Christopher M. Barker

The global distribution of the arbovirus vectors Aedes aegypti and Ae. albopictus

Dengue and chikungunya are increasing global public health concerns due to their rapid geographical spread and increasing disease burden. Knowledge of the contemporary distribution of their shared vectors, Aedes aegypti and Aedes albopictus remains incomplete and is complicated by an ongoing range expansion fuelled by increased global trade and travel. Mapping the global distribution of these vectors and the geographical determinants of their ranges is essential for public health planning. Here we compile the largest contemporary database for both species and pair it with relevant environmental variables predicting their global distribution. We show Aedes distributions to be the widest ever recorded; now extensive in all continents, including North America and Europe. These maps will help define the spatial limits of current autochthonous transmission of dengue and chikungunya viruses. It is only with this kind of rigorous entomological baseline that we can hope to project future health impacts of these viruses. DOI: http://dx.doi.org/10.7554/eLife.08347.001

Ross, Macdonald, and a Theory for the Dynamics and Control of Mosquito-Transmitted Pathogens

Ronald Ross and George Macdonald are credited with developing a mathematical model of mosquito-borne pathogen transmission. A systematic historical review suggests that several mathematicians and scientists contributed to development of the Ross-Macdonald model over a period of 70 years. Ross developed two different mathematical models, Macdonald a third, and various “Ross-Macdonald” mathematical models exist. Ross-Macdonald models are best defined by a consensus set of assumptions. The mathematical model is just one part of a theory for the dynamics and control of mosquito-transmitted pathogens that also includes epidemiological and entomological concepts and metrics for measuring transmission. All the basic elements of the theory had fallen into place by the end of the Global Malaria Eradication Programme (GMEP, 1955–1969) with the concept of vectorial capacity, methods for measuring key components of transmission by mosquitoes, and a quantitative theory of vector control. The Ross-Macdonald theory has since played a central role in development of research on mosquito-borne pathogen transmission and the development of strategies for mosquito-borne disease prevention.

A systematic review of mathematical models of mosquito-borne pathogen transmission: 1970-2010

Mathematical models of mosquito-borne pathogen transmission originated in the early twentieth century to provide insights into how to most effectively combat malaria. The foundations of the Ross–Macdonald theory were established by 1970. Since then, there has been a growing interest in reducing the public health burden of mosquito-borne pathogens and an expanding use of models to guide their control. To assess how theory has changed to confront evolving public health challenges, we compiled a bibliography of 325 publications from 1970 through 2010 that included at least one mathematical model of mosquito-borne pathogen transmission and then used a 79-part questionnaire to classify each of 388 associated models according to its biological assumptions. As a composite measure to interpret the multidimensional results of our survey, we assigned a numerical value to each model that measured its similarity to 15 core assumptions of the Ross–Macdonald model. Although the analysis illustrated a growing acknowledgement of geographical, ecological and epidemiological complexities in modelling transmission, most models during the past 40 years closely resemble the Ross–Macdonald model. Modern theory would benefit from an expansion around the concepts of heterogeneous mosquito biting, poorly mixed mosquito-host encounters, spatial heterogeneity and temporal variation in the transmission process.

The global compendium of Aedes aegypti and Ae. albopictus occurrence.

Aedes aegypti and Ae. albopictus are the main vectors transmitting dengue and chikungunya viruses. Despite being pathogens of global public health importance, knowledge of their vectors’ global distribution remains patchy and sparse. A global geographic database of known occurrences of Ae. aegypti and Ae. albopictus between 1960 and 2014 was compiled. Herein we present the database, which comprises occurrence data linked to point or polygon locations, derived from peer-reviewed literature and unpublished studies including national entomological surveys and expert networks. We describe all data collection processes, as well as geo-positioning methods, database management and quality-control procedures. This is the first comprehensive global database of Ae. aegypti and Ae. albopictus occurrence, consisting of 19,930 and 22,137 geo-positioned occurrence records respectively. Both datasets can be used for a variety of mapping and spatial analyses of the vectors and, by inference, the diseases they transmit.

DIFFERENTIAL IMPACT OF WEST NILE VIRUS ON CALIFORNIA BIRDS

Abstract. The strain of West Nile virus (WNV) currently epidemic in North America contains a genetic mutation elevating its virulence in birds, especially species in the family Corvidae. Although dead American Crows (Corvus brachyrhynchos) have been the hallmark of the epidemic, the overall impact of WNV on North America’s avifauna remains poorly understood and has not been addressed thoroughly in California. Here, we evaluate variation by species in the effect of WNV on California birds from 2004 to 2007 by using (1) seroprevalence in free-ranging birds, (2) percentage of carcasses of each species reported by the public that tested positive for WNV, (3) mortality determined from experimental infections, and (4) population declines detected by trend analysis of Breeding Bird Survey (BBS) data. Using Bayesian linear models, we extrapolate trends in BBS data from 1980–2003 (pre-WNV) to 2004–2007 (post-WNV). We attribute signifcant declines from expected abundance trends in areas supporting epiornitics to WNV transmission. We combine risk assessed from each of the four data sets to generate an overall score describing WNV risk by species. The susceptibility of California avifauna to WNV varies widely, with overall risk scores ranging from low for the refractory Rock Pigeon (Columba livia) through high for the susceptible American Crow. Other species at high risk include, in descending order, the House finch (Carpodacus mexicanus) , Black- crowned N i g h t - Heron ( Nycticorax nycticorax) , Western Scrub - Jay ( Aphelocoma californica), and Yellow-billed magpie (Pica nuttalli). Our analyses emphasize the importance of multiple data sources in assessing the effect of an invading pathogen.

Role of Corvids in Epidemiology of West Nile Virus in Southern California

Abstract The invasion of different southern California landscapes by West Nile virus (WNV) and its subsequent amplification to epidemic levels during 2004 enabled us to study the impact of differing corvid populations in three biomes: the hot Colorado desert with few corvids (Coachella Valley), the southern San Joaquin Valley (Kern County) with large western scrub-jay but small American crow populations, and the cool maritime coast (Los Angeles) with a large clustered American crow population. Similar surveillance programs in all three areas monitored infection rates in mosquitoes, seroconversion rates in sentinel chickens, seroprevalence in wild birds, numbers of dead birds reported by the public, and the occurrence of human cases. Infection rates in Culex tarsalis Coquillett and sentinel chicken seroconversion rates were statistically similar among all three areas, indicating that highly competent mosquito hosts were capable of maintaining enzootic WNV transmission among less competent and widely distributed avian hosts, most likely house sparrows and house finches. In contrast, infection rates in Culex pipiens quinquefasciatus Say were statistically higher in Kern and Los Angeles counties with elevated corvid populations than in Coachella Valley with few corvids. Spatial analyses of dead corvids showed significant clusters near known American crow roosts in Los Angeles that were congruent with clusters of human cases. In this area, the incidence of human and Cx. p. quinquefasciatus infection was significantly greater within corvid clusters than without, indicating their importance in virus amplification and as a risk factor for human infection. In contrast the uniform dispersion by territorial western scrub-jays resulted in a high, but evenly distributed, incidence of human disease in Kern County.

Recasting the theory of mosquito-borne pathogen transmission dynamics and control

Mosquito-borne diseases pose some of the greatest challenges in public health, especially in tropical and sub-tropical regions of the world. Efforts to control these diseases have been underpinned by a theoretical framework developed for malaria by Ross and Macdonald, including models, metrics for measuring transmission, and theory of control that identifies key vulnerabilities in the transmission cycle. That framework, especially Macdonalds formula for R0 and its entomological derivative, vectorial capacity, are now used to study dynamics and design interventions for many mosquito-borne diseases. A systematic review of 388 models published between 1970 and 2010 found that the vast majority adopted the Ross–Macdonald assumption of homogeneous transmission in a well-mixed population. Studies comparing models and data question these assumptions and point to the capacity to model heterogeneous, focal transmission as the most important but relatively unexplored component in current theory. Fine-scale heterogeneity causes transmission dynamics to be nonlinear, and poses problems for modeling, epidemiology and measurement. Novel mathematical approaches show how heterogeneity arises from the biology and the landscape on which the processes of mosquito biting and pathogen transmission unfold. Emerging theory focuses attention on the ecological and social context for mosquito blood feeding, the movement of both hosts and mosquitoes, and the relevant spatial scales for measuring transmission and for modeling dynamics and control.

Effects of Fluctuating Daily Temperatures at Critical Thermal Extremes on Aedes aegypti Life-History Traits

Background The effect of temperature on insect biology is well understood under constant temperature conditions, but less so under more natural, fluctuating conditions. A fluctuating temperature profile around a mean of 26°C can alter Aedes aegypti vector competence for dengue viruses as well as numerous life-history traits, however, the effect of fluctuations on mosquitoes at critical thermal limits is unknown. Methodology/Principal Findings We investigated the effects of large and small daily temperature fluctuations at low (16°C) and high (35–37°C) mean temperatures, after we identified these temperatures as being thresholds for immature development and/or adult reproduction under constant temperature conditions. We found that temperature effects on larval development time, larval survival and adult reproduction depend on the combination of mean temperature and magnitude of fluctuations. Importantly, observed degree-day estimates for mosquito development under fluctuating temperature profiles depart significantly (around 10–20%) from that predicted by constant temperatures of the same mean. At low mean temperatures, fluctuations reduce the thermal energy required to reach pupation relative to constant temperature, whereas at high mean temperatures additional thermal energy is required to complete development. A stage-structured model based on these empirical data predicts that fluctuations can significantly affect the intrinsic growth rate of mosquito populations. Conclusions/Significance Our results indicate that by using constant temperatures, one could under- or over-estimate values for numerous life-history traits compared to more natural field conditions dependent upon the mean temperature. This complexity may in turn reduce the accuracy of population dynamics modeling and downstream applications for mosquito surveillance and disease prevention.

Does Variation in Culex (Diptera: Culicidae) Vector Competence Enable Outbreaks of West Nile Virus in California

Abstract Since the invasion of California by West Nile virus (family Flaviviridae, genus Flavivirus, WNV) in 2003, we have annually monitored vector competence for the NY99 strain in Culex tarsalis Coquillett, Culex pipiens quinquefasciatus Say, Culex p. pipiens L., and Culex stigmatosoma Dyar populations from four areas: deserts of Coachella Valley, densely urbanized maritime Los Angeles, southern San Joaquin Valley in Kern County, and southern Sacramento Valley near Davis in Sacramento County. Overall, Cx. stigmatosoma was the most competent vector species, followed by Cx. tarsalis and the Cx. pipiens complex. The median infectious dose (ID50) of WNV required to infect 50% of the F1 female progeny reared from wild-caught females, a measure of mesenteronal susceptibility, ranged between 5 and 8 log10 plaque forming units/ml and was not correlated with annual human case incidence or summer maximum likelihood mosquito infection estimates. Odds ratios comparing nonoutbreak years with referent outbreak years were variable and failed to show a distinct pattern for Cx. tarsalis or Cx. pipiens complex females. Apparently factors other than midgut susceptibility within the ranges we measured enabled WNV outbreaks in California. Culex populations remained competent for St. Louis encephalitis virus, indicating that the disappearance of this virus was not related to a loss of vector competence.

Habitat Preferences and Phenology of Ochlerotatus triseriatus and Aedes albopictus (Diptera: Culicidae) in Southwestern Virginia

Abstract Recently, the number of reported human cases of La Crosse encephalitis, an illness caused by mosquito-borne La Crosse virus (LAC), has increased in southwestern Virginia, resulting in a need for better understanding of the virus cycle and the biology of its vectors in the region. This study examined the spatial and temporal distributions of the primary vector of LAC, Ochlerotatus triseriatus (Say), and a potential secondary vector, Aedes albopictus (Skuse). Ovitrapping surveys were conducted in 1998 and 1999 to determine distributions and oviposition habitat preferences of the two species in southwestern Virginia. Mosquitoes also were collected for virus assay from a tire dump and a human La Crosse encephalitis case site between 1998 and 2000. Oc. triseriatus and Ae. albopictus were collected from all ovitrap sites surveyed, and numbers of Oc. triseriatus eggs generally were higher than those of Ae. albopictus. Numbers of Oc. triseriatus remained high during most of the summer, while Ae. albopictus numbers increased gradually, reaching a peak in late August and declining thereafter. In Wise County, relative Ae. albopictus abundance was highest in sites with traps placed in open residential areas. Lowest numbers of both species were found in densely forested areas. Ovitrapping during consecutive years revealed that Ae. albopictus was well established and overwintering in the area. An oviposition comparison between the yard and adjacent forest at a human La Crosse encephalitis case site in 1999 showed that Ae. albopictus preferentially oviposited in the yard surrounding the home, but Oc. triseriatus showed no preference. LAC isolations from larval and adult collections of Oc. triseriatus females from the same case site indicated the occurrence of transovarial transmission.