases. Parasites play an important role in the invasion processes and successes of their hosts through multiple biological mechanisms such as "parasite release," "immunocompetence advantage," "biotic resistance" and "novel weapon." Parasites may also greatly increase the impact of invasions by spillover of parasites and other pathogens, introduced with invasive hosts, into new hosts, potentially leading to novel emerging diseases. Another potential impact is the ability of the invader to amplify local parasites by spillback. In both cases, local fauna and humans may be exposed to new health risks, which may decrease biodiversity and potentially cause increases in human morbidity and mortality. Here we review the current knowledge on these processes and propose some research priorities.

The diversity of microparasites of rodents: a comparative analysis that helps in identifying rodent-borne rich habitats in Southeast Asia.

BACKGROUND: Predicting habitats prone to favor disease transmission is challenging due to confounding information on habitats, reservoirs, and diseases. Comparative analysis, which aims at investigating ecological and evolutionary patterns among species, is a tool that may help. The emergence of zoonotic pathogens is a major health concern and is closely linked to habitat modifications by human activities. Risk assessment requires a better knowledge of the interactions between hosts, parasites, and the landscape. METHODS: We used information from a field spatial study that investigated the distribution of murid rodents, in various habitats of three countries in Southeast Asia, in combination with their status of infection by 10 taxa of microparasites obtained from the literature. Microparasite species richness was calculated by rodent species on 20,272 rodents of 13 species. Regression tree models and generalized linear models were used to explain microparasite diversity by the average distance between the trapping site and five categories of land cover: forest, steep agriculture land, flat agriculture land, water, and built-up surfaces. Another variable taken into account was the slope. RESULTS: We found that microparasite diversity was positively associated with flat agriculture land, in this context mainly rice fields, and negatively associated with slope. Microparasite diversity decreased sharply a 100 m or less from flat agriculture land. CONCLUSION: We conclude that there is high microparasite circulation in rodents of flooded farmlands, meaning possibly a higher risk of disease for human inhabitants.

Rodent-borne diseases in Thailand: targeting rodent carriers and risky habitats.

BACKGROUND: Comparative analysis, which aims at investigating ecological and evolutionary patterns among species, may help at targeting reservoirs of zoonotic diseases particularly in countries presenting high biodiversity. Here, we developed a simple method to target rodent reservoirs using published studies screening microparasite infections. METHODS: We compiled surveys of microparasites investigated in rodents trapped in Thailand. The data comprise a total of 17,358 rodents from 18 species that have been investigated for a total of 10 microparasites (viruses, bacteria and protozoans). We used residual variation of microparasite richness controlled for both rodent sample size and pathogens' screening effort to identify major rodent reservoirs and potential risky habitats. RESULTS: Microparasite species richness was positively related to rodent sample size and pathogens' screening effort. The investigation of the residual variations of microparasite species richness showed that several rodent species harboured more pathogens than expected by the regression model. Similarly, higher pathogen richness than expected was observed in rodents living in non-flooded lands, forests and paddy fields. CONCLUSION: Our results suggest to target some rodent species that are not commonly investigated for pathogen screening or surveillance such as R. adamanensis or B. savilei, and that non-flooded lands and forests should be more taken into caution, whereas much surveys focused on paddy rice fields and households.

The impact of multiple infections on wild animal hosts: a review.

Field parasitological studies consistently demonstrate the reality of polyparasitism in natural systems. However, only recently, studies from ecological and evolutionary fields have emphasised a broad spectrum of potential multiple infections-related impacts. The main goal of our review is to reunify the different approaches on the impacts of polyparasitism, not only from laboratory or human medical studies but also from field or theoretical studies. We put forward that ecological and epidemiological determinants to explain the level of polyparasitism, which regularly affects not only host body condition, survival or reproduction but also host metabolism, genetics or immune investment. Despite inherent limitations of all these studies, multiple infections should be considered more systematically in wildlife to better appreciate the importance of parasite diversity in wildlife, cumulative effects of parasitism on the ecology and evolution of their hosts.

Bat fly species richness in Neotropical bats: correlations with host ecology and host brain.

Patterns of ectoparasite species richness in mammals have been investigated in various terrestrial mammalian taxa such as primates, ungulates and carnivores. Several ecological or life traits of hosts are expected to explain much of the variability in species richness of parasites. In the present comparative analysis we investigate some determinants of parasite richness in bats, a large and understudied group of flying mammals, and their obligate blood-sucking ectoparasite, streblid bat flies (Diptera). We investigate the effects of host body size, geographical range, group size and roosting ecology on the species richness of bat flies in tropical areas of Venezuela and Peru, where both host and parasite diversities are high. We use the data from a major sampling effort on 138 bat species from nine families. We also investigate potential correlation between bat fly species richness and brain size (corrected for body size) in these tropical bats. We expect a relationship if there is a potential energetic trade-off between costly large brains and parasite-mediated impacts. We show that body size and roosting in cavities are positively correlated with bat fly species richness. No effects of bat range size and group size were observed. Our results also suggest an association between body mass-independent brain size and bat fly species richness.

Rodent sociality and parasite diversity.

The risk of parasitism is considered to be a general cost of sociality and individuals living in larger groups are typically considered to be more likely to be infected with parasites. However, contradictory results have been reported for the relationship between group size and infection by directly transmitted parasites. We used independent contrasts to examine the relationship between an index of sociality in rodents and the diversity of their macroparasites (helminths and arthropods such as fleas, ticks, suckling lice and mesostigmatid mites). We found that the species richness of directly transmitted ectoparasites, but not endoparasites, decreased significantly with the level of rodent sociality. A greater homogeneity in the biotic environment (i.e. a reduced number of cohabiting host species) of the more social species may have reduced ectoparasites' diversity by impairing ectoparasites transmission and exchange. Our finding may also result from beneficial outcomes of social living that include behavioural defences, like allogrooming, and the increased avoidance of parasites through dilution effects.