The Biology of Anopheles quadrimaculatus Say
Reproduced from the Proceedings of NJMCA. Please use the following citation when referring to this article:
O'Malley, C. 1992. The Biology of Anopheles quadrimaculatus SAY . Proceedings of the Seventy-Ninth Annual Meeting of the New Jersey Mosquito Control Association, Inc. pp 136-144.
CLAUDIA M. O'MALLEY, Burlington County Mosquito Extermination Commission, 49 Rancocas Road, Mount Holly, NJ 08060
Anopheles quadrimaculatus Say is the most important North American anopheline in the eastern United States (Kaiser et al. 1988). Its distribution includes the eastern and central U. S., north to southern Canada. It also occurs in Mexico and reaches its greatest abundance in the southeastern U. S. (Carpenter and LaCasse 1955).
The importance of An. quadrimaculatus lies mainly in the fact that it is the chief vector of malaria in the eastern, central and southern U. S. (James and Harwood 1969). This concern with disease has tended to overshadow that fact that it also serves a significant pest species (Horsfall 1972). An. quadrimaculatus has long been recognized as an important mosquito, but not always by this name. In John Smith's 1904 listing of New Jersey mosquitoes this species is referred to as Anopheles maculipennis, the "four-spotted Anopheles" (Headlee 1945). And, more recently, it has been discovered that An. quadrimaculatus is actually a complex of at least 4 sibling species (Narang se al. 1989).
An. quadrimaculatus females deposit eggs singly on the surface of the water. The entrapment of air in floats along the sides of the eggs, along with combination of hydrophilic and hydrophobic areas on each side causes the egg to remain properly oriented in the water. Since eggs float freely and each egg has its own positive meniscus, they tend to gravitate toward other positive meniscuses such as those around plant steins, other eggs and other objects that break the surface film of water. If a surface of water bearing eggs is lowered eggs may become stranded on stems or much at the margin (Horsfall 1972).
Females can oviposit 2 or 3 days after a bloodmeal. The eggs for the first spring brood are laid in April or early May (Siverly 1972). In laboratory studies with this mosquito, females laid from 9 to 12 batches of eggs during their lifetime, and each batch varied from 194 to 263 eggs (Carpenter an LaCasse 1955). Oviposition has not been observed during the day; rather, begins with waning light near dusk, and most eggs are deposited during the first 2 hours after nightfall (Horsfall 1972). Laboratory experiment sites with selection of oviposition sites have also shown that female An. quadrimaculatus regularly selected the pan with the darkest background of a series for oviposition (Bates 1970). In nature, An. quadrimaculatus eggs and larvae tend to be positively associated with aquatic vegetation. Eggs are usually found in meniscuses created by vegetation and flotage emerging through the surface film of permanent bodies of water.
The time between oviposition and hatching ranges between 24 and 50 hours. The highest temperature favorable for hatching is 35 degrees C; the developmental zero, the temperature at which development cannot take place 10 degrees C, and the optimum temperature for embryonic development is 33 degrees C (Horsfall 1972). Resistance for extremes of temperature and for a certain amount of desiccation have been demonstrated; however, freezing and temperatures in excess of 40 degrees C will kill most eggs (Bates 1970).
Although larvae of this species can first appear in New Jersey in April or May, Anopheles punctipennis is the more common spring anopheline, with numbers of An. quadrimaculatus increasing as the season progresses to reach peak numbers in July and August.
The rate of growth of mosquito larvae depends on three general factors: the environmental temperature, the genetic characteristics of the species and "threshold of development", that is, the temperature at which, on the descending scale, development definitely ceases and at which, on the ascending scale, development is initiated (Bates 1970). Huffaker (1944) judged the threshold for An. quadrimaculatus larval development to be approximately 7 degrees C. Temperatures above 35 degrees become progressively more unsatisfactory for larval development (Horsfall 1972). During the summer, the larval period lasts from about 12 to 20 days, depending on temperature and food supply (Carpenter and LaCasse 1955).
According to Howard, larvae of this species habitually remain immediately below the surface film, with the body practically horizontal. When the water temperature falls below 12-13 degrees C, larvae sink to the bottom, where they may be motionless for long periods (Horsfall 1972).
An. quadrimaculatus larvae are indiscriminate feeders whose natural food includes a wide range of aquatic organisms, both plant and animal, as well as detritus. This food may be living or dead at the time of ingestion. The main criterion in selecting food seems to be whether the suspended material is small enough to eat.
Differential feeding behavior among mosquito species is a reason why some formulations of B.t.i. are less effective against anopheline larvae. Culicine and aedine larvae are water filterers, whereas anopheline larvae are adapted to collect particles from the air-water interface. Feeding individuals remain in a horizontal position at the water surface and filter only particles present in the uppermost layers of the water. Particles which sink deeper than 1-2 mm are not ingested. Additionally, filtration rates of anopheline larvae and about 10-20 times smaller than those of larval Aedes or Culex, so that Anopheles larvae ingest water-suspended B.t.i. particles at lower rates (Aly et al. 1987).
When feeding, An. quadrimaculatus larvae lie horizontally, with the dorsal side just under the surface film. The head rotates 180 degrees horizontally so that it is actually upside down and the venter of the head is dorsal. Feeding is either "eddy feeding" or "interfacial feeding" (Horsfall 1972). Eddy feeding is employed for infusions when the surface contains islets of floating oil materials. Two eddies with converging streams unite in front of the larva to form a current toward the mouth from a distance of about half the length of the larva. Efferent currents flow outward at right angles to the body from the antenna. Particles too large to eat are held by the maxillae, drawn below the surface and discarded as the head is rotated to the normal position.
Interfacial feeding on the membranes of algae, bacteria, debris and fungi is common in nature. Feeding in this manner is accomplished by setting up currents which draw particles to the mouth from all directions in a straight line and at nearly equal velocities. Surface tension of the larval habitat determines the type of feeding. Eddy feeding occurs at a surface tension of less than 60 dynes per square cm; interfacial feeding is practiced in habitats with a surface tension above 62 dynes per square cm (Horsfall 1972).
The pupal stage of An. quadrimaculatus is fairly unremarkable. As with larvae, this stage varies in length according to temperature, but usually lasts from 2 to 6 days (Carpenter and LaCasse 1955). Laboratory studies have revealed the rather interesting point that the pupae are resistant to prolonged removal from water (Horsfall 1972).
Since An. quadrimaculatus overwinter as fertilized females, adult activity can occur whenever temperatures are favorable. The principal factor determining activity, and propagation occurs when a mean temperature of 21 degrees C (70 degrees F) is maintained (Watson and Bishop 1940). This species has several broods each year, but, as is also the case with An. punctipennis, the breeding is irregular and the broods overlap (Headlee 193 1). As was noted earlier, An. quadrimaculatus populations usually do not reach their peak in New Jersey until July or August.
Mating occurs as soon as the females emerge. Males wait in nearby vegetation and seek females as they begin to fly. Copulation is completed in flight and takes 10-15 seconds. One insemination is usually sufficient for the fertilization of all eggs (Horsfall 1972).
Mosquito feeding patterns are largely regulated by host availability and preference (Apperson and Lanzaro 1991). Female An. quadrimaculatus are primarily mammalian feeders and actively feed on man and on wild and domesticated animals (Crans 1964; Carpenter and LaCasse 1955). As noted previously, this is a significant pest species. Females repeatedly seek their hosts, often visiting the same feeding site several times during the course of a bloodmeal (Horsfall 1972). The biting rate for An. quadrimaculatus has been reported to be higher in fertilized than in unfertilized females (Bates 1970). An average complete bloodmeal for females of this species varies between 2.2 mg and 4.0 mg (Horsfall 1972).
The peaks of feeding are at dusk and dawn; however, females have been observed attacking at night and will also seek bloodmeals in daylight on warm days in the early spring. They will also feed occasionally during daylight hours on cloudy days and in dark buildings (Carpenter and LaCasse 1955; Siverly 1972).
Daylight hours are normally spent in resting sites. These must meet 3 general qualifications: 1) the resting site must be convenient to an oviposition site; 2) it must be close to a dependable source of blood; (3) it must have a favorable climate (Horsfall 1972). Among the types of areas utilized as resting sites are hollow trees, stumps, culverts and dams, particularly those which house animals at night. An. quadrimaculatus also enter houses readily.
The flight range of this species varies and depends to some extent on the number of adults produced within a given area and the proximity to suitable hosts. Under average conditions the flight range is 1 mile or less, but studies with marked mosquitoes have shown dispersal of 3 miles from production sites. These flights are individual, rather than in swarms (Carpenter and LaCasse 1955; Horsfall 1972; Siverly 1972).
As noted, An. quadrimaculatus overwinter as mated females. Overwintering sites vary through this mosquito's geographic range. In the southern part of their range, females usually overwinter in sites in or near quarters occupied by man or domestic animals. In the north, overwintering takes place in more isolated areas, such a storm drains, caves and hollow trees (Horsfall 1972). According to Headlee (1945), winter mortality of adults is high.
Information on the longevity of this species is limited. Overwintering females usually die immediately following a single oviposition effort in the spring. Studies with stained mosquitoes in the wild resulted in recapture of marked females as long as 25 days after emergence. In colonies maintained at 25-27 degrees C, 50% of females survived 21 days, and the maximum life span was 62 days. Males appear to be much shorter lived than females since 50% of them were dead 7 days after emergence (Horsfall 1972).
Larval Habitats and Associated Mosquito Species
In North America, most anophelines prefer habitats with well-developed beds of submergent, floating leaf or emergent aquatic vegetation. Larvae are typically found in sites with abundant rooted aquatic vegetation, such as rice fields and adjacent irrigation ditches, freshwater marshes and the vegetated margins of lakes, ponds and reservoirs. Investigators have suggested that aquatic vegetation promotes anopheline production because it provides a refuge for larvae from predators, such as Gambusia affinis. Additional hypotheses for the beneficial effects of aquatic vegetation include: enhanced food resources in vegetated regions, shelter from physical disturbance and favorable conditions for oviposition (Orr and Resh 1989).
I would like to digress from An. quadrimaculatus for a moment and first briefly discuss the larval habitats of the other anophelines found in New Jersey. These are An. atropos, Anopheles barberi, Anopheles bradleyi, Anopheles crucians, Anopheles earlei, An. punctipennis and Anopheles walkeri.
An. atropos: Larvae of this species are confined to saline waters for development. Larvae are found in permanent saltwater pools and in salt marshes. Ideal sites contain salty water in marsh pools over clay made firm by dense mats of roots of salt grass (Carpenter and LaCasse, 1955; Horsfall 1972).
An. barberi: This is a treehole mosquito; larvae can also be found in artificial containers and tires.
An. bradleyi: Larval sites for this mosquito have been characterized as pools, margins of ponds and marshes in brackish water where the salt concentration is about 1.5%. Larvae are usually found in stands of salt grass (Distichlis spicata) (Horsfall 1972).
An. crucians: Larvae are found in margins of lakes, ponds, swamps and semipermanent and permanent pools, associated with aquatic vegetation. This mosquito prefers acid water in the larval habitat (Carpenter and LaCasse 1955; Horsfall 1972).
An. earlei: This species develops in cold, clear water in the shallow margins of semipermanent and permanent ponds, associated with emergent and floating vegetation. It is occasionally found in woodland pools, open bogs, marshes and along the margins of sluggish streams (Carpenter and LaCasse 1955; Siverly 1972). This species may be found in association with An. quadrimaculatus.
An. punctipennis: Larvae are found in a wide variety of habitats, including semipermanent and permanent ponds, temporary pools, roadside ditches, bogs, the margins of streams among emergent and overhanging vegetation and artificial container. This species can tolerate pollution to a degree. It is not uncommon to find An. punctipennis in association with An. quadrimaculatus.
An. walkeri: Common larval habitats for this species are freshwater habitats with constant water levels and emergent vegetation, such as cattails. Shade provided by emergent or floating vegetation is an important factor within the larval habitat (Carpenter and LaCasse 1955: Horsfall 1972; Siverly, 1972).
To return to An. quadrimaculatus specifically, "the optimum larval environment is characterized by clear, unpolluted, neutral or slightly alkaline water, containing emergent vegetation which tends to produce or hold floating debris" (Watson and Bishop 1940). This species requires some sunshine and is rarely found in habitats with very dense shade. However, it also requires some darkness and is never found in waters that are totally unshaded, unless there is some type of flotage which casts narrow strips of shade where larvae may gather during daylight hours. (James and Harwood 1969).
An. quadrimaculatus larvae are found in permanent and semi-permanent fresh water in ponds, lakes, canals, marshes, swamps, ditches and stormwater management facilities containing surface-growing or emergent vegetation or floating debris. The last-named can be a very good site for An. quadrimaculatus production and usually in proximity to large numbers of humans. In New Jersey, An. quadrimaculatus larvae are very often associated with duckweed (Lemna minor). Normal detritus passing down a narrow stream that clogs the interstices of a fallen tree or branch and builds a dam creating impounded waters and also serves as an excellent habitat for this species (James and Harwood 1969). According to Headlee (1945), its larvae can also occur in brackish water on the salt marshes.
As noted, An. quadrimaculatus is a clean water-loving mosquito. The current wetlands regulations could be seen as actually impeding our efforts to control this mosquito. By improving water quality within water management project sites per the regulations, we are actually increasing the number of habitats available.
Schmitt (1945) reports that An. quadrimaculatus tends to be very restricted in its larval associations with other species. In New Jersey they have a strong association with Uranotaenia sapphirina and are also found with An. punctipennis and Culex territans quite frequently. Less common are associations with Culex pipiens, Culex restuans and Aedes vexans. Coquillettidia perturbans probably also occurs within some An. quadrimaculatus habitats considering the affinity for emergent vegetation within the larval habitat that both share. In Virginia, An. quadrimaculatus are frequently associated with Culex erraticus larvae (Horsfall 1972)
Since An. quadrimaculatus larvae usually remain just below the surface film with the body horizontal, they are easily collected with a standard dipper utilizing the "shallow skim" dipping technique (O'Malley 1989).
Adult An. quadrimaculatus are not readily attracted to light; therefor light trap collections do not give a true picture of incidence (Hagmann and Feldlaufer 1972; Huffaker 1943). They do, however, show a strong affinity carbon dioxide traps, i.e. CDC traps (Bordash et al. 1972). Since An. quadrimaculatus will feed on man quite readily, bite counts and landing rates can also be used successfully for monitoring adult populations. Headlee (1922) cautions that these collections must not be made in the open; instead, they should be made in and around sheltered sites.
Results from resting box collections give a better indication of An. quadrimaculatus populations levels than do results from light traps (Hagmann and Feldlaufer 1972). Resting boxes offer advantages for capturing adults this species compared to other methods that utilize light, CO2 or animal baits. They require little maintenance to ensure attraction; whereas other methods require sources of electricity or CO2 or the maintenance of animals. Also, most other methods sample the aerial populations, which are predominantly unfed females. Resting boxes provide unbiased samples of adult An. quadrimaculatus with regard to age and sex of the entire populations (Weathersbee and Meisch 1988).
Studies of An. quadrimaculatus with various types of artificial resting places have been made. Resting boxes one foot square were found to be to most attractive. Tests were conducted to ascertain the effect of height above ground, direction of opening, position in a horizontal row and different colors. Results obtained revealed significantly larger counts in boxes within 3 feet the ground, no effect with regard to direction of opening and higher collections in the end boxes in a row of boxes. The following colors were tested: white, yellow, red, green, blue and black. The largest number was collected from red boxes and the next largest collection from the black (Bates 1970).
Identification of larval anophelines can be very difficult. All Anopheles larvae are characterized by the absence of an air tube. The specifics for identifying An. quadrimaculatus are as follows: head hairs 5, 6 and 7 are long and plumose; hair 6 of abdominal segments IV through VI is not plumose; hair 0 on the 4th and 5th abdominal segments is inconspicuous and hair 2 is single or double; the basal tubercles of head hairs 2 and separated by at least the width of a basal tubercle; and hair 1 of the 2nd abdominal is fanlike and well developed (Siverly 1972).
Identification of adult Anopheles is not quite as difficult as larval identification. All Anopheles adults are characterized by an evenly rounded scutellum and palpi about as long as the proboscis. An. quadrimaculatus is a medium-sized species. Wings are entirely dark scaled and 4 mm or more in length. Scutal bristles are short and wings are spotted with patches of dark scales. The tip of the wing is dark without copper-colored fringe scales. The palpi have dark scales and are unbanded, and the wing has 4 distinct dark-scaled spots (Darsie and Ward 1981; Siverly 1972).
Role in Disease Transmission
The importance of An. quadrimaculatus is due primarily to the fact that it is the chief vector of malaria in the eastern, central and southern United States. This mosquito is susceptible to infection with Plasmodium falciparum, Plasmodium vivax and Plasmodium malariae (Carpenter and LaCasse 1955).
In addition to malaria, transmission of St. Louis encephalitis has been obtained with this species in laboratory experiment (Horsfall 1972). Also, An. quadrimaculatus has been found to be an excellent host for Dirofilaria immitis. According to Lewandowski et al. (1980), this is probably one of the most important species involved in the natural transmission of dog heartworm in Michigan. In central New York, this species was also the most efficient host of dog heartworm out of several species tested, both in the laboratory and the wild (Todaro and Morris 1975).
In conclusion, the transmission of malaria by indigenous mosquitoes experienced in New Jersey in 1991 should serve to remind us of the importance of this particular species of mosquito.
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