Heterogeneous Feeding Patterns of the Dengue Vector,Aedes aegypti,on Individual Human Hosts in Rural Thailand

Background

Mosquito biting frequency and how bites are distributed among different people can have significant epidemiologic effects. An improved understanding of mosquito vector-human interactions would refine knowledge of the entomological processes supporting pathogen transmission and could reveal targets for minimizing risk and breaking pathogen transmission cycles.

Methodology and principal findings

We used human DNA blood meal profiling of the dengue virus (DENV) vector, Aedes aegypti, to quantify its contact with human hosts and to infer epidemiologic implications of its blood feeding behavior. We determined the number of different people bitten, biting frequency by host age, size, mosquito age, and the number of times each person was bitten. Of 3,677 engorged mosquitoes collected and 1,186 complete DNA profiles, only 420 meals matched people from the study area, indicating that Ae. aegypti feed on people moving transiently through communities to conduct daily business. 10–13% of engorged mosquitoes fed on more than one person. No biting rate differences were detected between high- and low-dengue transmission seasons. We estimate that 43–46% of engorged mosquitoes bit more than one person within each gonotrophic cycle. Most multiple meals were from residents of the mosquito collection house or neighbors. People ≤25 years old were bitten less often than older people. Some hosts were fed on frequently, with three hosts bitten nine times. Interaction networks for mosquitoes and humans revealed biologically significant blood feeding hotspots, including community marketplaces.

Conclusion and significance

High multiple-feeding rates and feeding on community visitors are likely important features in the efficient transmission and rapid spread of DENV. These results help explain why reducing vector populations alone is difficult for dengue prevention and support the argument for additional studies of mosquito feeding behavior, which when integrated with a greater understanding of human behavior will refine estimates of risk and strategies for dengue control.     

Seasonal and diel patterns of biting midges (Ceratopogonidae) and mosquitoes (Culicidae) on the Parris Island Marine Corps Recruit Depot

The Marine Corps Recruit Depot on Parris Island, SC, is surrounded by tidal salt marshes, which are breeding habitats for many pestiferous biting flies. Knowledge of biting fly behavior patterns is needed to develop effective pest management strategies in urban areas adjacent to salt marshes. We measured biting midge (Ceratopogonidae) and mosquito (Culicidae) seasonal abundance and diel activity patterns on Parris Island using CO₂‐baited suction traps from November 2001 – November 2004. Of the three biting midge species collected, Culicoides furens was most abundant (86.2% of total) and was present in high numbers from late March to November. Culicoides hollensis (12.0% of total) was present during spring and fall but absent in summer and winter; and Culicoides melleus (1.7% of total) was present in spring through fall but absent in winter. Abundance of C. furens had a positive linear correlation with air temperature and rainfall. There were nonlinear correlations between air temperature and C. hollensis and C. melleus numbers, which were most abundant at moderate temperatures. Of 18 mosquito species collected, the most abundant were Aedes taeniorhynchus (42.7% of total), Aedes sollicitans (26.3% of total), Culex salinarius (15.6% of total), Culex quinquefasciatus (7.3% of total), and Aedes vexans (5.7% of total); other species comprised <5% of collections. Aedes taeniorhynchus numbers were positively correlated with temperature and rainfall, and Cx. salinarius was correlated with soil moisture. Activity of most biting midges and mosquitoes were highest the first two hours following sunset. Species of biting flies were present in all months, suggesting that year‐round control measures are necessary to reduce exposure to potential disease vectors and nuisance biting.     

Diversity,distribution, abundance,and feeding pattern of tropical ornithophilic mosquitoes

Bird–biting mosquitoes act as bridge vectors of diverse pathogens of emerging infectious diseases. In this study, we report for the first time the abundance, diversity, distribution, and feeding pattern of bird‐biting mosquitoes on an island where avifaunal diversity is rich. Monthly mosquito collections were done at six different habitats in three different climatic zones using bird‐baited traps over a year. Collected mosquitoes were identified using morphological and molecular tools. A total of 2,655 bird‐biting mosquitoes of eight genera and 25 species were identified. Of these, 52% were Culex species, which represents 35% of the Culex species in the country. The most abundant species were Culex sitiens, Cx. pseudovishnui, Cx. nigropunctatus and Cx. quinquefasciatus, whereas the latter two were common to all habitats. The highest abundance was reported in lowland forests (49.6%), while it was lowest in highland forests (22.3%). Highest species similarity was reported from highland forests. Seasonal variations of the most abundant species were significantly different in selected habitats (p< 0.05). Two distinct biting peaks were identified, from 06:00 to 21:00 and 22:00 to 02:00. The biting nature of identified ornithophilic mosquitoes suggests the potential vector status of these mosquitoes.     

Care of dogs and attitudes of dog owners in Port-au-Prince, the Republic of Haiti

This article reports the first known study on dogs in Port-au-Prince. Interviews with 1,290 residents provided information on 1,804 dogs. More than 57.7% of homes kept dogs. Not all the dogs received vaccinations for rabies (41.6%), even though 28.2% of households had had a household member bitten by a dog. Although the "owned" dog population had decreased as a result of the earthquake in January 2010, the number of roaming dogs appeared to have been uninfluenced by the disaster. Given that 64.8% of dogs probably had access to the street and only 6.0% of the females were spayed, to humanely contain the dog population will require both confinement and neutering. Although roaming dogs were considered a nuisance by 63.3% of respondents, 42.6% of households fed dogs they did not own.     

A Survey of Attitudes of Local Citizens of a Residential Area Toward Urban Stray Cats in Japan

This study surveyed the attitudes of local residents living in an urban area in Japan toward stray cats. An anonymous questionnaire asked local residents (359 houses) about their attitudes toward stray cats. Responses were received from126 houses (35%). Answers about nuisance, respondents' actions, and actions to be taken with regard to stray cats did not differ by place or type of residence of respondents. More than one third (36.7 ± 16.6%) of the respondents answered that the “bad smell of the feces and urine” was a nuisance. Respondents who lived in detached houses tended to like cats compared with those who lived in condominiums. Respondents who liked cats took care of cats more frequently, whereas those who disliked cats chased cats away and prevented their intrusion into their houses and land. However, it is noteworthy that one third or more (minimum value: 37.8%) of respondents of all kinds answered that neutering is one effective way to suppress the population of stray cats.     

Worker biting interactions and task performance in a swarm-founding eusocial wasp (Polybia occidentalis, Hymenoptera: Vespidae)

Workers in many insect societies interact via body contact withtheir nest mates, and social biting and other forms of contactmay play a general role in regulating task performance. HereI present evidence that social biting affects task performancewithout direct reproductive conflict in Polybia occidentalis,a swarm-founding eusocial wasp. Polybia occidentalis workersengaged in social biting with nest mates. Most workers thatwere active on the nest surface participated in biting interactions,but individuals differed significantly in their rates of biting and of being bitten. Rates of being bitten corresponded withnonreproductive task performance: more biting was directedat foragers than nonforagers, and foraging rates were correlatedwith rates of being bitten. Furthermore, some on-nest workersinitiated foraging activity immediately after they were bitten.Together these patterns suggest that social biting influencesforaging rates by increasing workers' probabilities of leavingthe nest. Variation in biting rates did not correspond withdifferences in reproductive physiology: highly active bitersand recipients did not differ in body size or in ovary development.In P. occidentalis and in other eusocial insects with largeworker forces, biting and other types of social contact amongworkers may regulate task performance independently of directreproductive competition.     

Economic Evaluation of an Area-Wide Integrated Pest Management Program to Control the Asian Tiger Mosquito in New Jersey

Aedes albopictus is the most invasive mosquito in the world, an important disease vector, and a biting nuisance that limits outdoor activities. Area-wide integrated pest management (AW-IPM) is the recommended control strategy. We conducted an economic evaluation of the AW-IPM project in Mercer and Monmouth Counties, New Jersey with a controlled design (AW-IPM vs. control) from 2009 through 2011. The study analyzed financial documents and staff time for AW-IPM and surveyed an average of 415 randomly chosen households in AW-IPM and control areas each fall from 2008 through 2011. Hours lost from yard and porch activities were calculated as differences between actual and potential hours of these activities in an average summer week if there had been no mosquito concerns. Net estimated benefits of AW-IPM were based on cross-over and difference-in-difference analyses. Reductions in hours lost were valued based on respondents'' willingness to pay for a hypothetical extra hour free of mosquitoes spent on yard or porch activities and literature on valuation of a quality adjusted life year (QALY). The incremental cost of AW-IPM per adult was $41.18 per year. Number of hours lost due to mosquitoes in AW-IPM areas between the base year (2008) and the intervention years (2009-2011) declined by 3.30 hours per summer week in AW-IPM areas compared to control areas. Survey respondents valued this improvement at $27.37 per adult per summer week. Over the 13-week summer, an average adult resident gained 42.96 hours of yard and porch time, worth $355.82. The net benefit over the summer was $314.63. With an average of 0.0027 QALYs gained per adult per year, AW-IPM was cost effective at $15,300 per QALY gained. The benefit-cost ratio from hours gained was 8.64, indicating that each $1 spent on AW-IPM gave adults additional porch and yard time worth over $8.     

The status of the Hen Harrier,Circus cyaneus,in the UK and Isle of Man in 2010

Capsule The fourth national survey of Hen Harrier showed that the population in the UK and the Isle of Man declined significantly between 2004 and 2010.

Aim To estimate the size of the breeding Hen Harrier population (with associated 95% confidence intervals) in the UK and Isle of Man, constituent countries and Scottish regions, in 2010 and calculate population change since previous surveys in 1998 and 2004.

Methods Complete surveys were made of 10-km squares likely to be occupied by breeding Hen Harriers in England, Wales, Northern Ireland and the Isle of Man, using standard methods developed for previous national surveys. In Scotland, a ‘census’ area was non-randomly selected for survey by volunteers, and randomly selected squares were surveyed in two strata covering the rest of the known range.

Results The UK and Isle of Man Hen Harrier population was estimated at 662 territorial pairs (95% confidence interval (CI): 576–770), a significant decline of 18% since 2004. Scotland holds the bulk (76%) of the population (505 territorial pairs; 95% CI: 417–612), with smaller numbers in Northern Ireland (59 pairs), Wales (57 pairs), the Isle of Man (29 pairs) and England (12 pairs). Declines of 49% and 20% were observed in the Isle of Man and in Scotland, respectively, whereas the Welsh population increased by 33%. A significant decrease was recorded in numbers of pairs using young and mature plantation forest in Scotland.

Conclusion The breeding population of Hen Harriers in the UK and Isle of Man declined between 2004 and 2010. Notable decreases in Scotland and the Isle of Man may be related to habitat change and illegal persecution. Illegal persecution continues to limit the population size of harriers in England to very low levels.     

Revisiting the basic reproductive number for malaria and its implications for malaria control

The prospects for the success of malaria control depend, in part, on the basic reproductive number for malaria, R0. Here, we estimate R0 in a novel way for 121 African populations, and thereby increase the number of R0 estimates for malaria by an order of magnitude. The estimates range from around one to more than 3,000. We also consider malaria transmission and control in finite human populations, of size H. We show that classic formulas approximate the expected number of mosquitoes that could trace infection back to one mosquito after one parasite generation, Z0(H), but they overestimate the expected number of infected humans per infected human, R0(H). Heterogeneous biting increases R0 and, as we show, Z0(H), but we also show that it sometimes reduces R0(H); those who are bitten most both infect many vectors and absorb infectious bites. The large range of R0 estimates strongly supports the long-held notion that malaria control presents variable challenges across its transmission spectrum. In populations where R0 is highest, malaria control will require multiple, integrated methods that target those who are bitten most. Therefore, strategic planning for malaria control should consider R0, the spatial scale of transmission, human population density, and heterogeneous biting.     

Sociodemographic predictors of knowledge,mosquito bite patterns and protective behaviors concerning vector borne disease: The case of dengue fever in Chinese subtropical city,Hong Kong

Geographic pattern of dengue fever is changing due to the global environmental and climate changes in the 21^st century. Evidence of community’s knowledge, mosquito bite patterns and protective behavior practices in non-endemic regions is limited. This study examined the knowledge of dengue, mosquito bite patterns, protective behavior practices and their associated factors in Hong Kong, a non-endemic subtropical city. A population-based random telephone survey (n = 590) was conducted three weeks after the government announcement of a local dengue outbreak in August 2018. Sociodemographic status, awareness, knowledge, protective measures, bite patterns of mosquito were collected. Results indicated high level of community awareness of the local outbreak (95.2%), symptom identification (84.0%) and adoption of at least one mosquito protective measures (nearly 80%). About 40% of respondents reported that they were bitten by mosquitoes during the study period, a high mosquito season in Hong Kong. Mosquito bites were prevalent near grassy area (63.4%), at home (42.6%) and at public transportation waiting spots (39.6%). Younger people (< 25 years old), female, those who lived on lower floors (≤the 6^th) and near grassy area were at higher risk of mosquito bites at home. Respondents perceived higher threat of dengue to society were more likely to practice mosquito prevention. While residential factors affected their indoor prevention, other socio-demographic factors affected the outdoor prevention. Practicing prevention behaviors were associated with self-reported mosquito bite at home. Furthermore, the general prevention uptake rate unchanged after the announcement of local dengue outbreak. Although the uptake rate of protective measures during August was high, 40% participants reported they were bitten. Also public locations are more common area for bites, which suggested stronger mosquito prevention and control on public environments and more personal protective behaviors should be advocated.     

The ecology of the scorpion Euscorpius flavicaudis in England

A large colony of Euscorpius flavicaudis was studied at Sheerness Docks, Isle of Sheppey, Kent. It was probably established in the late nineteenth century. The scorpions inhabit cracks in the dockyard perimeter wall where the mortar pointing has crumbled away. They are nocturnal, "sit-and-wait", generalist predators. They are extremely sedentary: females leave their cracks fewer than 10 times per year; males are more active as they become vagrant prior to the mating season, which occurs in summer. Marked adults were resighted at intervals of over a year and the distance scorpions moved between resightings was not proportional to the interval. The number of scorpions seen per night was influenced by temperature, amount of rainfall and phase of the moon. In winter, the scorpions retreated far into the wall and, by doing so, reduced the risk of suffering mortality due to cold. During this time, they were seldom active. In general, this species does not behave in any way that can be correlated with living in a temperate rather than a desert area. This illustrates the extreme adaptability of scorpions.     

Juvenile hormone regulation of the second biting cycle in Culex pipiens

Juvenile hormone regulation of the second biting cycle was studied in Culex pipiens by allatectomizing mosquitoes at daily intervals after the first blood meal. Mosquitoes oviposited and were tested for biting 2 days later. Allatectomy on days 1 through 4 prevented biting in a high percentage of females, indicating that juvenile hormone was required for a second biting cycle. When allatectomy was delayed 6 or more days after the first blood meal, the mosquitoes took a second blood meal after oviposition even though eggs were retained at the time of allatectomy. Thus, egg retention did not prevent mosquitoes from releasing juvenile hormone for a second biting cycle. Unoperated mosquitoes also bit when they were forced to retain eggs after the first blood meal. However, these mosquitoes only fed on blood if they were confined on or near the host; they would not feed in cages where host seeking was required to locate the host. Based on these findings, it appeared that oviposition was necessary to initiate host-seeking behaviour, whereas juvenile hormone release initiated biting. These results, in conjunction with earlier work demonstrating juvenile hormone induction of the first biting cycle, indicated that alternating periods of juvenile hormone production and oviposition regulate the cyclic patterns of biting and host-seeking behaviour throughout the life of the mosquito.     

The risk of a mosquito-borne infection in a heterogeneous environment

A common assumption about malaria, dengue, and other mosquito-borne infections is that the two main components of the risk of human infection—the rate at which people are bitten (human biting rate) and the proportion of mosquitoes that are infectious—are positively correlated. In fact, these two risk factors are generated by different processes and may be negatively correlated across space and time in heterogeneous environments. Uneven distribution of blood-meal hosts and larval habitat creates a spatial mosaic of demograPhic sources and sinks. Moreover, mosquito populations fluctuate temporally, forced by environmental variables such as rainfall, temperature, and humidity. These sources of spatial and temporal heterogeneity in the distribution of mosquito populations generate variability in the human biting rate, in the proportion of mosquitoes that are infectious, and in the risk of human infection. To understand how heterogeneity affects the epidemiology of mosquito-borne infections, we developed a set of simple models that incorporate heterogeneity in a stepwise fashion. These models predict that the human biting rate is highest shortly after the mosquito densities peak, near breeding sites where adult mosquitoes emerge, and around the edges of areas where humans are aggregated. In contrast, the proportion of mosquitoes that are infectious reflects the age structure of mosquito populations; it peaks where old mosquitoes are found, far from mosquito breeding habitat, and when mosquito population density is declining. Finally, we show that estimates for the average risk of infection that are based on the average entomological inoculation rate are strongly biased in heterogeneous environments.     

Roaming Companion Cats as Potential Causes of Conflict and Controversy: A Representative Questionnaire Study of the Danish Public

Cats have grown in popularity as companion animals, but there are also people who strongly dislike them. Companion cats allowed to roam freely outdoors are seen by some as a nuisance. This paper, drawing on research conducted in Denmark, aims to quantify potentially conflicting attitudes to cats among the public that may feed into cat-related conflicts and controversies. Questionnaire data were collected from a representative sample of the Danish population (n = 2,003), where 21% (n = 415) owned cats and 79% (n = 1,588) did not. In all, 65% of respondents confirmed that they liked cats, 21% reported that they did not, and 14% were undecided. The main reasons for disliking cats concerned “behavior,” not hazards such as the spread of diseases and predation. Of the 21% of the surveyed Danes who reported that they currently had a cat in the household, 72% allowed their cat to roam outdoors. Sixty percent of the respondents did not perceive this as a problem. However, the potential for conflict was demonstrated by the fact that 27% of respondents regarded outdoor roaming as problematic. Of these, about a quarter saw free-roaming cats as a big problem and as a cause of strife between neighbors. Comparatively fewer of those who owned cats saw their animals as a cause of problems. Thus, only 12% of those owning outdoor cats thought that problems were caused when their cats defecated in a neighbor’s garden, which compares with the 17% of the total population who are bothered by other people’s cats defecating in their gardens. Our data show that while the majority of Danes believe cats should be allowed to roam in public spaces, a significant minority strongly dislikes cats and would prefer restrictions on roaming.     

Conditioning individual mosquitoes to an odor: sex, source, and time

Olfactory conditioning of mosquitoes may have important implications for vector-pathogen-host dynamics. If mosquitoes learn about specific host attributes associated with pathogen infection, it may help to explain the heterogeneity of biting and disease patterns observed in the field. Sugar-feeding is a requirement for survival in both male and female mosquitoes. It provides a starting point for learning research in mosquitoes that avoids the confounding factors associated with the observer being a potential blood-host and has the capability to address certain areas of close-range mosquito learning behavior that have not previously been described. This study was designed to investigate the ability of the southern house mosquito, Culex quinquefasciatus Say to associate odor with a sugar-meal with emphasis on important experimental considerations of mosquito age (1.2 d old and 3-5 d old), sex (male and female), source (laboratory and wild), and the time between conditioning and testing (<5 min, 1 hr, 2.5 hr, 5 hr, 10 hr, and 24 hr). Mosquitoes were individually conditioned to an odor across these different experimental conditions. Details of the conditioning protocol are presented as well as the use of binary logistic regression to analyze the complex dataset generated from this experimental design. The results suggest that each of the experimental factors may be important in different ways. Both the source of the mosquitoes and sex of the mosquitoes had significant effects on conditioned responses. The largest effect on conditioning was observed in the lack of positive response following conditioning for females aged 3-5 d derived from a long established colony. Overall, this study provides a method for conditioning experiments involving individual mosquitoes at close range and provides for future discussion of the relevance and broader questions that can be asked of olfactory conditioning in mosquitoes.     

Individual piglets' contribution to the development of tail biting

Conflicting hypotheses exist about the contribution of individual pigs to the development of a tail-biting outbreak, but there is limited quantitative information to support or dismiss them. This study aims to quantify the development of tail-biting behaviour at pen and individual piglet level, before and after the first visible tail damage. Video recordings of 14 pens with tail-biting outbreaks and individually marked weaned piglets were used to observe tail-biting incidents (TBIs; piglet biting a penmate's tail). When visible tail damage was first observed in a pen (i.e. day of tail biting outbreak; D0), the video recordings of the previous 6 (till D-6) and the following 6 days (till D6) were analysed every other day for TBIs and the identities of the biter and bitten piglet were recorded. The average TBIs per individual piglet (within each pen) per observation day were analysed to quantify the development of tail-biting behaviour and to identify pronounced biters and/or bitten piglets. The (absence of) coherence for TBIs in a pen was used to test whether biters preferred a specific penmate. There was an exponential increase in the intensity (linear on log scale) of the TBIs from an average of 0.7 bites/h at D-6 to 2.3 bites/h at D6. An additional negative quadratic component suggests that a plateau for tail-biting behaviour was reached by the end of the observation period. Before any visible tail damage was observed (i.e. before D0), 82% of the piglets performed and 96% of them received tail bites. After D0, the figures were 99% and 100%, respectively. One or a few pronounced biters could be identified in almost all pens. These biters already showed more tail biting at D-6 than their penmates. Furthermore, these biters showed a greater increase in tail-biting behaviour during the observation period than the average scores of their penmates. In contrast, there was no apparent increase in the receipt of bites among the piglets that had already been bitten more than their penmates at D-6. Finally, there was no significant coherence between biters and bitten piglets, indicating that biters showed no preference for biting particular penmates, even when some of them had a damaged tail. These results show that, by using observations of TBIs, possible biters or bitten piglets can already be identified 6 days before tail damage is first apparent in a pen.     

Studies on effects of Pelargonium citrosa leaf extracts on malarial vector,Anopheles stephensi Liston

Methanol extracts of Pelargonium citrosa leaf were tested for their biological, larvicidal, pupicidal, adulticidal, antiovipositional activity, repellency and biting deterrency against Anopheles stephensi. Larval mortality was dose dependent with the highest dose of 4% plant extract evoking 98% mortality. The extracts affected pupicidal and adulticidal activity and significantly decreased fecundity and longevity of A. stephensi. The larval, pupal and adult development were completely inhibited by the treatment. At 4% the extracts evoked strong repellent action. They also interfered with oviposition, egg hatchability, and exhibited a growth inhibiting effect against larvae and good repellency against adults of A. stephensi. The leaf extract treatment significantly enhanced biting deterrency. As naturally occurring insecticides, these plant derived materials could be useful as an alternative for synthetic insecticides controlling field populations of mosquitoes.     

Determinants of Heterogeneous Blood Feeding Patterns by Aedes aegypti in Iquitos,Peru

Background

Heterogeneous mosquito biting results in different individuals in a population receiving an uneven number of bites. This is a feature of many vector-borne disease systems that, if understood, could guide preventative control efforts toward individuals who are expected to contribute most to pathogen transmission. We aimed to characterize factors determining biting patterns of Aedes aegypti, the principal mosquito vector of dengue virus.

Methodology/Principal Findings

Engorged female Ae. aegypti and human cheek swabs were collected from 19 houses in Iquitos, Peru. We recorded the body size, age, and sex of 275 consenting residents. Movement in and out of the house over a week (time in house) and mosquito abundance were recorded on eight separate occasions in each household over twelve months. We identified the individuals bitten by 96 engorged mosquitoes over this period by amplifying specific human microsatellite markers in mosquito blood meals and human cheek swabs. Using a multinomial model assuming a saturating relationship (power), we found that, relative to other residents of a home, an individual''s likelihood of being bitten in the home was directly proportional to time spent in their home and body surface area (p<0.05). A linear function fit the relationship equally well (ΔAIC<1).

Conclusions/Significance

Our results indicate that larger people and those who spend more time at home are more likely to receive Ae. aegypti bites in their homes than other household residents. These findings are consistent with the idea that measurable characteristics of individuals can inform predictions of the extent to which different people will be bitten. This has implications for an improved understanding of heterogeneity in different people''s contributions to pathogen transmission, and enhanced interventions that include the people and places that contribute most to pathogen amplification and spread.