Specialized avian Haemosporida trade reduced host breadth for increased prevalence

Parasite specialization on one or a few host species leads to a reduction in the total number of available host individuals, which may decrease transmission. However, specialists are thought to be able to compensate by increased prevalence in the host population and increased success in each individual host. Here, we use variation in host breadth among a community of avian Haemosporida to investigate consequences of generalist and specialist strategies on prevalence across hosts. We show that specialist parasites are more prevalent than generalist parasites in host populations that are shared between them. Moreover, the total number of infections of generalist and specialist parasites within the study area did not vary significantly with host breadth. This suggests that specialists can infect a similar number of host individuals as generalists, thus compensating for a reduction in host availability by achieving higher prevalence in a single host species. Specialist parasites also tended to infect older hosts, whereas infections by generalists were biased towards younger hosts. We suggest that this reflects different abilities of generalists and specialists to persist in hosts following infection. Higher abundance and increased persistence in hosts suggest that specialists are more effective parasites than generalists, supporting the existence of a trade‐off between host breadth and average host use among these parasites.     

Global warming will reshuffle the areas of high prevalence and richness of three genera of avian blood parasites

The importance of parasitism for host populations depends on local parasite richness and prevalence: usually host individuals face higher infection risk in areas where parasites are most diverse, and host dispersal to or from these areas may have fitness consequences. Knowing how parasites are and will be distributed in space and time (in a context of global change) is thus crucial from both an ecological and a biological conservation perspective. Nevertheless, most research articles focus just on elaborating models of parasite distribution instead of parasite diversity. We produced distribution models of the areas where haemosporidian parasites are currently highly diverse (both at community and at within‐host levels) and prevalent among Iberian populations of a model passerine host: the blackcap Sylvia atricapilla; and how these areas are expected to vary according to three scenarios of climate change. On the basis of these models, we analysed whether variation among populations in parasite richness or prevalence are expected to remain the same or change in the future, thereby reshuffling the geographic mosaic of host‐parasite interactions as we observe it today. Our models predict a rearrangement of areas of high prevalence and richness of parasites in the future, with Haemoproteus and Leucocytozoon parasites (today the most diverse genera in blackcaps) losing areas of high diversity and Plasmodium parasites (the most virulent ones) gaining them. Likewise, the prevalence of multiple infections and parasite infracommunity richness would be reduced. Importantly, differences among populations in the prevalence and richness of parasites are expected to decrease in the future, creating a more homogeneous parasitic landscape. This predicts an altered geographic mosaic of host‐parasite relationships, which will modify the interaction arena in which parasite virulence evolves.     

Host species,and not environment,predicts variation in blood parasite prevalence,distribution, and diversity along a humidity gradient in northern South America

Environmental factors strongly influence the ecology and evolution of vector‐borne infectious diseases. However, our understanding of the influence of climatic variation on host–parasite interactions in tropical systems is rudimentary. We studied five species of birds and their haemosporidian parasites (Plasmodium and Haemoproteus) at 16 sampling sites to understand how environmental heterogeneity influences patterns of parasite prevalence, distribution, and diversity across a marked gradient in water availability in northern South America. We used molecular methods to screen for parasite infections and to identify parasite lineages. To characterize spatial heterogeneity in water availability, we used weather‐station and remotely sensed climate data. We estimated parasite prevalence while accounting for spatial autocorrelation, and used a model selection approach to determine the effect of variables related to water availability and host species on prevalence. The prevalence, distribution, and lineage diversity of haemosporidian parasites varied among localities and host species, but we found no support for the hypothesis that the prevalence and diversity of parasites increase with increasing water availability. Host species and host × climate interactions had stronger effects on infection prevalence, and parasite lineages were strongly associated with particular host species. Because climatic variables had little effect on the overall prevalence and lineage diversity of haemosporidian parasites across study sites, our results suggest that independent host–parasite dynamics may influence patterns in parasitism in environmentally heterogeneous landscapes.     

Contrasting the seasonal and elevational prevalence of generalist avian haemosporidia in co‐occurring host species

Understanding the ecology and evolution of parasites is contingent on identifying the selection pressures they face across their infection landscape. Such a task is made challenging by the fact that these pressures will likely vary across time and space, as a result of seasonal and geographical differences in host susceptibility or transmission opportunities. Avian haemosporidian blood parasites are capable of infecting multiple co‐occurring hosts within their ranges, yet whether their distribution across time and space varies similarly in their different host species remains unclear. Here, we applied a new PCR method to detect avian haemosporidia (genera Haemoproteus, Leucocytozoon, and Plasmodium) and to determine parasite prevalence in two closely related and co‐occurring host species, blue tits (Cyanistes caeruleus, N = 529) and great tits (Parus major, N = 443). Our samples were collected between autumn and spring, along an elevational gradient in the French Pyrenees and over a three‐year period. Most parasites were found to infect both host species, and while these generalist parasites displayed similar elevational patterns of prevalence in the two host species, this was not always the case for seasonal prevalence patterns. For example, Leucocytozoon group A parasites showed inverse seasonal prevalence when comparing between the two host species, being highest in winter and spring in blue tits but higher in autumn in great tits. While Plasmodium relictum prevalence was overall lower in spring relative to winter or autumn in both species, spring prevalence was also lower in blue tits than in great tits. Together, these results reveal how generalist parasites can exhibit host‐specific epidemiology, which is likely to complicate predictions of host–parasite co‐evolution.     

Robust geographical determinants of infection prevalence and a contrasting latitudinal diversity gradient for haemosporidian parasites in Western Palearctic birds

Identifying robust environmental predictors of infection probability is central to forecasting and mitigating the ongoing impacts of climate change on vector‐borne disease threats. We applied phylogenetic hierarchical models to a data set of 2,171 Western Palearctic individual birds from 47 species to determine how climate and landscape variation influence infection probability for three genera of haemosporidian blood parasites (Haemoproteus, Leucocytozoon, and Plasmodium). Our comparative models found compelling evidence that birds in areas with higher vegetation density (captured by the normalized difference vegetation index [NDVI]) had higher likelihoods of carrying parasite infection. Magnitudes of this relationship were remarkably similar across parasite genera considering that these parasites use different arthropod vectors and are widely presumed to be epidemiologically distinct. However, we also uncovered key differences among genera that highlighted complexities in their climate responses. In particular, prevalences of Haemoproteus and Plasmodium showed strong but contrasting relationships with winter temperatures, supporting mounting evidence that winter warming is a key environmental filter impacting the dynamics of host‐parasite interactions. Parasite phylogenetic community diversities demonstrated a clear but contrasting latitudinal gradient, with Haemoproteus diversity increasing towards the equator and Leucocytozoon diversity increasing towards the poles. Haemoproteus diversity also increased in regions with higher vegetation density, supporting our evidence that summer vegetation density is important for structuring the distributions of these parasites. Ongoing variation in winter temperatures and vegetation characteristics will probably have far‐reaching consequences for the transmission and spread of vector‐borne diseases.     

Circannual variation in blood parasitism in a sub‐Saharan migrant passerine bird,the garden warbler

Knowing the natural dynamics of pathogens in migratory birds is important, for example, to understand the factors that influence the transport of pathogens to and their transmission in new geographical areas, whereas the transmission of other pathogens might be restricted to a specific area. We studied haemosporidian blood parasites of the genera Plasmodium, Haemoproteus and Leucocytozoon in a migratory bird, the garden warbler Sylvia borin. Birds were sampled in spring, summer and early autumn at breeding grounds in Sweden, on migration at Capri, Italy and on arrival and departure from wintering staging areas in West Africa: mapping recoveries of garden warblers ringed in Fennoscandia and Capri showed that these sites are most probably on the migratory flyway of garden warblers breeding at Kvismaren. Overall, haemosporidian prevalence was 39%, involving 24 different parasite lineages. Prevalence varied significantly over the migratory cycle, with relatively high prevalence of blood parasites in the population on breeding grounds and at the onset of autumn migration, followed by marked declines in prevalence during migration both on spring and autumn passage. Importantly, we found that when examining circannual variation in the different lineages, significantly different prevalence profiles emerged both between and within genera. Our results suggest that differences in prevalence profiles are the result of either different parasite transmission strategies or coevolution between the host and the various parasite lineages. When separating parasites into common vs. rare lineages, we found that two peaks in the prevalence of rare parasites occur; on arrival at Swedish breeding grounds, and after the wintering period in Africa. Our results stress the importance of appropriate taxonomic resolution when examining host‐parasite interactions, as variation in prevalence both between and within parasite genera can show markedly different patterns.     

Seasonal variation of tsetse fly species abundance and prevalence of trypanosomes in the Maasai Steppe,Tanzania

Tsetse flies, the vectors of trypanosomiasis, represent a threat to public health and economy in sub‐Saharan Africa. Despite these concerns, information on temporal and spatial dynamics of tsetse and trypanosomes remain limited and may be a reason that control strategies are less effective. The current study assessed the temporal variation of the relative abundance of tsetse fly species and trypanosome prevalence in relation to climate in the Maasai Steppe of Tanzania in 2014–2015. Tsetse flies were captured using odor‐baited Epsilon traps deployed in ten sites selected through random subsampling of the major vegetation types in the area. Fly species were identified morphologically and trypanosome species classified using PCR. The climate dataset was acquired from the African Flood and Drought Monitor repository. Three species of tsetse flies were identified: G. swynnertoni (70.8%), G. m. morsitans (23.4%), and G.pallidipes (5.8%). All species showed monthly changes in abundance with most of the flies collected in July. The relative abundance of G. m. morsitans and G. swynnertoni was negatively correlated with maximum and minimum temperature, respectively. Three trypanosome species were recorded: T. vivax (82.1%), T. brucei (8.93%), and T. congolense (3.57%). The peak of trypanosome infections in the flies was found in October and was three months after the tsetse abundance peak; prevalence was negatively correlated with tsetse abundance. A strong positive relationship was found between trypanosome prevalence and temperature. In conclusion, we find that trypanosome prevalence is dependent on fly availability, and temperature drives both tsetse fly relative abundance and trypanosome prevalence.     

Finding the appropriate variables to model the distribution of vector‐borne parasites with different environmental preferences: climate is not enough

Understanding how environmental variation influences the distribution of parasite diversity is critical if we are to anticipate disease emergence risks associated with global change. However, choosing the relevant variables for modelling current and future parasite distributions may be difficult: candidate predictors are many, and they seldom are statistically independent. This problem often leads to simplistic models of current and projected future parasite distributions, with climatic variables prioritized over potentially important landscape features or host population attributes. We studied avian blood parasites of the genera Plasmodium, Haemoproteus and Leucocytozoon (which are viewed as potential emergent pathogens) in 37 Iberian blackcap Sylvia atricapilla populations. We used Partial Least Squares regression to assess the relative importance of a wide array of putative determinants of variation in the diversity of these parasites, including climate, landscape features and host population migration. Both prevalence and richness of parasites were predominantly related to climate (an effect which was primarily, but not exclusively driven by variation in temperature), but landscape features and host migration also explained variation in parasite diversity. Remarkably, different models emerged for each parasite genus, although all parasites were studied in the same host species. Our results show that parasite distribution models, which are usually based on climatic variables alone, improve by including other types of predictors. Moreover, closely related parasites may show different relationships to the same environmental influences (both in magnitude and direction). Thus, a model used to develop one parasite distribution can probably not be applied identically even to the most similar host–parasite systems.     

Seasonal abundance, biting cycle and parity of the mosquito Haemagogus leucocelaenus in Trinidad, West Indies

Adult female populations of Haemagogus leucocelaenus (Dyar and Shannon), the sylvan vector of yellow fever, were monitored weekly during 1981–82 by human collectors on the ground at Point Gourde in Chaguaramas Forest, 16 km west of Port of Spain, Trinidad.
Hg.leucocelaenus showed only diurnal landing activity, from 06.00 to 18.00 hours (sunrise to sunset, universal time), with a single peak of activity between 10.00 and 14.00 hours.
Densities of Hg.leucocelaenus during the wet season (May–November) were about double the level recorded during the dry season (December–April).
Monthly parous rates averaged 53.9% (range 25–90%) and some females were up to five-pars. Retained eggs (range 2–6, mean 4/female) were found in the ovaries of 0.34% of landing females, all of which had stage 1 ovarian follicles for the next gonotrophic cycle. Therefore blood-feeding is not inhibited by egg retention. Hg. leucocelaenus vector potential is reappraised in the light of these findings.     

Individual genetic diversity and probability of infection by avian malaria parasites in blue tits (Cyanistes caeruleus)

Understanding the importance of host genetic diversity for coping with parasites and infectious diseases is a long‐standing goal in evolutionary biology. Here, we study the association between probability of infection by avian malaria (Plasmodium relictum) and individual genetic diversity in three blue tit (Cyanistes caeruleus) populations that strongly differ in prevalence of this parasite. For this purpose, we screened avian malaria infections and genotyped 789 blue tits across 26 microsatellite markers. We used two different arrays of markers: 14 loci classified as neutral and 12 loci classified as putatively functional. We found a significant relationship between probability of infection and host genetic diversity estimated at the subset of neutral markers that was not explained by strong local effects and did not differ among the studied populations. This relationship was not linear, and probability of infection increased up to values of homozygosity by locus (HL) around 0.15, reached a plateau at values of HL from 0.15 to 0.40 and finally declined among a small proportion of highly homozygous individuals (HL > 0.4). We did not find evidence for significant identity disequilibrium, which may have resulted from a low variance of inbreeding in the study populations and/or the small power of our set of markers to detect it. A combination of subtle positive and negative local effects and/or a saturation threshold in the association between probability of infection and host genetic diversity in combination with increased resistance to parasites in highly homozygous individuals may explain the observed negative quadratic relationship. Overall, our study highlights that parasites play an important role in shaping host genetic variation and suggests that the use of large sets of neutral markers may be more appropriate for the study of heterozygosity–fitness correlations.     

Seasonal abundance,biting cycle,parity and vector potential of the mosquito Haemagogus equines in Trinidad

Abstract. The mosquito Haemagogus equinus is a known vector of yellow fever (YF) in central America. Seasonal abundance, daily biting activity and the age composition of adult Hg. equinus female populations were monitored weekly during 1981–82 by human collectors on the ground at Point Gourde Forest, Chaguaramas, 16 km west of Port of Spain, Trinidad. 2. Landing collections of Hg.equinus showed diurnal activity from 06.00 to 20.00 hours (suntime), with a single peak between 08.00 and 14.00 hours. 3. Overall, 5.6% of Hg.equinus were collected during the dry season (December-April) and 94.4% during the wet season (May-November). 4. Mean density of Hg.equinus in relation to man ranged from 0.35/man-day in February to 133/man-day in July, with averages of 2.8 in the wet season, 36.9 in the dry season and 22/man-day for the whole year. 5. Monthly parous rates averaged 62.1% (range 0-88%); 2.8% of females were 2-pars, another 2.8% were 3-pars, but no older females of Hg.equinus were found (sample size 467). 6. These age-grading data indicate that Hg.equinus females have relatively short life expectancy and hence low vector potential, which may help to explain why YF virus has seldom been isolated from this vector species.     

Wolbachia infection alters the relative abundance of resident bacteria in adult Aedes aegypti mosquitoes,but not larvae

Insect–symbiont interactions are known to play key roles in host functions and fitness. The common insect endosymbiont Wolbachia can reduce the ability of several human pathogens, including arboviruses and the malaria parasite, to replicate in insect hosts. Wolbachia does not naturally infect Aedes aegypti, the primary vector of dengue virus, but transinfected Ae. aegypti have antidengue virus properties and are currently being trialled as a dengue biocontrol strategy. Here, we assess the impact of Wolbachia infection of Ae. aegypti on the microbiome of wild mosquito populations (adults and larvae) collected from release sites in Cairns, Australia, by profiling the 16S rRNA gene using next‐generation sequencing. Our data indicate that Wolbachia reduces the relative abundance of a large proportion of bacterial taxa in Ae. aegypti adults, that is in accordance with the known pathogen‐blocking effects of Wolbachia on a variety of bacteria and viruses. In adults, several of the most abundant bacterial genera were found to undergo significant shifts in relative abundance. However, the genera showing the greatest changes in relative abundance in Wolbachia‐infected adults represented a low proportion of the total microbiome. In addition, there was little effect of Wolbachia infection on the relative abundance of bacterial taxa in larvae, or on species diversity (accounting for species richness and evenness together) detected in adults or larvae. These results offer insight into the effects of Wolbachia on the Ae. aegypti microbiome in a native setting, an important consideration for field releases of Wolbachia into the population.     

Preceding crop affects soybean aphid abundance and predator–prey dynamics in soybean

Crop rotations alter the soil environment and physiology of the subsequent crop in ways that may affect the abundance of herbivores and their natural enemies. Soybean aphids are a consistent pest of soybean throughout North America, but little work has focused on how preceding crops may affect pest–predator dynamics. In a replicated experiment over three years, we examined how two preceding crops (spring wheat or an oat/pea mixture) affected seasonal soybean aphid pressure and the ratio of aphids to their predator community. Peak aphid populations were reduced by 40% and 75% in years 1 and 2 by planting spring wheat before soybeans (relative to the oat–pea mixture). Aphid densities were unaffected by preceding crop in the third year of study (aphids were at threshold in this year). Predators responded positively to aphid population increases and were unaffected by preceding crops. Additional research on how crop rotations can be used as a tool to manage soybean aphids warrants further attention.     

Rapid warming and drought negatively impact population size and reproductive dynamics of an avian predator in the arid southwest

Avian communities of arid ecosystems may be particularly vulnerable to global climate change due to the magnitude of projected change for desert regions and the inherent challenges for species residing in resource limited ecosystems. How arid‐zone birds will be affected by rapid increases in air temperature and increased drought frequency and severity is poorly understood because avian responses to climate change have primarily been studied in the relatively mesic northern temperate regions. We studied the effects of increasing air temperature and aridity on a Burrowing Owl (Athene cunicularia) population in the southwestern United States from 1998 to 2013. Over 16 years, the breeding population declined 98.1%, from 52 pairs to 1 pair, and nest success and fledgling output also declined significantly. These trends were strongly associated with the combined effects of decreased precipitation and increased air temperature. Arrival on the breeding grounds, pair formation, nest initiation, and hatch dates all showed significant delays ranging from 9.4 to 25.1 days over 9 years, which have negative effects on reproduction. Adult and juvenile body mass decreased significantly over time, with a loss of 7.9% mass in adult males and 10.9% mass in adult females over 16 years, and a loss of 20.0% mass in nestlings over 8 years. Taken together, these population and reproductive trends have serious implications for local population persistence. The southwestern United States has been identified as a climate change hotspot, with projections of warmer temperatures, less winter precipitation, and an increase in frequency and severity of extreme events including drought and heat waves. An increasingly warm and dry climate may contribute to this species' decline and may already be a driving force of their apparent decline in the desert southwest.     

Seasonal abundance and adult survival of bottlenose dolphins (Tursiops truncatus) in a community that cooperatively forages with fishermen in southern Brazil

A subgroup of a population of Tursiops truncatus in southern Brazil is known for a cooperative behavior with artisanal fishermen whereby the dolphins shoal fish towards net‐casting fishermen. Combining photo‐identification data collected between September 2007 and 2009 with mark‐recapture and Pollock's robust design models, we assessed abundance within seasons and survival and temporary emigration rates of dolphins between seasons. We also reanalyzed a previous data set collected during 1989–1991, and Cormack‐Jolly‐Seber models were applied to estimate survival rates for each of the study periods. The abundance of marked “cooperative” dolphins varied between seasons from 18 (CI: 17–24) to 21 (CI: 20–24). The total abundance varied from 59 in the winter of 2008 (CI: 49–72) to 50 in the autumn of 2009 (CI: 40–62). The annual adult survival was estimated to be 0.917 (CI: 0.876–0.961), close to that estimated from data collected in the 1990s (0.941; CI: 0.888–0.998). The emigration probability was low (0.031; CI: 0.011–0.084) and different capture probabilities between the “cooperative” and “noncooperative” dolphins indicated a degree of behavioral segregation. The precision of our estimates is likely to provide sufficient power to detect population change, but we recommend a precautionary management approach to protect this vulnerable dolphin community and its unique cooperative feeding tradition.