Print version ISSN 0074-0276
Mem. Inst. Oswaldo Cruz vol.98 no.2 Rio de Janeiro Mar. 2003
Mortality in Immatures of the Floodwater Mosquito Ochlerotatus albifasciatus (Diptera: Culicidae) and Effects of Parasitism by Strelkovimermis spiculatus (Nematoda: Mermithidae) in Buenos Aires Province, Argentina
Raúl Ernesto Campos; Victoria Elena Sy
Instituto de Limnología "Dr. Raúl A. Ringuelet", Universidad Nacional de La Plata, cc 712, (1900) La Plata, Argentina
Life tables were constructed for six cohorts of immature stages of the floodwater mosquito Ochlerotatus albifasciatus (Macquart) in a park in Buenos Aires, highlighting the mortality attributable to the parasitic nematode, Strelkovimermis spiculatus Poinar & Camino. Two cohorts were selected to compare parasite incidence in all mosquito stages when low and high parasitism occurred. Development time of Oc. albifasciatus from first instar to adult was 7.7-10 days in the spring, 6 days in the summer, and 10.9-21.9 days in the fall. Survival was estimated as 0-1.4% in the spring, 2% in the summer and 0.2-4.4% in the fall. The highest "K" value (Killing power) occurred during a fall cohort when prevalence of the parasite was 86.9%, and the lowest in a spring cohort. Parasitism occurred during all seasons, but S. spiculatus persisted to adult only in the summer and fall, when adult mosquitoes developed from parasitized third and fourth instars larvae. The abundance of S. spiculatus differed between old and young larvae only when parasite prevalence was the highest. Although pupae and adults of Oc. albifasciatus were parasitized, no pupal mortality attributable to parasitism was recorded. The proportion of parasitized adults ranged from 14.2% and 5.7% in the two cohorts compared. Pupal wet weight and adult wing lengths did not differ between parasitized and unparasitized individuals.
Keywords: Ochlerotatus albifasciatus - Aedes albifasciatus - mortality - floodwater mosquito - Strelkovimermis spiculatus - parasitism - Buenos Aires - Argentina
Ochlerotatus (Ochlerotatus) albifasciatus (Mac-quart) is a floodwater mosquito widely distributed in Argentina (Darsie & Mitchell 1985), incriminated in 1982 as a vector of Western Equine Encephalitis (WEE) (Mitchell et al. 1987). The bite of Oc. albifasciatus may also cause allergic reactions in persons who are hypersensitive to salivary allergens. These have been recently isolated and identified from this mosquito (Docena et al. 1999).
In the wet and temperate climate of Buenos Aires Province, Oc. albifasciatus occurs from spring to fall with occasional hatches in winter if temperature increases (Maciá et al. 1995). Temperature and rainfall were cited as the main factors that determine the fluctuation in the abundance of Oc. albifasciatus (Maciá et al. 1995, Fontanarrosa et al. 2000, García & Micieli 2000, Gleiser et al. 2000). However, it is known that mortality of the immature stages plays an important role in adult survival and abundance, as was reported by Andis and Meek (1985) for Psorophora columbiae.
García et al. (1994) and Maciá et al. (1995) studied the natural enemies of immature Oc. albifasciatus in temperate Argentina. Microsporidans, fungi and nematodes were frequently encountered being the mermithid Strelkovimermis spiculatus Poinar & Camino the main cause of epizootic.
S. spiculatus was discovered in 1986 from immature Oc. albifasciatus in Buenos Aires (Poinar & Camino 1986). At present, the parasite is known from the immature stages of five species of Ochlerotatus (Lynch-Arribalzaga) and Culex (L.) mosquitoes (García & Camino 1990, García et al. 1994). Two studies described the seasonal prevalence of S. spiculatus, one in Cx. pipiens L. (Campos et al. 1993) and the other in Oc. albifasciatus and Oc. crinifer (Theobald) (Maciá et al. 1995). Recently Micieli and García (1999) described the seasonal prevalence and sex ratio of S. spiculatus in eight cohorts of Oc. albifasciatus studiedover 19 months, and estimated the abundance of pre-parasites in pools.
Poinar and Camino (1986), suggested that this nematode shows promise as an agent for biological control of mosquitoes in Argentina. Camino and Reboredo (1994, 1996) studied the life cycle and mass production of S. spiculatus in the laboratory. However, discrepancies between the life histories of this nematode in the laboratory and the field suggest the need for more research on parasite-host dynamics in epizootic situations before using this nematode for mosquito control.
We developed our research with this intention, and to estimate the mortality, survival, and developmental rates of Oc. albifasciatus immatures in parasitized and unparasitized populations using life table methods appropriate for integrate mosquito control (Reisen & Siddiqui 1979). Although life budgets have been formulated for the immature stage of many mosquito species in nature (Service 1993), to date no life tables of parasitized Oc. albifasciatus are available.
The objectives of this study were to examine seasonal patterns of immature mortality and survival of Oc. albifasciatus, in six cohorts followed through the spring, summer and fall. In two cohorts, the mortality attributable to S. spiculatus was quantified and the parasitism of adult mosquitoes characterized.
MATERIALS AND METHODS
Study site - The study area is located in Argentina in the Pampeana biogeographic province (30 to 39°S) of the Neotropical region. Vegetation consists of Graminaceae pasture coexisting with a few shrub species. The climate is temperate (annual average from 13 to 17°C) with year-round rainfall (Cabrera & Willink 1980). The study site was located in the Pereyra Iraola Park (Buenos Aires Province) in a woodland situated near an urban area. The park was created in the 19th century with native and exotic trees. Some parcels of the park are cultivated by agriculturists and floriculturists, and others are used for cattle raising. The larval habitats of Oc. albifasciatus selected for the study consisted of four transient floodwater pools situated in open land. Pool surface areas were not estimated because the edges were not clearly discerned. The pool bottoms consisted of a layer of leaf litter and debris and water depth after a rainfall period was variable (0.10 to 0.50 m). In the summer, the pools became dry within 6 days but in fall and spring they remained waterlogged for 10 to 25 days.
Larval mortality and survival curves - From October 2000 through June 2001 immature Oc. albifasciatus were collected every day after pool inundation. One hundred dips were taken with a standard dipper of 450 ml. This routine was continued until all adults had emerged, or until the pool was dry. The number of larvae of each instar and pupae from each dip was recorded, and pupal sexes were determined. The individuals were sampled without replacement.
Daily air temperature data were provided by the Faculty of Astronomic and Geophysical Sciences of the National University of La Plata, whose meteorological station is situated approximately 20 km from the study site.
Estimation of accumulative larval development time was calculated from the percentage of larvae by instar (i) on each sampling day. These percentages were calculated and plotted against time on log x probability paper, in order to estimate time (t50) at which 50% of the larvae reach each successive instar (Enfield & Pritchard 1977). Instar durations (id) in days were calculated by subtracting t50 (i) values from t50 (i+1). Estimation of corrected density for each instar (dci) was calculated by multiplying the number of individuals sampled by the instar duration. Plotting the corrected density against larval and pupal age in days, vertical stage-specific frequency distributions were obtained and histograms were constructed. Survivorship curves were drawn connecting the midpoints of each histogram block by a straight line (Reisen et al. 1982). The number of individuals entering in each instar (Si) was estimated from the graph, and the stage-specific survivorship was calculated using procedures described by Service (1973, 1977a,b). Life tables were constructed following procedures used by Southwood (1966).
Parasitism caused by S. spiculatus- All larval instars were examined alive on a micro concavity slide for S. spiculatus parasites, at 100 magnification. For samples with less than 100 individuals, all were examined, for larger samples, a sub-sample of 100 larvae was randomly taken. Larvae parasitized with visible parasites in the body cavity were reared until parasite emergence. Unparasitized larvae were reared and checked every two days for potentially undetected parasites. Upon emergence from larvae, the post-parasite juvenile nematodes were counted.
In the fall cohorts, pupae from samples were weighed to an accuracy of 0.01 mg and kept in individual containers until the adult molt. Males and females were dissected for parasites, and wing length was measured (accuracy of 0.01 mm) from the alular notch to the distal margin excluding the fringe scales (Bock & Milby 1981). Because the proportion of the adult mosquitoes parasitized by mermithids in nature is low, an additional sample of pupae from 100 dippers was taken every day from the first record until the day when no pupae were observed.
Nematode parasitism was measured by the prevalence (number of parasitized hosts/number of examined hosts) x 100, mean intensity (number of parasites/number of parasitized hosts), and abundance (number of parasites/number of examined hosts) (Morales & Arelis Pino 1987).
Other pathogens, such as Microsporidia (Protozoa) were observed in Oc. albifasciatus, but no attempts were made to isolate and record their prevalences.
Larval developmental time and sexes- Abundance of Oc. albifasciatus increased from spring to fall by 2.8 times (mean ± standard deviation (SD): spring = 629.3 ± 633, fall = 1,792.5 ± 14.85); however, the population increase did not follow a linear function (P > 0.05).
Development time from first instar to adult in pools was 9.2 ± 1.30 days in spring; 6 in summer, and 16.4 ± 7.79 in fall. Duration of the first instar was short and homogeneous during all samples; the last fall cohort however, was shown to be half the time of the other cohorts. On the other hand, the second instar was twice as long in fall, with respect to the spring and summer cohorts. The third instar duration was the most heterogeneous and no seasonal pattern was detected. The fourth instar duration was the longest with bimodal peaks at the start of spring and at fall. Pupal stage duration ranged from 1.4 days in summer to 10.3 days in fall (Table I). However, Kruskal-Wallis ANOVA for pre-adult development times was not significantly different between cohorts (H = 5.26, df 5, P = 0.38). Contingency table of sex ratios (male/female) showed significant differences between seasons (c2 = 7.77, df 2, P < 0.05), females predominating in all cohorts except during summer (Table II).
During sampling of the cohorts, daily mean air temperature varied from 23°C in summer to 12°C at the end of fall (Fig. 1). Developmental time decreased progressively as temperature increased for subsequent cohorts in spring. The shortest developmental time occurred in the summer cohort (6 days) while during the fall it increased again, recording the longest developmental time in the early fall cohort (21.9 days). However, the mean developmental time of each cohort was not significantly correlated with temperature (rt°max. = -0.64, P = 0.17; r t°min. = -0.60, P = 0.21; r t°mean = -0.45, P = 0.37 n = 6), indicating that temperature per se is not the major determinant of the developmental time of immature Oc. albifasciatus in nature.
Horizontal stage-specific life tables and life expectancies- Percent survivorship of Oc. albifasciatus from first instars to adulthood was estimated as 1.4% in spring, 2% in summer, and 0.2-4.4% in fall. In cohort 1 (spring), no survival was recorded. Fifty percent of the deaths occurred in every cohort in later instars and pupae. The highest relative proportion dying (Pi) and daily proportion dying (Pdi) occurred in pupal stage in all cohorts (Table III). Comparing mortality by larval instar, relative and daily death was heterogeneous and differed between cohorts. The highest Pi, occurred in fourth instar in all cohorts except in cohort 2 (spring), where the third instar was the most susceptible. In contrast, the value of Pdi during the cohorts of spring was higher in early instars (Table III). The K value ["Killing power" of Varley & Gradwell (1960)] was higher in cohort 5 (fall) than in the other cohorts (Table III). Using survivorship curves (Fig. 2), a series of life tables was calculated using 1-day time increments. Survival curves analyzed by Wilcoxon and Log-rank tests show homogeneity between all cohorts (c2 = 8.00, df = 4, P = 0.092). The expectation of life (ex) progressively decreased from the early larvae until molting to pupa, except for the cohort 2 (spring) which showed an increment of ex at the third day (Fig. 3), when larvae molt to third instar. The pupal stage showed similar tendencies as the larval stages, except for cohort 5 (fall) where an increment of ex was observed when more than 50% of larvae reached the pupal stage (Figs 2, 3). Life expectancy distributions between cohorts did not differ significantly when tested by a Kolmogorov-Smirnov 2-sample test (Cohort 1/cohort 2: Dmax = 0.35, n1 = 9, n2 = 11; cohort 1/cohort 4: Dmax = 0.44, n4 = 7; cohort 2/cohort 4: Dmax = 0.53; cohort 5/cohort 6: Dmax = 0.40, n5 = 21, n6 = 12; cohort 4/cohort 6: Dmax = 0.54; P > 0.1. Cohort 4/cohort 6: Dmax = 0.57, P > 0.05).
Fig. 2: stage-specific age distribution and survivorship curves for immature stages of Ochlerotatus albifasciatus
Seasonal parasitism- S. spiculatus was present in all cohorts of Oc. albifasciatus, except for cohort 1 (spring) in which no parasitism occurred. Because the number of parasitized hosts was not recorded for spring and summer cohorts, parasite abundance was used as an index of parasitism. Abundance ranged from 0.09 to 0.52 in all cohorts except for cohort 5 (fall), where abundance was higher (range: 1.56-2.41). To compare seasonal abundance variability of S. spiculatus in Oc. albifasciatus larvae, we tested all cohorts by Kruskal-Wallis Anova on ranks and significant differences were observed (H = 41.50, df 4, P < 0.001). Multiple comparison by Dunn's test showed significant differences between cohort 5 (fall) and the other cohorts (P < 0.05).
To determine whether the abundance varied between ages of the hosts, early instars (I + II) were compared with late instars (III + IV) from all cohorts and seasons. The abundance was higher in later instars in all cohorts, although this difference was statistically significant only for cohort 5 (Table IV).
Comparative occurrence of Oc. albifasciatus parasitized by S. spiculatus, during the fall- S. spiculatus can occur in high and low levels of parasitism. Individuals of cohort 5 (high parasitism) and 6 (low parasitism) were compared for effects of parasite infesty.
In both cohorts, simple and multiple parasitism were recorded in all stages of the host. Prevalence of the nematode in Oc. albifasciatus in cohort 5 was 86.9%, and ranged from 33.3% in pupae to 96.2% in third instar. In cohort 6, prevalence was 14.6%, ranging from 4.3% in first instar to 24% in second instar (Fig. 4). The mean intensity of parasitism in Oc. albifasciatus during development of cohort 5 was significantly higher than during cohort 6 for all immature stages (Mann-Whitney rank sum test: T = 39.50, n = 5, P = 0.008). Distribution of instars did not differ between both cohorts (Kolmogorov-Smirnov 2-sample test, D max = 0.36, P > 0.1, n = 5).
At both levels of parasitism, parasite numbers were recorded in adult mosquitoes. These adults arose only from third and fourth instar larvae collected from the field; no parasitized first and second instars larvae survived to the adult stage. However the percentage of parasitized larvae of Oc. albifasciatus molting to adults was less than 2% in both cohorts (Table V).
In adult Oc. albifasciatus, larval parasites were located in the abdomen of mosquitoes, but when multiple parasitism occurred, nematodes invaded the thorax as well. The proportion of Oc. albifasciatus adults parasitized by S. spiculatus during the cohort 5 was 14.2%, and 5.7% in the cohort 6. In both cohorts, parasitized males (61.9% and 6.3% respectively) were not significantly different from parasitized female (38.1% and 4.8% respectively) (Cohort 5: Gadj = 1.02; Cohort 6: Gadj = 0.68; P > 0.1). To establish if parasitism affects the weight of pupa and size of adult O. albifasciatus mean values were compared by sex. Size and weight of parasitized individuals did not differ significantly from unparasitized (Table VI). Coefficients of variation of wing-lengths were 4.4% for males, and 5.8% for females. However, when comparing parasitized and unparasitized sexes, parasitized females (Table VI) was the most heterogeneous group.
Because multiple parasitism occurred in both male and female adults, the number of parasites per mosquito was compared in both cohorts. In the cohort 5, parasites per adult mosquito ranged from 1 to 7 (2.4 ± 1.46) in males, and from 1 to 6 (2.1 ± 1.56) in females. On the other hand in cohort 6 it ranged from 1 to 3 (1.8 ± 0.79) in males, and from 1 to 2 (1.3 ± 0.52) in females. However, no significant differences between groups were detected (Kruskal-Wallis Anova, H = 4.233, df = 3, P = 0.237).
Fava et al. (2001) reported that the developmental time of first, second and third instars, and pupa of Oc. albifasciatus in semi-natural conditions decreased as temperature increased. In contrast, the current study described no remarkable variation in developmental time among these instars. However, large variation occurred in fourth instar and pupal stage where developmental time increased when environmental temperature was low (cohorts of fall and early spring).
With respect to total immature development times, no significant differences were seen between cohorts from spring to fall. Fava et al. (2001), studying three groups of cohorts (two winter one spring), detected significant differences in development time between the first group from winter and the remaining groups. Fontanarrosa et al. (2000), in a study developed under natural conditions, reported Oc. albifasciatus development time ranging from 6 days to 32 days, associated with mean temperature (24ºC and 13°C respectively); however, these authors did not detect significant differences in the development time. All these studies indicate temperature as the major influence on development time of immature Oc. albifasciatus. However, significant differences were observed only in the winter, when lowest temperatures occurred.
Although Fontanarrosa et al. (2000) attributed this heterogeneity in the development time to seasonal temperature, the variation occurring in each cohort in a particular season is probably a consequence of other factors. Growth, development and survivorship of immature mosquitoes are affected by population density (e.g. Léonard & Juliano 1995, Gleiser et al. 2000) and by the presence of enemies (Nannini & Juliano 1997). Our results show how development of Oc. albifasciatus changes during two successive cohorts in fall. Development time of immatures in the second cohort was shorter than in the first, despite the lower temperature. Possibly, the high density of the host (which moreover favored the parasitism by S. spiculatus) may have slowed development time in cohort 5. In contrast, the cohort 6 experienced lower density and parasitism, and the developmental period was faster.
A survival curve constructed for Oc. albifasciatus was described as type II (Ludueña Almeida & Gorla 1995) with the risk of death approximately constant with age (Slobodkin 1962). In contrast, our life table in nature revealed low mortality in young instars, and higher in old instars as in an intermediate stage between Type III and I curves of mortality of Slobodkin (1962).
First instar/adult survivorship values for Oc. albifasciatus ranged from 0% to 4.4%. However, comparisons with previously published Oc. albifasciatus survival may be misleading because those studies did not include all immature stages. Averages for other field populations of mosquitoes, such Aedes cantans (Meigen) and Aedes africanus (Theobald) reported survivorship values of 6.2% and 9-17% (Service 1973, Lakhani & Service 1974) substantially higher than in our results.
Fava et al. (2001) attributed the mortality in young immature of Oc. albifasciatus to temperature variation. Because their experiments were made in a 500 ml flask, neither presence of natural enemies nor other natural causes of mortality were reported. Our results showed that the lowest "K" value (0.44) occurred in cohort 1 from early spring, coincident with the absence of S. spiculatus in the pool. In contrast, the highest "K" value (2.76) occurred in cohort 5 from fall, when the highest parasitism was recorded. In remaining cohorts although parasitism occurred, "K" values were lower and homogeneous. These results indicated S. spiculatus to be a remarkable natural enemy of the Oc. albifasciatus immature stages.
Although multiple parasitism occurred in all instars, the main mortality was recorded at the end of fourth larval instar (Table III). Low mortality in early instars may be a consequence of high tolerance of Oc. albifasciatus to the parasite. In contrast to Camino (1988) who reported that multiple parasitism kill first and second instars, we believe that a high proportion of multi-parasitized young larvae does not exactly kill this instars in nature. This assumption is supported by our data for abundance of S. spiculatus parasitizing Oc. albifasciatus, that show an increment in the later instars (Table IV).
Parasitism by S. spiculatus - The majority of surveys of S. spiculatus in Oc. albifasciatus were performed with a weekly or irregular design of sampling, and have reported prevalence of 80% (Maciá et al. 1995) and from 0% to 100% (Micieli & García 1999). Because the development time of Oc. albifasciatus is short, and the permanence of the larva in fourth instar is longer than in younger instars, the prevalence may be biased as a consequence of sampling frequency.
During the spring Maciá et al. (1995) and Micieli and García (2000) reported 12 and 67% of parasitism respectively, in third and fourth instar larvae. In the present study, no parasitism was recorded in the first spring cohort; however, in the later cohort, S. spiculatus was present in all instars with abundances ranging between 9% in first and second instars to 52% in third and fourth instars.
Both earlier reports indicated an absence of hatching of Oc. albifasciatus in summer (December to February). In contrast, we recorded a cohort rearing from the end of December to January with parasitism by S. spiculatus similar to spring and fall prevalence (except for cohort 5).
Comparative occurrence of parasitism - Although parasitism by S. spiculatus is known for five mosquito species in nature (Campos et al. 1993, García et al. 1994, Maciá et al. 1995), epizootic peaks were recorded only for Oc. albifasciatus (Maciá et al. 1995, Micieli & García 1999). Parasitism in Oc. albifasciatus occurred during all seasons, with peaks restricted to spring and fall (Maciá et al. 1995, Micieli & García 1999). Even though the causes of this increase are unknown, certainly they are closely related to the high density of Oc. albifasciatus immatures.
During the fall, we recorded two cohorts of Oc. albifasciatus parasitized by the mermithid. In cohort 6, penetration by the pre-parasite occurred mainly during the first instar of the host, and was reflected by the highest prevalence recorded in the second instar. Then prevalence progressively decreased, possibly as a consequence of the absence of pre-parasites; the mortality due to parasite emergence and, consequently, the proportional increase in the amount of remaining unparasitized larvae. However, in cohort 5, prevalence increased from first to third instar, possibly as a consequence of nematode hatches after a second rainfall.
Parasitic abundance was not significantly different between early and late instars in cohort 6. By contrast, the abundance was twice as high in late rather than early instar larvae during cohort 5. From high multiple parasitisms detected in fourth instar in cohort 5, the probability of this larvae surviving to adults was expected to be lower than cohort 6, with its low multiple parasitism. Surprisingly, 35.1% of parasitized fourth instar larvae pupated in both cohorts. This suggested that the proportion of parasitized adults emerging independs on the abundance of larval parasitism.
The abundance of parasites in third and fourth instar Oc. albifasciatus was explained by the presence of infective parasites in the pools (at least for 13 days at the time when larvae molted to third instar), or as consequence of new hatchings of S. spiculatus. Both hypotheses may be possible because during the development of cohort 5, rainfall on the 8th day, increased the surface area of the pool. Micieli and García (1999) made similar observations. They collected pre-parasites of S. spiculatus from a pool for 13 days, and reported that six days later, another rain occurred and new pre-parasites were found. These observations disagree with the survivorship of 48 h estimated for the pre-parasites by Camino and Reboredo (1994).
Parasitism occurred in adult mosquito - The only record of S. spiculatus parasitizing adults mosquito in nature was reported by García et al. (1994), who isolated a worm from a Cx. dolosus Lynch Arribálzaga female caught by CDC trap. Here we reported both sexesof adult Oc. albifasciatus parasitized by S. spiculatus, collected as third and fourth instar, and pupa from both cohort 5 (high parasitism) and 6 (low parasitism). Furthermore, parasitism occurring in first and second instars larvae culminated with the emergence of the nematode from late fourth instar Oc. albifasciatus.
As a result of the late parasitism occurred in previously parasitized larvae, parasites were observed in asynchronous development in some third and fourth instar Oc. albifasciatus. In these cases the emergence of the first nematode killed the host. However, when later parasitism occurred in third and fourth instar not previously parasitized, these nematodes were observed in the adult mosquito.
Larger individuals of mosquito have a greater tendency to disperse from the larval habitat (Nasci 1987) and hence may have greater potential to disperse S. spiculatus to new pools. Therefore the wing lengths of the of Oc. albifasciatus adults were compared to see if parasitized mosquitoes differed in size from unparasitized ones. No difference was detected between mean adult size of parasitized and unparasitized Oc. albifasciatus, even though multiple parasitism occurred. Apparently, parasitized adults have the same capacity of dispersion as and unparasitized ones and can carry S. spiculatus to others pools.
To Drs A Maciá (Facultad de Ciencias Naturales y Museo de La Plata, Universidad Nacional de La Plata, Argentina), and LP Lounibos (Florida Medical Entomology Laboratory, University of Florida, USA) for critical review.
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Raúl Ernesto Campos
Received 23 July 2002
Accepted 22 January 2003
This work, was supported by a Grant (PIP no. 700/98) from Consejo Nacional de Investigaciones Científicas y Técnicas (Conicet), Argentina. This paper is a scientific contribution no. 734 of the Instituto de Limnología "Dr. R. A. Ringuelet".