Exposure of yellow-legged gulls to Toxoplasma gondii along the Western Mediterranean coasts: Tales from a sentinel.

Efficiently tracking and anticipating the dynamics of infectious agents in wild populations requires the gathering of large numbers of samples, if possible at several locations and points in time, which can be a challenge for some species. Testing for the presence of specific maternal antibodies in egg yolks sampled on the colonies could represent an efficient way to quantify the exposure of breeding females to infectious agents, particularly when using an abundant and widespread species, such as the yellow-legged gull (Larus michahellis). We used such an approach to explore spatio-temporal patterns of exposure to Toxoplasma gondii, a pathogenic protozoan responsible of toxoplasmosis in humans and other warm-blooded vertebrates. First, we tested the validity of this approach by exploring the repeatability of the detection of specific antibodies at the egg level using two different immunoassays and at the clutch level using an occupancy model. Then, samples gathered in 15 colonies from France, Spain and Tunisia were analysed using an immunoassay detecting antibodies specifically directed against T. gondii. Prevalence of specific antibodies in eggs was overall high while varying significantly among colonies. These results revealed that T. gondii circulated at a large spatial scale in the western Mediterranean yellow-legged gull population, highlighting its potential role in the maintenance community of this parasite. Additionally, this study illustrates how species commensal to human populations like large gulls can be used as wildlife sentinels for the tracking of infectious agents at the human-wildlife interface, notably by sampling eggs.

Climate mediates the effects of disturbance on ant assemblage structure.

Many studies have focused on the impacts of climate change on biological assemblages, yet little is known about how climate interacts with other major anthropogenic influences on biodiversity, such as habitat disturbance. Using a unique global database of 1128 local ant assemblages, we examined whether climate mediates the effects of habitat disturbance on assemblage structure at a global scale. Species richness and evenness were associated positively with temperature, and negatively with disturbance. However, the interaction among temperature, precipitation and disturbance shaped species richness and evenness. The effect was manifested through a failure of species richness to increase substantially with temperature in transformed habitats at low precipitation. At low precipitation levels, evenness increased with temperature in undisturbed sites, peaked at medium temperatures in disturbed sites and remained low in transformed sites. In warmer climates with lower rainfall, the effects of increasing disturbance on species richness and evenness were akin to decreases in temperature of up to 9°C. Anthropogenic disturbance and ongoing climate change may interact in complicated ways to shape the structure of assemblages, with hot, arid environments likely to be at greatest risk.

Laridae: A neglected reservoir that could play a major role in avian influenza virus epidemiological dynamics.

Avian influenza viruses (AIVs) are of great concern worldwide due to their economic impact and the threat they represent to human health. As wild birds are the natural reservoirs of AIVs, understanding AIV dynamics in different avian taxa is essential for deciphering the epidemiological links between wildlife, poultry and humans. To date, only the Anatidae (ducks, geese and swans) have been widely studied. Here, we aim to shed light on the current state of knowledge on AIVs in Laridae (gulls, terns and kittiwakes) versus that in Anatidae by setting forth four fundamental questions: how, when, where and to which host species are AIVs transmitted? First, we describe ecological differences between Laridae and Anatidae and discuss how they may explain observed contrasts in preferential transmission routes and the evolution of specific AIV subtypes. Second, we highlight the dissimilarities in the temporal patterns of AIV shedding between Laridae and Anatidae and address the role that immunity likely plays in shaping these patterns. Third, we underscore that Laridae may be key in promoting intercontinental exchanges of AIVs. Finally, we emphasize the crucial epidemiological position that Laridae occupy between wildlife, domestic birds and humans.

Egg sampling as a possible alternative to blood sampling when monitoring the exposure of yellow-legged gulls (Larus michahellis) to avian influenza viruses.

We explored whether antibody detection in egg yolks could serve as an alternative to antibody detection in plasma samples when monitoring yellow-legged gulls (Larus michahellis) for exposure to avian influenza viruses (AIVs). We tested female plasma and eggs for anti-AIV antibodies and used the data we obtained to check whether the two sample types yielded the same antibody status (positive or negative) and to compare the antibody prevalence estimated from the blood data with that estimated from the yolk data. Our results showed that sampling one egg per clutch, regardless of that egg's position in the laying sequence, is sufficient to provide an unbiased estimate of antibody prevalence across clutches. The results also showed that almost 25% of the clutches laid by positive females contained only antibody-negative eggs, which suggests that yolk samples might underestimate female antibody prevalence. However, this result may stem from differences in the methods used to assess plasma versus yolk antibody status. Further research is needed to clarify this issue; while the number of false negatives could be reduced by adapting antibody detection techniques, it may be that they are an unavoidable consequence of natural avian maternal transfer dynamics.

Circulation of a Meaban-like virus in yellow-legged gulls and seabird ticks in the western Mediterranean basin.

In recent years, a number of zoonotic flaviviruses have emerged worldwide, and wild birds serve as their major reservoirs. Epidemiological surveys of bird populations at various geographical scales can clarify key aspects of the eco-epidemiology of these viruses. In this study, we aimed at exploring the presence of flaviviruses in the western Mediterranean by sampling breeding populations of the yellow-legged gull (Larus michahellis), a widely distributed, anthropophilic, and abundant seabird species. For 3 years, we sampled eggs from 19 breeding colonies in Spain, France, Algeria, and Tunisia. First, ELISAs were used to determine if the eggs contained antibodies against flaviviruses. Second, neutralization assays were used to identify the specific flaviviruses present. Finally, for colonies in which ELISA-positive eggs had been found, chick serum samples and potential vectors, culicid mosquitoes and soft ticks (Ornithodoros maritimus), were collected and analyzed using serology and PCR, respectively. The prevalence of flavivirus-specific antibodies in eggs was highly spatially heterogeneous. In northeastern Spain, on the Medes Islands and in the nearby village of L'Escala, 56% of eggs had antibodies against the flavivirus envelope protein, but were negative for neutralizing antibodies against three common flaviviruses: West Nile, Usutu, and tick-borne encephalitis viruses. Furthermore, little evidence of past flavivirus exposure was obtained for the other colonies. A subset of the Ornithodoros ticks from Medes screened for flaviviral RNA tested positive for a virus whose NS5 gene was 95% similar to that of Meaban virus, a flavivirus previously isolated from ticks of Larus argentatus in western France. All ELISA-positive samples subsequently tested positive for Meaban virus neutralizing antibodies. This study shows that gulls in the western Mediterranean Basin are exposed to a tick-borne Meaban-like virus, which underscores the need of exploring the spatial and temporal distribution of this flavivirus as well as its potential pathogenicity for animals and humans.

The effects of fire on ant trophic assemblage and sex allocation.

Fire plays a key role in ecosystem dynamics worldwide, altering energy flows and species community structure and composition. However, the functional mechanisms underlying these effects are not well understood. Many ground-dwelling animal species can shelter themselves from exposure to heat and therefore rarely suffer direct mortality. However, fire-induced alterations to the environment may change a species' relative trophic level within a food web and its mode of foraging. We assessed how fire could affect ant resource utilization at different scales in a Mediterranean forest. First, we conducted isotopic analyses on entire ant species assemblages and their potential food resources, which included plants and other arthropods, in burned and unburned plots 1 year postfire. Second, we measured the production of males and females by nests of a fire-resilient species, Aphaenogaster gibbosa, and analyzed the differences in isotopic values among workers, males, and females to test whether fire constrained resource allocation. We found that, in spite of major modifications in biotic and abiotic conditions, fire had little impact on the relative trophic position of ant species. The studied assemblage was composed of species with a wide array of diets. They ranged from being mostly herbivorous to completely omnivorous, and a given species' trophic level was the same in burned and unburned plots. In A. gibbosa nests, sexuals had greater δ(15)N values than workers in both burned and unburned plots, which suggests that the former had a more protein-rich diet than the latter. Fire also appeared to have a major effect on A. gibbosa sex allocation: The proportion of nests that produced male brood was greater on burned zones, as was the mean number of males produced per nest with the same reproductive investment. Our results show that generalist ants with relatively broad diets maintained a constant trophic position, even following a major disturbance like fire. However, the dramatically reduced production of females on burned zones compared to unburned zones 1 year postfire may result in considerably reduced recruitment of new colonies in the mid to long term, which could yield genetic bottlenecks and founder effects. Our study paves the way for future functional analyses of fire-induced modifications in ant populations and communities.

Maternal antibody transmission in relation to mother fluctuating asymmetry in a long-lived colonial seabird: the yellow-legged gull Larus michahellis.

Female birds transfer antibodies to their offspring via the egg yolk, thus possibly providing passive immunity against infectious diseases to which hatchlings may be exposed, thereby affecting their fitness. It is nonetheless unclear whether the amount of maternal antibodies transmitted into egg yolks varies with female quality and egg laying order. In this paper, we investigated the transfer of maternal antibodies against type A influenza viruses (anti-AIV antibodies) by a long-lived colonial seabird, the yellow-legged gull (Larus michahellis), in relation to fluctuating asymmetry in females, i.e. the random deviation from perfect symmetry in bilaterally symmetric morphological and anatomical traits. In particular, we tested whether females with greater asymmetry transmitted fewer antibodies to their eggs, and whether within-clutch variation in yolk antibodies varied according to the maternal level of fluctuating asymmetry. We found that asymmetric females were in worse physical condition, produced fewer antibodies, and transmitted lower amounts of antibodies to their eggs. We also found that, within a given clutch, yolk antibody level decreased with egg laying order, but this laying order effect was more pronounced in clutches laid by the more asymmetric females. Overall, our results support the hypothesis that maternal quality interacts with egg laying order in determining the amount of maternal antibodies transmitted to the yolks. They also highlight the usefulness of fluctuating asymmetry as a sensitive indicator of female quality and immunocompetence in birds.

Assembling an ant community: species functional traits reflect environmental filtering.

Species should only persist in local communities if they have functional traits that are compatible with habitat-specific environmental conditions. Consequently, pronounced regional environmental gradients should produce environmental filtering, or a trait-based spatial segregation of species. It is critical to quantify the links between species' functional traits and their environment in order to reveal the relative importance of this process to community assembly and promote understanding of the impacts of ongoing environmental changes. We investigated this relationship using epigaeic ants in an environmentally heterogeneous region of Florida. We found evidence for environmental filtering as environmental conditions such as groundcover, surface temperature, vapor pressure deficit, and plant diversity were strongly correlated with assemblage composition. Certain species traits appeared particularly important to persistence: (1) ants in environments with less groundcover have relatively longer legs but do not differ in size, (2) ants in hotter environments exhibit greater thermal tolerances, and (3) ants in hotter and drier environments do not exhibit greater desiccation resistance. These findings show surface complexity and temperature may interact with morphology and physiology to impact the spatial distribution of ants and underscore the importance of climate change. Climate warming is predicted to alter assemblage composition, competitive dynamics, and consequently impact ecosystem processes. We suggest environmental filters acting at regional scales, as shown here, act in tandem with more frequently studied local-scale competitive interactions to delimit ant community assemblages.

Prevalence of influenza A antibodies in yellow-legged gull (Larus michahellis) eggs and adults in southern Tunisia.

Investigating the prevalence of anti-influenza A viruses (AIV) antibodies in wild birds can provide important information for the understanding of bird exposure to AIV, as well as for prevention purposes. We investigated AIV exposure in nature by measuring the prevalence of anti-AIV antibodies in the nests and adults of an abundant and anthropophilic waterbird species common around the Mediterranean sea, the yellow-legged gull (Larus michahellis). Sampling took place in two colonies located in the gulf of Gabès in southern Tunisia: Sfax and Djerba. Antibodies were detected in the two sites, with higher prevalence in adults, eggs, and nests at Sfax than Djerba. Across both colonies, clutches that were laid later in the season, and, thus, more likely by younger parents, showed lower prevalence. Using patch occupancy modeling applied to egg clutches, we found that it is unnecessary to sample all the eggs in a given nest; nest status (antibody positive or negative) can be reliably estimated from a single egg. Differences in the density of birds, notably Larids, between the two sites may explain the observed differences in prevalence. The higher concentration of Larids in the Sfax colony could favor the transmission of AIV to yellow-legged gulls. This study highlights the importance of further developing ecological-based approaches to the factors determining the circulation of infectious agents in species such as the yellow-legged gull, which exist at the interface between diverse biological communities and human activities.

Seabirds and the circulation of Lyme borreliosis bacteria in the North Pacific.

Seabirds act as natural reservoirs to Lyme borreliosis spirochetes and may play a significant role in the global circulation of these pathogens. While Borrelia burgdorferi sensu lato (Bbsl) has been shown to occur in ticks collected from certain locations in the North Pacific, little is known about interspecific differences in exposure within the seabird communities of this region. We examined the prevalence of anti-Bbsl antibodies in 805 individuals of nine seabird species breeding across the North Pacific. Seroprevalence varied strongly among species and locations. Murres (Uria spp.) showed the highest antibody prevalence and may play a major role in facilitating Bbsl circulation at a worldwide scale. Other species showed little or no signs of exposure, despite being present in multispecific colonies with seropositive birds. Complex dynamics may be operating in this wide scale, natural host-parasite system, possibly mediated by the host immune system and host specialization of the tick vector.

Fast food in ant communities: how competing species find resources.

An understanding of foraging behavior is crucial to understanding higher level community dynamics; in particular, there is a lack of information about how different species discover food resources. We examined the effect of forager number and forager discovery capacity on food discovery in two disparate temperate ant communities, located in Texas and Arizona. We defined forager discovery capacity as the per capita rate of resource discovery, or how quickly individual ants arrived at resources. In general, resources were discovered more quickly when more foragers were present; this was true both within communities, where species identity was ignored, as well as within species. This pattern suggests that resource discovery is a matter of random processes, with ants essentially bumping into resources at a rate mediated by their abundance. In contrast, species that were better discoverers, as defined by the proportion of resources discovered first, did not have higher numbers of mean foragers. Instead, both mean forager number and mean forager discovery capacity determined discovery success. The Texas species used both forager number and capacity, whereas the Arizona species used only forager capacity. There was a negative correlation between a species' prevalence in the environment and the discovery capacity of its foragers, suggesting that a given species cannot exploit both high numbers and high discovery capacity as a strategy. These results highlight that while forager number is crucial to determining time to discovery at the community level and within species, individual forager characteristics influence the outcome of exploitative competition in ant communities.

Roles of human disturbance, precipitation, and a pathogen on the survival and reproductive probabilities of deer mice.

Climate change, human disturbance, and disease can have large impacts on the dynamics of a species by affecting the likelihood of survival and reproduction of individuals. We investigated the roles of precipitation, off-road vehicle (ORV) alteration of habitat, and infection with Sin Nombre virus on the survival and reproductive probabilities of deer mice (Peromyscus maniculatus). We used generalized linear mixed models to estimate the effects of these factors and their interactions by fitting capture-recapture data collected seasonally from 2002 to 2007 at 17 sites in the Great Basin Desert of central Utah, USA. During periods with high precipitation, we found no difference in survival and reproductive probabilities between seasons, but during drier periods, we found a reduction of overwinter survival and fall reproductive activity. Precipitation also interacted with disturbance to affect survival probabilities and female reproduction; in periods with low precipitation, deer mice on highly disturbed sites had extremely low survival probabilities and low reproductive probabilities of females compared to those of individuals from low-disturbance sites. However, high precipitation ameliorated the effect of disturbance on both parameters. Deer mice from sites with high impact of ORV disturbance also had low survival over summer. Additionally, male reproductive probabilities were diminished on highly disturbed sites in both seasons; in contrast, they were reduced only in the fall on low-disturbance sites. Density had an overall negative effect on survival and reproductive probabilities of deer mice. For females, the negative effect on reproductive activity was amplified in highly disturbed sites. We found no effect of hantavirus infection on survival probabilities of deer mice. Overall, this study revealed complexity in the determinants of deer mouse survival and reproduction given by the effects of a number of significant interactions among explanatory variables. Thus, factors that may not appear to have a strong effect when investigated alone can still be influential by modulating the effect of a different factor.

How host population dynamics translate into time-lagged prevalence: an investigation of Sin Nombre virus in deer mice.

Human cases of hantavirus pulmonary syndrome caused by Sin Nombre virus are the endpoint of complex ecological cascade from weather conditions, population dynamics of deer mice, to prevalence of SNV in deer mice. Using population trajectories from the literature and mathematical modeling, we analyze the time lag between deer mouse population peaks and peaks in SNV antibody prevalence in deer mice. Because the virus is not transmitted vertically, rapid population growth can lead initially to reduced prevalence, but the resulting higher population size may later increase contact rates and generate increased prevalence. Incorporating these factors, the predicted time lag ranges from 0 to 18 months, and takes on larger values when host population size varies with a longer period or higher amplitude, when mean prevalence is low and when transmission is frequency-dependent. Population size variation due to variation in birth rates rather than death rates also increases the lag. Predicting future human outbreaks of hantavirus pulmonary syndrome may require taking these effects into account.

Differential regulation of pathogens: the role of habitat disturbance in predicting prevalence of Sin Nombre virus.

Deer mice (Peromyscus maniculatus) are the primary reservoir for Sin Nombre virus (SNV), a North American hantavirus that causes disease with high mortality in humans. Recent studies have proposed that habitat disturbance affects prevalence of SNV in deer mice; however, the outcomes proposed in these studies are in opposition to each other. Our objectives were to test these divergent hypotheses by: (1) measuring SNV infection in deer mice within a patchwork of disturbance; and (2) evaluating the relationships between SNV prevalence, population density and demography as possible mechanisms. In 2003 and 2004, we sampled 1,297 deer mice from 17 sites with varying levels of disturbance in the Great Basin Desert. Across sites and years, SNV prevalence varied from 0.0 to 38.9%. We found a negative relationship between SNV prevalence and disturbance. Although we found no direct relationship between SNV prevalence and deer mouse density, we found that density was highest on sites with the lowest levels of disturbance. The number of deer mice that survived across seasons (e.g., trans-seasonal survivors) differed across levels of disturbance and was greatest on our least disturbed study sites [Formula: see text] moderate on sites with intermediate levels of disturbance (x = 5.61%) and zero on highly disturbed sites. On low-disturbance sites, a greater proportion of trans-seasonal survivors were SNV seropositive (28.80%) compared to the intermediate-disturbance sites (16.67). Collectively, our results indicate that habitat disturbance plays a predictive role in SNV prevalence, with highly disturbed sites having reduced long-term survival of deer mice, including survival of infected individuals.

The origin of human pathogens: evaluating the role of agriculture and domestic animals in the evolution of human disease.

Many significant diseases of human civilization are thought to have arisen concurrently with the advent of agriculture in human society. It has been hypothesised that the food produced by farming increased population sizes to allow the maintenance of virulent pathogens, i.e. civilization pathogens, while domestic animals provided sources of disease to humans. To determine the relationship between pathogens in humans and domestic animals, I examined phylogenetic data for several human pathogens that are commonly evolutionarily linked to domestic animals: measles, pertussis, smallpox, tuberculosis, taenid worms, and falciparal malaria. The majority are civilization pathogens, although I have included others whose evolutionary origins have traditionally been ascribed to domestic animals. The strongest evidence for a domestic-animal origin exists for measles and pertussis, although the data do not exclude a non-domestic origin. As for the other pathogens, the evidence currently available makes it difficult to determine if the domestic-origin hypothesis is supported or refuted; in fact, intriguing data for tuberculosis and taenid worms suggests that transmission may occur as easily from humans to domestic animals. These findings do not abrogate the importance of agriculture in disease transmission; rather, if anything, they suggest an alternative, more complex series of effects than previously elucidated. Rather than domestication, the broader force for human pathogen evolution could be ecological change, namely anthropogenic modification of the environment. This is supported by evidence that many current emerging infectious diseases are associated with human modification of the environment. Agriculture may have changed the transmission ecology of pre-existing human pathogens, increased the success of pre-existing pathogen vectors, resulted in novel interactions between humans and wildlife, and, through the domestication of animals, provided a stable conduit for human infection by wildlife diseases.

Changes in sin nombre virus antibody prevalence in deer mice across seasons: the interaction between habitat, sex, and infection in deer mice.

We examined the impact of season and habitat on Sin Nombre virus (SNV) seroprevalence in deer mice (Peromyscus maniculatus) in Utah's Great Basin Desert from May 2002 through summer 2003. Low mouse captures in 2002 limited analysis for that year. In two seasons during 2003, mouse density and sagebrush cover were positively linked (spring: r = 0.8, P = 0.01; summer: r = 0.8, P = 0.04). In the spring, seroprevalence was negatively correlated with density (r = -0.9, P< 0.01); male and female antibody prevalence did not differ; and scarring was unrelated to antibody status. In the summer, density and antibody prevalence were unrelated; male seroprevalence was higher (chi(2) = 3.6, P = 0.05); and seropositive mice had more scars (t = 2.5, P = 0.02). We speculate nesting behavior could maintain SNV over the winter, whereas summer territoriality could be responsible for transmission.