ECOLOGICAL STUDIES ON AEDES NOTOSCRIPTUS (DIPTERA : CULICIDAE)
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1 ECOLOGICAL STUDIES ON AEDES NOTOSCRIPTUS (DIPTERA : CULICIDAE) MARION A. FOOT, (nee Hill) Plant Diseases Division, D.S.I.R.*, Auckland. SUMMARY Aedes notoscriptus was reared in the laboratory, but eggs from these cultures did not hatch. At least one blood meal was necessary for complete development of the ovaries; and the presence of spernlatozoa in the spermathecae of the female was not necessary. Oviposition is described. Site preferences were found to be domestic containers in shaded places in or near trees and shrub covers, particularly m above ground level. Biting activity was found to have marked peaks at dusk and at dawn when light intensity was between 1 and 10 foot candles. INTRODUCTION The mosquito Aedes (Finlaya) notoscriptus Skuse occurs widely in the Australian zoo-geographical region, having been recorded in Australia, Indonesia, Papua, New Caledonia and New Zealand. In New Zealand it is abundant around Auckland, Whangarei and Nelson; and is thought to have been introduced through commerce from Australia (Belkin, 1962). This mosquito has been studied by Skuse (1888), Graham (l929), Miller and Phillipps (l952), Belkin (1962) and Dumbleton (1968). It is essentially sylvan in habit, but is reported as breeding in any small semi-permanent bodies of organically rich, scum- free water. It has become known as the "day-biting" mosquito because this habit contrasts with that of the other common species, which bite at night. This paper deals with rearing investigations, ovarian develop- ment, oviposition preferences, and the biting cycle of A. notoscriptus. Field work was carried out at Muriwai Beach 48 km north of Auckland. The study area was sited approximately 0.8 km from the coast, and consisted of open lawn backed by a tree- clad cliff. The forest was secondary (mainly manuka: Leptospermum scoparium J. R. & G. Forst., and kawakawa: Macropiper excelsum Forst.) with a m high canopy. I. REARING INVESTIGATIONS There is no apparent previous record of A. notoscriptus having been reared in the laboratory. In this attempt, rearing from fieldcollected eggs to adults was accomplished, but eggs obtained from these adults failed to hatch. *This contribution is based on work done as part of a B.Sc. course at Auckland University in 1966.
2 Eggs and early instar larvae were collected in the fiield and placed in rearing containers in a room temperature of C. For small batches of larvae, plastic bowls (11.5 cm diameter x 4.5 cm deep) were used, and for large numbers a plastic aquarium (30 x 15 x 13 cm) was used. The rearing medium consisted of water stagnated for several days together with leaf litter, and the containers were topped up daily with this. Prior to emergence, pupae were placed in the adult cage which was constructed from a 30 x 15 x 13 cm plastic aquarium placed on its side, the front being covered with cotton cloth with a 10 cm diameter sleeve stitched into it. Adults were fed on a wad of cotton wool soaked in 10% sucrose, and blood meals were supplied by exposing an arm in the cage once a day for fifteen minutes. Glass jars, 10 x 5 cm were filled with larval rearing medium and kept in the cage for egg-laying. Eggs generally hatched within twenty-four hours of being brought in from the field and covered with larval medium. The larvae took eleven to twelve days to develop from the first to the end of the fourth instar. They varied in length from one millimeter in the first instal- to eight millimeters in the fourth. Pupae hatched into adults after twenty-four to forty-eight hours, and the adults lived for up to six weeks, with the females outliving the males. Body length of the females ranged from 4.5 to 5.5 mm, while that of the males from mm. In the field much greater variability in body lengths and duration of the stadia was exhibited, probably as a result of variable larval nutrition. For exan~ple, adult females were found to range from three to seven millimeters in length. Several batches of early instar larvae were collected in the field and placed in the large gauze-covered larval rearing container. Adults were removed and sexed as they emerged. Of a total of 717 adults 361 were males and 356 females, indicating a 1 : 1 sex-ratio. A continuous laboratory colony was not established because eggs produced in the laboratory failed to hatch. These may have been in diapause, but several attempts at breaking this condition were unsuccessful. Clements (1963) described at length the physiology of egg diapause in the aedine genera Aed~es, Psorophora and Haemagogus. A more probable factor may have been mating failure. Certain easily-reared culicine species will mate in small cages and are said to be stenogamous, but many aedine species are eurygamous, that is, they require large spaces for mating. In-cage matings of A. notoscriptus were never seen in the present study, and time prevented attempts at inducing mating similar to those described by McDaniel and Horsfall (1957), Burchanl (1957), Wheeler '& Jones (1963), or Miura (1967). It is recommended that this important aspect be investigated fully by other workers attempting to colonise A. notoscriptus.
3 11. OVARIAN DEVELOPMENT Female mosquitoes of several species are able to develop normal, viable eggs without first having taken a blood meal (Bates, 1949, and Clements, 1963). In other species, egg development after a blood meal depends on the presence of spermatozoa in the spermathecae. Aedes aepypti, which is superficially similar to A. notoscriptus, requires a blood meal for full ovarian development; and although one strain of A. aegypti requires the presence of spermatozoa in the spermathecae as a stimulus to ovarian development, this is by no means usual (Christophers, 1960). Methods and Results Two sets of female A. notoscriptus were tested on three types of diet. One set was unmated, and the other reared in the presence of males. The three diets were (a) water, (b) sugar solution (lo%), and (c) blood meals with water between meals. Ovaries were examined at intervals from twenty-four hours to fifteen days. Three stages in the development of the ovaries are illustrated in Fig. 1, and are described with approximate dimensions, as follows : (A) Ovary 0.7 mm long and 0.2 mm wide. Ova difficult to distinguish, transparent, spherical and 0.07 nlm in diameter. (B) Ovary 1.0 mm long and 0.4 mm wide. Ova fairly easy to distinguish, with large opaque centres. Each has a definitely ovoid shape, and a small apical follicle cell. The long axis measures 0.1 mm. (C) Ovaries filling abdominal cavity. chorion visible. Eggs ready to be laid. Ova 0.6 mm long, with The effect of diet on ovarian development was investigated, using fourteen females. Dive were fed on water and showed no development beyond stage 1; two were fed on sucrose solution and developed to only stage 2 after seven to ten days from the first feed; and seven were given blood meals and showed complete development within seven days of the first meal. There was no obvious differences in ovarian development between virgin females and those reared in the presence of males. In both cases the ovaries developed fully after a blood meal, so that the presence of spermatozoa in the spermathecae does not appear to be necessary for complete egg development. Females were given one, two or three blood meals and the number of eggs in their ovaries, counted one to two weeks later, were as follows.-fed once: 40 eggs and 30 eggs; fed twice: 39 eggs, 17 eggs and 24 eggs; fed thrice: 22 eggs. There thus appeared to be no correlation between the number of eggs developed and the number of blood meals taken.
4 Fig. 1: Ovarian development jn Aedes notoscriptus. A. First stage. B. Second stage C. Thi~d stage t.f.-terminal filament; f.c.-follicle cell; 0.v.-ovum. 1.od-lateral oviduct; cod--common oviduct; sp.-spermatheca EGG LAYING There have been several conflicting descriptions of the act of oviposition in A. notoscriptus. Skuse (1888) described the eggs as being laid in boat-shaped masses on the surface of the water. Graham (1929) described them as being laid singly on the surface of the water, sometimes running together end to end to form starshaped masses. He also found the breeding places of A. noto-
5 scriptus to be domestic containers, tree holes, and leaf axils; and that there was a preference for organically rich water in shaded places. Oviposition Oviposition was observed in the laboratory. Gravid females congregated around the shaded egg-laying jar, usually standing passively on the surface of the water, or on the inside walls of the jar. Females about to lay, however, moved restlessly around the sides of the bowl at the water's edge, testing it with the tips of their abdomens. When a suitable location was found, the female gripped the side of the jar with her fore- and mid-legs, while her hind-legs were spread out behind her on the surface of the water. She then bent her abdomen sharply under her until it touched the side of the jar at the meniscus. After a final "exploration" with her abdomen she deposited an egg. She then moved to one side of this egg and deposited another. This was repeated until up to six or eight eggs had been laid, after which a new location was sought. The eggs were white when first deposited, but after a minute or two took on their characteristic black colouration. Oviposition was not observed in the field. However, all eggs collected were found attached to the sides of containers in the above described manner, and not as stated by Graham (1929). Egg-laying Prefe~rences At Muriwai nine glass jars of water were used to gain information on egg-laying preferences. Two jars, one clean water and one organically rich water, were located at each of three elevations, namely, ground level and 4.6 and 7.6 m above ground level; and in each of three degrees of shade, namely, none, partial, and full shade. The jars of clean tap water were changed regularly to prevent contamination with litter. Organically rich water consisted of larval rearing medium with a bottom layer of soil. Old donlestic containers scattered throughout formed a semi-permanent breeding ground in this area. TABLE 1 Numbers of A. notoscriptus larvae collected from oviposition jars in the field. April-August, 1966, Muriwai, North Island. Ground Level 4.6m Stratum 7.6m Stratum Degree of Stagnant Clean Stagnant Clean Stagnant Shade Water Water Water Water Water None Partial* Full? *Edge of forest: at the foot of the first trees; direct sunlight over about 50% of the area. +Inside forest: very little direct sunlight.
6 The collections of this experiment are presented in Table 1. Every week, any larvae found in the jars were removed for counting and identification. It was not possible to do this with the jar at 7.6 m as it was almost inaccessible. It was recovered at the end of the experiment and the number of eggs and larvae counted. The experiment extended through the eleven week period, 3rd April - 24th July, The results in Table 1 suggest a pronounced preference for organically rich water and semi-shade, particularly at the 4.6 metre stratum. In the forest, larvae were found in the jar of organically rich water, particularly in late June and July. This rise in numbers coincided with a decline at the edge of the forest, as shown in Figure 2. It may mean that there was a preference for laying eggs further inside the forest with approaching winter. partial shade46m up,,, -- partial shade,ground level.,..., full shade,ground level Time (Months) Fig. 2: Recovery of larvae of A. notoscriptus at varying elevation and shade regimes. April-July, 1966, Muriwai Beach N. Island. 25
7 The overall numbers dwindled from autumn to winter. By early August, there were still small numbers of larvae in several breeding places, and there is no reason to doubt that this would continue until the onset of spring or summer when the numbers would rise again. Three jars of sea water at various dilutions with tap water (undiluted, 50%, 25% ) were placed in semi-shade at 4.6 m and in the jar of 25% sea water one larva was found. It subsequently developed into a normal adult female in the usual length of the, and indicated that larvae of this species could breed in the slightly saline water within reach of salt spray from the beach. Several other species of Aedes are also capable of survival in varying salinities (Clements, 1963). In the course of this work larvae of Culex pervigilam Bergroth were found in only the two jars of water at ground level at the edge of the forest. Weekly recordings of relative humidity and water temperatures were taken at the four main sites between and hours. Figure 3 shows that water temperature may have had some influence as there was an average difference of 1.7"C between the partially shaded jars at ground level and those at the 4.6 m level, coincident with a preference for the latter site (the warmer). Rel. Hum Nos. Noshade Semi Shade Full Shade 15 ft Up (semi shade) Fig. 3: Mean water temperature and relative humidity, and total larval numbers recorded at various shade and elevation regimes April-July, 1966, Muriwai Beach, N. Island.
8 Although water temperature was high at the no shade site, no eggs were laid, possibly because of the deterrent effects of wind and lack of shade. Relative humidity appeared to have little effect on the preference of sites. In summary, four factors important in a desirable egg-laying site appear to be: shade, organically rich water, lack of wind, and high water temperature. In the laboratory, three clear glass egg-laying jars were placed in a cage containing approximately 200 mosquitoes. These contained (I) organically rich water (larval rearing medium), (2) clean tap water, and (3) clean tap water, jar completely blackened. The females were offered a daily blood meal, and after a period of six weeks, the jars were removed and numbers of eggs counted. The only jars containing eggs were 1 and 3 with 43 and 26 eggs respectively. The choice of sites must, therefore, have been visual as colour was the only difference between 2 (no eggs) and 3 (26 eggs). Breeding Places in the Field Larvae were found in almost every water filled, man-made container observed, provided it was relatively well shaded. In several cases larvae were found together with those of C. pervigilans but the water was always only slightly polluted, and the relative abundance of the two species varied greatly. A. notoscriptus preferred more polluted conditions than C. pervigilam. Little time was spent searching for natural breedings places, and none was discovered. Graham (1929) found eggs and larvae in such places as tree holes, leaf axils, etc. The present results on egg-laying preferences agree with his findings, since there was a strong preference for laying eggs above ground level. IV. BITING ACTIVITY A. notoscriptus is commonly referred to as the "day-biting" mosquito. A series of four, twenty-four hour collections were carried out at Muriwai Beach to study its biting activity. Methods The location was nine meters inside the edge of secondary forest covering the cliff at Muriwai. The canopy was 4.6 metres above ground level, and under-growth was sparse. A natural spring was situated 3 metres away and the ground was soft and damp. For the first collection two hours in every three were spent collecting, but in the last three collections this was reduced to one hour in two. The author's (Caucasian, female) bare legs from ankle to knee height were used as the attractant, and any mosquito which began to bite was removed with an aspirator. At the end of each hour the mosquitoes were counted and identified. During the hours of darkness it was necessary to use a torch, but this was used as little as possible, and is assumed not to have affected the biting activity.
9 Throughout the collection, hourly readings were taken of temperature, relative humidity, and light intensity. Light intensity was recorded with a Weston light meter, from the light reflected off a horizontally placed sheet of white paper, holding the instrument 15 cm away and at an angle of 45" to the paper; and readings were later converted into foot-candles. Relative humidity was recorded from a hair hygrometer hung 61 cm above the ground, and temperature was recorded from a similar position. Results and Discussion The collections were made on the 5th and 19th of March, and 2nd and 16th of April. A. notoscriptus was the most numerous mosquito; and only two other species were present: C. pervigilans and Aedes antipodeus (Edwards). Figure 4 shows that A. notoscriptus has a typical crepuscular (dawn/dusk) biting cycle, and is not a true day-biter as was first thought. A small peak always occurred at the commencement of each collection. This was created by mosquitoes already resting nearby. They formed no part in diurnal biting activity brought about by females flying in search of food. sunset Time of Day (hrs) sunrise Fig. 4: The biting activity of Aedes notoscriptus as shown by four twenty-four hour collections. 2 8
10 Light intensity appeared to have the greatest influence on biting activity. In all cases peak activity occurred when the light intensity was between 1-10 ft/c. Relative humidity was high throughout and no definite influence could be established. Rain did not deter biting activity, as two hours of steady rain at dawn on the 2nd April in no way suppressed the dawn peak. The two other species collected were present in much smaller numbers: 26 C. pervigilans and 29 A. antipodeus. Biting cycles for these species could not be established from these numbers. ACKNOWLEDGMENTS I wish to thank Professor J. G. Pendergrast formerly of Auckland University, who supervised my work and helped me in many ways. I also wish to thank my parents, Mr. and Mrs. S. Hill of Muriwai Beach, for their co-operation with my field work. REFERENCES BAKER, R. H., 1964: Mating problems as related to the establishment and maintenance of Laboratory colonies of mosquitoes. Bull. World Health Organ. 31: BATES, H., 1949: "The Natural History of Mosquitoes". New York, Macmillan. BURCHAM, E., 1957: Artificial insemination of Aedes aegypti (L). Canad. Ent. 89: BELKIN, J. H., 1962: "The Mosquitoes of the South Pacific." Vol. 1-11: University of California Press. CHRISTOPHERS, R., 1960: "Aedes aegypti". Cambridge University Press. CLEMENTS, A. N., 1963: "The Physiology of Mosquitoes". Vol. 17. Zoology Division. Int'l Series of Monographs on Pure and Applied Biology. Macmillan, New York. DUMBLETON, L. J., 1968: A synopsis of the New Zealand mosquitoes (DIPTERA : CULICIDAE), and a key to the larvae. Tuatara 16: GRAHAM, D. H., 1929: Mosquitoes of the Auckland District. Trans. Proc. N.Z. Inst. 60: HADDOW, A. J. and CORBET, P. S., 1962: Entomological studies from a high tower in Mpanga Forest, Uganda. Trans. R. ent. Soc. London 113: McDANIEL, I. N. and HORSFALL, W. R., 1957: Induced copulation of aedine mosquitoes. Science 125: 745. MILLER, D. and PHILLIPPS, W. J., 1952: Identification of New Zealand mosquitoes. Cawthron Institute, Nelson, N.Z. MIURA, T., 1967: Establishment and maitenance of a laboratory colony of Aedcs nigromaculis (Ludlow) (Diptera : Culicidae) by induced mating. Calif. Vector Views 14 (9):
11 SKUSE, FREDERICK A. A., 1888: Diptera of Australia. Proc. Linn. Soc. N.S.W. 3, SSENKUBUGE, T., 1965: Entomological studies from a high steel tower in Zika Forest, Uganda. Part 1. The biting activity of mosquitoes and Tabanids as shown by twenty-four hour catches. Trans. R. ent. Soc. Lond. 117: WHEELER, R. E. and JONES, J. C., 1963: A technique for artificial insemination of Aedes mosquitoes. Mosquito News 23 (4) :
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