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Evidence of Culiseta mosquitoes as vectors for Plasmodium parasites in Alaska

Mosquito vectors play a crucial role in the distribution of avian Plasmodium parasites worldwide. At northern latitudes, where climate warming is most pronounced, there are questions about possible changes in the abundance and distribution of Plasmodium parasites, their vectors, and their impacts to avian hosts. To better understand the transmission of Plasmodium among local birds and to gather baseline data on potential vectors, we sampled a total of 3,909 mosquitoes from three locations in south‐central Alaska during the summer of 2016. We screened mosquitoes for the presence of Plasmodium parasites using molecular techniques and estimated Plasmodium infection rates per 1,000 mosquitoes using maximum likelihood methods. We found low estimated infection rates across all mosquitoes (1.28 per 1,000), with significantly higher rates in Culiseta mosquitoes (7.91 per 1,000) than in Aedes mosquitoes (0.57 per 1,000). We detected Plasmodium in a single head/thorax sample of Culiseta , indicating potential for transmission of these parasites by mosquitoes of this genus. Plasmodium parasite DNA isolated from mosquitoes showed a 100% identity match to the BT7 Plasmodium lineage that has been detected in numerous avian species worldwide. Additionally, microscopic analysis of blood smears collected from black‐capped chickadees ( Poecile atricapillus ) at the same locations revealed infection by parasites preliminarily identified as Plasmodium circumflexum . Results from our study provide the first information on Plasmodium infection rates in Alaskan mosquitoes and evidence that Culiseta species may play a role in the transmission and maintenance of Plasmodium parasites in this region.

Alaska

Diverse novel and avian-associated viruses in the ileal viromes of northern mockingbird (Mimus polyglottos)

Viruses are the most abundant and diverse organisms on Earth, though only a small portion cause disease. Understanding viral diversity is key to understanding and predicting pathogen emergence and zoonotic spillover. Here, we use meta-transcriptomic sequencing to examine the viral communities in the ileum of 25 Northern Mockingbirds ( Mimus polyglottos ) from various locations across Texas. We assembled high-quality genomes of 43 viral species (40 species identified to 13 families, one to kingdom, and two to realm), 38 of which were novel. They tentatively represent avian- (n = 3), arthropod- (n = 21), plant- (n = 5) and fungi- (n = 4) associated, or other (n = 10) viruses. The arthropod-associated Dicistroviridae family was the most dominant, comprising known and potentially new species. Of potential epidemiological importance were three novel and avian-associated viruses: members of the families Hepeviridae and Picornaviridae , and a new Matryoshka RNA virus. The Matryoshka RNA virus 8 (MaRNAV-8) is sister to other Matryoshka RNA viruses, and its co-occurrence with haemosporida further supports the nested virus-parasite-vector-vertebrate host relationship of this group of viruses, with potential implications for parasite evolution, fitness and load and vector competence. The Picornaviridae virus is a member of an avian hepatovirus clade, found nested within a clade containing both the mammalian pathogens Hepatovirus A – I and the avian Tremovirus pathogens, suggestive of a newly discovered pathogen of Northern Mockingbird. Although the recovered Hepeviridae virus is of unknown pathology, its family members include the Hepatitis E viruses. With the great diversity and novelty described from ileal viromes, discriminating potential pathogens and commensal microbiota from viruses associated with food items remains challenging. A deeper understanding of virus transmission and the risk of potential zoonosis can be enhanced by tracking viruses through the food web and via inter-specific and predator-prey interactions, particular in areas subject to land-use change, where human-wildlife interactions are increased and the risks from emerging pathogens of veterinary and medical importance are more pronounced.

Texas

Effects of Climate and land use on diversity, prevalence, and seasonal transmission of avian hematozoa in American Samoa

The indigenous forest birds of American Samoa are increasingly threatened by changing patterns of rainfall and temperature that are associated with climate change as well as environmental stressors associated with agricultural and urban development, invasive species, and new introductions of avian diseases and disease vectors. Long term changes in their distribution, diversity, and population sizes could have significant impacts on the ecological integrity of the islands because of their critical role as pollinators and seed dispersers. We documented diversity of vector borne parasites on Tutuila and Ta‘u Islands over a 10-year period to expand earlier observations of Plasmodium, Trypanosoma , and filarial parasites, to provide better parasite identifications, and to create a better baseline for detecting new parasite introductions. We also identified potential mosquito vectors of avian Plasmodium and Trypanosoma , determined whether land clearing and habitat alterations associated with subsistence farming within the National Park of American Samoa can influence parasite prevalence, and determined whether parasite prevalence is correlated with seasonal changes in rainfall, temperature and wind speed. Three taxonomically distinct lineages of Plasmodium were identified from mosquito vectors and forest birds based on partial sequence data from parasite mitochondrial genes. All three have been described from passerine and galliform birds in Australasia. Two lineages, SCEDEN01 and ORW1, had elongate gametocytes and large schizonts that were consistent with species of Plasmodium in the subgenus Giavannolaia, but were taxonomically distinct from known morphological species of Plasmodium based on a Bayesian phylogenetic analysis of a 478 bp region of the parasite cytochrome b gene. Both are candidates for description as new species. The third lineage (GALLUS02) was detected only in mosquito vectors on Tutuila and was similar in cytochrome b sequence to P. juxtanucleare , a pathogenic species of Plasmodium from chickens and other galliform birds from Australasia, Africa, and South America. Plasmodium relictum , the malarial parasite that has had such a devastating impact on Hawaiian forest birds, was not detected. We observed large, striated trypanosomes in avian hosts from both Tutuila and Ta‘u Islands that fell within the same taxonomic clade as T. corvi and T. culicavium based on 18S ribosomal DNA sequence. We also observed sheathed microfilariae with pointed tails that had some morphological similarities to microfilaria from species of Pelecitus, Struthiofilaria and Eulimdana , but identification will require recovery and examination of adult filarial worms from the connective tissue or body cavities of infected birds. We also observed one or more species of haemococcidians (Isospora, synonym = Atoxoplasma ) within circulating lymphocytes from multiple avian host species. Overall prevalence of Plasmodium was higher on Ta‘u (22%, 75/341) than Tutuila (9.2%, 27/294), with most infections occurring in Polynesian starlings, Samoan starlings, Wattled honeyeaters, and Cardinal honeyeaters. Prevalence was relatively constant from year to year and between seasons at individual study sites, but varied among study sites, with highest rates of infection in areas with agricultural activity at Faleasao (37.4%, 73/195, Ta‘u Island) and Amalau Valley (9.7%, 21/216, Tutuila Island). Prevalence in more remote areas of the National Park of American Samoa was lower, ranging from 1.4% (2/146) at Laufuti and Luatele on Ta‘u to 7.7% (6/78) at Olo Ridge on Tutuila. Similar trends were evident for infections with Trypanosoma and filarial worms. Overall prevalence was not influenced significantly by warmer, wet (summer) or cooler, dry (winter) season. We detected Plasmodium infections in Culex sitiens and C. quinquefasciatus through either salivary gland and midgut dissections or PCR amplification of parasite cytochrome b genes in pooled or individual samples of mosquitoes that were collected on Tutuila. Pooled or individual Aedes oceanicus, A. polynesiensis, A. tutuilae, A. upolensis, A. nocturnus, Aedes (Finlaya) (mixed pools of A. samoanus, A. oceanicus, A. tutuilae), Aedes (Stegomyia) (mixed pools of A. aegypti, A. upolensis, A. polynesiensis ), and C. annulirostris were negative for Plasmodium , but we detected infections with Trypanosoma through midgut and salivary gland dissections in a single C. sitiens from Amalau Valley, Tutuila and three A. oceanicus from Faleasao, Ta‘u. Two of the A. oceanicus from Faleasao amplified successfully with Trypanosoma primers, but sequences were distinctly different from those obtained from avian hosts. We found a strong association between land use and prevalence of mosquito-transmitted parasites on Ta‘u Island with odds of being infected more than 20 times greater in agricultural plots than more remote native forest. This relationship was evident on Tutuila Island but not statistically significant because of the close proximity of study sites and observed movement of birds between native forest and agricultural land. Our data support previous studies that have suggested that Plasmodium and other vector-borne parasites are part of the indigenous parasite fauna in American Samoa. Transmission dynamics appear to be affected by environmental changes associated with land use practices.

HI

Effect of climate change on disease spread in wildlife

A growing body of evidence indicates that climate change alone, or acting synergistically with current anthropogenic threats, is affecting the health of wild populations of aquatic and terrestrial wildlife. Measurable by-products of climate change include elevated atmospheric concentrations of greenhouse gases, higher average global temperatures; variations in global precipitation patterns, rising and warming oceans, altered hydrographs of rivers, and increased mid-continental drying during summer. These consequences affect the terrestrial environment through shifts in phenology, vegetation cover, and fire regimes. Warmer ocean temperatures, increased acidification, rise in sea levels, and reduction in sea ice cover are also leading to widespread ecological changes in marine systems. Wildlife populations face a variety of climate-related pressures, such as changes in animal distribution or density, limitation of food resources, and alteration to critical habitats. The increased potential for emergence and resurgence of diseases that are responsive to environmental conditions also has implications for wildlife populations. Shifts in temperature or other climatic factors may directly affect the incidence of disease in wildlife by altering host-pathogen interactions, promoting vector populations or allowing new ranges for vectors, or reducing development times for parasites. A number of examples from both field and laboratory studies have demonstrated a clear link between warming environments and disease spread. Many climate-related environmental changes also influence wildlife health indirectly. For example, increasing temperatures, in combination with shifts in rainfall and humidity, may aggravate current trends for water resource limitation and habitat degradation or destruction and lead to increased crowding of animal populations, thereby promoting transmission opportunities of pathogens within populations or across species. Although it may be difficult to disentangle the influences of other anthropogenic changes from the direct effects of warming, some ecosystems provide especially useful models for studying climate-related disease spread in wildlife. For example, the effects of climate change on parasite dynamics may be easily observed in the Arctic, where environmental changes are occurring rapidly, anthropogenic influences are relatively limited, and biodiversity is generally low. Marine ecosystems are also undergoing rapid rates of change and may be vulnerable to a variety of natural and anthropogenic perturbations. Although many factors affect the health of organisms in ocean environments, temperature has been clearly linked to an increase in disease prevalence among sessile organisms such as corals. In this chapter, we discuss observed and predicted changes to wildlife health resulting from climate change. Our review will not include all aspects of wildlife health, but will instead focus on established or suspected links between climate drivers and disease spread and discuss examples from the current literature. Here, we define disease spread to include: 1) change in geographical or altitudinal distribution of pathogens, parasites, and vectors and the diseases they cause; 2) change in prevalence or severity of disease; and 3) emergence of novel diseases. Additionally, because wildlife species serve as reservoirs for zoonotic diseases that affect both animals and humans, we include select examples of the effect of climate change on the capacity of wildlife to harbor and spread these disease agents.

Book chapter

Fostering real-time climate adaptation: Analyzing past, current, and forecast temperature to understand the dynamic risk to Hawaiian honeycreepers from avian malaria

Various vector control options are increasingly being considered to safeguard forest birds in their natural habitats from avian malaria transmission. However, vector control options require localized deployment that is not logistically, ethically, ecologically, nor economically viable everywhere and all the time. Based on thermal tolerances of the sporogonic stages of avian malaria (Plasmodium relictum) parasite and its vector, the southern house mosquito (Culex quinquefasciatus), we examined the long-term weather trends for three high value, forest bird refuges (Alakai Wilderness Preserve on Kaua’i, Hanawi Natural Area Reserve on Maui, and Hakalau Forest National Wildlife Refuge on Hawai’i Island) to understand the temporal and site-specific differences of temperature-driven suitability for localized avian malaria transmission. On average, Alakai had mean ambient temperatures suitable for both the vector’s immature stage development and parasite sporogonic development most of the time (85.3%), indicating that observed variability in vector abundance or disease transmission may be driven by other factors. At higher elevation sites like Hakalau and Hanawi, current mean ambient temperatures suitable only for vector development prevail (91.7% and 96.6%, respectively), while mean ambient temperatures for both vector and parasite sporogonic development seldom occur (4.4% and 0% respectively). Our results not only show differences in the temperature suitability for transmission across elevation, but also different levels of vulnerability to avian malaria transmission with any additional projected increase in temperature. For instance, under a conservative warming scenario of 1.0 °C, the joint temperature suitability of parasite and vector development increases at higher elevation sites such as Hakalau (+35.8%) and Hanawi (+15.4%). While mean ambient temperatures suitable for both vector and parasite development already occur most of the time at Alakai, the occurrence also increases (+8.4%) as well under this conservative warming scenario. By linking current site-specific weather data to real-time weather forecasts, we developed a real-time avian malaria warning system to assist managers in identifying conditions when vector control is most needed at these three selected study sites. This online tool determines when conditions are likely to be suitable for local development of P. relictum and C. quinquefasciatus at Alakai, Hanawi, and Hakalau. This tool illustrates how managers can incorporate climate and current weather patterns into decision making without having to consider the uncertainties of long-term climatic and ecological projections.

Hawaii

Imported Asian swamp eels (Synbranchidae: Monopterus) in North American live food markets: Potential vectors of non-native parasites

Since the 1990s, possibly earlier, large numbers of Asian swamp eels (Synbranchidae: Monopterus spp.), some wild-caught, have been imported live from various countries in Asia and sold in ethnic food markets in cities throughout the USA and parts of Canada. Such markets are the likely introduction pathway of some, perhaps most, of the five known wild populations of Asian swamp eels present in the continental United States. This paper presents results of a pilot study intended to gather baseline data on the occurrence and abundance of internal macroparasites infecting swamp eels imported from Asia to North American retail food markets. These data are important in assessing the potential role that imported swamp eels may play as possible vectors of non-native parasites. Examination of the gastrointestinal tracts and associated tissues of 19 adult-sized swamp eels—identified as M. albus "Clade C"—imported from Vietnam and present in a U.S. retail food market revealed that 18 (95%) contained macroparasites. The 394 individual parasites recovered included a mix of nematodes, acanthocephalans, cestodes, digeneans, and pentastomes. The findings raise concern because of the likelihood that some parasites infecting market swamp eels imported from Asia are themselves Asian taxa, some possibly new to North America. The ecological risk is exacerbated because swamp eels sold in food markets are occasionally retained live by customers and a few reportedly released into the wild. For comparative purposes, M. albus "Clade C" swamp eels from a non-native population in Florida (USA) were also examined and most (84%) were found to be infected with internal macroparasites. The current level of analysis does not allow us to confirm whether these are non-native parasites.

Aquatic Invasions

Host population persistence in the face of introduced vector-borne diseases: Hawaii amakihi and avian malaria

The past quarter century has seen an unprecedented increase in the number of new and emerging infectious diseases throughout the world, with serious implications for human and wildlife populations. We examined host persistence in the face of introduced vector-borne diseases in Hawaii, where introduced avian malaria and introduced vectors have had a negative impact on most populations of Hawaiian forest birds for nearly a century. We studied birds, parasites, and vectors in nine study areas from 0 to 1,800 m on Mauna Loa Volcano, Hawaii from January to October, 2002. Contrary to predictions of prior work, we found that Hawaii amakihi (Hemignathus virens), a native species susceptible to malaria, comprised from 24.5% to 51.9% of the avian community at three low-elevation forests (55-270 m). Amakihi were more abundant at low elevations than at disease-free high elevations, and were resident and breeding there. Infection rates were 24-40% by microscopy and 55-83% by serology, with most infected individuals experiencing low-intensity, chronic infections. Mosquito trapping and diagnostics provided strong evidence for year-round local transmission. Moreover, we present evidence that Hawaii amakihi have increased in low elevation habitats on south-eastern Hawaii Island over the past decade. The recent emergent phenomenon of recovering amakihi populations at low elevations, despite extremely high prevalence of avian malaria, suggests that ecological or evolutionary processes acting on hosts or parasites have allowed this species to recolonize low-elevation habitats. A better understanding of the mechanisms allowing coexistence of hosts and parasites may ultimately lead to tools for mitigating disease impacts on wildlife and human populations.

Proceedings of the National Academy of Sciences of

Prevalence, transmission, and genetic diversity of blood parasites infecting tundra-nesting geese in Alaska

A total of 842 blood samples collected from five species of tundra-nesting geese in Alaska was screened for haemosporidian parasites using molecular techniques. Parasites of the genera Leucocytozoon Danilewsky, 1890, Haemoproteus Kruse, 1890, and Plasmodium Marchiafava and Celli, 1885 were detected in 169 (20%), 3 (<1%), and 0 (0%) samples, respectively. Occupancy modeling was used to estimate prevalence of Leucocytozoon parasites and assess variation relative to species, age, sex, geographic area, year, and decade. Species, age, and decade were identified as important in explaining differences in prevalence of Leucocytozoon parasites. Leucocytozoon parasites were detected in goslings sampled along the Arctic Coastal Plain using both historic and contemporary samples, which provided support for transmission in the North American Arctic. In contrast, lack of detection of Haemoproteus and Plasmodium parasites in goslings ( n = 238) provided evidence to suggest that the transmission of parasites of these genera may not occur among waterfowl using tundra habitats in Alaska, or alternatively, may only occur at low levels. Five haemosporidian genetic lineages shared among different species of geese sampled from two geographic areas were indicative of interspecies parasite transmission and supported broad parasite or vector distributions. However, identical Leucocytozoon and Haemoproteus lineages on public databases were limited to waterfowl hosts suggesting constraints in the range of parasite hosts.

Alaska

Concentration and retention of Toxoplasma gondii surrogates from seawater by red abalone (Haliotis rufescens)

Small marine snails and abalone have been identified as high- and low-risk prey items, respectively, for exposure of threatened southern sea otters to Toxoplasma gondii , a zoonotic parasite that can cause fatal encephalitis in animals and humans. While recent work has characterized snails as paratenic hosts for T. gondii , the ability of abalone to vector the parasite has not been evaluated. To further elucidate why abalone predation may be protective against T. gondii exposure, this study aimed to determine whether: (1) abalone are physiologically capable of acquiring T. gondii ; and (2) abalone and snails differ in their ability to concentrate and retain the parasite. Abalone were exposed to T. gondii surrogate microspheres for 24 h, and fecal samples were examined for 2 weeks following exposure. Concentration of surrogates was 2–3 orders of magnitude greater in abalone feces than in the spiked seawater, and excretion of surrogates continued for 14 days post-exposure. These results indicate that, physiologically, abalone and snails can equally vector T. gondii as paratenic hosts. Reduced risk of T. gondii infection in abalone-specializing otters may therefore result from abalone's high nutritional value, which implies otters must consume fewer animals to meet their caloric needs.

Parasitology

Prevalence and diversity of avian blood parasites in a resident northern passerine

Background: Climate-related changes are expected to influence the prevalence and distribution of vector-borne haemosporidian parasites at northern latitudes, although baseline information about resident birds is still lacking. In this study, we investigated prevalence and genetic diversity of Plasmodium, Haemoproteus, and Leucocytozoon parasites infecting the Northwestern Crow (Corvus caurinus), a non-migratory passerine with unique life-history characteristics. This species occupies both intertidal and forested habitats and is subject to high prevalence of avian keratin disorder (AKD), a disease that causes gross beak deformities. Investigation of avian blood parasites in Northwestern Crows at sites broadly distributed across coastal Alaska provided an opportunity to evaluate specific host factors related to parasite infection status and assess geographic patterns of prevalence. Results: We used molecular methods to screen for haemosporidian parasites in Northwestern Crows and estimated genus-specific parasite prevalence with occupancy modeling that accounts for imperfect detection of parasite infection. We observed considerable geographic and annual variation in prevalence of Plasmodium, Haemoproteus, and Leucocytozoon , but these patterns were not correlated with indices of local climatic conditions. Our models also did not provide support for relationships between the probability of parasite infection and body condition or the occurrence of co-infections with other parasite genera or clinical signs of AKD. In our phylogenetic analyses, we identified multiple lineages of each parasite genus, with Leucocytozoon showing greater diversity than Plasmodium or Haemoproteus. Conclusions: Results from this study expand our knowledge about the prevalence and diversity of avian blood parasites in northern resident birds as well as corvids worldwide. We detected all three genera of avian haemosporidians in Northwestern Crows in Alaska, although only Leucocytozoon occurred at all sites in both years. Given the strong geographic and interannual variation in parasite prevalence and apparent lack of correlation with climatic variables, it appears that there are other key factors responsible for driving transmission dynamics in this region. Thus, caution is warranted when using standard climatic or geographic attributes in a predictive framework. Our phylogenetic results demonstrate lower host specificity for some lineages of Leucocytozoon than is typically reported and provide insights about genetic diversity of local haemosporidian parasites in Alaska.

Parasites & Vectors

Changes in the prevalence of avian disease and mosquito vectors at Hakalau Forest National Wildlife Refuge: a 14-year perspective and assessment of future risk

Throughout the main Hawaiian Islands, introduced mosquito-borne disease has had, and continues to have, a profound impact on the distributions and abundance of native Hawaiian forest birds. Populations of remaining native forest birds are largely restricted to high elevation forests where mean temperatures are marginal for vector and parasite development and limited availability of larval mosquito habitat constrains mosquito populations and disease transmission. Hakalau Forest National Wildlife Refuge (HFNWR) was established for the preservation of endemic avifauna in 1985. Since its creation, native bird communities there have remained intact and most species populations are stable or increasing. However, avian malaria had been detected at HFNWR in the past and, in light of documented climate change, new concerns have been raised regarding the long-term fate of the refuge&rsquo;s forest birds. To examine the possible changes in avian malaria transmission at HFNWR we sampled forest birds for blood parasites, trapped adult mosquitoes and surveyed larval mosquito habitat at three sites during 2012 and compared our results with similar data collected between 1998 and 1999. We tested blood samples by polymerase chain reaction (PCR), immunoblotting, and microscopy to determine prevalence of acute and chronic infection and used attractive gravid traps to sample the vector mosquito Culex quinquefasciatus. Our study documented spatial trends and temporal changes in the prevalence of avian malaria, mosquito presence, larval mosquito habitat and feral pig activity at HFNWR. We found evidence of local transmission in high elevation forests, a general pattern of increasing prevalence at lower elevations and along a South to North gradient and a two-fold decrease in the prevalence of avian malaria in the intervening 14 years. Despite considerable effort, we were unable to detect larval C. quinquefasciatus and captured only one adult indicating that the vector of avian malaria has a very limited presence at HFNWR. We did, however, document the establishment of another invasive mosquito, Aedes japonicus japonicus , and its occurrence in tree fern cavities and rock pools as larval habitat in the lower forests of HFNWR. We suggest that interspecific competition by A. j. japonicus and predation by a suite of native predators may provide biotic resistance to the establishment of permanent C. quinquefasciatus populations. While current predictions of climate change in the Hawaiian Islands include a gradual warming and enhanced transmission by mid-century, the current cooling trend recorded at high elevation HFNWR illustrates the importance of monitoring to document fine scale temporal and site specific changes in prevalence. Long term changes in precipitation may have a more profound effect on local transmission of malaria than temperature and we may have already seen some potential impacts of an extended drought at HFNWR with a decrease in feral pig activity and pig associated larval mosquito habitat and increases in stream-associated larval mosquito habitat.

Hawaii

Bottlenecks and multiple introductions: Population genetics of the vector of avian malaria in Hawaii

Avian malaria has had a profound impact on the demographics and behaviour of Hawaiian forest birds since its vector, Culex quinquefasciatus the southern house mosquito, was first introduced to Hawaii around 1830. In order to understand the dynamics of the disease in Hawaii and gain insights into the evolution of vector-mediated parasite&ndash;host interactions in general we studied the population genetics of Cx. quinquefasciatus in the Hawaiian Islands. We used both microsatellite and mitochondrial loci. Not surprisingly we found that mosquitoes in Midway, a small island in the Western group, are quite distinct from the populations in the main Hawaiian Islands. However, we also found that in general mosquito populations are relatively isolated even among the main islands, in particular between Hawaii (the Big Island) and the remaining Hawaiian Islands. We found evidence of bottlenecks among populations within the Big Island and an excess of alleles in Maui, the site of the original introduction. The mitochondrial diversity was typically low but higher than expected. The current distribution of mitochondrial haplotypes combined with the microsatellite information lead us to conclude that there have been several introductions and to speculate on some processes that may be responsible for the current population genetics of vectors of avian malaria in Hawaii.

Hawai'i

Biological control of Aedes mosquito larvae with carnivorous aquatic plant, Utricularia macrorhiza

Background Biological controls with predators of larval mosquito vectors have historically focused almost exclusively on insectivorous animals, with few studies examining predatory plants as potential larvacidal agents. In this study, we experimentally evaluate a generalist plant predator of North America, Utricularia macrorhiza, the common bladderwort, and evaluate its larvacidal efficiency for the mosquito vectors Aedes aegypti and Aedes albopictus in no-choice, laboratory experiments. We sought to determine first, whether U. macrorhiza is a competent predator of container-breeding mosquitoes, and second, its predation efficiency for early and late instar larvae of each mosquito species. Methods Newly hatched, first instar Aedes albopictus and Aedes aegypti larvae were separately exposed in cohorts of 10 to field collected U. macrorhiza cuttings. Data on development time and larval survival were collected on a daily basis to ascertain the effectiveness of U. macrorhiza as a larval predator. Survival models were used to assess differences in larval survival between cohorts that were exposed to U. macrorhiza and those that were not. A permutation analysis was used to investigate whether storing U. macrorhiza in laboratory conditions for extended periods of time (1 month vs. 6 months) affected its predation efficiency. Results Our results indicated a 100% and 95% reduction of survival of Ae. aegypti and Ae. albopictus larvae respectively, in the presence of U. macrorhiza relative to controls within five days, with peak larvacidal efficiency in plant cuttings from ponds collected in August. Utricularia macrorhiza cuttings, which were prey-deprived, and maintained in laboratory conditions for 6 months were more effective larval predators than cuttings, which were maintained prey-free for 1 month. Conclusions Due to the combination of high predation efficiency and the unique biological feature of facultative predation, we suggest that U. macrorhiza warrants further development as a method for larval mosquito control.

Rhode Island

Adverse moisture events predict seasonal abundance of Lyme disease vector ticks (Ixodes scapularis)

Background : Lyme borreliosis (LB) is the most commonly reported vector-borne disease in north temperate regions worldwide, affecting an estimated 300,000 people annually in the United States alone. The incidence of LB is correlated with human exposure to its vector, the blacklegged tick ( Ixodes scapularis ). To date, attempts to model tick encounter risk based on environmental parameters have been equivocal. Previous studies have not considered (1) the differences between relative humidity (RH) in leaf litter and at weather stations, (2) the RH threshold that affects nymphal blacklegged tick survival, and (3) the time required below the threshold to induce mortality. We clarify the association between environmental moisture and tick survival by presenting a significant relationship between the total number of tick adverse moisture events (TAMEs - calculated as microclimatic periods below a RH threshold) and tick abundance each year. Methods : We used a 14-year continuous statewide tick surveillance database and corresponding weather data from Rhode Island (RI), USA, to assess the effects of TAMEs on nymphal populations of I. scapularis . These TAMEs were defined as extended periods of time (>8 h below 82% RH in leaf litter). We fit a sigmoid curve comparing weather station data to those collected by loggers placed in tick habitats to estimate RH experienced by nymphal ticks, and compiled the number of historical TAMEs during the 14-year record. Results : The total number of TAMEs in June of each year was negatively related to total seasonal nymphal tick densities, suggesting that sub-threshold humidity episodes >8 h in duration naturally lowered nymphal blacklegged tick abundance. Furthermore, TAMEs were positively related to the ratio of tick abundance early in the season when compared to late season, suggesting that lower than average tick abundance for a given year resulted from tick mortality and not from other factors. Conclusions : Our results clarify the mechanism by which environmental moisture affects blacklegged tick populations, and offers the possibility to more accurately predict tick abundance and human LB incidence. We describe a method to forecast LB risk in endemic regions and identify the predictive role of microclimatic moisture conditions on tick encounter risk.

Rhode Island

Avian malaria in a boreal resident species: long-term temporal variability, and increased prevalence in birds with avian keratin disorder

The prevalence of vector-borne parasitic diseases is widely influenced by biological and ecological factors. Environmental conditions such as temperature and precipitation can have a marked effect on haemosporidian parasites ( Plasmodium spp.) that cause malaria and those that cause other malaria-like diseases in birds. However, there have been few long-term studies monitoring haemosporidian infections in birds in northern latitudes, where weather conditions can be highly variable and the effects of climate change are becoming more pronounced. We used molecular methods to screen more than 2,000 blood samples collected from black-capped chickadees ( Poecile atricapillus ), a resident passerine bird. Samples were collected over a 10 year period, mostly during the non-breeding season, at seven sites in Alaska, USA. We tested for associations between Plasmodium prevalence and local environmental conditions including temperature, precipitation, site, year and season. We also evaluated the relationship between parasite prevalence and individual host factors of age, sex and presence or absence of avian keratin disorder. This disease, which causes accelerated keratin growth in the beak, provided a natural study system in which to test the interaction between disease state and malaria prevalence. Prevalence of Plasmodium infection varied by year, site, age and individual disease status but there was no support for an effect of sex or seasonal period. Significantly, birds with avian keratin disorder were 2.6 times more likely to be infected by Plasmodium than birds without the disorder. Interannual variation in the prevalence of Plasmodium infection at different sites was positively correlated with summer temperatures at the local but not statewide scale. Sequence analysis of the parasite cytochrome b gene revealed a single Plasmodium spp. lineage, P43. Our results demonstrate associations between prevalence of avian malaria and a variety of biological and ecological factors. These results also provide important baseline data that will be informative for predicting future changes in Plasmodium prevalence in the subarctic.

Alaska

Comparison of survival patterns of northern and southern genotypes of the North American tick Ixodes scapularis (Acari: Ixodidae) under northern and southern conditions

Background Several investigators have reported genetic differences between northern and southern populations of Ixodes scapularis in North America, as well as differences in patterns of disease transmission. Ecological and behavioral correlates of these genetic differences, which might have implications for disease transmission, have not been reported. We compared survival of northern with that of southern genotypes under both northern and southern environmental conditions in laboratory trials. Methods Subadult I. scapularis from laboratory colonies that originated from adults collected from deer from several sites in the northeastern, north central, and southern U.S. were exposed to controlled conditions in environmental chambers. Northern and southern genotypes were exposed to light:dark and temperature conditions of northern and southern sites with controlled relative humidities, and mortality through time was recorded. Results Ticks from different geographical locations differed in survival patterns, with larvae from Wisconsin surviving longer than larvae from Massachusetts, South Carolina or Georgia, when held under the same conditions. In another experiment, larvae from Florida survived longer than larvae from Michigan. Therefore, survival patterns of regional genotypes did not follow a simple north–south gradient. The most consistent result was that larvae from all locations generally survived longer under northern conditions than under southern conditions. Conclusions Our results suggest that conditions in southern North America are less hospitable than in the north to populations of I. scapularis . Southern conditions might have resulted in ecological or behavioral adaptations that contribute to the relative rarity of I. scapularis borne diseases, such as Lyme borreliosis, in the southern compared to the northern United States.

Parasites & Vectors

International meeting on sarcoptic mange in wildlife, June 2018, Blacksburg, Virginia, USA

Sarcoptic mange is a globally distributed disease caused by the burrowing mite Sarcoptes scabiei , which also causes scabies in humans. A wide and increasing number of wild mammal species are reported to be susceptible to mange; however, the impacts of the disease in wildlife populations, mechanisms involved in its eco-epidemiological dynamics, and risks to public and ecosystem health are still unclear. Major gaps exist concerning S. scabiei host specificity and the mechanisms involved in the different presentations of the disease, which change between individuals and species. Immunological responses to the mite may have a relevant role explaining these different susceptibilities, as these affect the clinical signs, and consequently, the severity of the disease. Recently, some studies have suggested sarcoptic mange as an emerging threat for wildlife, based on several outbreaks with increased severity, geographical expansions, and novel wild hosts affected. Disease ecology experts convened for the “International Meeting on Sarcoptic Mange in Wildlife” on 4–5 June 2018, hosted by the Department of Fish and Wildlife Conservation at Virginia Tech in Blacksburg, Virginia, USA. The meeting had a structure of (i) pre-workshop review; (ii) presentation and discussions; and (iii) identification of priority research questions to understand sarcoptic mange in wildlife. The workgroup concluded that research priorities should be on determining the variation in modes of transmission for S. scabiei in wildlife, factors associated with the variation of disease severity among species, and long-terms effects of the mange in wildlife populations. In this note we summarize the main discussions and research gaps identified by the experts.

Parasites & Vectors

Optimal temperature for malaria transmission is dramaticallylower than previously predicted

The ecology of mosquito vectors and malaria parasites affect the incidence, seasonal transmission and geographical range of malaria. Most malaria models to date assume constant or linear responses of mosquito and parasite life-history traits to temperature, predicting optimal transmission at 31 °C. These models are at odds with field observations of transmission dating back nearly a century. We build a model with more realistic ecological assumptions about the thermal physiology of insects. Our model, which includes empirically derived nonlinear thermal responses, predicts optimal malaria transmission at 25 °C (6 °C lower than previous models). Moreover, the model predicts that transmission decreases dramatically at temperatures > 28 °C, altering predictions about how climate change will affect malaria. A large data set on malaria transmission risk in Africa validates both the 25 °C optimum and the decline above 28 °C. Using these more accurate nonlinear thermal-response models will aid in understanding the effects of current and future temperature regimes on disease transmission.

Ecology Letters