- freely available
Int. J. Environ. Res. Public Health 2014, 11(3), 3256-3270; doi:10.3390/ijerph110303256
Published: 19 March 2014
Abstract: Infrastructure degradation in many post-industrial cities has increased the availability of potential mosquito habitats, including container habitats that support infestations of invasive disease-vectors. This study is unique in examining both immature and adult mosquito abundance across the fine-scale variability in socio-economic condition that occurs block-to-block in many cities. We hypothesized that abundant garbage associated with infrastructure degradation would support greater mosquito production but instead, found more mosquito larvae and host-seeking adults (86%) in parcels across the higher socio-economic, low-decay block. Aedes albopictus and Culex pipiens were 5.61 (p < 0.001) and 4.60 (p = 0.001) times more abundant, respectively. Most discarded (garbage) containers were dry during peak mosquito production, which occurred during the 5th hottest July on record. Containers associated with human residence were more likely to hold water and contain immature mosquitoes. We propose that mosquito production switches from rain-fed unmanaged containers early in the season to container habitats that are purposefully shaded or watered by mid-season. This study suggests that residents living in higher socioeconomic areas with low urban decay may be at greater risk of mosquito-borne disease during peak mosquito production when local container habitats are effectively decoupled from environmental constraints.
More than 80% of the population of the United States lives in cities . However, over the past several decades eleven of the fifteen largest cities in the United States have experienced population declines  and similar urban declines have occurred globally . These declines have been associated with the disappearance of industrial jobs , government policies and spending programs that subsidize out-migration to the suburbs , and a history of real estate practices that have resulted in racial segregation and neighborhood decline [6,7,8]. During population shrinkage, cities typically experience infrastructure abandonment and associated decay that can significantly alter the biotic environment . This process of urban decay tends to exacerbate itself, causing increasing inequities in social, economic, and environmental conditions [4,10,11]. The most visible sign of this process is often the deterioration of buildings and associated accumulation of garbage. Vacant buildings thus not only serve as outcomes of urban decline, but as markers of the symptom [12,13]. The abandonment of one building can adversely affect nearby residents, often leading to further abandonments and a number of other issues, including increased crime and exposure to disease vectors [14,15,16].
The emergence and re-emergence of mosquito-borne disease has increasingly been associated with urban landscapes, including West Nile virus (WNV), dengue virus, La Crosse virus (LACV), and chikungunya virus [17,18,19,20,21,22]. While host composition is important for zoonotic pathogen amplification [23,24,25,26], the production of mosquito vector species in close proximity to humans is a fundamental determinant of the distribution and incidence of human disease [27,28,29].
The Asian tiger mosquito, Aedes albopictus (Skuse) and northern house mosquito Culex pipiens L., readily occupy human dominated landscapes. Both species utilize artificial water-filled containers (i.e., trash, bird baths, planters) during immature development e.g., [16,30], and as adults, take bloodmeals from humans, domestic pets, and urban wildlife . Aedes albopictus was first documented in the continental United States in Texas in 1985, and has since spread throughout cities across the south-eastern and mid-Atlantic United States to become the predominant human-biting urban mosquito [16,31,32,33,34]. Aedes albopictus is a competent vector for pathogens found in the eastern U.S., including WNV, LACV, and Eastern equine encephalitis [17,35,36], as well as for potential emergent pathogens such as chikungunya and dengue viruses [29,37]. Aedes albopictus commonly co-occur with the resident invasive mosquito Culex pipiens, which invaded North America over 200 years ago and is common in cities throughout the northern United States . Laboratory and field studies implicate Cx. pipiens as the principal WNV vector in this region [35,39,40,41].
Vegetation, abundance of water-filled containers, and proximity to standing water have all been associated with the distribution and abundance of vector species [30,33,42,43]. Adult mosquitoesrequire access to vegetation for food and resting sites, aquatic habitats for developmental stages (eggs and larvae), and host blood meals. However, ecological processes occurring at early developmental life-stages likely play a primary role in regulating the distribution and abundance of adult mosquitoes [44,45]. The rate of immature development and pupation depends on abiotic conditions (e.g., water quality, temperature), biotic processes (e.g., microbial food resources, competition, predation) and their interactions [45,46,47,48,49,50,51,52,53,54]. Habitat that supports both immature development and adult mosquito populations is likely heterogeneous across an urban landscape but remains understudied [55,56]. Vegetation cover, container habitat, and densities of both predators and host species can vary between neighborhoods [16,33,57]. The quality and abundance of individual container habitats or adult resting sites vary at even finer spatial scales [30,58,59]. Previous studies have found both positive and negative associations among suitable mosquito habitat, mosquito abundance, and neighborhood socio-economic status [14,16,30,59,60,61,62,63,64]. However, few studies have gone beyond income to examine the specific associations between the physical symptoms of urban poverty and the abundance of blood-seeking adult mosquitoes . Symptoms of physical disrepair such as holes, water damage, peeling paint, and garbage accumulation have been associated with the presence and abundance of indoor pests [65,66]. However, the specific importance of infrastructure deterioration for maintaining mosquito infestations is not well understood. Vacant buildings are increasingly abundant in many U.S. cities and when abandoned, the associated physical disrepair may indicate increased mosquito habitat (e.g., Figure 1). Degraded structures are often associated with unmanaged and semi-permanent garbage collections that can hold water, facilitate immature mosquito development  and increased production of biting adults.
This study examines the relationship between the physical degradation of an urban residential landscape and the production and composition of mosquito communities at both larval and adult stages. Specifically, we compared immature and adult mosquito abundance on individual parcels across two city blocks in Baltimore, Maryland that varied in urban decay, as defined by the density of roofless, vacant houses. We expected that the buildings and associated garbage would reflect increased habitat for immature mosquito development. We hypothesized that neighborhoods with more roofless, vacant buildings would have more unmanaged larval habitat and greater relative abundance of adult mosquitoes than neighborhoods with fewer vacant houses.
2. Experimental Section
Baltimore City, Maryland lost 31.4% of its population between 1950 and 2000 and has a 19.5% household poverty rate, which is well above the national average (11.1%; US Census Bureau, 2010). The city has more than 16,000 vacant and abandoned buildings , which are an easily identifiable metric of urban infrastructure decay in impoverished neighborhoods. We focused on two city blocks located in West Baltimore that were similar in area and original row house structure. We quantified the total number of vacant buildings on each block as a proxy measure of urban decay using information provided by the City of Baltimore’s Open Data Catalog . We used Google Earth (images acquired in 2010) to identity roof damage (Figure 2) and then confirmed counts of vacant and deteriorating buildings during a site visit in June 2012. We selected focal blocks that contained relatively high and low numbers of vacant and deteriorating buildings (Table 1). As part of a larger study, Knowledge, Attitude, and Practice (KAP) surveys were conducted with one resident at each participating household (unpublished data). Voluntary information on education and income levels confirm that higher socio-economic households were generally located on the low decay block (52% college degree and 35% earning more than 95,000 annually versus 0 households reporting these levels in the high decay block). We also ensured visually that blocks adjacent to each of our focal blocks were similar in number of vacant buildings to the adjacent focal block. The study blocks were located approximately 800 meters apart to maximize spatial independence at the scale of mosquito dispersal but maintain continuity in physiographic characteristics. The predominant mosquito species from previous larval surveys in West Baltimore  was Ae. albopictus, which usually disperses no more than 150–200 m from larval development sites and rarely more than 800 m [69,70,71].
|Table 1. Block-level summaries.|
|Parcels (includes empty lots)||58||77|
|Vacant Buildings with missing roof||1||21|
2.1. Adult Mosquito Samples
Mosquitoes were trapped at two locations per block for two days during the week starting 22 July 2012 and two days during the following week starting, 29 July 2012. Adult trap locations were selected to minimize trap exposure to sunlight, wind, and rain, since traps set in exposed areas may collect fewer mosquitoes . Due to this relatively low sample size, we limit interpretation of our results to the comparison between high and low urban decay sites during this specific and important time period, which has been previously demonstrated to be the peak season for both Ae. albopictus and Cx. pipiens in this region [73,74,75].
Traps were set at 2 PM and collected the next day at 9 AM. To maximize our ability to collect both Culex and Aedes mosquitoes, traps were set in pairs consisting of a CDC Light Trap and a Biogents ® (BG) Sentinel trap located within 0.5 meters of each other and baited with CO2 (300 g dry ice in a blue insulated canister). Replicate trap pairs were placed at two trap locations per block on each trap day, for a total of 8 samples per trap type per block. Collected samples were labeled and transported on dry ice back to a lab where they were identified and enumerated. Mean daily rainfall during July 2012 was 28 mm, which is consistent with the 5-year July mean . However, there was only one precipitation event (5.84 cm) during the two week sampling period of this study, which occurred on 26 July, after both the immature survey (see below) and the initial adult collection. Local mean temperature in July 2012 was 27.44 °C, the 5th hottest July in over 100 years on record .
2.2. Immature Mosquito Samples
Immature mosquito surveys were conducted at the parcel-level on each of our focal blocks during the first week of adult sampling 22–25 July 2012. Each parcel was surveyed for standing water and all accessible water-holding containers were sampled at: (1) Occupied houses whose residents permitted access, (2) vacant lots with permission from Baltimore City, and (3) public access alleys. Container habitats were recorded as either being useful (e.g., garden planter, trash can, drain spout), discarded garbage (e.g., cup, can, food wrapper, tire) or structural disrepair (building material, puddle). After the water was homogenized, up to 1 L was collected from each container and mosquito larvae and pupae were enumerated and identified to species (larvae) or genus (pupae) level . Nine (of 28, 32.1%) container habitats held more than 1 L of water and the total larvae for these samples was calculated as the density of sampled larvae per L multiplied by the total volume (L) of water. All but two containers held 0.02 L–7.0 L water. Two containers were much larger, including a trash can that was estimated to hold 50 L of water and a bucket with 20 L of water. In calculating the total mosquito abundance of these two containers, we limited the total volume to 10 L because mosquitoes appeared to be at a similar density as our sampled L only in the top 10 L of water. We consider this a reasonable approach that is supported by other studies that demonstrate that mosquito density should decline with depth .
All analyses were conducted in the R statistical package using standard generalized (Poisson) linear regression (GLM function). The unit of inference was considered to be the individual parcel, and container density and mosquito densities (total and by species) were summed on a per parcel basis. In each model, a binary variable was used to assess differences between the high (0) and low (1) decay block.
3. Results and Discussion
3.1. Adult Sampling
A total of 1,162 adult mosquitoes were collected, of which 588 were female Ae. albopictus (50.6%) and 549 male Ae. albopictus (47.2%). The second most common species collected was Cx. pipiens, with only 29 females sampled (0 males). Other species collected were Aedes vexans (<0.1%), Ochlerotatus cantator (<0.1%), and Ochlerotatus sollicitans (<0.1%). The majority of all samples were collected in BG Sentinel traps (97% and 98% of Ae. albopictus and Cx. pipiens, respectively). Further analyses use summed mosquito abundance from each trap pair for each sampling date.
Eighty-six percent of the adult mosquitoes were collected from the low-decay block. Female Ae. albopictus were 5.61 times more abundant (z = −5.875, p < 0.001) and Cx. pipiens were 4.60 times more abundant (z = −3.191, p = 0.001) in the low-decay block vs. the high-decay block. The proportion of male Ae. albopictus relative to females in the same trap ranged from 0.07 to 0.71 (mean proportion male 0.49 ± 0.21). Mean male-to-female ratio was not statistically different between samples from the high- vs. low-decay blocks (0.46 ± 0.16 vs. 0.37 ± 0.23, respectively). No males of other species were collected.
3.2. Immature Sampling
A total of 1,275 fourth-instar larvae and 79 pupae were sampled from container habitats across both blocks (772 larvae and 65 pupae in the low-decay block, 503 larvae and 14 pupae in the high-decay block). Of these, 379 larvae (29.7%) and 45 (56.9%) pupae were Ae. albopictus, and 832 larvae (65.3%) and 34 (43.0%) pupae were Cx. pipiens. Other species collected included fourth instar Culex restuans (0.04%), Aedes triseriatus (<0.01%) and unidentified mosquito species (0.01%).
Yard access varied between the two blocks, with greater numbers of fenced yards and fewer residents home during the day to grant access in the low-decay block vs. the high-decay block. We sampled ten parcels (17.24%) in the low-decay block, including eight with occupied buildings and two grass lots. Water-holding containers were found on all parcels sampled on the low-decay block (Table 2). With the exception of one discarded tire, all mosquito infested containers in the low-decay block were classified as useful and appeared to be used for yard maintenance and care (e.g., trash cans, bird baths, buckets, planters). While there was more abundant potential container habitat in discarded garbage and structural disrepair around the vacant buildings in the high-decay block (personal observation), most of these containers were dry when surveyed. Of the 42 parcels surveyed in the high-decay block, 16.7% had water-holding containers and only 7.1% had immature mosquitoes.
|Table 2. Larval sampling metrics.|
|Parcels surveyed (#)||17.24% (10)||58.33% (42)|
|Parcels with accessible water , % surveyed||100.00%||16.67%|
|Parcels with mosquito larvae, % surveyed||60.00%||7.14%|
|Containers per parcel, mean (se)||2.57 (0.26)||0.26 (0.08)|
|Containers with larvae, %||50.00%||22.22%|
|Containers with pupae, %||27.78%||22.22%|
|Mean larvae per surveyed parcel, Ae. albopictus (se)||14.78 (6.36)||2.69 (1.92)|
|Mean larvae per surveyed parcel, Cx. pipiens (se)||26.22 (14.12)||8.57 (6.30)|
|Mean adult per trap night, Ae. albopictus (se)||70.57 (13.45)||11.00 (3.40)|
|Mean adult per trap night, Cx. pipiens (se)||3.29 (1.32)||0.63 (0.50)|
Mosquito pupae were only found in seven containers sampled on two parcels in each neighborhood; six of the pupae positive containers were categorized as useful (uncovered trash cans and one plastic tarp) and one was a large puddle in an alley in the high-decay block. All were adjacent to or on occupied parcels. Total numbers of Aedes and Culex pupae were similar (45 versus 48), although Aedes pupae were only sampled from container habitat in the low-decay block. Aedes and Culex pupae were not sampled concurrently from any container, although earlier immature stages (larvae) were commonly found together.
The relative abundance of both Ae. albopictus (z = 13.80, p < 0.0001) and Cx. pipiens (z = 13.78, p < 0.0001) larvae per parcel was significantly higher in the low-decay block compared to the high-decay block. However, the presence of immatures in a particular container was not well predicted by the block decay status (Ae. albopictus: p = 0.081 and Cx. pipiens p = 0.080, respectively). Larvae of both species co-occurred in most (73%) mosquito-positive containers. However, abundance of Ae. albopictus larvae was negatively associated with container volume (z = 4.098, p = 0.00004) while abundance of Cx. pipiens larvae was positively related to container volume (z = 10.354, p < 0.0001). Both species occurred at higher abundances in useful vs. discarded garbage containers during this survey (Aedes: z = 4.053, p = 0.00005; Culex z = −2.606, 0.0092).
Relative abundances of immature and adult mosquitoes were consistent between blocks, with greater abundance of both in the low-decay vs. high-decay block. However, interspecific adult abundance was not well predicted by the immature sampling. Although Ae. albopictus comprised almost all the collected adults, Cx. pipiens was quite abundant at the larval stage. However, Culex pupae were sampled from parcels on both blocks, while Aedes pupae were not collected from any containers in the high-decay block. The apparent mismatch between immature and adult presence and relative abundances could be a result of interspecific differences in immature development rates, survival, trap sensitivity or adult dispersal. While our CO2 baited CDC traps were intended to target Culex samples, we actually sampled more of both species in the BGS traps. Future efforts will need to employ gravid traps to directly sample ovipositing females, in addition to BGS traps. Exactly how abiotic and biotic processes act on the immature stages of mosquitoes to regulate the abundances of biting adults is often complex and our findings highlight a clear research need for evaluating these processes in an urban landscape.
The simplest ecological mechanism driving adult abundance is immature survival, whereby low immature survival directly leads to low adult emergence. Our findings suggest greater Ae. albopictus survival to emergence and that adult mosquito production in the high-decay block is limited by persistence of aquatic habitat during an exceptionally hot and dry period. While garbage containers were abundant, they were almost always dry (personal observation). In general, disused garbage containers are likely to dry more quickly than larger containers, making them less important mosquito habitat in dry conditions [33,78]. In addition to affecting adult abundance through immature survival, abiotic and biotic processes acting on the immature stages of mosquitoes can indirectly affect adult abundances through changes in adult body size, longevity and fecundity [46,79,80], as well as affect adult biting rates and vector competence [81,82,83,84]. Evaluating the effects of container mosquito ecology on adult life-history and disease transmission is particularly important within urban landscapes where mosquitoes are in close proximity to humans and habitat gradients vary with social context.
Our findings regarding container habitat importance were similar to other surveys in the region that identify planters, buckets and uncovered trash cans as important Ae. albopictus habitat [30,33], although somewhat in contrast to findings that discarded garbage and infrastructure decay may also create productive habitat [16,30,62]. Garden planters and buckets often held a higher volume of water than what precipitation could have provided. If planters and other container habitats in the low-decay block are regularly watered or purposefully shaded by residents, then this common mosquito habitat can be effectively decoupled from the dry weather conditions that limited mosquito production in disused garbage containers.
While heat and low precipitation levels are normal for July, 2012 was hotter than average . Higher temperatures can increase immature development rate [85,86], although heat can also directly reduce persistence of aquatic container habitat . Numerous studies have shown that numbers of water-filled containers and larval mosquitoes are both less abundant in dry conditions [73,87,88]. Thus, extreme heat may reduce adult mosquito production in urban areas where disused containers are the predominant habitat for immature development. While the abundant container habitat in the high-decay block was dry during our study, it may play an important role in early season population growth and in seasons with cooler, wetter conditions as indicated in prior studies .
This study is among the few to compare both immature and adult mosquito abundances across fine-scale variation in socio-economic context. By being conducted during dry conditions it removes large variations in mosquito abundances that may be seen between periods of dry and wet conditions over an entire season, which in turn can mask differences across fine spatial scales such as city blocks. By examining both immature and adult abundances, this study highlights some important aspects of mosquito ecology in socio-economically diverse urban landscapes. Populations are likely to be regulated at multiple life-stages in a species-specific manner and resident-based yard upkeep and gardening may be important for maintaining mosquito populations during hot and dry periods.
Vacant and abandoned buildings are a visible sign of neighborhood socioeconomic status in many post-industrial cities. Prior studies in this region of the U.S. have reported positive association between neighborhood socio-economic status and mosquito infestation [16,33,89]. We hypothesized that the infrastructure damage and garbage accumulation associated with vacant buildings would provide more unmanaged container habitat that would result in higher immature densities and greater production of adult mosquitoes. While vacant houses in the high-decay (lower socio-economic status) block in this study did have a higher proportion of containers categorized as garbage relative to the low-decay block, we found both more total water-holding containers per parcel and greater densities of immature mosquitoes per container in the higher socio-economic status (low-decay) block. Containers associated with human residence and outdoor activity (e.g., planters, trash cans) were more likely to both hold water and contain immature mosquitoes at the time of our study.
The vast majority of immature and all adult mosquitoes were either the invasive Ae. albopictus or resident invasive Cx. pipiens. Both of these species utilize water-holding artificial containers in urban landscapes and are known vectors for a range of arboviruses, including the endemic West Nile virus . Our data suggest that residents on the low-decay block may be at greater immediate risk of mosquito-borne disease than residents in the (lower socio-economic status) high-decay block.
Our results may not reflect differences in mosquito abundances under wet conditions; previous work in this region suggests that lower socioeconomic neighborhoods can support greater larval habitat over the entire mosquito season . We’ve highlighted a critical need for developing better understanding of what spatial and temporal scales are important for forecasting and managing mosquito populations and disease risk in urban landscapes. Future studies should rigorously explore spatial dynamics of both immature and adult mosquito abundances during both dry and wet periods, preferably over multiple summer seasons, to gain a fuller understanding of temporal and spatial mosquitoes populations in urban landscapes.
This study represents undergraduate research by Brian Becker, who was supported by the NSF-funded Research Experiences for Undergraduates (REU) Program at the Cary Institute of Ecosystem Studies. The authors wish to thank Danielle Bodner, the University of Maryland field crew, Heather Goodman and especially, the generous West Baltimore residents who made this work possible. The National Science Foundation supported this work under their Coupled Natural Human Systems program (DEB-1211797) and Long-term Ecological Research Program support for the Baltimore Ecosystem Study (DEB-0423476), which facilitated community access and outreach activities. Human subjects approval was obtained from the Cary Institute Institutional Review Board (Protocol # 117-2012).
Work presented here was conceived of, implemented and analyzed by Brian Becker, Shannon L. LaDeau and Paul T. Leisnham.
Conflicts of Interest
The authors declare no conflict of interest.
- Brown, D.G.; Johnson, K.M.; Loveland, T.R.; Theobald, D.M. Rural land-use trends in the conterminous United States, 1950–2000. Ecol. Appl. 2005, 15, 1851–1863. [Google Scholar] [CrossRef]
- Glaeser, E.L.; Gyourko, J. Urban decline and durable housing. J. Polit. Econ. 2005, 113, 345–375. [Google Scholar] [CrossRef]
- Grossmann, K.; Bontje, M.; Haase, A. Shrinking cities: Notes for the further research agenda. Cities 2013, 35, 221–225. [Google Scholar] [CrossRef]
- Wilson, W.J. When Work Disappears: The World of the New Urban Poor; Vintage: New York, NY, USA, 1996. [Google Scholar]
- Beauregard, R.A. Federal policy and postwar urban decline: A case of government complicity? Hous. Policy Debate 2001, 12, 129–151. [Google Scholar] [CrossRef]
- Semyonov, M.; Haberfeld, Y.; Cohen, Y.; Lewin-Epstein, N. Racial composition and occupational segregation and inequality across American cities. Soc. Sci. Res. 2000, 29, 175–187. [Google Scholar] [CrossRef]
- Cohen, P.N. Race, class and labor markets: The White working class and racial composition of US metropolitan areas. Soc. Sci. Res. 2001, 30, 146–169. [Google Scholar] [CrossRef]
- Cohen, J.E. Human population grows up. Sci. Am. 2005, 293, 48–55. [Google Scholar] [CrossRef]
- Haase, D. Urban ecology of shrinking cities: An unrecognized opportunity? Nat. Cult. 2008, 3, 1–8. [Google Scholar]
- Pickett, S.T.A.; Boone, C.G.; McGrath, B.P.; Cadenasso, M.L.; Childers, D.L.; Ogden, L.A.; McHale, M.; Grove, J.M. Ecological science and transformation to the sustainable city. Cities 2013, 32, S10–S20. [Google Scholar] [CrossRef]
- Kelling, G.L.; Coles, C.M. Fixing Broken Windows: Restoring Order and Reducing Crime in Our Communities; Manhattan Institute for Policy Research Inc.: New York, NY, USA, 1996. [Google Scholar]
- Kraut, D.T. Hanging out the no vacancy sign: Eliminating the blight of vacant buildings from urban areas. N. Y. Univ. Law Rev. 1999, 74, 1139–1177. [Google Scholar]
- Skogan, W.G. The national crime survey redesign. Public Opin. Q. 1990, 54, 256–272. [Google Scholar] [CrossRef]
- Reisen, W.K.; Takahashi, R.M.; Carroll, B.D.; Quiring, R. Delinquent mortgages, neglected swimming pools, and West Nile virus, California. Emerg. Infect. Dis. 2008, 14, 1747–1749. [Google Scholar] [CrossRef]
- Frazier, A.E.; Bagchi-Sen, S.; Knight, J. The spatio-temporal impacts of demolition land use policy and crime in a shrinking city. Appl. Geogr. 2013, 41, 55–64. [Google Scholar] [CrossRef]
- LaDeau, S.L.; Leisnham, P.T.; Biehler, D.; Bodner, D. Higher mosquito production in low-income neighborhoods of Baltimore and Washington, DC: Understanding ecological drivers and mosquito-borne disease risk in temperate cities. Int. J. Environ. Res. Public Health 2013, 10, 1505–1526. [Google Scholar] [CrossRef]
- Leisnham, P.T.; Juliano, S.A. Impacts of climate, land use, and biological invasion on the ecology of immature Aedes mosquitoes: Implications for La Crosse emergence. Ecohealth 2012, 9, 217–228. [Google Scholar] [CrossRef]
- Leisnham, P.T.; Slaney, D.P. Urbanization and the Increasing Risk from Mosquito-Borne Diseases: Linking Human Well-Being with Ecosystem Health. In Focus on Urbanization Trends; De Smet, L.M., Ed.; Nova Science Publishers Inc.: New York, NY, USA, 2009; pp. 47–82. [Google Scholar]
- LaDeau, S.L.; Calder, C.A.; Doran, P.J.; Marra, P.P. West Nile virus impacts in American crow populations are associated with human land use and climate. Ecol. Res. 2011, 26, 909–916. [Google Scholar] [CrossRef]
- Alemu, A.; Tsegaye, W.; Golassa, L.; Abebe, G. Urban malaria and associated risk factors in Jimma town, south-west Ethiopia. Malar. J. 2011, 10. [Google Scholar] [CrossRef]
- Delatte, H.; Bagny, L.; Brengue, C.; Bouetard, A.; Paupy, C.; Fontenille, D. The invaders: Phylogeography of dengue and chikungunya viruses Aedes vectors, on the South West islands of the Indian Ocean. Infec. Genet. Evol. 2011, 11, 1769–1781. [Google Scholar] [CrossRef]
- Patz, J.A.; Graczyk, T.K.; Geller, N.; Vittor, A.Y. Effects of environmental change on emerging parasitic diseases. Int. J. Parasitol. 2000, 30, 1395–1405. [Google Scholar] [CrossRef]
- Keesing, F.; Brunner, J.; Duerr, S.; Killilea, M.; LoGiudice, K.; Schmidt, K.; Vuong, H.; Ostfeld, S.R. Hosts as ecological traps for the vector of Lyme disease. P. Roy. Soc. BBio. Sci. 2009, 276, 3911–3919. [Google Scholar] [CrossRef]
- Allan, B.F.; Langerhans, R.B.; Ryberg, W.A.; Landesman, W.J.; Griffin, N.W.; Katz, R.S.; Oberle, B.J.; Schutzenhofer, M.R.; Smyth, K.N.; de St Maurice, A.; et al. Ecological correlates of risk and incidence of West Nile virus in the United States. Oecologia 2009, 158, 699–708. [Google Scholar] [CrossRef]
- Kilpatrick, A.M.; Daszak, P.; Jones, M.J.; Marra, P.P.; Kramer, L.D. Host heterogeneity dominates West Nile virus transmission. P. Roy. Soc. B Bio. Sci. 2006, 273, 2327–2333. [Google Scholar] [CrossRef]
- Kilpatrick, A.M.; Kramer, L.D.; Jones, M.J.; Marra, P.P.; Daszak, P. West Nile virus epidemics in North America are driven by shifts in mosquito feeding behavior. PloS Biol. 2006, 4, 606–610. [Google Scholar]
- Juliano, S.A.; Lounibos, L.P. Ecology of invasive mosquitoes: Effects on resident species and on human health. Ecol. Lett. 2005, 8, 558–574. [Google Scholar] [CrossRef]
- Gratz, N.G. Emerging and resurging vector-borne diseases. Annu. Rev. Entomol. 1999, 44, 51–75. [Google Scholar] [CrossRef]
- Gratz, N.G. Critical review of the vector status of Aedes albopictus. Med. Vet. Entomol. 2004, 18, 215–227. [Google Scholar] [CrossRef]
- Dowling, Z.; Ladeau, S.L.; Armbruster, P.; Biehler, D.; Leisnham, P.T. Socioeconomic status affects mosquito (Diptera: Culicidae) larval habitat type availability and infestation level. J. Med. Entomol. 2013, 50, 764–772. [Google Scholar] [CrossRef]
- Rochlin, I.; Ninivaggi, D.V.; Hutchinson, M.L.; Farajollahi, A. Climate change and range expansion of the Asian tiger mosquito (Aedes albopictus) in Northeastern USA: Implications for public health practitioners. PloS One 2013, 8. [Google Scholar] [CrossRef]
- Moore, C.G.; Mitchell, C.J. Aedes albopictus in the United States: Ten-year presence and public health implications. Emerg. Infect. Dis. 1997, 3, 329–334. [Google Scholar] [CrossRef]
- Bartlett-Healy, K.; Unlu, I.; Obenauer, P.; Hughes, T.; Healy, S.; Crepeau, T.; Farajollahi, A.; Kesavaraju, B.; Fonseca, D.; Schoeler, G.; et al. Larval mosquito habitat utilization and community dynamics of Aedes albopictus and Aedes japonicus (Diptera: Culicidae). J. Med. Entomol. 2012, 49, 813–824. [Google Scholar] [CrossRef]
- Leisnham, P.T.; Juliano, S.A. Spatial and temporal patterns of coexistence between competing Aedes mosquitoes in urban Florida. Oecologia 2009, 160, 343–352. [Google Scholar] [CrossRef]
- Turell, M.J.; Dohm, D.J.; Sardelis, M.R.; Oguinn, M.L.; Andreadis, T.G.; Blow, J.A. An update on the potential of North American mosquitoes (Diptera: Culicidae) to transmit West Nile virus. J. Med. Entomol. 2005, 42, 57–62. [Google Scholar] [CrossRef]
- Gerhardt, R.R.; Gottfried, K.L.; Apperson, C.S.; Davis, B.S.; Erwin, P.C.; Smith, A.B.; Panella, N.A.; Powell, E.E.; Nasci, R.S. First isolation of La Crosse virus from naturally infected Aedes albopictus. Emerg. Infect. Dis. 2001, 7, 807–811. [Google Scholar] [CrossRef]
- Ibanez-Bernal, S.; Briseno, B.; Mutebi, J.P.; Argot, E.; Rodriguez, G.; Martinez-Campos, C.; Paz, R.; de la Fuente-San Roman, P.; Tapia-Conyer, R.; Flisser, A. First record in America of Aedes albopictus naturally infected with dengue virus during the 1995 outbreak at Reynosa, Mexico. Med. Vet. Entomol. 1997, 11, 305–309. [Google Scholar] [CrossRef]
- Darsie, R.; Ward, R. Identification and Geographical Distribution of the Mosquitoes of North America, North of Mexico; University of Florida Press: Gainesville, FL, USA, 2005. [Google Scholar]
- Sardelis, M.R.; Turell, M.J.; Dohm, D.J.; O’Guinn, M.L. Vector competence of selected North American Culex and Coquillettidia mosquitoes for West Nile virus. Emerg. Infect. Dis. 2001, 7, 1018–1022. [Google Scholar] [CrossRef]
- Farajollahi, A.; Fonseca, D.M.; Kramer, L.D.; Marm Kilpatrick, A. “Bird biting” mosquitoes and human disease: A review of the role of Culex pipiens complex mosquitoes in epidemiology. Infect. Genet. Evol. 2011, 11, 1577–1585. [Google Scholar] [CrossRef]
- Fonseca, D.M.; Keyghobadi, N.; Malcolm, C.A.; Mehmet, C.; Schaffner, F.; Mogi, M.; Fleischer, R.C.; Wilkerson, R.C. Emerging vectors in the Culex pipiens complex. Science 2004, 303, 1535–1538. [Google Scholar] [CrossRef]
- Diuk-Wasser, M.A.; Brown, H.E.; Andreadis, T.G.; Fish, D. Modeling the spatial distribution of mosquito vectors for West Nile virus in Connecticut, USA. Vector Borne Zoonotic Dis. 2006, 6, 283–295. [Google Scholar]
- Brown, H.; Diuk-Wasser, M.; Andreadis, T.; Fish, D. Remotely-sensed vegetation indices identify mosquito clusters of West Nile virus vectors in an urban landscape in the northeastern United States. Vector Borne Zoonotic Dis. 2008, 8, 197–206. [Google Scholar] [CrossRef]
- Juliano, S.A. Population dynamics. J. Am. Mosq. Control Assoc. 2007, 23, 265–275. [Google Scholar] [CrossRef]
- Juliano, S.A. Species Interactions Among Larval Mosquitoes: Context Dependence Across Habitat Gradients. Annu. Rev. Entomol. 2009, 54, 37–56. [Google Scholar] [CrossRef]
- Lounibos, L.P.; Nishimura, N.; Escher, R.L. Fitness of a treehole mosquito—Influences of food type and predation. Oikos 1993, 66, 114–118. [Google Scholar] [CrossRef]
- Su, T.Y.; Mulla, M.S. Effects of temperature on development, mortality, mating and blood feeding behavior of Culiseta incidens (Diptera: Culicidae). J. Vector Ecol. 2001, 26, 83–92. [Google Scholar]
- Blaustein, L.; Kiflawi, M.; Eitam, A.; Mangel, M.; Cohen, J.E. Oviposition habitat selection in response to risk of predation in temporary pools: Mode of detection and consistency across experimental venue. Oecologia 2004, 138, 300–305. [Google Scholar] [CrossRef]
- Stav, G.; Blaustein, L.; Margalit, Y. Individual and interactive effects of a predator and controphic species on mosquito populations. Ecol. Appl. 2005, 15, 587–598. [Google Scholar] [CrossRef]
- Yee, D.A.; Juliano, S.A. Consequences of detritus type in an aquatic microsystem: Effects on water quality, micro-organisms and performance of the dominant consumers. Freshw. Biol. 2006, 51, 448–459. [Google Scholar] [CrossRef]
- Blaustein, L.; Chase, J.M. Interactions between mosquito larvae and species that share the same trophic level. Annu. Rev. Entomol. 2007, 52, 489–507. [Google Scholar] [CrossRef]
- Delatte, H.; Gimonneau, G.; Triboire, A.; Fontenille, D. Influence of temperature on immature development, survival, longevity, fecundity, and gonotrophic cycles of Aedes albopictus, vector of chikungunya and dengue in the Indian Ocean. J. Med. Entomol. 2009, 46, 33–41. [Google Scholar]
- Chase, J.M.; Shulman, R.S. Wetland isolation facilitates larval mosquito density through the reduction of predators. Ecol. Entomol. 2009, 34, 741–747. [Google Scholar] [CrossRef]
- Costanzo, K.S.; Kesavaraju, B.; Juliano, S.A. Condition-specific competition in container mosquitoes: The role of noncompeting life-history stages. Ecology 2005, 86, 3289–3295. [Google Scholar] [CrossRef]
- Buyantuyev, A.; Wu, J.G. Urban heat islands and landscape heterogeneity: Linking spatiotemporal variations in surface temperatures to land-cover and socioeconomic patterns. Landsc. Ecol. 2010, 25, 17–33. [Google Scholar] [CrossRef]
- Landau, K.I.; van Leeuwen, W.J.D. Fine scale spatial urban land cover factors associated with adult mosquito abundance and risk in Tucson, Arizona. J. Vector Ecol. 2012, 37, 407–418. [Google Scholar] [CrossRef]
- Richards, S.L.; Ghosh, S.K.; Zeichner, B.C.; Apperson, C.S. Impact of source reduction on the spatial distribution of larvae and pupae of Aedes albopictus (Diptera: Culicidae) in suburban neighborhoods of a Piedmont community in North Carolina. J. Med. Entomol. 2008, 45, 617–628. [Google Scholar] [CrossRef]
- Yee, D.A.; Allgood, D.; Kneitel, J.M.; Kuehn, K.A. Constitutive differences between natural and artificial container mosquito habitats: Vector communities, resources, microorganisms, and habitat parameters. J. Med. Entomol. 2012, 49, 482–491. [Google Scholar]
- Yee, D.A. Tires as habitats for mosquitoes: A review of studies within the eastern United States. J. Med. Entomol. 2008, 45, 581–593. [Google Scholar]
- Reisen, W.K.; Meyer, R.P.; Tempelis, C.H.; Spoehel, J.J. Mosquito abundance and bionomics in residential communities in Orange and Los Angeles counties, California. J. Med. Entomol. 1990, 27, 356–367. [Google Scholar]
- Reisen, W.K.; Carroll, B.D.; Takahashi, R.; Fang, Y.; Garcia, S.; Martinez, V.M.; Quiring, R. Repeated West Nile virus epidemic transmission in Kern County, California, 2004–2007. J. Med. Entomol. 2009, 46, 139–157. [Google Scholar] [CrossRef]
- Harrigan, R.J.; Thomassen, H.A.; Buermann, W.; Cummings, R.F.; Kahn, M.E.; Smith, T.B. Economic conditions predict prevalence of West Nile virus. PloS One 2010, 5. [Google Scholar] [CrossRef]
- Joshi, V.; Sharma, R.C.; Sharma, Y.; Adha, S.; Sharma, K.; Singh, H.; Purohit, A.; Singhi, M. Importance of socioeconomic status and tree holes in distribution of Aedes mosquitoes (Diptera: Culicidae) in Jodhpur, Rajasthan, India. J. Med. Entomol. 2006, 43, 330–336. [Google Scholar] [CrossRef]
- Unlu, I.; Farajollahi, A.; Healy, S.P.; Crepeau, T.; Bartlett-Healy, K.; Williges, E.; Strickman, D.; Clark, G.G.; Gaugler, R.; Fonseca, D.M. Area-wide management of Aedes albopictus: Choice of study sites based on geospatial characteristics, socioeconomic factors and mosquito populations. Pest Manag. Sci. 2011, 67, 965–974. [Google Scholar] [CrossRef]
- Bradman, A.; Chevrier, J.; Tager, I.; Lipsett, M.; Sedgwick, J.; Macher, J.; Vargas, A.B.; Cabrera, E.B.; Camacho, J.M.; Weldon, R.; et al. Association of housing disrepair indicators with cockroach and rodent infestations in a cohort of pregnant Latina women and their children. Environ. Health Perspect. 2005, 113, 1795–1801. [Google Scholar] [CrossRef]
- Rauh, V.A.; Chew, G.L.; Garfinkel, R.S. Deteriorated housing contributes to high cockroach allergen levels in inner-city households. Environ. Health Perspect. 2002, 110, 323–327. [Google Scholar] [CrossRef]
- Baltimore City: Vacant Building Index. Available online: http://cityview.baltimorecity.gov/vacantbuildings/ (accessed on 7 February 2012).
- Baltimore City: Open Data Catalog. Available online: http://cityview.baltimorecity.gov/ (accessed on 7 February 2012).
- Honorio, N.A.; Silva, W.D.; Leite, P.J.; Goncalves, J.M.; Lounibos, L.P.; Lourenco-de-Oliveira, R. Dispersal of Aedes aegypti and Aedes albopictus (Diptera: Culicidae) in an urban endemic dengue area in the State of Rio de Janeiro, Brazil. Mem. Inst. Oswaldo Cruz. 2003, 98, 191–198. [Google Scholar]
- Cianci, D.; van den Broek, J.; Caputo, B.; Marini, F.; Della Torre, A.; Heesterbeek, H.; Hartemink, N. Estimating mosquito population size from mark-release-recapture data. J. Med. Entomol. 2013, 50, 533–542. [Google Scholar] [CrossRef]
- Marini, F.; Caputo, B.; Pombi, M.; tarsitani, G.; della Torre, A. Study of Aedes albopictus dispersal in Rome, Italy, using sticky traps in mark-release-recapture experiments. Med. Vet. Entomol. 2010, 24, 361–368. [Google Scholar] [CrossRef]
- Crepeau, T.N.; Healy, S.P.; Bartlett-Healy, K.; Unlu, I.; Farajollahi, A.; Fonseca, D.M. Effects of biogents sentinel trap field placement on capture rates of adult Asian tiger mosquitoes, Aedes albopictus. PloS One 2013, 8. [Google Scholar] [CrossRef]
- Leisnham, P.T.; Lounibos, L.P.; O’Meara, G.F.; Juliano, S.A. Interpopulation divergence in competitive interactions of the mosquito Aedes albopictus. Ecology 2009, 90, 2405–2413. [Google Scholar]
- Johnson, B.J.; Sukhdeo, M.V. Successional mosquito dynamics in surrogate treehole and ground-container habitats in the northeastern United States: Where does Aedes albopictus fit in? J. Vector Ecol. 2013, 38, 168–174. [Google Scholar]
- Johnson, B.J.; Sukhdeo, M.V.K. Drought-Induced amplification of local and regional West Nile virus infection rates in New Jersey. J. Med. Entomol. 2013, 50, 195–204. [Google Scholar] [CrossRef]
- Maryland Climatological Data: Baltimore, Inner Harbor. Available online: http://w1.weather.gov/obhistory/KDMH.html (accessed on 7 February 2012).
- Silver, J.B. Mosquito Ecology: Field Sampling Methods; Springer: New York, NY, USA, 2008. [Google Scholar]
- Bartlett-Healy, K.; Healy, S.P.; Hamilton, G.C. A model to predict evaporation rates in habitats used by container-dwelling mosquitoes. J. Med. Entomol. 2011, 48, 712–716. [Google Scholar] [CrossRef]
- Renshaw, M.; Service, M.W.; Birley, M.H. Size variation and reproductive success in the mosquito Aedes Cantans. Med. Vet Entomol. 1994, 8, 179–186. [Google Scholar] [CrossRef]
- Alto, B.W.; Muturi, E.J.; Lampman, R.L. Effects of nutrition and density in Culex pipiens. Med. Vet. Entomol. 2012, 26, 396–406. [Google Scholar]
- Nasci, R.S.; Mitchell, C.J. Larval diet, adult size, and susceptibility of Aedes aegypti (Diptera: Culicidae) to infection with Ross River virus. J. Med. Entomol. 1994, 31, 123–126. [Google Scholar]
- Westbrook, C.J.; Reiskind, M.H.; Pesko, K.N.; Greene, K.E.; Lounibos, L.P. Larval environmental temperature and the susceptibility of Aedes albopictus Skuse (Diptera: Culicidae) to Chikungunya virus. Vector Borne Zoonotic Dis. 2010, 10, 241–247. [Google Scholar] [CrossRef]
- Alto, B.W.; Lounibos, L.P.; Mores, C.N.; Reiskind, M.H. Larval competition alters susceptibility of adult Aedes mosquitoes to dengue infection. P. Roy. Soc. B Biol. Sci. 2008, 275, 463–471. [Google Scholar] [CrossRef]
- Alto, B.W.; Lounibos, L.P.; Higgs, S.; Juliano, S.A. Larval competition differentially affects arbovirus infection in Aedes mosquitoes. Ecology 2005, 86, 3279–3288. [Google Scholar] [CrossRef]
- Juliano, S.A.; Stoffregen, T.L. Effects of habitat drying on size at and time to metamorphosis in the tree hole mosquito Aedes triseriatus. Oecologia 1994, 97, 369–376. [Google Scholar]
- Teng, H.J.; Apperson, C.S. Development and survival of immature Aedes albopictus and Aedes triseriatus (Diptera: Culicidae) in the laboratory: Effects of density, food, and competition on response to temperature. J. Med. Entomol. 2000, 37, 40–52. [Google Scholar] [CrossRef]
- Leisnham, P.T.; LaDeau, S.L.; Juliano, S.A. Spatial and temporal habitat segregation of mosquitoes in urban Florida. PLoS One 2014, 9. [Google Scholar] [CrossRef]
- Juliano, S.A.; O’Meara, G.F.; Morrill, J.R.; Cutwa, M.M. Desiccation and thermal tolerance of eggs and the coexistence of competing mosquitoes. Oecologia 2002, 130, 458–469. [Google Scholar] [CrossRef]
- Dowling, Z.; Armbruster, P.; LaDeau, S.L.; DeCotiis, M.; Mottley, J.; Leisnham, P.T. Linking mosquito infestation to resident socioeconomic status, knowledge, and source reduction practices in suburban Washington, DC. Ecohealth 2013, 10, 36–47. [Google Scholar] [CrossRef]
© 2014 by the authors; licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution license (http://creativecommons.org/licenses/by/3.0/).