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Description of $ of Rhadinopsylla media
satisfactory understanding of the taxonomy and ecological relationships of this poorly known taxon. Acknowledgments: We are grateful to F. G. A. M. Smit for continuous assistance in the preparation of this paper; to Edwin F. Cook, University of Minnesota, and Nixon Wilson, University of Northern Iowa for permitting us to examine specimens in their respective collections; and to Nan Kane and Veronica Tyan for preparation of the illustrations. Norman T. Baker, Elmer C. Birney, and Roger D. Price critically reviewed the manuscript. LITERATURE CITED
Hopkins, G. H. E. & M. Rothschild. 1962. An illustrated catalogue of the Rothschild Collection of fleas (Siphonaptera) in the British Museum (Natural History): Hystrichopsyllidae. Cam-
bridge Univ. Press, Cambridge. 3. ix -f 560 p. Smit, F. G. A. M. 1957. New hystrichopsyllid Siphonaptera. Bull. Brit. Mus. (Nat. Hist.), Ent. 6: 41-76. Wilson, N. & W. J. Johnson. 1971. Ectoparasites of Isle Royale, Michigan. Michigan Ent. 4: 109-15.
J. Med. Ent. Vol. 13, no. 4-5: 475-485
31 January 1977
ACARINE PARASITES OF MOSQUITOES IV. Taxonomy, life history and behavior of Thyas barbigera and Thyasides sphagnorum (Hydrachnellae:
Thyasidae)1
By Gary R. Mullen2 Although the larvae of a few terrestrial groups of mites are occasionally found parasitizing adult mosquitoes, the majority of acarine parasites on mosquitoes are water mites. Among these water include females of Aedes abserratus, Ae. canadensis, Ae. cinereus, Ae. mites are a number of species generally recognized excrucians, Ae. fitchii, Ae. punctor, Ae. stimulans, Ae. trichurus and as members of the family Thyasidae. Cook (1974) Ae. vexans, in addition to adult tipulids. Thyasides sphagnorum parasitizes both sexes of Ae. abserratus, Ae. canadensis, Ae. excrucians, has chosen to regard these mites as one of 10 subAe. punctor and Culiseta ??iorsitans. Thyasides sphagnorum typically families of the Hydryphantidae, but as yet this view attaches to adult mosquitoes as they emerge from the pupal has not been widely accepted by other acarologists. stage, in contrast to T. barbigera which normally attaches to Thyasid mites occur chiefly in temporary ponds, ovipositing females. Female mosquitoes carrying T. sphagnorum are nulliparous whereas hosts parasitized by T. barbigera are springs, cold streams, and seepage areas where the bright orange or red nymphs and adults are often typically parous. The life history and behavior of these mites including insemination via spermatophores, oviposition, attachseen crawling about the substrate. Like most water ment sites on host, parasite loads, seasonal incidence of paramites, they are presumed to be parasitic during their sitism, developmental times, longevity, overwintering of nymphs larval stage on the adults of aquatic or semiaquatic and adults, and the feeding behavior of the postlarval stages insects. Based on the limited host data available, are discussed. flies in the families Culicidae, Tipulidae, Ptychop'Taken in part from a thesis presented to the Graduate School teridae, Chloropidae and Empididae appear to of Cornell University in partial fulfillment of requirements for constitute the principal hosts. In addition, a the degree of Doctor of Philosophy in Entomology. "Department of Entomology, Cornell University, Ithaca, New Panisus sp. has been reported parasitizing the York, 14850, U.S.A. Present address: Department of Zoologybraconid wasp Gyrocampa ulignosa (Lundblad 1927). Entomology, Auburn University, Auburn, Alabama 36830, Mites belonging to 4 thyasid genera have been U.S.A. Abstract:
Larvae of Thyas barbigera and Thyasides sphagnorum
commonly parasitize mosquitoes in the northeastern United States. Characters are provided for distinguishing the larvae of these mites from that of Thyas stolli, a closely related species mistakenly reported as a mosquito parasite. Hosts of T. barbigera
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counts for the occurrence of R. media on weasels. The division of R. fraterna into 6 species by Smit was an important first step toward bringing the taxonomy of American Rhadinopsylla into a satisfactory arrangement. Unfortunately, members of this genus are comparatively rare in collections. Individual variation is difficult to evaluate from such limited collections, and it is possible that some of the described species represent subspecies of a single transcontinental species or individual variations within a single species. In the species under consideration, 7 males were previously known from the type-locality of Mingan, Quebec on the east coast of Canada and from Kicking Horse Canyon, British Columbia some 3000 mi. (4800 km) to the west. The specimens discussed herein represent a significant collection intermediate between the 2 previously known sites. Many more such collections are needed if we are to arrive at a
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length of seta b and approximately equal in thickness (FIG. 4). Dorsal plate 60-68 (JL in length. Tarsus III, 105-110(x Thyasides sphagnorum
For descriptions and a key to the adult stage of these mites, see Cook (1959).
Thyas barbigera Viets, 1908 Thyas barbigera is a holarctic species originally described from Europe but now known to occur in New Brunswick, Maine, New Jersey, Maryland,
Insemination via spermatophores
The concentration of adult mites in the moss along the edge of pools in the spring enhances the prospect for successful insemination of females. As is probably the case for all thyasids, insemination is accomplished indirectly via spermatophores. During the 1st week of April 1973, numerous stalked spermatophores were discovered in a rearing cham-
FIG. 1-3. Idiosomae of thyasid larvae, dorsal view. 1, Thyas stolli. 2, Thyas barbigera. 3, Thyasides sphagnorum. dp, dorsal plate; dlh, dorsolateral hysterosomal setae; dmh,.,, dorsomedian hysterosomal setae; s1} anterior sensilla; s8, posterior sensilla.
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recorded as parasites on mosquitoes (see Mullen Michigan and Minnesota (Cook 1959), as well as 1974, 1975a): Thyas, Thyasides3 Euthyas, and Panisop- New York and Indiana (Mullen 1975a). Except sis. This paper deals primarily with Thyas barbigera for the occurrence of nymphs and adults in temporary pools, little information has been previously and Thyasides sphagnorum, the 2 most commonly encountered thyasid parasites of mosquitoes in the reported concerning its biology or hosts. northeastern United States. Shortly after the ice begins to clear from the The following artificial key is provided as an aid water surface in the early spring, T. barbigera nymphs in recognizing the larvae of T. barbigera and T. and adults can be observed crawling slowly over sphagnorum and distinguishing them from that of the leafy debris at the bottom of woodland pools. a 3rd common mite, Thyas stolli, which has been In New York this generally occurs during early to mistakenly reported as a mosquito parasite. mid-March, indicating that T. barbigera overwinters 1. Sensilla on dorsal plate very long, 2 or more times the as both nymphs and adults. Based on samples length of the other dorsal plate setae (FIG. 2) taken on 3 different occasions during early April, Thyas barbigera the sex ratio of overwintered adults is approximately Sensilla on dorsal plate noticeably shorter, less than 2 X the length of the other dorsal plate setae (FIG. 1, 3) 2 equal. Gradually these mites make their way to 2. Genu II with proximodorsal seta a quite hyaline, less the margins of the pools where they exhibit a than 1 /2 length of and more slender than seta b just predilection for submerged moss growing in the distal to it (FIG. 5). Dorsal plate 67-84 y. in length. shallow water or on the base of trees, rocks or other Tarsus III, 120-130 (x Thyas stolli Genu II with proximodorsal seta a 2/3 or more the objects covered by the high, spring water level.
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477
Oviposition and the egg stage
Oviposition commences in the field as early as mid-April, although adult females collected during late March will begin depositing eggs within a couple of days if maintained at room temperature. Adult T. barbigera females collected in mid-April failed to deposit eggs when kept below 13°C. At 13-15 °C oviposition commenced within a 2- to 3-week period, in contrast to only a few days at room temperatures. This suggests that temperature alone plays a significant role in egg maturation and in inducing oviposition. A threshold temperature of 13-15 °C is consistent with the water temperature of vernal pools in mid to late April in the northeastern U.S.
FIG. 4-5. Thyasid larvae, genu III. 4, Thyasides sphagnorum. 5, Thyas stolli. a, nude proximodorsal seta; b, branched dorsal seta.
egg masses to submerged vegetation, T. barbigera tends to release them in loose aggregations. Under laboratory conditions the eggs were usually scattered freely on the bottom of the holding containers with only a few adhering to the vegetation. This may account for the difficulty in locating T. barbigera eggs in the field. Freshly deposited T. barbigera eggs are generally orange, 170-200 y. in diameter, and individually surrounded by a translucent, cloudy layer which is often quite irregular in thickness (80-120 (x). In contrast, T. stolli eggs are slightly larger, bright Unlike Thyas stolli which typically deposits its red, and are provided with a thicker, more uniform eggs in small clusters of 3 to 12 eggs each, seldom totalling more than 3 dozen per female, T. barbigera mucilaginous coat. This protective coating is probably important in preventing desiccation when commonly produces up to 45 or more eggs, often the water level drops below that at which the eggs deposited at one time. Oviposition takes place were originally deposited. As a result, eggs stranded in the moss along the shallow pool margins or in up to 12 or more cm above the water line in midmoss growing on the submerged surfaces of tree June still developed normally and produced larvae. trunks, logs, or other objects. Whereas T. stolli The period from oviposition to hatching was 30-40 and Thyasides sphagnorum carefully secure their
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ber containing several T. barbigera adults collected in the field 4 days earlier. These spermatophores, measuring approximately 400 [i from their point of attachment to the tip, were readily discernible under the low power of a dissecting microscope when viewed against a dark background. Borne at the tip of the thread-like stalk, the head was displaced to one side and consisted of an elongate capsular structure containing a yellowish globule of sperm (FIG. 6). Although deposition by the male was not witnessed, a single female was observed picking up several of these spermatophores. Upon encountering one, she raised herself and carefully positioned her genital field over the spermatophore capsule. With her genital valves open she then lowered herself onto the spermatophore until almost reaching the substrate; she then elevated herself again, slowly drawing the stalk to its full length. Hesitating several seconds, she then released the spermatophore and promptly moved forward, leaving behind the empty, ruptured capsule still situated atop the stalk. Upon encountering another nearby spermatophore the procedure was repeated, each time requiring only about 10 seconds to complete the process. The deposition of spermatophores by Hydryphantes ruber, another primitive water mite, has been described in detail by Mitchell (1958), although females were not observed picking up the spermatophores.
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days at 13-15°C, compared with 13-20 days for eggs maintained at room temperature. Larval stage
FIG. 6. Thyas barbigera spermatophores. a and b, intact capsules; c, crushed capsule with sperm packet removed.
body, pressing them against the water surface as the first 2 pairs of legs are drawn close to the body; then by some unexplained release mechanism the larval mite is snapped or catapulted upward and laterally for some distance. Motas (1929) briefly discussed various larval jumping mechanisms employed by Euthyas, Thyas and Calonyx species. He questioned Lundblad's (1926) description of T. barbigera utilizing its 2 anterior pairs of legs in jumping. It is generally believed that this ability to jump facilitates attachment to a host, although the manner in which this is accomplished has not been observed. Miinchberg (1937) noted that in certain cases thyasid larvae can actually grasp an insect in flight. The earliest date on which T. barbigera larvae were found in thefieldwas 5 June. Appreciable numbers of T. barbigera larvae seldom occurred until midJune. Free-living larvae were not found after the 3rd week of August. In the laboratory, unengorged T. barbigera larvae commonly lived 3 to 4 weeks after hatching from eggs; longest survival was 6-1/2 weeks. Host species
Thyas barbigera larvae are primarily parasites on Aedes mosquitoes. The following 9 species were found to be hosts in New York: Aedes abserratus, Ae. canadensis, Ae. cinereus, Ae. excrucians, Ae. jitchii, Ae. punctor, Ae. stimulans, Ae. trichurus, and Ae. vexans.
All of these species typically breed in temporary water, particularly vernal pools, the same habitat in which T. barbigera occurs. This mite was not found on any other mosquito genus. Larvae of T. barbigera were also found attached to crane fly adults (Tipulidae) in 3 study areas in Tompkins County, New York. Those records are
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Emerging from the egg, the larva makes its way to the water surface by crawling upward on the moss or some other object. This distance is seldom great. Generally the larvae first penetrate the water surface with their palps and then, aided by some object breaking the interface, pull their legs through 1 at a time. This effort is assisted in part by the numerous long hydrophobic setae on the legs and body which, when drawn against one another, serve to repel the water and thus break the surface tension. Some larvae successfully penetrate the surface anterior end first whereas others free their legs on one side and then the other. The sequence of legs penetrating the surface film appears to be random. The larva may also seize an object with its palps and proceed to push its hind legs through the surface film, gaining the upper surface backwards. Other larvae upon reaching the surface walk about with ease on the underside of the surface film. Even in the absence of an object to which they can cling, larvae can successfully pierce the water film with their palps and pull themselves through. However, they risk the chance of losing their hold and sinking to the bottom where they must once again seek a way back to the surface. On several occasions, larvae in the laboratory were observed ascending to the surface clinging to air bubbles which they had dislodged from submerged vegetation. This manner of reaching the surface is probably accidental. Once on the water surface, the larval mite proceeds to groom itself. The legs are drawn forward, 1 at a time, and the tarsal segments are repeatedly stroked by the palps. This tarsal grooming appears to be necessary before the mite can walk about the surface freely. Such grooming may, in fact, be the primary function of the highly modified setae and other palpal structures characteristic of thyasid larvae. It is also possible that a hydrophobic chemical originating from oral glands is applied to the tarsi at this time; however, the existence of such glands has not been demonstrated. Like other thyasid mites, T. barbigera larvae walk on the water surface with considerable ease. Concentrated along the margin of the pools they clamber about the wet moss and leaf litter, seldom venturing very far out on open water. They are quite capable of jumping, especially if disturbed. This is accomplished as the mite curls its hind legs beneath the
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as follows: Michigan Hollow, 16 June 1971; McLean Bog, 17 June 1971; Ringwood Preserve, 24 July 1972. The host species were not determined. Since no effort was being made to sample tipulid adults, there is no way of knowing how commonly T. barbigera utilizes these insects as hosts. Judging, however, by their occurrence on tipulids collected only incidentally in sweep nets, it is possible that crane flies represent another significant host group for T. barbigera.
SPECIES A. Obserrotus
A. cinereus
Larval attachment to host
Considerable difference of opinion has been expressed with regard to the circumstances under which thyasid larvae normally attach to their hosts. According to Jalil & Mitchell (1972), the larval mites "are attracted by, and will rest on, the breathing tubes of the mosquito pupae. At ecdysis of the host they climb onto the body of the emerging adult mosquito or they may attack adult hosts resting on the water." The same authors
AUGUST
1
C • 1
1 1
cz ZZ3
A. excrucians A,
fitchii
[
A.
punctor
C
A.
stimulans
A.
trichurus
SEPT.
3 r-' i
1
1
1 [
i
FIG. 7. Seasonal occurrence of Thyas barbigera larvae on adult Aedes mosquitoes, Tompkins County, New York, 1971-1972.
further noted that "post-ecdysis attachments" are probably uncommon. Corbet (1963), on the other hand, observed that thyasid mites occurred about as frequently on pars as on nullipars (i.e., females which have oviposited versus those that have not), suggesting that the mites are able to infest female mosquitoes at both emergence and oviposition. The attachment of larval water mites to an ovipositing dipteran host has been previously reported only for a Piona sp. parasitic on Cricotopus, a chironomid midge (Leger & Motas 1928). My study of Thyas barbigera in New York clearly demonstrates that in this species larval attachment to the host does not normally occur when the mosquito emerges as an adult but rather when the females subsequently return to the water to oviposit. The following observations support this contention: (1) Although T. barbigera females in New York may begin depositing eggs in late April and early May, the eggs do not begin hatching until the end of May or early June. Aedes mosquitoes breeding in the same pools start to emerge as adults about mid-May, with the last species completing its emergence by the end of the 1st week in June. At this time very few T. barbigera larvae are present, with the vast majority of mite eggs still unhatched (FIG. 8). (2) Thyas barbigera larvae do not attach to mosquito pupae to await the emergence of the adults. Examination of nearly 15,000 Aedes pupae collected from vernal pools in which T. barbigera abounded yielded no mite larvae. In laboratory experiments in which T. barbigera larvae were placed on the water surface of vials containing Aedes pupae, the mite larvae showed no discernible interest in the potential hosts. Occasionally a few mites aggregated about the respiratory trumpets where they broke the surface film, but this was interpreted as
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FIG. 7 summarizes the seasonal incidence of T. barbigera larvae on Aedes mosquitoes based on collections in Tompkins County, New York, during 1971 1972. The first parasitized hosts appeared during the last week of May and the first part of June. Unlike the other host species which emerge as adults during the late spring, Ae. vexans tends to develop later in the season as temporary pools are filled by rain and flood waters. Thus, parasitized Ae. vexans adults were not encountered until the end of June and were present intermittently until late August. T. barbigera mites were found on Ae. trichurus only during a 2- to 3-week period in June. Ae. excrucians was similarly parasitized for a relatively short time from mid-June to mid-July. The remaining host species were collected with T. barbigera larvae well into August and as late as the 1st week of September in the case of Ae. stimulans. The incidence of parasitism was difficult to assess quantitatively due to the low percentage of parasitized hosts for any given mosquito species and the difficulty in monitoring these populations continuously throughout the summer months. The incidence in most collections was less than 1.0% and seldom exceeded 5.0% to 8.0% in any given sample. The highest percentages of parasitism (up to 31%) occurred in samples collected along the edges of woodland pools where recently oviposited females were particularly abundant. It is thus impractical to speak in terms of "peaks of parasitism."
JULY
JUNE
A. conadensis
A. vexans
Seasonal incidence of parasitism
MAY
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J. Med. Ent.
in this study: Ae. canadensis, Ae. excrucians, and Ae.
punctor. If the mites normally attached to their hosts as the adults emerged from the water, one would expect to find both males and females equally parasitized. If not, some means of sex discrimination on the part of the mite larvae would have to be involved. This has not been exhibited by any other water mites which have been investigated. (5) The fact that T. barbigera larvae are found almost exclusively on Aedes females suggests that the behavior of the female mosquito plays a major role in host location by the mite. The most likely
opportunity for contacting female mosquitoes is when they return to the pools to oviposit. (6) Generally T. barbigera larvae occur in wet moss and litter along the margins of temporary pools, the same zone wherein Aedes females deposit their eggs. (7) Dissections of 306 Aedes females parasitized by T. barbigera revealed that, with the exception of 3 individuals, all hosts were parous (TABLE l). Even early in the season when more than 90% of the females in the host populations were still nulliparous, the few hosts parasitized by T. barbigera were all parous. (8) In several cases in which Aedes females bearing completely unengorged T. barbigera larvae were collected along the edge of woodland pools, dissections showed that oviposition of the host had very recently taken place, as evidenced by the retention of 1 or more eggs in the oviducts. (9) Aedes females oviposit up to 5 or more times during their lifetime which may extend into early fall. These successive ovipositions are not synchronized within a population, since several independent variables (e.g., success in finding a mate, obtaining a blood meal, and locating a suitable oviposition site) are operative. Thus if T. barbigera larvae attach and detach when the hosts oviposit, the continuous occurrence of parasitized mosquitoes throughout the season without well-defined peaks is easily explained. Larval attachment sites and parasite load
The most common attachment site for T. barbigera, irrespective of the host species, is on the posterior aspect of the thorax just above the hind coxae, where 72.3% of the mites in this study were found. These
Thyas barbigera FIG. 8. Oviposition and egg hatch of Thyas barbigera in
15 MAY
I I JUNE
relation to adult emergence of 6 potential Aides hosts, Ringwood Wildlife Preserve, Tompkins County, New York, 1971. Amplitudes of the individual emergence peaks represent the relative abundance of each Aedes sp. at this study site based on emergence-trap collections.
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simply a convenient resting site encountered by chance. The mites responded similarly to other objects breaking the surface. The larvae in no way attempted to cling to the respiratory organs and were easily dislodged when the mosquito pupae moved. Indeed, it would be impractical for an aerial larva on the water surface to attach to the submerged stage of its host. (3) Since most of the Aedes hosts are univoltine with their emergence as adults in late spring, a pronounced peak in the incidence of parasitism should occur at this time if the mite larvae are attaching at this point in the mosquito life cycle. The level of parasitism should then decline progressively as the larval mites detach. This is not the case. Using emergence traps, over 7000 Aedes adults were collected from pools containing wellestablished populations of T. barbigera during the spring of 1972 and not a single specimen was parasitized. Not only is there no peak of parasitism coinciding with the host emergence, but T. barbigera larvae can be found on their univoltine Aedes hosts throughout the summer months. (4) Only 3 Aedes males were found parasitized
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1977
TABLE 1. Parity data for Aedes °.°. parasitized by Thyas barbigera larvae based on examination of the ovarian tracheal system, Tompkins County, New York, 1972-1973. 1972 No. dissections
HOST SPECIES Ae. Ae. Ae. Ae. Ae. Ae.
% parous 100.0 77.7 100.0 97.1 100.0 100.0 96.0
24 9 2 34 3 2 74
abserratus-punctor canadensis cinereus stimulans group trichurus vexans
All hosts
— 201 5 2 232
—
100.0 100.0 100.0 100.0
long setae on the legs and body. Measuring 200240 [i in length at the time of attachment to a host, the larval mites swell to several times that length while feeding. Engorged larvae, greatly distended and globose, are usually bright orange to red and are thus quite conspicuous on parasitized mosquitoes. Complete engorgement requires 5 to 8 days. If detached from the host when less than 500 JL in length, partially engorged larvae seldom complete their development to the nymphal stage. Fully engorged larvae whose parasitic feeding had not been interrupted reached 780 y. in length (X = 629, SE = 19.4, n = 16). Unlike Arrenurus mites parasitizing mosquitoes, thyasid larvae do not produce stylostomes (feeding tubes) and may or may not leave a discernible scar at the site of attachment (see Corbet 1963). Larval detachment from female hosts normally occurs when the mosquito oviposits. Postlarval stages
Once detached from the host, the engorged larvae, their mobility severely limited, crawl into protected recesses such as the leaf axils of moss, among rootlets, or between the moist layers of leaf litter or other soil debris. Without attaching to the substrate the engorged larvae become quiescent as a prelude to nymphal development. The subsequent nymphochrysalid stage, which is normally passed amidst Engorgement and detachment from mosquito host Unengorged T. barbigera larvae are orange, the moss and litter, can also be completed while sometimes straw-colored, with 2 pairs of dark eye floating on the water surface, although this is probably an uncommon situation. Nymphs emerge spots and a bristly appearance due to the numerous TABLE 2. Attachment sites of Thyas barbigera larvae on adult Aedes mosquitoes based on collections in Tompkins County, New York, 1972. HOST Ae. Ae. Ae. Ae. Ae. Ae. Ae. Ae.
abserratus-punctor canadensis cinereus excrucians fitchii stimulans trichurus vexans
All hosts
TOTAL NO. OF MITES
115 33 11 36 37 196
Cervix 12.2 3.0
20.0 8.6 5.9 8.7
56
11.5
6 490
— 9.3
Lateral thorax 15.7 27.3 10.0 28.6 23.6 16.4 15.4 16.6 18.3
Posterior thorax 72.1 69.7 70.0 62.8 70.5 74.3 73.1 83.4 72.3
Abdomen
0.6 — — 0.002
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mites also attach to the cervical region and the lateral aspect of the thorax but are rarely found on the host abdomen (TABLE 2). The number of T. barbigera larvae per host can be quite variable and in the Tompkins County collections did not exceed 14. Usually there were not more than 4 mites per specimen (TABLE 3). Occasionally heavier infestations were encountered, as in the case of an Ae. vexans female collected in Essex County, Vermont (27 June 1972) which had 20 T. barbigera larvae attached. Even within a very localized geographic area, the parasite load may differ greatly from one collection site to another. In contrast, the parasite load for mosquitoes bearing Arrenurus mites is much greater, with up to 30 or more mites per host being common. This can be explained by the difference in the mode of attachment to the host. Since Arrenurus larvae typically search out the pupal stage of the mosquito, a given pupa is exposed for 2 or more days to hostseeking mites. However, in the case of Thyas barbigera which attaches to ovipositing females, an Aedes adult is vulnerable to attack for only a matter of minutes at any one time. The chances for a large number of mites to locate a single potential host are thus substantially reduced.
1973 No. dissections % parous 2 100.0 21 100.0
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TABLE 3. Number of Thyas barbigera larvae per Aedes host based on collections in Tompkins County, New York, 1972.
HOST Ae. Ae. Ae. Ae. Ae. Ae. Ae. Ae.
abserratus-punctor canadensis cinereus excrucians fitchii stimulans trichurus vexans
All hosts
N O . PARASITIZED HOSTS EXAMINED
42
22 12 13 23 98 21 6 237
No. OF MITES/HOST
Mean
Maximum
2.7 1.8 1.6 3.0 1.8 2.1 2.7 1.5 1.7
14 8 5 12 4 10 9
2 14
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form of irregular-shaped integumental plates on various parts of the body. Adults which were of the 1st type at the time they were collected assumed the appearance of the 2nd type after being maintained for a year or longer in the laboratory. This suggests that the 2 types of adults described above represent young and old individuals and that adults of the 2nd type are in their 2nd year. Longevity
9 to 16 days after detachment of the engorged larvae from the host. Since they usually do not have access to open water upon their emergence, the nymphs are limited to crawling around within a small radius of the point at which they detached from the host. This mobility is further curtailed as the season progresses and the substrate becomes increasingly drier, forcing the nymphs to burrow deeper to avoid desiccation. Laboratory observations indicate that such nymphs may remain relatively dormant for months at a time, but become active within minutes when the substrate is flooded with water. Although limited feeding may occur, nymphs probably remain in Feeding behavior of nymphs and adults this inactive state throughout the rest of the summer A major drawback to developmental studies of and fall months. With the onset of winter they thyasid mites has been a lack of knowledge conburrow deep enough to survive the freezing surface cerning the feeding habits of the postlarval stages. temperatures. Recent evidence however has shown that both Although nymphs developing from larvae during nymphs and adults of Thyas barbigera and T. stolli the early summer may reach the adult stage before readily prey on mosquito eggs, suggesting that this overwintering, no evidence could be obtained to may represent the principal food source for these confirm this. No T. barbigera teleiochrysalids were mites (Mullen 1975b). Since engorged T. barbigera found under natural conditions. However, a nymph larvae detach from their female hosts when they collected during May entered the teleiochrysalid oviposit and the mobility of the ensuing nymphs is stage during the last week of July and the adult so restricted, the eggs of the host species provide emerged about 10 days later. No other nymphs, an abundant and readily accessible source of either field-collected or reared from larvae, comnutrients. pleted their development to adults in the laboratory, Other aquatic organisms including oligochaetes, despite their surviving up to a year or more as ostracods, planarians, mayfly nymphs, chironomid nymphs. Lack of an available food source may larvae and the immature stages of other aquatic account for this failure to develop further. Diptera and Coleoptera were not preyed upon by Two types of adult Thyas barbigera females were either T. barbigera or T. stolli. distinguished based on their external appearance. Laboratory observations of T. stolli suggest that One was smaller than the other, less than 850 (x, the eggs and quiescent stages of water mites may with a smoother integument and a lighter, more also serve as a potential food source for thyasid uniform coloration, more closely resembling nymphs. mites. On 1 occasion a T. stolli adult was observed The 2nd type was greater than 850 jx in length with to pierce with its chelicerae the outer integument a more wrinkled integument and was darker orange, of a Fiona teleiochrysalis. However, no apparent often red in color. The latter was also commonly harm was incurred since the Fiona continued its characterized by secondary sclerotization in the development to produce a normal adult. In
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Under laboratory conditions both adult males and females collected in the spring survived up to 15 months without any apparent source of food. Throughout this period they were kept in small glass vials containing only water, a disc of filter paper, and a sprig of moss. Nymphs reared from fully engorged larvae survived up to 12-1/2 months utilizing only stored reserves obtained during the parasitic larval state. This prolonged longevity of the postlarval stages may characterize many other thyasid species, since Thyas stolli and Thyasides sphagnorum were also found to live for comparable periods. One T. sphagnorum male survived 11 months after being collected as an adult, while T. stolli adults lived up to 16 months. The 1st winter is probably passed as a nymph and the 2nd as an adult.
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another instance, a T. stolli female was observed probing with her palps a cluster of 8 recently deposited eggs of her own species. Crawling slowly over the surface of the eggs, she would stop and press her chelicerae against the thick coating surrounding one of the eggs, causing it to depress and then spring back again as she released the pressure. In 1 case, however, she actually pierced the coating and remained quite motionless for a minute or more with her mouthparts inserted. No dissolution of the egg itself could be detected. The mite then withdrew her chelicerae leaving a hole 70 by 20 (x. All of the eggs developed normally and hatched. This observation adds credence to the belief that the thick coating about thyasid eggs serves as protection against predators as well as desiccation.
tion vial. Measuring 180-190 fjt. in diameter, the bright red, spherical eggs were individually coated with a white mucoid material. In contrast to T. barbigera and T. stolli eggs, however, this coating was comparatively thin, measuring less than 40 \L. Hatching was completed in 7 to 8 days with 98% egg viability. The resultant larvae in some vials were able to successfully make their way to the surface, while in others they remained at the bottom. Few in either situation survived more than 2 weeks, with the majority dying in 7 to 10 days in the absence of a host. Adult mosquitoes parasitized by T. sphagnorum larvae were collected at the following 3 study sites in Tompkins County, New York: McLean Wildlife Reservation, Town of Groton; Ringwood Wildlife Preserve, Town of Dryden; Michigan Hollow, Town of Danby. Hosts at these sites included Ae. abserratus, Ae. canadensis, Ae. excrucians, Ae. punctor, and Culiseta morsitans. A Cs. morsitans female para-
sitized by T. sphagnorum was also collected near Syracuse, New York. In contrast to Thyas barbigera Thyasides sphagnorum Habeeb, 1958 which is found almost exclusively on female hosts, Thyasides sphagnorum, the only member of this genus T. sphagnorum was found to occur on either sex of reported from North America, was described from the host species, as evidenced by parasitized males adults collected in a sphagnum bog in New Brunsof Ae. excrucians, Ae. punctor and Cs. morsitans in New wick, Canada (Habeeb 1958). It has since been York. recorded from temporary waters, especially those With the exception of a single Cs. morsitans female associated with bogs, in Michigan (Cook 1959) and taken on 1 August, all of the hosts parasitized by more recently from New York (Mullen 1975a). T. sphagnorum were collected between 24 May and Virtually nothing has been reported concerning 27 June despite continued sampling at the same the biology or hosts of this mite. sites throughout the summer months. Even when On 11 May 1971, 11 T. sphagnorum adults (6 $$, the mites were found, the incidence of parasitism 5 $$) were collected from submerged sphagnum was very low (
Benton & Timm:
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Description of $ of Rhadinopsylla media
satisfactory understanding of the taxonomy and ecological relationships of this poorly known taxon. Acknowledgments: We are grateful to F. G. A. M. Smit for continuous assistance in the preparation of this paper; to Edwin F. Cook, University of Minnesota, and Nixon Wilson, University of Northern Iowa for permitting us to examine specimens in their respective collections; and to Nan Kane and Veronica Tyan for preparation of the illustrations. Norman T. Baker, Elmer C. Birney, and Roger D. Price critically reviewed the manuscript. LITERATURE CITED
Hopkins, G. H. E. & M. Rothschild. 1962. An illustrated catalogue of the Rothschild Collection of fleas (Siphonaptera) in the British Museum (Natural History): Hystrichopsyllidae. Cam-
bridge Univ. Press, Cambridge. 3. ix -f 560 p. Smit, F. G. A. M. 1957. New hystrichopsyllid Siphonaptera. Bull. Brit. Mus. (Nat. Hist.), Ent. 6: 41-76. Wilson, N. & W. J. Johnson. 1971. Ectoparasites of Isle Royale, Michigan. Michigan Ent. 4: 109-15.
J. Med. Ent. Vol. 13, no. 4-5: 475-485
31 January 1977
ACARINE PARASITES OF MOSQUITOES IV. Taxonomy, life history and behavior of Thyas barbigera and Thyasides sphagnorum (Hydrachnellae:
Thyasidae)1
By Gary R. Mullen2 Although the larvae of a few terrestrial groups of mites are occasionally found parasitizing adult mosquitoes, the majority of acarine parasites on mosquitoes are water mites. Among these water include females of Aedes abserratus, Ae. canadensis, Ae. cinereus, Ae. mites are a number of species generally recognized excrucians, Ae. fitchii, Ae. punctor, Ae. stimulans, Ae. trichurus and as members of the family Thyasidae. Cook (1974) Ae. vexans, in addition to adult tipulids. Thyasides sphagnorum parasitizes both sexes of Ae. abserratus, Ae. canadensis, Ae. excrucians, has chosen to regard these mites as one of 10 subAe. punctor and Culiseta ??iorsitans. Thyasides sphagnorum typically families of the Hydryphantidae, but as yet this view attaches to adult mosquitoes as they emerge from the pupal has not been widely accepted by other acarologists. stage, in contrast to T. barbigera which normally attaches to Thyasid mites occur chiefly in temporary ponds, ovipositing females. Female mosquitoes carrying T. sphagnorum are nulliparous whereas hosts parasitized by T. barbigera are springs, cold streams, and seepage areas where the bright orange or red nymphs and adults are often typically parous. The life history and behavior of these mites including insemination via spermatophores, oviposition, attachseen crawling about the substrate. Like most water ment sites on host, parasite loads, seasonal incidence of paramites, they are presumed to be parasitic during their sitism, developmental times, longevity, overwintering of nymphs larval stage on the adults of aquatic or semiaquatic and adults, and the feeding behavior of the postlarval stages insects. Based on the limited host data available, are discussed. flies in the families Culicidae, Tipulidae, Ptychop'Taken in part from a thesis presented to the Graduate School teridae, Chloropidae and Empididae appear to of Cornell University in partial fulfillment of requirements for constitute the principal hosts. In addition, a the degree of Doctor of Philosophy in Entomology. "Department of Entomology, Cornell University, Ithaca, New Panisus sp. has been reported parasitizing the York, 14850, U.S.A. Present address: Department of Zoologybraconid wasp Gyrocampa ulignosa (Lundblad 1927). Entomology, Auburn University, Auburn, Alabama 36830, Mites belonging to 4 thyasid genera have been U.S.A. Abstract:
Larvae of Thyas barbigera and Thyasides sphagnorum
commonly parasitize mosquitoes in the northeastern United States. Characters are provided for distinguishing the larvae of these mites from that of Thyas stolli, a closely related species mistakenly reported as a mosquito parasite. Hosts of T. barbigera
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counts for the occurrence of R. media on weasels. The division of R. fraterna into 6 species by Smit was an important first step toward bringing the taxonomy of American Rhadinopsylla into a satisfactory arrangement. Unfortunately, members of this genus are comparatively rare in collections. Individual variation is difficult to evaluate from such limited collections, and it is possible that some of the described species represent subspecies of a single transcontinental species or individual variations within a single species. In the species under consideration, 7 males were previously known from the type-locality of Mingan, Quebec on the east coast of Canada and from Kicking Horse Canyon, British Columbia some 3000 mi. (4800 km) to the west. The specimens discussed herein represent a significant collection intermediate between the 2 previously known sites. Many more such collections are needed if we are to arrive at a
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length of seta b and approximately equal in thickness (FIG. 4). Dorsal plate 60-68 (JL in length. Tarsus III, 105-110(x Thyasides sphagnorum
For descriptions and a key to the adult stage of these mites, see Cook (1959).
Thyas barbigera Viets, 1908 Thyas barbigera is a holarctic species originally described from Europe but now known to occur in New Brunswick, Maine, New Jersey, Maryland,
Insemination via spermatophores
The concentration of adult mites in the moss along the edge of pools in the spring enhances the prospect for successful insemination of females. As is probably the case for all thyasids, insemination is accomplished indirectly via spermatophores. During the 1st week of April 1973, numerous stalked spermatophores were discovered in a rearing cham-
FIG. 1-3. Idiosomae of thyasid larvae, dorsal view. 1, Thyas stolli. 2, Thyas barbigera. 3, Thyasides sphagnorum. dp, dorsal plate; dlh, dorsolateral hysterosomal setae; dmh,.,, dorsomedian hysterosomal setae; s1} anterior sensilla; s8, posterior sensilla.
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recorded as parasites on mosquitoes (see Mullen Michigan and Minnesota (Cook 1959), as well as 1974, 1975a): Thyas, Thyasides3 Euthyas, and Panisop- New York and Indiana (Mullen 1975a). Except sis. This paper deals primarily with Thyas barbigera for the occurrence of nymphs and adults in temporary pools, little information has been previously and Thyasides sphagnorum, the 2 most commonly encountered thyasid parasites of mosquitoes in the reported concerning its biology or hosts. northeastern United States. Shortly after the ice begins to clear from the The following artificial key is provided as an aid water surface in the early spring, T. barbigera nymphs in recognizing the larvae of T. barbigera and T. and adults can be observed crawling slowly over sphagnorum and distinguishing them from that of the leafy debris at the bottom of woodland pools. a 3rd common mite, Thyas stolli, which has been In New York this generally occurs during early to mistakenly reported as a mosquito parasite. mid-March, indicating that T. barbigera overwinters 1. Sensilla on dorsal plate very long, 2 or more times the as both nymphs and adults. Based on samples length of the other dorsal plate setae (FIG. 2) taken on 3 different occasions during early April, Thyas barbigera the sex ratio of overwintered adults is approximately Sensilla on dorsal plate noticeably shorter, less than 2 X the length of the other dorsal plate setae (FIG. 1, 3) 2 equal. Gradually these mites make their way to 2. Genu II with proximodorsal seta a quite hyaline, less the margins of the pools where they exhibit a than 1 /2 length of and more slender than seta b just predilection for submerged moss growing in the distal to it (FIG. 5). Dorsal plate 67-84 y. in length. shallow water or on the base of trees, rocks or other Tarsus III, 120-130 (x Thyas stolli Genu II with proximodorsal seta a 2/3 or more the objects covered by the high, spring water level.
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477
Oviposition and the egg stage
Oviposition commences in the field as early as mid-April, although adult females collected during late March will begin depositing eggs within a couple of days if maintained at room temperature. Adult T. barbigera females collected in mid-April failed to deposit eggs when kept below 13°C. At 13-15 °C oviposition commenced within a 2- to 3-week period, in contrast to only a few days at room temperatures. This suggests that temperature alone plays a significant role in egg maturation and in inducing oviposition. A threshold temperature of 13-15 °C is consistent with the water temperature of vernal pools in mid to late April in the northeastern U.S.
FIG. 4-5. Thyasid larvae, genu III. 4, Thyasides sphagnorum. 5, Thyas stolli. a, nude proximodorsal seta; b, branched dorsal seta.
egg masses to submerged vegetation, T. barbigera tends to release them in loose aggregations. Under laboratory conditions the eggs were usually scattered freely on the bottom of the holding containers with only a few adhering to the vegetation. This may account for the difficulty in locating T. barbigera eggs in the field. Freshly deposited T. barbigera eggs are generally orange, 170-200 y. in diameter, and individually surrounded by a translucent, cloudy layer which is often quite irregular in thickness (80-120 (x). In contrast, T. stolli eggs are slightly larger, bright Unlike Thyas stolli which typically deposits its red, and are provided with a thicker, more uniform eggs in small clusters of 3 to 12 eggs each, seldom totalling more than 3 dozen per female, T. barbigera mucilaginous coat. This protective coating is probably important in preventing desiccation when commonly produces up to 45 or more eggs, often the water level drops below that at which the eggs deposited at one time. Oviposition takes place were originally deposited. As a result, eggs stranded in the moss along the shallow pool margins or in up to 12 or more cm above the water line in midmoss growing on the submerged surfaces of tree June still developed normally and produced larvae. trunks, logs, or other objects. Whereas T. stolli The period from oviposition to hatching was 30-40 and Thyasides sphagnorum carefully secure their
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ber containing several T. barbigera adults collected in the field 4 days earlier. These spermatophores, measuring approximately 400 [i from their point of attachment to the tip, were readily discernible under the low power of a dissecting microscope when viewed against a dark background. Borne at the tip of the thread-like stalk, the head was displaced to one side and consisted of an elongate capsular structure containing a yellowish globule of sperm (FIG. 6). Although deposition by the male was not witnessed, a single female was observed picking up several of these spermatophores. Upon encountering one, she raised herself and carefully positioned her genital field over the spermatophore capsule. With her genital valves open she then lowered herself onto the spermatophore until almost reaching the substrate; she then elevated herself again, slowly drawing the stalk to its full length. Hesitating several seconds, she then released the spermatophore and promptly moved forward, leaving behind the empty, ruptured capsule still situated atop the stalk. Upon encountering another nearby spermatophore the procedure was repeated, each time requiring only about 10 seconds to complete the process. The deposition of spermatophores by Hydryphantes ruber, another primitive water mite, has been described in detail by Mitchell (1958), although females were not observed picking up the spermatophores.
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days at 13-15°C, compared with 13-20 days for eggs maintained at room temperature. Larval stage
FIG. 6. Thyas barbigera spermatophores. a and b, intact capsules; c, crushed capsule with sperm packet removed.
body, pressing them against the water surface as the first 2 pairs of legs are drawn close to the body; then by some unexplained release mechanism the larval mite is snapped or catapulted upward and laterally for some distance. Motas (1929) briefly discussed various larval jumping mechanisms employed by Euthyas, Thyas and Calonyx species. He questioned Lundblad's (1926) description of T. barbigera utilizing its 2 anterior pairs of legs in jumping. It is generally believed that this ability to jump facilitates attachment to a host, although the manner in which this is accomplished has not been observed. Miinchberg (1937) noted that in certain cases thyasid larvae can actually grasp an insect in flight. The earliest date on which T. barbigera larvae were found in thefieldwas 5 June. Appreciable numbers of T. barbigera larvae seldom occurred until midJune. Free-living larvae were not found after the 3rd week of August. In the laboratory, unengorged T. barbigera larvae commonly lived 3 to 4 weeks after hatching from eggs; longest survival was 6-1/2 weeks. Host species
Thyas barbigera larvae are primarily parasites on Aedes mosquitoes. The following 9 species were found to be hosts in New York: Aedes abserratus, Ae. canadensis, Ae. cinereus, Ae. excrucians, Ae. jitchii, Ae. punctor, Ae. stimulans, Ae. trichurus, and Ae. vexans.
All of these species typically breed in temporary water, particularly vernal pools, the same habitat in which T. barbigera occurs. This mite was not found on any other mosquito genus. Larvae of T. barbigera were also found attached to crane fly adults (Tipulidae) in 3 study areas in Tompkins County, New York. Those records are
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Emerging from the egg, the larva makes its way to the water surface by crawling upward on the moss or some other object. This distance is seldom great. Generally the larvae first penetrate the water surface with their palps and then, aided by some object breaking the interface, pull their legs through 1 at a time. This effort is assisted in part by the numerous long hydrophobic setae on the legs and body which, when drawn against one another, serve to repel the water and thus break the surface tension. Some larvae successfully penetrate the surface anterior end first whereas others free their legs on one side and then the other. The sequence of legs penetrating the surface film appears to be random. The larva may also seize an object with its palps and proceed to push its hind legs through the surface film, gaining the upper surface backwards. Other larvae upon reaching the surface walk about with ease on the underside of the surface film. Even in the absence of an object to which they can cling, larvae can successfully pierce the water film with their palps and pull themselves through. However, they risk the chance of losing their hold and sinking to the bottom where they must once again seek a way back to the surface. On several occasions, larvae in the laboratory were observed ascending to the surface clinging to air bubbles which they had dislodged from submerged vegetation. This manner of reaching the surface is probably accidental. Once on the water surface, the larval mite proceeds to groom itself. The legs are drawn forward, 1 at a time, and the tarsal segments are repeatedly stroked by the palps. This tarsal grooming appears to be necessary before the mite can walk about the surface freely. Such grooming may, in fact, be the primary function of the highly modified setae and other palpal structures characteristic of thyasid larvae. It is also possible that a hydrophobic chemical originating from oral glands is applied to the tarsi at this time; however, the existence of such glands has not been demonstrated. Like other thyasid mites, T. barbigera larvae walk on the water surface with considerable ease. Concentrated along the margin of the pools they clamber about the wet moss and leaf litter, seldom venturing very far out on open water. They are quite capable of jumping, especially if disturbed. This is accomplished as the mite curls its hind legs beneath the
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as follows: Michigan Hollow, 16 June 1971; McLean Bog, 17 June 1971; Ringwood Preserve, 24 July 1972. The host species were not determined. Since no effort was being made to sample tipulid adults, there is no way of knowing how commonly T. barbigera utilizes these insects as hosts. Judging, however, by their occurrence on tipulids collected only incidentally in sweep nets, it is possible that crane flies represent another significant host group for T. barbigera.
SPECIES A. Obserrotus
A. cinereus
Larval attachment to host
Considerable difference of opinion has been expressed with regard to the circumstances under which thyasid larvae normally attach to their hosts. According to Jalil & Mitchell (1972), the larval mites "are attracted by, and will rest on, the breathing tubes of the mosquito pupae. At ecdysis of the host they climb onto the body of the emerging adult mosquito or they may attack adult hosts resting on the water." The same authors
AUGUST
1
C • 1
1 1
cz ZZ3
A. excrucians A,
fitchii
[
A.
punctor
C
A.
stimulans
A.
trichurus
SEPT.
3 r-' i
1
1
1 [
i
FIG. 7. Seasonal occurrence of Thyas barbigera larvae on adult Aedes mosquitoes, Tompkins County, New York, 1971-1972.
further noted that "post-ecdysis attachments" are probably uncommon. Corbet (1963), on the other hand, observed that thyasid mites occurred about as frequently on pars as on nullipars (i.e., females which have oviposited versus those that have not), suggesting that the mites are able to infest female mosquitoes at both emergence and oviposition. The attachment of larval water mites to an ovipositing dipteran host has been previously reported only for a Piona sp. parasitic on Cricotopus, a chironomid midge (Leger & Motas 1928). My study of Thyas barbigera in New York clearly demonstrates that in this species larval attachment to the host does not normally occur when the mosquito emerges as an adult but rather when the females subsequently return to the water to oviposit. The following observations support this contention: (1) Although T. barbigera females in New York may begin depositing eggs in late April and early May, the eggs do not begin hatching until the end of May or early June. Aedes mosquitoes breeding in the same pools start to emerge as adults about mid-May, with the last species completing its emergence by the end of the 1st week in June. At this time very few T. barbigera larvae are present, with the vast majority of mite eggs still unhatched (FIG. 8). (2) Thyas barbigera larvae do not attach to mosquito pupae to await the emergence of the adults. Examination of nearly 15,000 Aedes pupae collected from vernal pools in which T. barbigera abounded yielded no mite larvae. In laboratory experiments in which T. barbigera larvae were placed on the water surface of vials containing Aedes pupae, the mite larvae showed no discernible interest in the potential hosts. Occasionally a few mites aggregated about the respiratory trumpets where they broke the surface film, but this was interpreted as
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FIG. 7 summarizes the seasonal incidence of T. barbigera larvae on Aedes mosquitoes based on collections in Tompkins County, New York, during 1971 1972. The first parasitized hosts appeared during the last week of May and the first part of June. Unlike the other host species which emerge as adults during the late spring, Ae. vexans tends to develop later in the season as temporary pools are filled by rain and flood waters. Thus, parasitized Ae. vexans adults were not encountered until the end of June and were present intermittently until late August. T. barbigera mites were found on Ae. trichurus only during a 2- to 3-week period in June. Ae. excrucians was similarly parasitized for a relatively short time from mid-June to mid-July. The remaining host species were collected with T. barbigera larvae well into August and as late as the 1st week of September in the case of Ae. stimulans. The incidence of parasitism was difficult to assess quantitatively due to the low percentage of parasitized hosts for any given mosquito species and the difficulty in monitoring these populations continuously throughout the summer months. The incidence in most collections was less than 1.0% and seldom exceeded 5.0% to 8.0% in any given sample. The highest percentages of parasitism (up to 31%) occurred in samples collected along the edges of woodland pools where recently oviposited females were particularly abundant. It is thus impractical to speak in terms of "peaks of parasitism."
JULY
JUNE
A. conadensis
A. vexans
Seasonal incidence of parasitism
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J. Med. Ent.
in this study: Ae. canadensis, Ae. excrucians, and Ae.
punctor. If the mites normally attached to their hosts as the adults emerged from the water, one would expect to find both males and females equally parasitized. If not, some means of sex discrimination on the part of the mite larvae would have to be involved. This has not been exhibited by any other water mites which have been investigated. (5) The fact that T. barbigera larvae are found almost exclusively on Aedes females suggests that the behavior of the female mosquito plays a major role in host location by the mite. The most likely
opportunity for contacting female mosquitoes is when they return to the pools to oviposit. (6) Generally T. barbigera larvae occur in wet moss and litter along the margins of temporary pools, the same zone wherein Aedes females deposit their eggs. (7) Dissections of 306 Aedes females parasitized by T. barbigera revealed that, with the exception of 3 individuals, all hosts were parous (TABLE l). Even early in the season when more than 90% of the females in the host populations were still nulliparous, the few hosts parasitized by T. barbigera were all parous. (8) In several cases in which Aedes females bearing completely unengorged T. barbigera larvae were collected along the edge of woodland pools, dissections showed that oviposition of the host had very recently taken place, as evidenced by the retention of 1 or more eggs in the oviducts. (9) Aedes females oviposit up to 5 or more times during their lifetime which may extend into early fall. These successive ovipositions are not synchronized within a population, since several independent variables (e.g., success in finding a mate, obtaining a blood meal, and locating a suitable oviposition site) are operative. Thus if T. barbigera larvae attach and detach when the hosts oviposit, the continuous occurrence of parasitized mosquitoes throughout the season without well-defined peaks is easily explained. Larval attachment sites and parasite load
The most common attachment site for T. barbigera, irrespective of the host species, is on the posterior aspect of the thorax just above the hind coxae, where 72.3% of the mites in this study were found. These
Thyas barbigera FIG. 8. Oviposition and egg hatch of Thyas barbigera in
15 MAY
I I JUNE
relation to adult emergence of 6 potential Aides hosts, Ringwood Wildlife Preserve, Tompkins County, New York, 1971. Amplitudes of the individual emergence peaks represent the relative abundance of each Aedes sp. at this study site based on emergence-trap collections.
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simply a convenient resting site encountered by chance. The mites responded similarly to other objects breaking the surface. The larvae in no way attempted to cling to the respiratory organs and were easily dislodged when the mosquito pupae moved. Indeed, it would be impractical for an aerial larva on the water surface to attach to the submerged stage of its host. (3) Since most of the Aedes hosts are univoltine with their emergence as adults in late spring, a pronounced peak in the incidence of parasitism should occur at this time if the mite larvae are attaching at this point in the mosquito life cycle. The level of parasitism should then decline progressively as the larval mites detach. This is not the case. Using emergence traps, over 7000 Aedes adults were collected from pools containing wellestablished populations of T. barbigera during the spring of 1972 and not a single specimen was parasitized. Not only is there no peak of parasitism coinciding with the host emergence, but T. barbigera larvae can be found on their univoltine Aedes hosts throughout the summer months. (4) Only 3 Aedes males were found parasitized
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TABLE 1. Parity data for Aedes °.°. parasitized by Thyas barbigera larvae based on examination of the ovarian tracheal system, Tompkins County, New York, 1972-1973. 1972 No. dissections
HOST SPECIES Ae. Ae. Ae. Ae. Ae. Ae.
% parous 100.0 77.7 100.0 97.1 100.0 100.0 96.0
24 9 2 34 3 2 74
abserratus-punctor canadensis cinereus stimulans group trichurus vexans
All hosts
— 201 5 2 232
—
100.0 100.0 100.0 100.0
long setae on the legs and body. Measuring 200240 [i in length at the time of attachment to a host, the larval mites swell to several times that length while feeding. Engorged larvae, greatly distended and globose, are usually bright orange to red and are thus quite conspicuous on parasitized mosquitoes. Complete engorgement requires 5 to 8 days. If detached from the host when less than 500 JL in length, partially engorged larvae seldom complete their development to the nymphal stage. Fully engorged larvae whose parasitic feeding had not been interrupted reached 780 y. in length (X = 629, SE = 19.4, n = 16). Unlike Arrenurus mites parasitizing mosquitoes, thyasid larvae do not produce stylostomes (feeding tubes) and may or may not leave a discernible scar at the site of attachment (see Corbet 1963). Larval detachment from female hosts normally occurs when the mosquito oviposits. Postlarval stages
Once detached from the host, the engorged larvae, their mobility severely limited, crawl into protected recesses such as the leaf axils of moss, among rootlets, or between the moist layers of leaf litter or other soil debris. Without attaching to the substrate the engorged larvae become quiescent as a prelude to nymphal development. The subsequent nymphochrysalid stage, which is normally passed amidst Engorgement and detachment from mosquito host Unengorged T. barbigera larvae are orange, the moss and litter, can also be completed while sometimes straw-colored, with 2 pairs of dark eye floating on the water surface, although this is probably an uncommon situation. Nymphs emerge spots and a bristly appearance due to the numerous TABLE 2. Attachment sites of Thyas barbigera larvae on adult Aedes mosquitoes based on collections in Tompkins County, New York, 1972. HOST Ae. Ae. Ae. Ae. Ae. Ae. Ae. Ae.
abserratus-punctor canadensis cinereus excrucians fitchii stimulans trichurus vexans
All hosts
TOTAL NO. OF MITES
115 33 11 36 37 196
Cervix 12.2 3.0
20.0 8.6 5.9 8.7
56
11.5
6 490
— 9.3
Lateral thorax 15.7 27.3 10.0 28.6 23.6 16.4 15.4 16.6 18.3
Posterior thorax 72.1 69.7 70.0 62.8 70.5 74.3 73.1 83.4 72.3
Abdomen
0.6 — — 0.002
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mites also attach to the cervical region and the lateral aspect of the thorax but are rarely found on the host abdomen (TABLE 2). The number of T. barbigera larvae per host can be quite variable and in the Tompkins County collections did not exceed 14. Usually there were not more than 4 mites per specimen (TABLE 3). Occasionally heavier infestations were encountered, as in the case of an Ae. vexans female collected in Essex County, Vermont (27 June 1972) which had 20 T. barbigera larvae attached. Even within a very localized geographic area, the parasite load may differ greatly from one collection site to another. In contrast, the parasite load for mosquitoes bearing Arrenurus mites is much greater, with up to 30 or more mites per host being common. This can be explained by the difference in the mode of attachment to the host. Since Arrenurus larvae typically search out the pupal stage of the mosquito, a given pupa is exposed for 2 or more days to hostseeking mites. However, in the case of Thyas barbigera which attaches to ovipositing females, an Aedes adult is vulnerable to attack for only a matter of minutes at any one time. The chances for a large number of mites to locate a single potential host are thus substantially reduced.
1973 No. dissections % parous 2 100.0 21 100.0
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TABLE 3. Number of Thyas barbigera larvae per Aedes host based on collections in Tompkins County, New York, 1972.
HOST Ae. Ae. Ae. Ae. Ae. Ae. Ae. Ae.
abserratus-punctor canadensis cinereus excrucians fitchii stimulans trichurus vexans
All hosts
N O . PARASITIZED HOSTS EXAMINED
42
22 12 13 23 98 21 6 237
No. OF MITES/HOST
Mean
Maximum
2.7 1.8 1.6 3.0 1.8 2.1 2.7 1.5 1.7
14 8 5 12 4 10 9
2 14
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form of irregular-shaped integumental plates on various parts of the body. Adults which were of the 1st type at the time they were collected assumed the appearance of the 2nd type after being maintained for a year or longer in the laboratory. This suggests that the 2 types of adults described above represent young and old individuals and that adults of the 2nd type are in their 2nd year. Longevity
9 to 16 days after detachment of the engorged larvae from the host. Since they usually do not have access to open water upon their emergence, the nymphs are limited to crawling around within a small radius of the point at which they detached from the host. This mobility is further curtailed as the season progresses and the substrate becomes increasingly drier, forcing the nymphs to burrow deeper to avoid desiccation. Laboratory observations indicate that such nymphs may remain relatively dormant for months at a time, but become active within minutes when the substrate is flooded with water. Although limited feeding may occur, nymphs probably remain in Feeding behavior of nymphs and adults this inactive state throughout the rest of the summer A major drawback to developmental studies of and fall months. With the onset of winter they thyasid mites has been a lack of knowledge conburrow deep enough to survive the freezing surface cerning the feeding habits of the postlarval stages. temperatures. Recent evidence however has shown that both Although nymphs developing from larvae during nymphs and adults of Thyas barbigera and T. stolli the early summer may reach the adult stage before readily prey on mosquito eggs, suggesting that this overwintering, no evidence could be obtained to may represent the principal food source for these confirm this. No T. barbigera teleiochrysalids were mites (Mullen 1975b). Since engorged T. barbigera found under natural conditions. However, a nymph larvae detach from their female hosts when they collected during May entered the teleiochrysalid oviposit and the mobility of the ensuing nymphs is stage during the last week of July and the adult so restricted, the eggs of the host species provide emerged about 10 days later. No other nymphs, an abundant and readily accessible source of either field-collected or reared from larvae, comnutrients. pleted their development to adults in the laboratory, Other aquatic organisms including oligochaetes, despite their surviving up to a year or more as ostracods, planarians, mayfly nymphs, chironomid nymphs. Lack of an available food source may larvae and the immature stages of other aquatic account for this failure to develop further. Diptera and Coleoptera were not preyed upon by Two types of adult Thyas barbigera females were either T. barbigera or T. stolli. distinguished based on their external appearance. Laboratory observations of T. stolli suggest that One was smaller than the other, less than 850 (x, the eggs and quiescent stages of water mites may with a smoother integument and a lighter, more also serve as a potential food source for thyasid uniform coloration, more closely resembling nymphs. mites. On 1 occasion a T. stolli adult was observed The 2nd type was greater than 850 jx in length with to pierce with its chelicerae the outer integument a more wrinkled integument and was darker orange, of a Fiona teleiochrysalis. However, no apparent often red in color. The latter was also commonly harm was incurred since the Fiona continued its characterized by secondary sclerotization in the development to produce a normal adult. In
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Under laboratory conditions both adult males and females collected in the spring survived up to 15 months without any apparent source of food. Throughout this period they were kept in small glass vials containing only water, a disc of filter paper, and a sprig of moss. Nymphs reared from fully engorged larvae survived up to 12-1/2 months utilizing only stored reserves obtained during the parasitic larval state. This prolonged longevity of the postlarval stages may characterize many other thyasid species, since Thyas stolli and Thyasides sphagnorum were also found to live for comparable periods. One T. sphagnorum male survived 11 months after being collected as an adult, while T. stolli adults lived up to 16 months. The 1st winter is probably passed as a nymph and the 2nd as an adult.
Mullen: Acarine mosquito parasites, IV
1977
another instance, a T. stolli female was observed probing with her palps a cluster of 8 recently deposited eggs of her own species. Crawling slowly over the surface of the eggs, she would stop and press her chelicerae against the thick coating surrounding one of the eggs, causing it to depress and then spring back again as she released the pressure. In 1 case, however, she actually pierced the coating and remained quite motionless for a minute or more with her mouthparts inserted. No dissolution of the egg itself could be detected. The mite then withdrew her chelicerae leaving a hole 70 by 20 (x. All of the eggs developed normally and hatched. This observation adds credence to the belief that the thick coating about thyasid eggs serves as protection against predators as well as desiccation.
tion vial. Measuring 180-190 fjt. in diameter, the bright red, spherical eggs were individually coated with a white mucoid material. In contrast to T. barbigera and T. stolli eggs, however, this coating was comparatively thin, measuring less than 40 \L. Hatching was completed in 7 to 8 days with 98% egg viability. The resultant larvae in some vials were able to successfully make their way to the surface, while in others they remained at the bottom. Few in either situation survived more than 2 weeks, with the majority dying in 7 to 10 days in the absence of a host. Adult mosquitoes parasitized by T. sphagnorum larvae were collected at the following 3 study sites in Tompkins County, New York: McLean Wildlife Reservation, Town of Groton; Ringwood Wildlife Preserve, Town of Dryden; Michigan Hollow, Town of Danby. Hosts at these sites included Ae. abserratus, Ae. canadensis, Ae. excrucians, Ae. punctor, and Culiseta morsitans. A Cs. morsitans female para-
sitized by T. sphagnorum was also collected near Syracuse, New York. In contrast to Thyas barbigera Thyasides sphagnorum Habeeb, 1958 which is found almost exclusively on female hosts, Thyasides sphagnorum, the only member of this genus T. sphagnorum was found to occur on either sex of reported from North America, was described from the host species, as evidenced by parasitized males adults collected in a sphagnum bog in New Brunsof Ae. excrucians, Ae. punctor and Cs. morsitans in New wick, Canada (Habeeb 1958). It has since been York. recorded from temporary waters, especially those With the exception of a single Cs. morsitans female associated with bogs, in Michigan (Cook 1959) and taken on 1 August, all of the hosts parasitized by more recently from New York (Mullen 1975a). T. sphagnorum were collected between 24 May and Virtually nothing has been reported concerning 27 June despite continued sampling at the same the biology or hosts of this mite. sites throughout the summer months. Even when On 11 May 1971, 11 T. sphagnorum adults (6 $$, the mites were found, the incidence of parasitism 5 $$) were collected from submerged sphagnum was very low (
