Laboratory study of competition between United States strains of Aedes albopictus and Aedes aegypti (Diptera: Culicidae)

Mosquito abatement workers in Houston, Tex., and New Orleans, La., have observed that the recent introduction of Aedes albopictus (Skuse) has been accompanied by a decline and virtual disappearance of Ae. aegypti (L.). This suggests competitive displacement but contradicts the direction of displacement observed in native habitats of Ae. albopictus. The paper reports a series of laboratory studies on competition between U.S. strains of the two species. Larval survivorship, size, and development time were monitored in increasing densities of pure and mixed cultures of the two species under limited and optimal diets. Oviposition preferences were examined by offering gravid females cups containing first or fourth instars of either species. Ethological isolation was studied by simultaneously offering virgin females of one species to males of both species and monitoring courtship behavior as well as rates of oviposition, percentage of hatch, and embryonation. The results of the larval competition studies suggest that interspecific competition increased development time only slightly and had no effect on survival of Ae. albopictus. Competition increased survival in Ae. aegypti. Size of both species was influenced by interspecific competition, but the magnitude and direction of the effect was inconsistent between strains and diets such that neither species emerged consistently larger. The results of the oviposition study indicated a higher fecundity in Ae. aegypti but otherwise demonstrated that both species oviposit without regard to the presence, age, or species of larvae in the oviposition container. The ethological isolation tests demonstrated that Ae. aegypti males were more sexually aggressive than males or Ae. albopictus. However, Ae. albopitus females placed with increasing densities of Ae. aegypti males demonstrated no decrease in rates of oviposition, and eggs laid showed equal rates of hatch and embryonation. In general, the results do not suggest that the U.S Ae. albopictus population is inherently more competitive in the laboratory than Ae. aegypti. Other reasons for the observed decline in Ae. aegypti in the United States are discussed.     

Effect of malathion on larval competition between Aedes albopictus and Aedes atropalpus (Diptera: Culicidae)

Aedes albopictus (Skuse) and Aedes atropalpus (Coquillett) (Diptera: Culicidae) are container-dwelling mosquito species that are well established in the eastern United States. Interspecific larval competition studies have shown Ae. albopictus to be a superior competitor over many species. A laboratory experiment was conducted in artificial containers to evaluate the effects of malathion on larval interactions between Ae. albopictus and Ae. atropalpus. The survivorship of Ae. albopictus increased with increasing Ae. atropalpus densities in control but decreased with increasing Ae. atropalpus densities in the presence of malathion. Alternatively, Ae. atropalpus survivorship did not differ between control and malathion treatments. Developmental times were not affected by interspecific competition in both treatments for either species. These results show that malathion could facilitate coexistence between Ae. albopictus and Ae. atropalpus. This demonstrates how sublethal concentrations of malathion (and perhaps other pesticides with similar modes of action) can enable an inferior competitor to coexist in the same habitat with a superior competitor. This is the first report of synergistic survival of a weaker mosquito competitor in the presence of a pesticide due to condition-specific competition.     

Interspecific larval competition between Aedes albopictus and Aedes japonicus (Diptera: Culicidae) in northern Virginia

Aedes albopictus (Skuse) and Aedes japonicus (Theobald) are two of the most recent and widespread invasive mosquito species to have become established in the United States. The two species co-occur in water-filled artificial containers, where crowding and limiting resources are likely to promote inter- or intraspecific larval competition. The performance of northern Virginia populations of Ae. japonicus and Ae. albopictus competing as larvae under field conditions was evaluated. Per capita rates of population increase for each species were estimated, and the effects of species composition and larval density were determined. In water-containing cups provided with oak leaves, Ae. albopictus larvae exhibited a competitive advantage over Ae. japonicus as a consequence of higher survivorship, shorter developmental time, and a significantly higher estimated population growth rate under conditions of interspecific competition. Intraspecific competition constrained population performance of Ae. albopictus significantly more than competition with Ae. japonicus. In the context of the Lotka-Volterra model of competition, these findings suggest competitive exclusion of Ae. japonicus in those habitats where this species co-occurs with Ae. albopictus.     

A simple parafilm M-based method for blood-feeding Aedes aegypti and Aedes albopictus (Diptera: Culicidae)

A simple device for blood-feeding Aedes (Stegomyia) mosquitoes is described. Parafilm M is stretched and pressed into fiberglass window screen to form a packet for holding warmed blood. The method has been used successfully to maintain Aedes albopictus colonies for >2 yr. In typical blood-feeding trials, 53 +/- 0.8% (+/-SE) of Aedes aegypti (Linnaeus) and 31 +/- 6% of Ae. albopictus (Skuse) fed to repletion.     

Invertebrate carcasses as a resource for competing Aedes albopictus and Aedes aegypti (Diptera: Culicidae)

Terrestrial invertebrate carcasses are an important resource for insects developing in pitcher plants. However, little is known of the role of these carcasses in other containers, which also receive leaf fall and stemflow inputs. This experiment investigated effects of accumulated invertebrate carcasses as a resource for two competing mosquitoes, Aedes albopictus (Skuse) and Aedes aegypti (L.), whether either species differentially benefited from accumulated carcasses, and if such a benefit affected interspecific competition. First, we measured accumulation of invertebrate carcasses in standard containers at a field site. We then used a replacement series with five different species ratios at the same total density, and varied the input of invertebrate carcasses [dead Drosophila melanogaster (Meigen) ] in three levels: none, the average input from our field site, or the maximum input recorded at our field site. Survivorship, development time, and mass were measured for each mosquito species as correlates of population growth, and were used to calculate a population performance index, lambda'. There were strong positive effects of invertebrate carcass additions on all growth correlates and lambda'. Differences in performance between species were pronounced in small or no carcass additions and absent in large inputs of invertebrate carcasses, but there was little evidence that inputs of invertebrate carcasses altered the competitive advantage in this system. These results suggest that terrestrial invertebrate carcasses may be an important resource for many types of container communities, and large accumulations of dead invertebrates may reduce resource competition between these mosquitoes, thus favoring coexistence. We propose that the total amount of resource, including accumulated invertebrate carcasses, may explain observed patterns of replacement involving these mosquitoes.     

Reproductive and metabolic differences between Aedes aegypti and Ae. albopictus (Diptera: Culicidae).

Aedes albopictus (Skuse) females were more likely to develop eggs after they ingested small blood meals than were Aedes aegypti (L.) when both species were maintained under the same suboptimal adult nutritional regimen. The longevity of adult female Ae. albopictus under conditions of starvation was also significantly greater than that of Ae. aegypti. Analyses of total body proteins, lipids, and glycogen indicated that the increased reproductive efficiency of Ae. albopictus may be a result of its greater reserves accumulated during a longer larval period.     

Convergent habitat segregation of Aedes aegypti and Aedes albopictus (Diptera: Culicidae) in southeastern Brazil and Florida

During the rainy season of 2001, the incidence of the dengue vectors Aedes aegypti and Ae. albopictus was examined in different habitats of two cities (Rio de Janeiro and Nova Igua?u) in Rio de Janeiro State, Brazil, and in two cities (Palm Beach and Boca Raton) in Florida. Oviposition trap collections were performed in urban, suburban, and rural habitats in both areas. Our hypothesis that the abundances and frequencies of occurrence of Ae. aegypti and Ae albopictus are affected in opposite ways by increasing urbanization was only partially supported. City, habitat, and their interaction significantly affected the abundance of both species. Cities with high abundance of Ae. aegypti also had a high abundance of Ae. albopictus. The two species were most abundant in the cities of Rio de Janeiro state and the lowest in Boca Raton. Habitat had a significant but opposite effect on the abundances of Ae. aegypti and Ae. albopictus. In general, Ae. aegypti was most prevalent in highly urbanized areas and Ae. albopictus in rural, suburban, and vegetated urban areas in Rio de Janeiro state and Florida. However, abundances of the two species were similar in most suburban areas. Analyses of frequencies of occurrence showed an unexpected high level of co-occurrence of both species in the same oviposition trap. Despite the different geographical origins of Ae. albopictus in Brazil and the United States, the habitats used by this recent invader are remarkably similar in the two countries.     

Susceptibility of selected strains of Aedes aegypti and Aedes albopictus (Diptera: Culicidae) to chikungunya virus.

The relative susceptibility of selected strains of Aedes aegypti (L.) and Aedes albopictus (Skuse) fed on a viremic monkey to infection with chikungunya virus was determined. Infection rates were consistently higher in 10 strains of Ae. albopictus tested than in 7 strains of Ae. aegypti tested, regardless of the geographic location from which the strains originated or the dose of virus ingested. Similarly, virus dissemination rates were higher in the Ae. albopictus strains compared with the Ae. aegypti strains. For nearly all (11 of 12) strains tested of both species, groups of mosquitoes with one or more females with a disseminated infection transmitted virus by bite to weanling mice. Based on these studies, Ae. albopictus appears to be a more competent laboratory vector of chikungunya virus than does Ae. aegypti.     

Vector competence of Aedes aegypti and Aedes albopictus (Diptera: Culicidae) for dengue virus in the Florida Keys

In 2009-2011, Monroe County in southern Florida experienced locally acquired and traveler-imported focal dengue outbreaks. Aedes aegypti (L.) is the primary vector of dengue virus (DENV) worldwide, is prevalent in Monroe County, and is the suspected vector in Florida. Ae. albopictus (Skuse) is also known to be an important vector of DENV and this species is ubiquitous in Florida; however, it is not yet established in Monroe County. Florida Ae. aegypti (Key West and Stock Island geographic colonies) and Ae. albopictus (Vero Beach geographic colony) were fed blood containing 3.7 Log10 plaque-forming unit equivalents of DENV serotype 1 isolated from a patient involved in the Key West, FL, outbreak in 2010. Mosquitoes were maintained at extrinsic incubation temperatures of 28 or 30 degrees C for an incubation period of 14 d. Vector competence was assessed using rates of infection (percent with virus-positive bodies), dissemination (percent infected with virus-positive legs), and transmission (percent infected with virus-positive saliva). No significant differences were observed in rates of infection or dissemination between Ae. aegypti or Ae. albopictus at either extrinsic incubation temperature. Transmission was observed only at 28 degrees C in both Ae. aegypti (Key West) and Ae. albopictus. The assessment of local mosquito populations for their DENV vector competence is essential and will aid mosquito control operators interested in pinpointing specific vector populations for control. The extent to which vector competence is affected by seasonal changes in temperature is discussed and provides baseline risk assessment data to mosquito control agencies.     

Wing shape as an indicator of larval rearing conditions for Aedes albopictus and Aedes aegypti (Diptera: Culicidae)

Estimating a mosquito's vector competence, or likelihood of transmitting disease, if it takes an infectious bloodmeal, is an important aspect of predicting when and where outbreaks of infectious diseases will occur. Vector competence can be affected by rearing temperature and inter- and intraspecific competition experienced by the individual mosquito during its larval development. This research investigates whether a new morphological indicator of larval rearing conditions, wing shape, can be used to distinguish reliably temperature and competitive conditions experienced during larval stages. Aedes albopictus (Skuse) and Aedes aegypti (L.) (Diptera: Culicidae) larvae were reared in low intraspecific, high intraspecific, or high interspecific competition treatments at either 22 or 32 degrees C. The right wing of each dried female was removed and photographed. Nineteen landmarks and 20 semilandmarks were digitized on each wing. Shape variables were calculated using geometric morphometric software. Canonical variate analysis, randomization multivariate analysis of variance, and visualization of landmark movement using deformation grids provided evidence that although semilandmark position was significantly affected by larval competition and temperature for both species, the differences in position did not translate into differences in wing shape, as shown in deformation grids. Two classification procedures yielded success rates of 26 - 49%. Accounting for wing size produced no increase in classification success. There seemed to be a significant relationship between shape and size. These results, particularly the low success rate of classification based on wing shape, show that shape is unlikely to be a reliable indicator of larval rearing competition and temperature conditions for Ae. albopictus and Ae. aegypti.     

Differential survival of Aedes aegypti and Aedes albopictus (Diptera: Culicidae) larvae exposed to low temperatures in Taiwan

Aedes aegypti (L.) and Aedes albopictus (Skuse) differ in their distribution in Taiwan. The former species is distributed in the south of Taiwan, whereas the latter is found throughout the island. One possible explanation proposes that low temperatures in the winter prevent the expansion of Ae. aegypti. Hence, the impact of low temperatures on immatures of both species was studied in the laboratory and in the field. Our study showed that, under most conditions, Ae. aegypti were more sensitive to low temperatures than Ae. albopictus both in the laboratory and in the field. The survival rates at 10 degrees C for the first and fourth instars of Ae. albopictus were significantly better than those of Ae. aegypti. At 2.5 and 5.0 degrees C, the first instars of Ae. albopictus survived better than the same stadium of Ae. aegypti, but the fourth instars of Ae. aegypti survived better. Short exposures to low temperatures did not affect the acclimatization of Ae. aegypti immatures but longer exposures did increase the physiological adaptation to low temperatures. For Ae. albopictus, exposure to low temperatures increases the acclimatization of this species. In field experiments, Ae. aegypti larvae had a significantly higher mortality than Ae. albopictus during exposures to cold fronts in the 2004 winter. We conclude that low temperatures in northern and central Taiwan have a negative impact on the distribution of Ae. aegypti, but this factor alone is not sufficient to prevent this species from occupying the rest of Taiwan.     

The effects of resource type and ratio on competition with Aedes albopictus and Culex pipiens (Diptera:Culicidae)

The introduction of Aedes albopictus (Skuse) in the United States has been associated with declines in abundance of resident mosquito species, presumably because of resource competition, as larvae of Ae. albopictus have been illustrated as superior competitors under certain resource conditions. We evaluated the hypothesis that varying the type and ratio of two food resources (Foxtail grass: American elm) alters the competitive outcome of Ae. albopictus and Culex pipiens (L.). We measured survivorship, development time, size, and adult longevity, and estimated the population growth index (A') of populations raised both alone and in equal number with the interspecific competitor, across five ratios of the two food resources. Competition was asymmetric with Ae. albopictus, the superior competitor across all resource treatments; however, the competitive advantage Ae. albopictus had over Cx. pipiens was reduced as grass became the predominant resource. With elm as the predominant resource, the population growth index (A') for both Ae. albopictus and Cx. pipiens was lower in intraspecific and interspecific competition treatments, respectively. The treatments also impacted adult life history, as life spans of both Ae. albopictus and Cx. pipiens varied when they emerged from larval conditions with different resource and competition treatments. We discuss the possible differences in the two species' efficiencies in exploiting the two resource types. Despite some resource conditions alleviating the competitive effects of Ae. albopictus on Cx. pipiens, competition remained asymmetric; thus, additional mechanisms are likely operating under field conditions when the two species coexist.     

Sindbis virus-associated pathology in Aedes albopictus (Diptera: Culicidae)

Virus dissemination and associated pathology were examined in Aedes albopictus after intrathoracic inoculation of Sindbis virus (SIN), the prototypic Alphavirus. At 10 days postinfection, virus RNA was detected in all three-body segments of the insect. Colocalization of virus antigen with structural pathology was observed in mosquito salivary glands and midgut-associated visceral muscles, representing yet another example of arbovirus-associated pathology in a mosquito host. SIN antigen and gross pathology were detected in lateral lobes, but not the medial lobe of salivary glands, whereas virus antigen, vacuolated cytoplasm, and myofilament misalignment were detected in the visceral muscles at the midgut exterior surface. Early in the midgut infection, virus antigen was localized in small foci on the organ surface that progressed to a grate work-like banding pattern that eventually cleared. Both the salivary glands and the midgut are essential to insect survival and reproduction. Additionally, these organs provide a pathway for virus transmission in nature. Although SIN infection may not shorten the mosquito life span, persistent coexistence could permit survival of both host and microbe as well as contribute to alterations in insect behavior.     

Sublethal effects of atrazine and glyphosate on life history traits of Aedes aegypti and Aedes albopictus (Diptera: Culicidae)

Although exposure of mosquito larvae to agricultural chemicals such as herbicides is common and widespread, our understanding of how these chemicals affect mosquito ecology and behavior is limited. This study investigated how an environmentally relevant concentration of two herbicides, atrazine and glyphosate, affects mosquito life history traits. One hundred and fifty (150) first instar Aedes (Stegomyia) aegypti (L.) or Aedes (Stegomyia) albopictus (Skuse) larvae were reared in 1.6 L of live oak leaf (Quercus virginiana) infusion in the presence (5 mg/L) or absence (0 mg/L) of atrazine or glyphosate. The containers were monitored daily to determine the emergence rates, sex ratio, male and female emergence times, and female body size. Emergence rates of A. aegypti from atrazine treatment were significantly higher relative to either glyphosate or control treatments (A. aegypti: atrazine?=?93?±?6 % (±95 % CI), glyphosate?=?82?±?5 %, control?=?78?±?5 %), while emergence rates of A. albopictus in atrazine treatments were significantly higher than in glyphosate treatments but not in controls (A. albopictus: atrazine?=?84?±?5 %, glyphosate?=?76?±?4 %, control?=?78?±?4 %). For both mosquito species, a sex ratio distortion with male bias was observed in control and glyphosate treatments, but not in atrazine treatments (A. aegypti: atrazine?=?0.90?±?0.17 (±SE), glyphosate?=?1.63?±?0.21, control?=?1.69?±?0.26; A. albopictus: atrazine?=?1.09?±?0.08, glyphosate?=?1.88?±?0.12, control?=?1.37?±?0.11). Emergence times for both sexes of the two mosquito species were significantly longer in atrazine treatments compared to glyphosate or control treatments (A. aegypti: females: atrazine?=?11.20?±?0.50 (days?±?95 % CI), glyphosate?=?9.71?±?0.23, control?=?9.87?±?0.21; males: atrazine?=?9.46?±?0.27, glyphosate?=?8.80?±?0.25, control?=?8.85?±?0.24; A. albopictus: females: atrazine?=?17.40?±?1.70, glyphosate?=?12.4?±?0.40, control?=?12.5?±?0.30; males: atrazine?=?12.96?±?0.41, glyphosate?=?10.48?±?0.24, control?=?10.64?±?0.37). For A. albopictus but not A. aegypti, adult females from atrazine treatment had significantly longer wing lengths compared to those from glyphosate or control treatments (A. albopictus: atrazine?=?3.06?±?0.07 (mm?±?95 % CI), glyphosate?=?2.80?±?0.07, control?=?2.83?±?0.06). These results demonstrate the potential for atrazine, a widely used herbicide, to influence epidemiologically relevant life history traits of mosquitoes.     

Asymmetrical competition and patterns of abundance of Aedes albopictus and Culex pipiens (Diptera: Culicidae)

We tested for competitive advantage among larvae of Aedes albopictus (Skuse) and Culex pipiens L. in a laboratory experiment and determined the frequency and spatial and temporal patterns of co-occurrence in the field in East St. Louis, IL. In a laboratory competition experiment at multiple combined densities of Ae. albopictus and Cx. pipiens larvae, Ae. albopictus survivorship and developmental times were significantly affected by conspecific densities but not by Cx. pipiens densities. In contrast, Cx. pipiens survivorship and developmental times were significantly affected by both conspecific and Ae. albopictus densities. Per capita rate of increase (r') for Ae. albopictus cohorts declined significantly due to density of conspecifics, but not density of Cx. pipiens. Interspecific competition between Ae. albopictus and Cx. pipiens under these laboratory conditions was strong and asymmetrical, with the effect of Ae. albopictus on Cx. pipiens much stronger than the reverse. In monthly samples from tire sites in East St. Louis, Ae. albopictus was highly seasonal, occurring in relatively low abundance from early May to July and increasing in abundance in August and September. Co-occurrence corresponded to the seasonality of Ae. albopictus, with Cx. pipiens encountering Ae. albopictus in more tires and at higher numbers within a tire, in August and September. Abundance of both species was high in residential areas and was unrelated to overstory cover, total nitrogen, and total phosphorus. Abundance of Ae. albopictus, but not of Cx. pipiens, was positively associated with conductivity. We expect Cx. pipiens to suffer from the effects of interspecific competition in tires in which it encounters Ae. albopictus. Interspecific competition between these species may be of both ecological and medical importance.     

Comparative potential of Aedes triseriatus, Aedes albopictus, and Aedes aegypti (Diptera: Culicidae) to transovarially transmit La Crosse virus

Aedes triseriatus (Say) (Diptera: Culicidae), the major vector of La Crosse (LAC) virus, efficiently transmits LAC virus both horizontally and transovarially. We compared the vector competence and transovarial transmission ability of Ae. triseriatus, Aedes albopictus Skuse, and Aedes aegypti (L.) for LAC virus. Ae. triseriatus and Ae. albopictus were significantly more susceptible to oral infection with LAC virus than Ae. aegypti. The three species also differed in oral and disseminated infection rates (DIRs). Transovarial transmission (TOT) rates and filial infection rates (FIRs) were greater for Ae. triseriatus than either Ae. albopictus or Ae. aegypti. These measures were integrated into a single numerical score, the transmission amplification potential (TAP) for each species. Differences in TAP scores were due mainly to the differences in DIRs and FIRs among these mosquitoes. Although the TAP score for Ae. albopictus was lower than that of Ae. triseriatus, it was 10-fold greater than that for Ae. aegypti.     

Microsporidiosis (Microsporidia: Culicosporidae) alters blood-feeding responses and DEET repellency in Aedes aegypti (Diptera: Culicidae)

Infection of Aedes aegypti (L.) (Diptera: Culicidae) with Edhazardia aedis (Microsporidia: Culicosporidae) reduced mean human host attraction and landing/probing rates in female mosquitoes by 53 and 62%, respectively, compared with rates in microsporidia-free females. Infection with E. aedis reduced the average weight of unfed female mosquitoes by 4%, caused them to imbibe 23% less blood, and to lay 30% fewer eggs than healthy females. In contrast, E. aedis-infected mosquitoes required 20% more time (>1 h) than healthy females to bite skin treated with 15% DEET. Statistically significant morbidity in E. aedis-infected females was indicated by reductions in host attraction and landing/probing responses, the mass of unfed and blood-engorged females, and fecundity, and by increased DEET repellency.     

Interspecific competition among Aedes aegypti, Ae. albopictus, and Ae. triseriatus (Diptera: Culicidae): larval development in mixed cultures

Interactions among the larvae of Aedes aegypti (L.), Ae. albopictus (Skuse), and Ae. triseriatus (Say) were studied in trispecific and bispecific mixed populations under laboratory and field conditions. Competitive stress (as evidenced by the average time to first, 50, and 75% pupation and the total pupation periods for mixed populations of each species in comparison with their single species controls) was more pronounced in mixed cultures reared in glass jars in the laboratory than in tires under field conditions. In the laboratory, the larval development of Ae. aegypti reared together with Ae. albopictus or Ae. triseriatus, or both, larvae was accelerated significantly. Conversely, the time to pupation for Ae. albopictus and Ae. triseriatus was delayed when reared with Ae. aegypti. However, the average wing length of female Ae. albopictus and Ae. triseriatus was greater in the mixed cultures than in single species cultures. These data indicated that the effect of intraspecific competition was greater than interspecific competition. Adequate food and higher temperature appeared to promote rapid development and higher survival of the immature stages of the three Aedes species in tires placed in the field. In general, Ae. triseriatus larvae required a longer period for larval development and had greater larval mortality than either Ae. aegypti or Ae. albopictus. In mixed populations of Ae, albopictus and Ae. aegypti in the jars and food-rich tires, the periods needed to attain first, 50, and 75% cumulative pupation were not significantly different than in single species controls. We conclude that no clear-cut displacement occurred in mixed experimental populations of Ae. aegypti and Ae. albopictus.