Feeding and related behavior of female Simuliidae (Diptera)

PARASITOLOGICAL

EXPERIMENTAL

15,439-470

PARASITOLOGY

Feeding

REVIEWS

(1964)

and

Related

Behavior

Simuliidae

of

Female

and

University

(Diptera)

A. M. Fallis Department

of Parasitology,

Ontario

Research Toronto,

I. II.

Introduction Feeding

................................ Preferences

.........................

III.

Importance

as Pests

IV.

Importance

as Vectors

V.

Biting

Sites

VI.

Biting

Activities

VII.

Longevity

IX.

Flight

X. XI.

I.

.............. ............

.

..................... .................

Size and Digestion

VIII.

of Blood

Meal

.

....................... Range

Feeding

Foundation

and

.

.

.

.

.

... .. . . . . . .. . .. . ....

.................... Climate

Summary

.......................

References

.......................

of

Toronto,

Canada

.............

.. ... ..

INTRODUCTION

............ ............ ............ ............ ............ ............ ............ ............ ............ ............ ............ ............

...... ...... ...... ...... ...... ...... ...... ...... ...... ...... ...... ......

439 440 448 449 450 452 455 456 456 458 460 461

largely qualitative, and pertains to only a few Speciesof Simuliidae occur throughout the of the described species. Some of it may be world in rapid streams where conditions are biased becauseof the availability of only certain kinds of animals in the area under study, suitable for larval development. Environmental factors acting on the eggs,larvae, and and these animals are not necessarily those pupae possibly determine the speciesand their most preferred by the flies under observation. abundance more than factors that affect Other uncertainties prevail also, as the work of Rothfels (1956), Syme and Davies (1958), adults. Nevertheless the dispersal, longevity, and feeding habits of the adults, as well as Dunbar (1959), Rubtzov (1956), and Lanthe availability of food and environmental dau (1962) reveals taxonomic complexes conditions favorable to obtaining it, are un- among individuals hitherto considered single doubtedly important. Knowledge of the feed- species.In spite of taxonomic uncertainties, it ing habits of speciesthat are annoying pests is hoped that a review of observations on and vectors of parasites and pathogens is of feeding and related behavior will be useful. further interest since the importance of simu- The namesof most specieshave been accepted liids as vectors dependson their feeding habits without comment, although taxonomists will as well as on their suitability as hosts for regard some as synonyms and may disagree parasites. Information on feeding is scattered, with some used herein. 439

440

PARASITOLOGICAL

II.

FEEDINGPREFERENCES

Femalesof most simuliids have piercing and sucking mouth parts and take at least one blood meal from mammals or birds, although some occur in places where homoiothermous animals are unknown (Rubtzov 1956). Peterson (1956) found Sivnulium vittatum feeding on an ant, but there is no evidence that insects are attacked commonly. The reduced mouth parts in Cnephia dacotensis, Prosimulium alpestre, Gymnopaius holopticus and G. dichopticus suggest that they feed on nectar or not at all (Nicholson, 1945; Davies and Peterson, 1956). Stone (1952) noted a similar morphology in Cnephia emergens,as did Dorogostajskij et al. (1935) in some flies in Russia. Some species with nonfunctional mouth parts are listed in Table I. Shewell (1955) suggests that the large basal tooth on the tarsal claw of several species is an adaptation for feeding on birds. Certainly in North America S. rugglesi, S. latipes, S. aureum, S. croxtoni, “H,” (described recently by Wood (1963) as S. anatinum), S. euryadminiculum S. quebecense, Prosimulizcm decemarticulatum, and Cnephia ornithophilia possessthe toothed claw, and all feed on birds (Fallis et al., 1956, 1958, 1961, 1962; Bennett, 1960). Others possessingthe claw are Prosimulium vernate, Cnephia denaria, C. aquirrei, C. abdita, C. saskatchewana, C. vittosa, C. johannseni, S. emarginatum, S. gouldingi, S. impar, S. innocens, S. rivuli, and S. yepocapense (Shewell and Fredeen, 1958; De Foliart and Peterson, 1960; Peterson, 1962; Davies et al., 1962; Dalmat, 1949). de Meillon (1930) noted the claw on the following African species: S. nigritarsis, S. griseicolle, S. diversipes, S. bickeri, S. cervicornutum, S. palmeri, S. blacklocki, S. alcocki, S. unicornutum, S. hirsutum, and S. aureosimile; Crosskey (1959a) lists S. ruficorne also. Edwards ( 1915) noted the claw on S. latipes and S. subexcisumand a smaller one on S. ornatum. Many of these are known to feed on birds (Table I). “If,” says Crosskey

REVIEWS

(1959b), “toothed claws really do indicate bird-feeding it would seemthat ornithophily is very much the rule among Ethiopian black flies since 80 per cent of the speciesin this zoogeographical region have toothed claws.” Crosskey notes exceptions also, as S. albivirgulatum has a simple claw but feedson birds. Simulium venustum likewise has a simpleclaw but feeds to a limited extent on some birds (Fallis and Bennett, 1958). Similium damnosum has a toothed claw but feeds on the lesshairy parts of man, although Fain (1950) states there are places in Africa where it does not bite man; there are records from birds also (Hargreaves, 1925; LeRoux, 1929). Lewis (1953, 1958) found pollen grains and plant sugarsin specimensof S. damnosumand observed S. griseicolle on flowers. Davies and Peterson (1956) have evidence that other blood-sucking speciesfeed on plants also. Clearly some simuliids have more specific feeding habits than others (Table I). Notable differences have been observed, too, for the same species in different places. Similium damnosum,for example, feeds readily on man (Balfour, 1906; Austen, 1906; King, 1908, 1911); although in parts of Africa it is not known to do so (Wanson, 1950, as quoted by Lewis, 1957; de Meillon, 1957; Lewis, 1962). It is recorded from goats, donkeys, and dogs (Blacklock, 1962b; Lewis, 1948; Crosskey, 195.5) and from birds and game (Hargreaves, 1925; Le Roux, 1929). If S. damnosum should prove to be a complex of speciesnot easily discernible it might account for someof the observed differences. The preference of this fly for dark skinned people (Hughes and Daly, 1951; Crosskey, 1955) may be related to scent and/or color. Dalmat (1954, 1955), from experiments to determine the vectors of onchocerciasis in Guatemala, concluded that S. ochraceum, S. metal&urn, S. callidum, S. exiguum, S. veracruzanum, S. haematopotum, S. downsi, and Cnephia pacheco-lunai attack man, but the last two only rarely. The last species was

FEEDING

BEHAVIOR

OF

FEMALE

TABLE Feeding Records Fly”

S. wellmani

Coq. de Meill. Roub.

S. woodi de Meill. Wans. and

S. olbivirgulatum

Hen. S. aureosimile Porn. S. bovis de Meill. S. damnosum

I Some Simuliidae

Host and site of feeding

AFRICA S. den-i Porn. S. faini S. gariepensis de Meill. S. imerinae Roub. S. kauntzeum Gibb. S. medusaeforme Job.-Porn. S. merops de Meill. S. neireti Roub. S. nigritarsis S. nyaslundicum

of

441

SIMULIIDAE

man (head, neck, ears) man man man man man man man (eyes, forehead, under helmet) man man man man man, birds man, birds (ankles, legs) man, cattle

Theo.

man, cattle, donkey, sheep, goat, dog, birds (legs), flowers

S. griseicolle Becker

man, birds, guinea-fowl, key, flowers

S. neavei Roub.

man, mule

S. gracilipes Edw. Porn. de Meij. S. falcoe Shiraki S. vorax Porn. S. hirsutum Porn. S. kenyae de Meill. S. ruficorne Macq. ASIA S. cholodkowskii Rub. S. decimatum Dorog. et al. S. japonica Mats. S. transiens Rub. S. aokii Taka. S. buissoni Roub.

mule birds fowl, owl hawk donkey fowl fowl birds

S. alcocki S. stratum

S. venusturn Say S. yezoense Shiraki S. argyrocinctum

de Meij.

0 A., Austrosimulium;

man man man man horse, man man, fowl horse, cow, man cow, horse, man cattle, horses, water (ears)

C., Cnepkia;

E., Eusimufium;

don-

buffalo

Reference Gibbins, 1934, 1935; Bequaert, 1938 Wanson, 1950 de Meillon, 1957 de Meillon, 1957 Bequaert, 1938 Schwetz, 1930 de Meillon, 1957 de Meillon, 1957 Bequaert, 1938 de Meillon, 1957 Wellman, 1908; de Meillon, 1930; Gibbins, 1938; Bequaert, 1938; Freeman and de Meillon, 1953 de Meillon, 1957 Wanson, 1950; Crosskey, 1959b Crosskey, 1959a; Duke, 1962a de Meillon, 1930; Bequaert, 1938; Gibbins, 1938; Crosskey, 1954b, 1959a Austen, 1906; King, 1908; Hargreaves, 1925; Le Roux, 1929; de Meillon, 1930; Schwetz, 1930; Gibbins, 1935 ; Bequaert, 1938; Wanson, 1950; Lewis, 1953; Crosskey, 1954a; Crisp, 1956; Lewis, 1957; Duke, 1962b King, 1908 Gibbins, 1937, 1938; Lewis, 1953 ; 1957; de Meillon, 1957; Crosskey, 1959b Gibbins, 1935, 1937, 1938; Bequaert, 1938; Crosskey, 1959a Edwards, 192 1 Gibbins, 1938, 1941; Crosskey, 1959b Friederichs, 1925 Gibbins, 1937 Pomeroy, 1922; de Meillon, 1930 Duke, 1962a Duke, 1962a Crosskey, 1959b Gutzevich, 1939 Gutzevich, 1939 Ogata et al., 1956 Gutzevich, 1939 Ogata et al., 1956 Edwards, 1932, from Bequaert, 1938 Rubtzov, 1939; Ogata et al., 1956 Ogata et al., 1956 Friederichs, 1925

P., Prosimulium;

S.,

Simulium.

442

PARASITOLOGICAL

TABLE Host

Flya S. S. S. S. S. S. S. S. S.

atratum de Meij. falcoe Shiraki fiavipes Austen gurneyae Sen.-White itidescens de Meij. Zatistriatum Sen.-White ornatum Mg. pattoni Sen.-White salopiense Edw.

REVIEWS

I (Continued)

and site of feeding

fowl hawk horses cattle cattle, horses, cattle horse, cow cattle cow, horse

water

buffalo

Reference Friederichs, 1925 Shiraki, 1935, from Austen, 1921 Senior-White, 1922 Friederichs, 1925 Senior-White, 1922 Ogata et al., 1956 Senior-White, 1922 Ogata et al., 1956

Ogata

et al., 1956

AUSTRALIA S. melatum S. nicholsoni A. bancrofti

Wharton Mack. Tayl.

A. furiosum S. ornatipes A. pestilens

Skuse Skuse Mack.

and Mack.

and

Mack

man man man,

horse,

rabbit

(belly)

man, rabbit (legs) man, cattle, horses cattle, sheep, dogs, wallaby (face)

kangaroo,

Dyce and Lee, 1962 Mackerras and Mackerras, 1948 Drummond, 1933 ; Mackerras and Mackerras, 1948; Lee et al., 1957; Dyce and Lee, 1962 Lee et al., 1957; Dyce and Lee, 1962 Swan, 1937; Taylor, 1944 Mackerras and Mackerras, 1948; McCarthy, 1961

EUROPE S. erythrocephalum = argyreatum

de Geer (Mg.) Ldst.

man,

S. galli Edw. = rufipes S. (SchBnbaueria) mathiesseni End. S. morsitans Edw. P. hirtipes (Fries)

man man

S. aureum Fries = bracteatum coq. S. columbaczense Schoen.

S. costatum Fried. S. decimatum Dorog., and Vlas. S. Zutipes Mg.

S. monticola S. ornatum

S. reptans

Fried. Mg.

L.

Rub.

ox

man man.

cattle

fowl,

man

Edwards, 1915; Friederichs, sen, 1924; Smart, 1944; Coluzzi, 1962 Galli-Valerio, 193 2 Bening, 1924

cattle and other mals (mouth, ears, abdomen) man, cattle man, animals cows

(teats),

domestic nose,

anieyes,

man

cow, horse, sheep, goat, man cattle, horse (ears, nose, eyes, belly, thighs), man (nose, eyebrows, hand)

cow,

horse,

Edwards, 1915; Smart, 1944 Austen, 1906; Edwards, 1915; Dorogostajskij et al., 1935; Smart, 1936; Edwards et al., 1939; L. Davies, 1961 Edwards et al., 1939; Rivosecchi and Coiuzzi, 1962 Leon, 1909

Edwards, 1915; Dorogostajskij Dorogostajskij et al., 1935 birds,

man,

dog

1921b; PeterRivosecchi and

et al., 1935

Edwards, 1920; Pillers, 1927, as in Steward, 1931; Dorogostajskij et al., 1935; Smart, 1944; L. Davies et al., 1962 Friederichs, 1921b; L. Davies et al., 1962 Edwards, 1920; Friederichs, 1921b; GaliiVaierio. 1923; Petersen, 1924; Steward, 1931; Dorogostajskij et al., 1935; Edwards et al., 1939; Lohmann, 1942; L. Davies et al., 1962 Edwards, 1915; Friederichs, 1921b; Smart, 1936, 1944; Rivosecchi and Coluzzi, 1962; L. Davies et al., 1962

FEEDING

BEHAVIOR

TABLE Fly”

OF

FEMALE

S. tuberosum

Ldst.

man, cattle, horse, dog, bird

S. variegatum

Mg.

cow, horse, sheep, goat, dog (nose, eyes, belly), man (nose, eyes) horse (inside ears) horse, cattle, sheep (ears)

S. sericatum S. strigatum S. alpestre

Mg.

Enderl. Dorog., Rub. and

443

I (Continued)

Host and site of feeding

S. cinercum Macq. S. equinum L. = maculatum and lineatum S. pus&m Fries

SIMULIIDAE

Reference Edwards, 1915; Smart, 1944; Downe and Morrison, 1957; L. Davies et al., 1962 Edwards, 1920; Dorogostajskij et al., 1935; Smart, 1944; L. Davies et al., 1962

cattle, horses (inner legs) cattle domestic animals nonblood sucker

du Buysson, 1921 Edwards, 1915; Friederichs, 1921a; Petersen, 1924 Dem’yanchenko, 1960 Enderlein, 1921; Lohmann, 1942 Enderlein, 1924 Dorogostajskij et al., 1935

ivy flowers man, cattle mammals man, cattle man man man man man, cattle rodents, man, cattle man, cattle, dogs man, cattle

Smart, 1943 Carlsson, 1962 Carlsson, 1962 Carlsson, 1962 Carlsson, 1962 Carlsson, 1962 Carlsson, 1962 Carlsson, 1962 Carlsson, 1962 Carlsson, 1962 Carlsson, 1962 Carlsson, 1962

Vlas. S. saliopense Edw. Helodon ferrugineus Wahlb. P. nigripes End. Stegopterna richteri End. C. pallipes Fries C. tredecimata Edw.

C. fuscipes Fries Ldst. annulitarsis Gnus forsi Carlsson S. vulgare Rub. S. pitense Carlsson E. angustitarse Schfinbaueria

Zt.

MEXICO AND CENTRAL C. pacheco-Zunui (De L.) S. avidum Hoffm. = metallicum Bell. S. callidum D. and S. = mooseri S. S. exiguum Roub. S. gonzalezi Varg. and Dias Naj. S. haematopotum Mall. S. metallicurn Bell. S. S. S. S. S. S. S. S.

AMERICA man (rarely) man man, horse, mule, cattle, pig, tayra, birds (lower body) man, horse, mule, cattle, birds (lower limbs, belly) man

man (lower limbs) man, horse, mule, pig, sheep, deer, ocelot, tayra, birds (lower body) man, horse, donkey, tayra, ochraceum Wlk. birds (upper man, lower horse) veracruzunum V., M. and D. man (lower limbs) horse hippovorum Mall. mexicanurn Bell. horse, mule, donkey, birds (belly, ears, nose) horse virgatum Coq. acetenangoensis Dalmat horse (belly) horse, mule, cattle, sheep, pig, downsi V., M. and D. birds (ears, belly) horse, mule, cattle (belly, ears) pulverulentum Knab

Dalmat, 1954 Hoffman, 1930; Hoffman and Vargas, 1931 Hoffman, 1930; Strong et al., 1934; mat, 1954, 1955 Dalmat, 1954, 1955

Dal-

Biagi et al., 1958 Dalmat, 1954, 1955 Strong et al., 1934; Dalmat, 1954, 1955 Hoffman, 1930; Strong et al., 1934; Dalmat, 1954, 1955 Dalmat, 1954, 1955 Edwards, 1915 Strong et al., 1934; Bequaert, 1938 Strong et al., 1934; Bequaert, 1938 Dalmat, 1955 Dalmat, 1955 Dalmat, 1955

444

PARASITOLOGICAL

TABLE

REVIEWS

I (Continued)

Host and site of feeding

Fly a

Reference Dalmat, 1955

S. smarti Vargas

horse, mule, cattle (belly, ears, hind legs) horse, mule, cattle (belly, ears)

NORTH AMERICA P. fuscum S. and D.

man, horse, cow, deer

S. corbis Twinn S. longistylatum

man man

Davies and Syme, 1958; Anderson and De Foliart, 1961 Sailer, 1953 Davies and Peterson, 1956; Davies et al., 1962 Root, 1922

Knab

S. rubicund&m

Shew.

End.= quadriLw. S. sanguinem Knab C. mutata (Mall.)

man

S. pecuarum

man, cattle, horse, flowers

S. mallochi vittatum

Riley

man deer, horse, cow, man (ear)

P. fulvum

Coq.

man, livestock

P. hirtifies

(Fries)

man, deer

P. P.

novum D. and S. mixtum S. and D.

man, horse man, horse (ear)

S. arcticurn Mall. = simile

man, cattle, horse, mule

S. decorum

deer, horse, man (chest, belly)

Wlk.

S. forbesi Mall. S. jenningsi Mall.

S. hunteri S. latipes

Mall. (Mg.)

man, horse, cow chicken, birds, man

S. Zuggeri N. and M. S. meridionale

man, horse horse, cattle, mule, man, turkey (ear, head, neck)

Riley

horse, cow turkey, chicken (comb, wattle), pheasant, dove, starling, man (around eyes)

Dalmat, 1955

Knab, 1915 Frohne and Sleeper, 1951; Davies and Peterson, 19.56; Anderson and De Fohart, 1961 Webster, 1914; MaiIoch, 1914; Fitch, 1918; Travis et al., 1951; Robertson, 1928, from Hocking, 1953 Hearle, 1932 ; Travis, 1949; Sailer, 1953; Sommerman et al., 1955; Shewell, 1957 Sanderson, 1910; Jenkins, 1948; Nicholson and Mickel, 1950; DeFoiiart, 1951; Hocking and Richards, 1952; Sailer, 1953; Stone and Jamnback, 1955; Sommerman et al., 1955; Davies and Peterson, 1956; Shewell, 1957; Wolfe and Peterson, 1959 Hearle, 1932 Davies and Syme, 1958; Anderson and De Foliart, 1961; Davies et al., 1962 Cameron, 1922; Hearle, 1932; Knowlton and Maddock, 1944; Sailer, 1953; Sommerman et al., 1955; Sheweli, 1957 Hocking and Richards, 1952 ; Sailer, 1953 ; Sommerman et al., 1955; Davies and Peterson, 1956; Shewell, 1957; Anderson and DeFoiiart, 1961; Davies et al., 1962 Malloch, 1914 Malloch, 1914; Underhill, 1939, 1940, 1944; Jones and Richey, 1956; Anderson and DeFoliart, 1961; Davies et al., 1962 Hearle, 1932 Steward, 1931; Hocking and Richards, 1952; Stone and Jamnback, 1955; Davies and Peterson, 1956; Anderson, 1956; Shewell, 1957; Fallis and Bennett, 1958; Peterson, 1959b; Bennett, 1960; Anderson and DeFoiiart, 1961 Anderson and DeFoGart, 1961 Edgar, 1953; Shewell, 1957; Anderson and DeFoliart, 1961

FEEDING

BEHAVIOR

OF

TABLE Fly” S. parnassum

S. pictipes

FEMALE

I (Continued)

Host and site of feeding D. and S.

Hagen

man, woodchuck,

nectar

birds, cattle man, horse, cow, sheep (ear)

Anderson

S. tuberosum Ldst.

man, ground nectar

S. venusturn Say

man, deer, dog, sheep, cattle, horse, mule, grackle, crow, blue heron

S. vittatum

cattle, horse, sheep (chest, belly, inside ear), man (chest, inside ear), nectar

C. invent&a invenustum

(Wlk.) =S.

S. mugnum D. and S.

Reference Fuller, 1940; DeFoliart, 1951; Hocking and Richards, 1952; Stone and Jamnback, 1955; Wolfe and Peterson, 1959; Davies et al., 1962 Malloch, 1914; Jobbins-Pomeroy, 1916; Smart, 1934 ; Nicholson and Mickel, 1950 Rempel and Arnason, 1947; DeFoliart, 1951; Hocking and Richards, 1952 ; Jamnback, 1952; Peterson, 1956; Wolfe and Peterson, 1959 Lugger, 1896, from Davies et al., 1962; Sanderson, 1910; Jobbins-Pomeroy, 1916 ; Cameron, 1922; Hearle, 1932; Edwards et nl., 1939; Twinn et al., 1948; Jenkins, 1948 ; Travis, 1949 ; Nicholson and Mickel, 1950; DeFoliart, 1951; Frohne and Sleeper, 1951; Travis et al., 1951; Hocking and Richards, 1952; Jamnback, 1952 ; Davies, 1953; Hocking, 1953 ; Sailer, 1953 ; Hocking and Pickering, 1954; Sommerman et al., 1955 ; Stone and Jamnback, 1955; Anderson, 1956; Fallis et al., 1956; Davies and Peterson, 1956; Shewell, 1957; Wolfe and Peterson, 1959; Anderson and DeFoliart, 1961 Malloch, 1914; Jobbins-Pomeroy, 1916; Cameron, 1922 ; Hearle, 1932 ; Knowlton, 1935 ; Knowlton and Maddock, 1944; Travis, 1949; Hocking, 1953; Sailer, 1953 ; Stone and Jamnback, 1955 ; Peterson, 1956; Shewell, 1957; Jones, 1961 Webster, 1914; Bennett, 1960

horse, mule, moose, man

Zett.

445

SIMULIIDAE

squirrel, cattle,

and DeFoliart, 1961; Davies 1962 Knowlton, 193.5 Anderson and Voskuil, 1963 Hall and Wigdor, 1918 Jones, 1961 Knab, 1915 Anderson and Voskuil, 1963 Knowlton, 1935 Bennett, 1960 et al.,

S. bivittatum Mall. S. argus Will. S. molesturn Harris S. piperi D. and S. S. placidum Knab S. trivittatum Mall. S. venator D. and S. C. ornithophilia D., P., and W. = “U” (-y “TN C. taeniotifrons (End.) E. johonnseni (Hart) P. decenwrticulatum

S. aureum Fries

(Twinn)

horse horse, dog sheep horse, horse, horse birds

cattle (shorn belly) mule (ears) cow, man (ventral side)

turkey, duck turkey turkey, chicken, pheasant, duck birds turkey, pheasant, chicken, duck, dove

Anderson and DeFoliart, 1961 Anderson et al., 1961 Anderson et al., 1961; Anderson and De Foliirt, 1961 Bennett, 1960 Fallis and Bennett, 1958; Bennett, 1960; Anderson and DeFoliart, 1961; L. Davies et al., 1962

446

PARASITOLOGICAL

TABLE Fly a

Host

S. canonicolum

D. and S.

birds,

I (Continued)

and site of feeding hawk,

S. clarum D. and S. = canonicolum S. congareenarum (D. and S.)

long-eared

S. croxtoni

birds

chicken, owl

(head)

Anderson

S. bafinense Twinn Twinnia tibblesi Stone

nonbiting nonbiting

man

Enderlein,

man man man man man man man man man, domestic animals domestic animals domestic animals man, domestic animals

Floch and Abonnenc, 1946a Floch and Abonnenc, 1946b Lutz et al., 1918 Lutz et al., 1918 Lane and Porto, 1940 Lane and Porto, 1940 Figueroa, 1917 Floch and Abonnenc, 1946a Lutz, 1917, 1922 Lutz, 1922 Lutz, 1922 Lutz et al., 1918; Lutz, 1922

animals animals horse (orbital margin) domestic animals horse

Lane and Porto, 1940 Lane and Porto, 1940 Lutz et al., 1918 Lutz, 1922 Lutz et al., 1918

SOUTH

Davies

birds, duck?, common loon (head, neck) duck, geese, turkey, chicken, pheasant, dove, crane

S.)

turkey

N. and M.

S. sZossonae

(D.

and

neck)

1957;

turkey birds flowers nonbiting nonbiting nonbiting nonbiting nonbiting nonbiting nonbiting nonbiting

S. rugglesi

(head,

Fitch et al., 1946; Shewell, and Voskuil, 1963 Hearle, 1932

S. occidentale Townsend S. quebecense Twinn S. furculatum Shew. C. dacotense D. and S. C. emergens Stone C. ermites Shew. Gymnopais dichopticus Stone G. holopticus Stone P. alpestre D., R. and V. P. perspicuum Somm. P. gibsoni (Twinn)

S. euryadminiculum

turkey

turkey

Reference

Jones and Richey, 1956; Bennett, 1960; Davies et al., 1962 Shewell, 1957; Davies and Peterson, 1956; Bennett, 1960 Davies and Peterson, 1956; Shewell, 1957; Lowther, 1962 Shewell, 1955; Davies and Peterson, 1956; Fallis et al., 1956; Anderson, 1956; Shewell, 1957 ; Bennett, 1960; Anderson and DeFoliart, 1961 Skidmore, 1932; Underhill, 1939, 1940; Jones and Richey, 1956 Skidmore, 1932 Bennett, 1960 Hocking and Pickering, 1954 Shewell, 1957 Shewell, 1957 Shewell, 1957 Shewell, 1957 Shewell, 1957 Sommerman, 1958 Sommerman, 1958 Sailer, 1953; Sommerman et al., 1955; Davies et al., 1962 Peterson, 1959b Shewell, 1957

N. and M.

birds,

REVIEWS

(head,

neck)

AMERICA

Psaroniocompsa opalinifrons End. S. antillarum Jenn. S. guianense Wise S. paraguayense Schrottky S. parense Schrottky S. pilosum Lane and Porto S. sintillatum L. and P. S. simile Fig. S. tarsale Will. S. amazonicum Goeldi S. nitidum Mall. S. minus&urn Lutz S. inexorable Schrottky = pertinux Kollar S. antunesi L. and P. S. major L. and P. S. orbitale Lutz S. pruinosum Lutz S. subvirde Lutz et al.

1934

FEEDING

BEHAVIOR

OF

taken at an altitude of 8000 feet in a region uninhabited by man. Presumably it feeds on other animals, such as sheep, that occupy the area. Simulium ochraceum showed a strong preference for man rather than horse, mule, donkey, pig, cow, sheep, goat, dog, cat, chicken, turkey, duck, or pigeon. This confirms the report of Hoffman and Vargas (1931) that S. ochraceum and S. mooseri (= callidum) prefer man to animals. Simulium metallicurn was taken more often from the horse, mule, and cow than from man. Some S. metallicum were taken from ducks and a few from other birds. Several species in Central America feed on animals other than man. Simulium adersi, bovis, and nigritarsis bite man in some countries (Gibbins, 1941) but not in the Sudan (Lewis, 1957). Rivosecchi and Coluzzi (1962) found S. erythrocephalum biting man in northern but not southern Italy. Similarly S. reptans bites man occasionally in northern Tuscany but not near Rome. Possibly these are species complexes. It is of interest also that the above authors report S. aureum as a man biter but not Melusina maculata, Prosimulium hirtipes, S. liriense, and S. mediterraneum. Lewis (1948) refers to early reports (Waddington and Hanbury, 1822; Riippell, 1829; Haskins, 1825) of attacks on humans by flies that were presumably S. damnosum and S. griseicolle. Many of the latter, he says, walk over the skin and are annoying pests, but few engorge. He states that King (1923) found S. griseicolle on donkeys occasionally, and on hawks, parrots, pigeons, and sparrows, and that it causes death of pigeons and sparrows. Conceivably, in some instances, death could be caused by parasites transmitted by the flies rather than directly by them. If not numerous it attacks birds rather than cattle and donkeys, according to King, Crosskey and Crosskey (1958) imply that it feeds on birds rather than man. Downe and Morrison (1957) showed by

FEMALE

SIMULIIDAE

447

means of precipitin tests that horses and cows but rarely pigs and chickens were attacked by S. vittatum, S. parnassum, S. decorum, S. tuberosum,S. corbis, P. hirtipes, and C. mutata. Simulium vittatum and S. venustum attacked horsesin preference to cows. Hosts on which feeding occurred may depend partially on animals that were available on which to feed; there was little possibility in this instance of flies feeding on wild mammals or birds. No indication was obtained of multiple feeding by a fly. Davies et al. (1962), using the same technique on engorgedblack flies taken in light traps in Scotland, found that S. tuberosum fed on man, cow, horse, dog, bird; S. reptans fed mostly on cow, and lesson horse and man; S. monticola fed mostly on cow, and lesson man, horse, sheep; S. variegatum fed on cow, horse, man, sheep, and dog; S. ornatum fed on cow and horse; and S. latipes fed largely on birds but also on an unidentified rodent, cow, horse, man, dog, and sheep. The results of these tests, as the authors point out, could be biased by the proximity of somekinds of animals and not others. Nevertheless, the authors were convinced that the flies were potential vectors of parasites to birds, man, and domestic animals. Rempel and Arnason (1947) noted the preference of S. arcticum for older cattle presumably becausethey had shorter hair than young cattle. Horses were bitten too and sheared sheep were bitten severely. Observations by Anderson and DeFoliart (1961) indicated that other mammalophilic species fed more on large than on small mammals. Simulium venustum fed on horsesin preference to man, dog, or cat; presumably the host, rather than the size of the animal alone, was important. Possibly, too, somefeeding records of S. venustum are actually those of the closely related speciesS. verecundum that was described recently by Stone and Jamnback (1955). Bennett (1960)) Anderson and DeFoliart (1961), and Anderson et al. (1962) showedin

448

PARASITOLOGICAL

their studiesof feeding preferencesof ornithophilic flies that many more S. rugglesi fed on ducks than several other kinds of birds, although some engorged specimenswere taken from six other speciesof birds. They found also that most S. rugglesi fed on ducks near water. The flies appeared, therefore, to prefer certain habitats as well as certain hosts. Anderson et al. (1962) reported as many as 1000 flies per hour feeding on ducks, and noticed that the number was related to the size of the host. Anderson and DeFoliart (1961) found, too, that the attractiveness of a duck for S. rugglesi is affected by its visibility to the insect. Other speciesof ornithophilic flies likewise were collected more frequently and in larger numbers from certain habitats and birds than others. Feeding is closely associated with the ovarian development in some species. Lewis (1960a) noted that parous females of S. damnosum tend to bite at midday in Tanganyika. He observed that most parous flies of S. neavei which bite in the afternoon do so earlier than most of the nulliparous flies, and often several flies attack in quick succession.Davies ( 1961) observedthat Prosimulium mixtum dispersed more rapidly following emergencethan P. juscum, presumably becausethe former was seeking a blood meal essentialfor ovarian development. Nulliparous femalesof the latter speciesapparently produced the first ovarian cycle without a blood meal, which explains their slow dispersal and tendency to stay close to the emergence site, Apparently only the parous individuals of this species, and only a small percentage of them, are involved in biting, and consequently it is unlikely that this speciesis an important vector of parasites. Prosimulium mixtum is a potential vector since nulliparous as well as parous individuals feed on man and survive longer than P. juscum. Davies’ data tend to refute Rubtzov’s thesis, which Davies discusses,i.e., that the need for a blood meal is influenced directly by environmental factors such as the nutrition

REVIEWS

of the larvae although Davies (1957b) relates the feeding of S. ornatum to the amount of fat-body in the fly. III.

IMPORTANCE

AS PESTS

All simuliids that take a blood meal may properly be considered pests. Those with a short life and small population, such as Cnephia ornithophilia, may be lessimportant pests but effective hosts and vectors of parasites (Fallis and Bennett, 1962). Some have been troublesome pests for centuries: S. coZumbaczensecausesillness and mortality in cattle, horses, sheep, and goats in Germany, Yugoslavia, Hungary, Rumania, and Bulgaria (Ciurea and Dinulescu, 1924; Wilhelmini and Saling, 1928; Steward, 1931; Baranov, 1935). Outbreaks of diseasepresumably causedby it from A.D. 930 to 1876 are recorded by Rethly (1925). Simulium venustum and P. hirtipes are annoying pests of man in North America. Early accounts of attacks by simuliids most probably refer to these species(Agassiz, 1850, as cited by Nicholson and Mickel, 1950; and Harris, 1862, as cited by Twinn, 1933). Sim&urn venustum is considered responsiblefor lowered milk production and loss of weight in cattle. Deaths of various animals following bites of different speciesare reported: for example, mules in Arkansas following bites of S. pecuarum (Bradley, 1935) ; cattle in Saskatchewan from S. arcticurn (Cameron, 1918; Fredeen, 1958); wallabies in Australia from A. pestilens (Mackerras and Mackerras, 1948) ; poultry in Iowa (Biester and Schwarte, 1948, as in Garside and Darling, 1952); young hawks in California (Fitch et al., 1946); and buffalo and other domestic animals in Russia from S. tarnogradski and S. znojkoi (Abusalimov, 1947). The symptoms causedby the last two speciesresembled those of hemorrhagic septicemia and anthrax. Simulium vittatum is perhapsa lessimportant pest of man and animals (Fredeen, 1958). Decreased egg production in poultry in Ala-

FEEDING BEHAVIOR OF FEMALE

bama resulted from attack by S. meridionale (Edgar, 1953), and Anderson and Voskuil (1963) observed similar effects by S. canonico2um in California. The belly of some animals bitten by S. arcticurn is raw and edematous (Rempel and Arnason, 1947). Millar and Rempel (1944) believe injection of foreign proteins by this fly causesdeath in cattle from shock. Steward (1937) noted white patches on the inside of ears of horses following bites of S. ornatum. Davies (1957a) reports scar tissue formation around the navel of cattle bitten by the same species. Zahar ( 1951) says this speciescausesedematousswelling of the udder of cows and the sheath in bullocks and horses. Simulium trivittatum produces weals on cattle and is the cause of lowered milk production (Anderson and Voskuil, 1963). Cnephia ornithophilia causes lacerations, hemorrhage, and inflammation which persist for 3 days on young birds (Bennett, 1960). IV.

IMPORTANCE

AS VECTORS

The feeding of several simuliids is intimately associated with the transmission of various parasites. Fifty years ago some believed (Hunter, 1913) that black flies were associated with pellagra, but the following year Jennings ( 1914) showedthis was erroneous. Considerableattention has been directed toward speciesshown to transmit the nematodes causing onchocerciasis in Africa and Central America. The work of Blacklock (1926a, b, 1927) incriminated S. damnosum as the vector of this parasite in Africa. Dry (1921) a few years before had associatedskin lesionsin Africans with the bites of S. neavei. Subsequently the importance of S. damnosum and S. neavei in the transmission of Onchocerca volvuZus in Africa was shown by several researchers (Hissette, 1932; Bryant, 1935; Gibbins, 1937; Wanson et al., 1945; Kirk, 1947; Lewis, 1948; Wanson and Lebied, 1948; Lewis, 1953; Crosskey, 1954a,b; Barnley, 1958; Lewis, 196Oa,b). Six to 13 days

SIMULIIDAE

449

are required for development of the larvae in the fly. The possibility of discovering other suitable vectors in Africa cannot be overlooked as Duke (1962a) found filarioid larvae in S. aureosimile, and suspectsit may be the host of 0. volvulus. Simulium damnosummay be a host for nonhuman filarioids also, as Crisp (1956) found microfilariae in specimens that fed on cattle. Clearly, as Nelson and Pester (1962) point out, caution is necessary in interpreting infection rates for filarioid nematodesin man-biting simuliids. In America, S. ochraceum, S. metallicurn, and S. callidum support the development of microfilariae of 0. volvulus (Strong et al., 1934; Dalmat, 1954) although S. ochraceum, because of its habits, is considered the important vector. Another species,S. amazonicum, is reported by Cerquiera in Brazil, as cited by Nelson and Pester (1962), to be host to Mansonella ozzardi, a human filarioid which develops also in Culicoides furens (Buckley, 1934). Gibson and Dalmat (1952) report development of Onchocerca in S. exiguum, S. veracruzanum, and S. haematopotum. Probably some of the filarioid larvae seen in these American flies originated from blood meals on horsesor cattle infected with filarioids, as Gibson (1955) observed skininhabiting microfilariae in many cattle and horses, and S. metallicurn and S. callidum feed by preference on these animals. Gibson and Dalmat (1952) believe that S. exiguum may be a natural vector of Onchocerca of cattle. Steward (1937) showed, and Gnedina (1950) confirmed, that 0. gutterosa is transmitted by S. ornatum in Britain. Dampf ( 1933) believed the microfilariae accumulated in the skin closeto the point where the fly fed. Strong et al. (1934) make a similar claim but de Hooghe (1934) disagrees.Van den Berghe (1941) comments on the different distribution of the lesionsof onchocerciasisin Guatemala and Africa. This difference results, he believes, from the vectors feeding on different parts of the body in the two countries. Ker-

450

PARASITOLOGICAL

shaw (1958) found the microfilariae of 0. volvulus concentrated most in the skin of those parts of the body bitten most frequently. The survival of S. damnosum is apparently not altered significantly by developing larvae of 0. voEvuZus (Kershaw, 1958; Duke, 1962~) unless there are more than 20 per fly, although infection may limit the flight range. Strong et aZ. (1934) considered it unlikely that onchocerciasis would be spread to distant places by S. ochraceum, S. metallicurn, and S. callidum. Button (1952) and Brown et al. (1956) observed simuliids feeding on the ear of a rabbit and wondered if they might be vectors of myxomatosis. Dyce and Lee (1962) took two species of simuliids from rabbits with cone traps; precipitin tests indicated the flies had fed on rabbits. Ratcliffe (1955), too, suspected simuliids might be vectors, and Lee et a2. (1957) state that Mykytowycz (1957) implicated S. melatum as a vector. Georgevitch (1909) described Crithidia simuliae in S. columbaczense in Europe, and Jobbins-Pomeroy (1916) reported the same species from S. venustum in the United States. Conceivably, in view of the work of Bennett (1961), these crithidia could be the intermediate stages of trypanosomes of birds, as every species of simuliid tested thus far by Bennett has proven a suitable host for an avian trypanosome. It would be of interest to examine simuliids in Africa and elsewhere for flagellates and transfer these to birds and mammals to see if trypanosomes developed from them. The tendency of flies to expel fluid from the rectum while taking a blood meal presumably favors transmission of avian trypanosomes, although proof of their mode of entry to a host is lacking. The role of simuliids in transmitting other avian blood parasites has been the subject of several recent researches. Walker (1927) noted mortality in goslings and attributed it to the black fly, S. bracteatum, which Shewell (1955) later identified as S. rugglesi. This was

REVIEWS

followed by the work of Skidmore (1932), Twinn (1933), O’Roke (1934), Johnson et al. (1938)) Underhill (1944)) Fallis et al. (1951, 1956, 1961, 1962), Jones and Richey (1956), and Wehr (1962), which established various species of simuliids as hosts and vectors of species of Leucocytozoon which cause disease and mortality in ducks, geese, turkeys, and possibly other kinds of birds. Anderson’s discovery (1956) that certain simuliids are hosts for a filarioid nematode of ducks prompts speculation that simuliids are hosts for other filarioids of birds also. His observations are of particular interest as he found worms developed in S. venusturn as well as in the ornithophilic fly, S. rugglesi. These researches revealed noticeable differences in feeding preferences of vectors and the importance of these in the maintenance of parasites. The possibility of ornithophilic simuliids serving as vectors of viruses should not be overlooked in view of recent work by Anderson et al. (1961)) who isolated EE virus from a pool of S. meridionale. V.

BITING

SITES

Simulium damnosum feeds especially on the lower part of man, usually below the knees (King, 1908; Blacklock, 1927; Bryant, 1935; Gibbins, 1937; Bequaert, 1938; Lewis, 1953; Crisp, 1956; Hocking and Hocking, 1962) although Wellman (1908) remarks, “it crawls up one’s neck and down one’s sleeves and bites visciously . . . ,” but does not mention attack on the ankles. Van den Berghe (1941) noticed that S. damnosum seldom bit children standing on a table 2-3 feet above the ground, while those children nearby on the ground were bitten on the legs and ankles. If the children squatted, all parts of the body including the face were bitten. Blacklock (1926a) reported 80% of the bites by the species were below the knee but said the loins and buttocks were attacked if the body was in a squatting position. Crosskey (1955) states the legs were still preferred even when

FEEDING

BEHAVIOR

OF

a man was lying down. Austrosimulium furiosum (Lee et al., 1957) and S. aureosimile (Duke, 1926a) also bite man on the legs. Prosimulium hirtipes bites the upper part of the body (Jenkins, 1948). Simulium ornatum feeds on the nose, eyebrow, and hand of man (Edwards, 1920). Simulium griseicolle attacks the face and hands of man (Balfour, 1906), along the collar and hat band (Lewis, 1948), head and shoulders (King, 1923, as reported by Garside and Darling, 1952), or any part of man (de Meillon, 1930). The preferred site on birds is not given. Simulium neavei prefers the lower part of the body but will feed on the upper part if man is sitting (de Meillon, 1957). Brown (1960) observed 850/o of a sample of this species feeding on or below the knees. Strong et al. (1934) found that S. ochraceum, S. metal&cum, and S. callidum fed on exposed parts of man but did not crawl beneath the clothing. Dalmat (1954, 1955), in more extensive observations, concluded that S. ochraceum preferred the upper body, but it bit lower if the upper part was protected. Conversely, S. metallicum and S. callidum preferred the lower part, but if it was covered they would bite the upper part. Crosskey (1959a) reports S. ochraceum feeding on the head, neck, and shoulders; S. cdlidum mostly on the legs; and S. m&zllicum indiscriminately. Lewis and Ibbfiez de Aldecoa ( 1962) found S. metallicum feeding more often below the knees while S. exiguum was taken from the upper as well as lower parts of the body. Simulium venustum feeds on the back of the neck and behind the ears more than on the forearms and ankles (Wolfe and Peterson, 1960), but it also feeds along the edges of the clothing. The same species is reported from the nose, ears, and eyes of beaver (Davies and Peterson, 1956). Simulium colzlmbaczense attacks several parts of cattIe (Ciurea and Dinulescu, 1924), although Leon (1909) and Schmidt (1916)) according to Baranov (1934), reported it

FEMALE

SIMULIIDAE

451

more often on hairless areas. Davies (1957b) states S. ornatum landed and fed most often on the under side of cattle, especially near the navel, Eight to 25% of the flies landing fed. Simulium arcticurn feeds on the less hairy parts of horses and cattle, under the belly, in the inguinal region, and just behind the front legs; few attack the face (Rempel and Arnason, 1947). Jones (1961) noticed 5’. vittatum feeding in the ears of sheep and S. piperi on the shorn belly. McCarthy (1961) calls attention to the attack of Austrosimulium pestilens around the face of kangaroos and wallabies, causing obstruction of vision that indirectly causes death. Davies and Peterson (1956) quote Knowlton and Rowe (1934), who took many S. vittatum from the ear of a horse. Teskey (1960) found it feeding on the inner ear of cattle. Knowlton and Maddock (1944), as stated by Peterson (1959a), collected S. arcticum and a few S. vittatum from the head, neck, shoulders, back, front legs, brisket, underbelly, and ears of horsesin Utah. Underhill (1939) noted S. slossonaefeeding on the head and neck of turkeys. Dem’yanchenko (1960) observed most Schoenbaueria pusilla alight on the abdomen of cattle and fewer on the limbs and udder. Breev (1950) observed more simuliids alighting on the belly and legs of reindeer, where there is lesshair than elsewhere. He concluded, from observations on a model and on living animals, that simuIiids preferred the shaded part of the animal and that visual stimuli were the important factors in attraction. Zahar (1951) refers to the attack of several specieson the under side of horses. Fredeen’s ( 1961) collections of S. arcticum in a silhouette trap supports this view, as he found flies were attracted to the darkened interior of the trap, although temperature of the trap may have been a factor also. Wenk and SchlGrer (1963) made interesting observations on the attacking behavior of Wilhelmia equina, W. salopiensis,Boophtora erythrocephala, and Eusimulium latipes.

4.52

PARASITOLOGICAL

The first two species feed on the ears of the horse and cow but the third on the ventral surface only. The flies showed a similar attacking behavior to a moving silhouette trap of a horse. The preference of the flies for different parts of the body appears related to mating habits. Mating of W. equina takes place as the flies approach the ears, but mating of W. salopiensis and B. erythrocephala takes place some distance away. These three flies and Eusimulium Eatipes distinguished between silhouette traps of a horse and a crow that were placed 3-5 meters apart. Among the ornithophilic species, Crtephia ornithoph&a feeds around the anus and the heels (Bennett, 1960), and S. euryadminiculum on the head and neck of loons (Lowther, 1962). Simulium rugglesi approaches the shaded ventral side of ducks and lands at the base of the legs and on the breast (Anderson and DeFoliart, 1961). Interesting observations by Lowther (1962), subsequently extended by Davies et al. (1962), indicate that odor is especially important in attracting S. euryadminiculum to the common loon. Lowther took hundreds of engorged specimens from the head and neck of the bird. Flies continued to land on the skin after it was taken from a bird, even after washing the skin in Varsol to clean the feathers. Some of the attractable material was apparently dissolved in the Varsol, for many flies landed on the rock on which the Varsol was poured after it was used to wash the skin. Observations by Davies and Peterson (1957) of many S. euryadminiculqqum over water are of interest in light of the feeding preference suggested by Lowther’s observations. The importance of odors is shown also by work of Davis and James ( 1957)) who collected S. vittatum in traps baited with minced beef that was allowed to putrefy. Carlsson (1962), in an extensive paper on Scandinavian black flies, noted that males of C. tide&n&urn were attracted to cuprisite. Clearly, various sites are selected by dif-

REVIEWS

ferent flies. The selection probably results from the interaction of several factors, namely temperature, light, odor, and appearance, the dominance of any one of which may vary from species to species and throughout the biting cycle. The relative importance of each factor to different species should be investigated. VI.

BITING

ACTIVITIES

Leon (1909) described the mouth parts and associated muscIes and their action of females of S. pus&m and noted similarities to descriptions for S. reptans given by Becker in 1882. Emery (1913) and Hungerford (1913), as cited by Smart (1935), described the anatomy of S. vittatum. Smart gave a detailed description of the mouth parts of S. ornutum. Cameron (1922) described the morphology of S. arcticum. Gibbons (1938) described and commented on the function of the mouth parts of S. damnosum. The scissor-like action of the mandibles snip the skin and permit the insertion of the maxillae that presumably tear the tissue apart to enlarge the wound. The recurved teeth on the maxillae, operated more or less vertically by protractor and retractor muscles, tear at the edge of the wound rather than scratching the surface. Blacklock’s (1926b) observation of cellular elements in specimens of Simulium, killed while biting, support the view that destruction of the tissue occurs while the fly is feeding. The puncture is enlarged sufficiently to allow the mouth parts to reach the blood. Cragg (1913) believes, as stated by Gibbins (1938), that the labrum-epipharynx is held in position at a suitable depth by the chitinized curved teeth that are bent upward like a hook on the distal end of the labrum. He suggests that the spines at the apex of the labrum-epipharynx and hypopharynx act as a sieve to prevent large particles entering the food channel. Gibbons states they may also trap some microfilariae ingested by the fly. Wenk (1962) says the mandibles, maxillae, and hypo-

FEEDING

BEHAVIOR

OF

pharynx of Wilhelmia equinu penetrate 120150 p into the tissues and perhaps more by opening the wound. The activity of flies after landing on a suitable host and immediately before feeding varies with the species. King (1908)) Austen (1909), and Lewis (1953) state that S. damnosum often moves about over the skin, patting it with the forelegs before beginning to feed. Marr (1962) noted that more caged S. damnosum fed when the flies were relatively inactive. He noted, too, a delay between landing and feeding and thought it indicative of some stimulus by the host. Stokes (1914) refers to the hurried movement of S. venusturn after alighting, the constant movements of the front legs, the rapid insertion of the mouth parts, and their tenacious attachment to the host once they are inserted. Blacklock (1926a) observed that S. damnosum was not easily disturbed once feeding began. It remained attached to the leg of a man even when the leg was immersed in water. One fly completed its meal under water, came to the surface, and flew away. Others remained attached until the leg was removed from water. The head of the fly was close to the skin, and the abdomen was raised above the surface during feeding. Bennett (1960) found that several ornithophilic species are not easily dislodged from their hosts. Rempel and Arnason (1947) reported similar observations for S. arcticurn. The effects of the bite, whether by the same or different species, undoubtedly differ from host to host (Stokes, 1914). King (1908) refers to the irritation and swelling resulting from the bite of S. damnosum and the trickle of blood that oozes from the wound. In discussing the same species Wellman (1908) says, “This tiny fly is possibly one of the most successful destroyers of patience, and provokers of profanity in the colony.” Following the bite, a red weal develops which itches and persists for some time. It is of interest that no reference is made to feeding on the

FEMALE

SIMULIIDAE

453

ankles, which, according to later investigators, are a favorite site. Austen (1909) remarks on the severity of the bite, the itching that follows, and the formation of a drop of blood at the site of the bite. Bryant (1935) says the bite of S. damnosum is not felt immediately, which supports Leon’s contention (1909) that the saliva of simuliids is mildly narcotic. Bryant noted formation of a weal that itched intensely about 24 hours following a bite. In some individuals “the face becomes swollen, the eyelids edematous, and the conjunctiva bloodshot.” Stokes (1914)) observing S. venustum, confirmed an observation of Megnin in 1895 that flies tend to bite near the point where other flies have fed, or are feeding. Stokes gives a detailed account of the reactions to the bite of S. venustum, which initially is painless. A hyperemic areola forms around the point where the tly is attached. A small hemorrhage of varying extent occurs at the puncture wound following withdrawal of the proboscis. The hemorrhage is beneath the skin as well as external, thus causing an enchymosis that may be a mere pinpoint or several millimeters in diameter. The cycle of changes in the skin following a bite may extend over several days and depends on the individual, his susceptibility, and past history. Adenopathy is often “a unique and distinctive feature of the clinical picture” (Stokes, 1914). The histological appearance of the lesion plus the possibility of producing a lesion by injecting alcohol-preserved flies suggests that it results from a toxin injected by the fly. The principal change following a bite occurs in the corium. A vascular dilation, perivascular edema, and a polymorphous perivascular infiltration result. A local eosinophilia and an increase in mast and small round cells are notable features. A localized edema and swelling of papillary bodies occurs. Stokes’ experimental studies indicated, but did not define, a toxic agent in the head and thorax. Other recent studies concerned with reactions to bites include those by Gud-

4.54

PARASITOLOGICAL

gel and Grauer (1954) and McKiel and West (1961). Frohne and Sleeper (1951) stated that a swelling appears at the site of the bite within 30 minutes but disappears in less than 24 hours, and that no pain is associated with it. By way of contrast S. wellmani produces large weals that irritate for days (de Meillon, 1930). Hemorrhages do not occur around the puncture wounds of some species, e.g., S. griseicolle, but other species including some that feed on birds do cause bleeding and inflammation that may persist for 2 or 3 days (Bennett, 1960). Simulium columbaczense causes inflammation and lowering of temperature in man, as well as a high mortality rate in cattle and to a lesser extent in horses, pigs, sheep, and goats. Leon (1909), Schmidt (1916), and Ciurea and Dinulescu (1924) call attention to the labored breathing, stumbling gait, rapid pulse, painful swelling, and often rapid death in cattle bitten by this fly. Bang (1918) reports similarly from Sweden, as does Miessner (1916) from Germany (according to de Meil-

Time

Fly S. damnosum

S. ochraceum S. metallicurn S. callidum

S. veracrusanum S. exiguum S. haematopotum

S. columbaczense S. nigroparvum S. griseicolle S. venusturn

P. hirtipes S. rugglesi

Taken

by

REVIEWS

lon, 1930). They believe death is due to a poison from the salivary glands. Certainly, Georgevitch (1923) found an extract from the heads of flies that was virulent to mice, guinea pigs, and rabbits. Animals surviving an initial dose of such an extract were more tolerant to subsequent injections. Dem’yanchenko (1960) concluded from experiments that a toxin is present in the thorax, including the salivary glands, of Simulium (Schiinbaueriu) pusilla. The time taken for engorgement differs as much among individuals of the same species as among different species (Table II) and probably depends on the host and the site selected. For example, Lewis (1948) reports that Wanson and Fain found that S. griseicolle fed slowly on man, but Roubaud and Grenier noticed that it fed rapidly on birds, which are apparently the preferred host. Crosskey’s observations (1962) on S. damnosum suggested that “. , . feeding may be significantly prolonged on subjects with atrophic skin changes.” Loewenthal (1943) asso-

TABLE II Female Simuliids to Engorge

Approximate time (minutes) 23 1s-5 4-6 0.5-18.5 1.5-13 1-19 1-31 l-15 4-9 4-5 z-5.5 3-7 5 2-3 4-16 3.5-4 3-7 l-10 1-8

4.5-12

witk

Blood

Authority King, 1908 Blacklock, 1926a Crosskey, 19.55 Crosskey, 1962 Marr, 1962 Dalmat, 1955 Dalmat, 195.5 Dalmat, 1955 Dalmat, 1955 Dalmat, 1955 Lewis and Ibafiez de Aldecoa, 1962 Dalmat, 1955 Ciurea and Dinulescu, 1924 Underhill, 1940 Lewis, 1948 Hocking and Pickering, 1954 Davies and Peterson, 1956 Wolfe and Peterson, 1960 Daviesand Peterson, 1956 Faliis and Smith (unpublished)

FEEDING BEHAVIOR OF FEMALE

ciated skin changes with infection with Onchocerca rather than with repeated bites of the fly. Hocking and Pickering (1954) have a similar observation on S. venustum, which took less time to penetrate the skin of a dog than a man. Some ornithophilic flies are known to remain on a bird for 4 hours (Bennett, 1960) but the proportion of the time spent in feeding is unknown. Speciessuch as S. metallicurn and S. callidum may land several times and move about the skin before penetrating it with their mouth parts, but S. ochraceum movesabout on the skin very little before piercing it and taking its meal. Once feeding begins the latter speciesis interrupted less easily than either of the other two (Dalmat, 1955). VII.

SIZE AND DIGESTION

OF BLOOD MEAL

The size of the blood meal has been determined for a few specieseither by weighing them before and after feeding or by use of radioisotopes in the blood of the animals on which the flies fed. The amount of blood ingested is undoubtedly larger than indicated as neither method considers the excretion of fluid that may occur during or just after feeding (Crosskey, 1962; Bennett, 1963). The isotope method is therefore likely to give the higher value. Crosskey (1962), using the gravimetric method, found that S. damnosum ingested slightly more than its own weight of blood, namely 1.08 mg = 1.02 cm if the specific gravity of human blood is 1.06. He obtained no indication that flies feeding slowly took more blood than those engorging rapidly. Crosskey (1958) noted differences in the mean weights of S. damnosum feeding at different times during the day and stressed the necessity for comparing the fed and unfed weights of flies biting at the same period. Anderson et a2. (1962) report an average of 1.4 mg per fly of blood ingestedby S. rugglesi. Bennett (1963), using P32 in the blood of ducks and a banty hen, and collecting engorged flies from them, calculated the amounts

SIMULIIDAE

455

of blood taken from different flies as follows (volume in mm3) : Prosimulium decemarticuDatum, 2.2 (1.1-3.8); S. aureum, 2.9 (1.84.8); S. croxtoni, 3.3 (2.3-5.2); S. latipes, 2.7 (1.9-4.1); S. quebecense,2.1 (1.1-3.0); and S. rugglesi, 1.9 (053.6). It does not follow necessarily that the flies that engorge the most blood ingest the most parasites from a particular host or are the most suitable host for the parasites.The problem requires further attention, for Jordan and Goatly (1962) found that the uptake of microfilariae of Wuchereria bancrofti by Culex fatigans was not related to the weight of the blood meal. Lewis (1953) reported the formation of a peritrophic membrane around the blood meal of S. damnosumand noted the membrane did not form after ingestion of a sugar solution. The membranewas well defined s hour after a meal and had a laminated appearance in 1 hour. The lamination results presumably from successivelayers of material secreted by the midgut. epithelium. The membrane after 90 minutes was 63 p thick in places. He thought it possibly thicker after a small meal than after a large one. The membrane broke in 48 hours in flies kept at 23”-25°C. Bennett and Fallis (unpublished data) observed a peritrophic membraneof varying thickness in all speciesof flies, viz., S. rugglesi, S. anatinum, S. aureum, S. latipes, S. quebecense,S. croxtoni, P. decemarticulatum, C. ornithophilia, S. venustum, and P. hirtipes, which they used in their studies of the transmission of blood parasites. No membrane, or only a delicate one, was noticed in S. metallicurn 4 hours after feeding (Lewis and Garnham, 1960), and the membrane in S. neavei was only 7 p in thickness 7 hours after feeding (Lewis, 1960a). No membrane was noticed by Cameron (1922) in S. arcticurn. The presence of a membrane may curtail the movement of parasites to the stomach wall (Lewis, 1953; Fallis and Bennett, 1961). Blacklock (1926a) noticed that the blood formed a globular mass in the stomach and retained this

456

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shape. Bennett and Fallis have similar observations (unpublished) and noted that digestion takes place from outside of the mass. The cells in the center of the mass may retain their shape and structure for 48 hours or more although the surrounding cells have broken down. Temperature influences the rate of digestion. Downe (1957) noticed digestion was completed in a few specimens of S. venusturn in less than 60 hours at 67”-70°F and 7580% relative humidity. Digestion in S. vugglesi was completed in 4-6 days at 67”-70°F (Bennett and Fallis, unpublished observations) , VIII. LONGEVITY The lifespan and number of blood meals taken by individual flies of various species could affect significantly the transmission of parasites. Knowledge of the longevity of several species is derived from observations on adults after the last known emergence from breeding sites, or on adults held in captivity. Blacklock (1926a), Wanson et al. (1945), and Lewis (1953) kept S. damnosum for 19, 11, and 10 days, respectively, but Lewis believes some may live for weeks even during the dry season. He noticed (1957) they were suddenly common in the Sudan when the rivers began to flow after being dry for 14 weeks, although it is uncertain the flies had survived throughout this dry period. Longevity of 5’. damnosum was not decreased by infection with Onchocerca unless more than 20 microfilariae were ingested (Duke, 1926b,c). This is at variance with the report of Lebied (1950), as cited by Dalmat (1955), who believed the developing larvae in the thoracic muscles restricted the flight of the flies. Dalmat (1955), too, from observations on infected Guatemalan flies, was of the opinion that infection with Onchocerca reduced their flight and longevity. Some S. vittatum and S. jenningsi survived 18 days on a diet of sugar solution (Wu, 1931). Bequaert (1938) kept a few S. metalZicum for 6 days. Davies (1953) kept S.

REVIEWS

venustum 2%63 days in the laboratory, and believes it lives 2 or 3 weeks in nature. Baranov (1934) kept S. columbaczense for 10-12 days in the laboratory. Friederichs (1921b) kept S. muculatum on sugar solution for 23 days. Dalmat (1952) gives the first experimental data on longevity. Using dyes as marking techniques, he recovered a specimen of S. metallicurn that lived 85 days, one S. ocbaceum that lived 27 days, and one S. callidum that lived 20 days, As the ages of the flies were unknown at the time of marking, it is reasonable to assume that some flies survived for longer periods. Potentially, therefore, these flies with an extensive flight range and long lives could be of parasites. Bennett important vectors (1963), using radioactive phosphorus, showed that some S. vugglesi lived at least 28 days and fed at 5-7-day intervals. Previously, Fallis et al. (1956) had kept some of the same species for 18 days in the laboratory. Obviously, therefore, this fly could be an efficient vector. Wolfe and Peterson (1959) collected P. hirtipes 30 days after the last known emergence. They believe that S. venustum survives equally well. Recovery of the ornithophilic flies, C. ornithophitia and S. anatinum, for rather short periods in late May (Bennett, 1960) suggests a relatively short survival. Some of the former live long enough to take at least two blood meals, and the latter may take three or more. IX.

FLIGHT

RANGE

The epizootiology and extent of spread of diseases transmitted by black flies, and the geographical distribution of the flies, will be affected by their flight range. Indeed the general activity may determine partially the biting activity. Most reports of such movements are based on observations of flies in relation to their known breeding places, although all of these in particular localities were not necessarily known at the time of the reports. Dalmat (1950) was the first to report

FEEDING

BEHAVIOR

OF

experimental studies to determine the flight range. Balfour (1906) says that S. damnosum will travel miles from a river, but S. griseicoUe is not found more than one-half mile from it (de Meillon, 1930; Edwards et al., 1939). Hargreaves (1925) records movements of 25 miles for S. damnosum. Gibbins ( 1937) gives the distance as 40-50 miles from the nearest breeding site in Uganda. Lewis (1957) noted the species 20km from rivers in the Sudan. He believes it moves 6-12 miles commonly but rarely 18 miles. Vegetation appears to restrict movement and the flight range may be increased by bush clearings (Lewis, 196Ob, 1962), thereby extending the range for transmission of disease. Lebied (1950), from de Meillon (1957), suggests microfilariae developing in the thoracic muscles of S. damnosum may impair its flight and explain why onchocerciasis in Africa is often confined to small foci. However, Lewis has found flies 12 miles from the nearest breeding site. Crosskey, too (1955)) noted infected flies 10 miles from the breeding site, and they were common 3-7 miles from it. Wanson and Henrard (1945), from Nicholson and Mickel (1950), give the range as 9-12 miles. Control measures directed against S. damnosum in the Congo by Wanson (1950) indicate that it may move up to 20 miles from the breeding site. Absence of flies does not mean necessarily that they cannot, or do not, move particular distances as their movement may be curtailed by the type of country (Lewis, 1953) or they may be carried for miles by winds. Glick (1939), using adhesive screens on aeroplanes, found some at 5000 feet altitude. Crisp (1956) captured S. damnosum 600 feet above a breeding site and noted transmission of parasites by it 5 miles from a river. McMahon (1940) found S. neavei 700 yards from a stream and thinks this approaches the maximum which may be higher in dull weather. Kirk (1947) found the same species biting 1000 yards from a river. Barnley (1958), from indirect evidence

FEMALE

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457

on the distribution of onchocerciasis in Uganda, implies that the vector may move 10 miles. Dalmat (1950), using aniline dye to mark vectors of 0. VOZVUZUSin Guatemala, concluded that S. metallicurn might fly 7.4 miles and S. callidum and S. ochraceum 4-6 miles; other species flew shorter distances. He found a single specimen of S. metallicurn that had moved 9.7 miles. Dalmat and Gibson (1952) found an S. ochraceum that moved 2.9 miles in 2-3 days and one S. callidum that moved 2.7 miles in 3-4 days. Other kinds of flies may range over greater distances. Cameron (1922) considered wind important in dissemination of S. arcticurn for 12-15 miles. Rempel and Arnason ( 1947) report a 60-mile range for this fly, and Fredeen (1958) thinks it may move 140 miles. He gave a range of 10 miles for S. venustum. Underhill (1939) gave a range of 10-15 miles for S. jenningsi and later (1944) stated it was 20-30 miles. Ogata et al. (1956) found S. aokii 1000 meters from the nearest breeding site. Bennett (1963) found S. rugglesi moved 2-6 miles. Hocking and Richards (1952) got indirect evidence, by clearing larvae from certain streams, that P. hirtipes may move less than 2 miles during a season and that S. venustum may move as much as 6 miles. Peterson and Wolfe (1958) and Wolfe and Peterson (1959) took S. venustum and P. hirtipes in forested areas 5 miles from the nearest breeding site and believed they would travel further in open areas. Hocking (1953)) in an experimental study of the range and speed of flight of insects, calculated the maximum range of flight of an unfed S. venustum in still air as 116 km, and as 104 km for S. vittatum. He observed also that S. venustum and S. vittatum would fly continuously at 55°F and intermittently down to 48°F. Malloch (1914) believes S. forbesi travels at least 5 miles. Baranov (1937) concluded that S. columbaczense spreads out from emergence sites and moves by active and passive migration high in the air as far

458

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as 60-160 miles from the Danube. Serious outbreaks of this fly in Yugoslavia are associated with low, warm water in the Danube; high air temperature and pressure; cloudy, calm weather; and lack of rain. X.

FEEDING

AND

CLIMATE

Knowledge of the relation of simuliid feeding to topography, weather, and climate is based on general observations on several species and limited quantitative data for a few. Simulium damnosum females bite mostly in the early morning and before dusk, but feeding continues throughout the day in dull weather (Blacklock, 1926a, 1927; Van den Berghe, 1941). Lewis (1953) noticed they bit man more in the open than in the woods. Dense vegetation seemed to restrict their movements (Lewis, 1957, 1960a). Clearing land may result in an extension of the range of flight. Lewis found them biting after sunset in the Sudan. They fed also in light rain and bright sunshine. In colder parts of the country biting did not begin until after 10 A.M., but in other places it abated after 10 A.M. and was most intense after 3.30 P.M. (Hocking and Hocking, 1962). Blacklock (1926a) noted that man was seldom bit while bathing outdoors but was attacked ferociously on the banks. Moderate shade and rather open country is favored. de Meillon (1930) states that Hargreaves ( 192 5) found S. damnosum was most prevalent in the driest months in Uganda and was common in dense vegetation that affords shelter from wind. Perhaps lower light intensity in such a situation is important also. Hissette (1932) found S. damnosum numerous in cultivated fields in wooded valleys, and not on crests of ravines unless a nearby forest provided shade, in which case the site was favorable for a high incidence of infection with Onchocerca. Abreu (1960) studied the activity of S. damnosum in relation to temperature. Activity was noted at 27’-30°C but not below 18’C or above 4O’C. The flies were active early in the morning if

REVIEWS

the temperature was favorable. Activity stopped abrupty at the beginning of the tropical night. A morning and afternoon peak of activity was noticed when temperature was high during midday. Fain (1950) found S. damnosum feeding on man at altitudes of 2500-3000 feet but not above 5000 feet. He believes it is adapted for feeding on animals other than man at higher altitudes. Crisp (1956) remarks that feeding of S. damnosum increases with falling pressure. Among the other vectors of Onchocerca, Dry (1921) noted S. neavei was especially active in the afternoon and was found mostly in dense forest. McMahon (1947) refers to more activity on dull days although feeding occurs in sunlight if there is shade nearby. Lewis (1960a) noted peaks of biting activity in the morning and afternoon and less at noon if the temperature was higher. Strong et al. (1934) observed S. ochraceum, S. metallicum, and S. callidum feeding from 6 A.M. to 6 P.M. in Guatemala at elevations of 25005000 feet. Dalmat (19.54, 1955), from extensive studies of three species, concluded that S. ochraceum prefers more shade than S. metallicurn or S. callidum and is more active if humidity is high. He found S. ochraceum fed during the day or night and even inside buildings, but most fed between 8 A.M. and 10 A.M. Optimum temperature was 34”-35°C for S. ochraceum and slightly lower for the other two species. Simulium callidum fed when the temperature was below 13°C and continued until 30°C in the sun and 34°C in the shade. It did not feed above 34°C. Simulium ochraceum and S. callidum are known to bite at heights up to 112 feet above ground. Simulium griseicolle feeds from sunrise to sunset although more so at sunrise and sunset (Balfour, 1906; King, 1908; Austen, 1909). Lewis (1957) notes the species is a pest in northern Sudan but not in the south and wonders if it is stimulated by the extreme dryness prevailing in the north. Abreu (1961) states that S. albivirgulatum is active through-

FEEDING

BEHAVIOR

out the day in Africa and that maximum activity was noted between 4 and 5.30 P.M. Simulium aureosimile and S. adersi bite at sunrise and sunset (Gibbins, 1934; Duke, 1962a), and 5’. antillarum bites in open country and especially in the morning in Guadeloupe (Floch and Abonnenc, 1946a). Root (1922) says that S. quadrivittatum feeds in hot sunlight in the middle of the day in Puerto Rico. Simulium buissoni bites fiercely from sunrise to sunset on the Marquesas Islands (Mumford and Adamson, 1934). The Goulbatz fly, S. columbaczense, is said to attack until 10 A.M. and for 4 hours in the evening, but not during the heat of the day (Ciurea and Dinulescu, 1924; Baranov, 1934). The latter author says some females lose their positive phototropism, enter buildings, and attack man and animals after dark. Ionescu-Braila and Dinulescu (1939) concluded that attacks by this fly were not related closely to temperature and rainfall although prevailing dryness in April favored the spread and persistence of the fly in some localities. Underhill (1939, 1940) noted more S. nigroparvum feeding in mid-morning and mid-afternoon. Eighty-five % of his sample fed between 75” and 85°F and few fed below 70°F or above 90°F. Ogata (1954) observed that activity of S. venustum in Japan was inhibited below 9 “C, but above 13’C illumination became the controlling factor. High illumination suppressed activity; as light decreased in the afternoon the activity increased providing the temperature was satisfactory. Usova and Kulokiva (1958) expressed a similar view which explains the tendency for feeding in the morning and evening rather than during midday. Davies (1952), working with this species in Canada, reported that more flies landed on man when the temperature was 55”-65°F. Edwards et al. (1939), citing Rubtzov, state that optimum temperature for activity of black flies is 19’-20°C with a range of 14’-22°C. Biting occurred in light as low as 1 foot-candle. Rempel and

OF

FEMALE

SIMULIIDAE

459

Arnason (1947) found S. arcticurn most active on hot, sunny days, during daylight. Feeding was noticed once in a well-lighted barn. Twinn (1952) noted a decrease of biting activity on man as temperature declined; none occurred below 50’F and after dark. Berzina (1953) reported that the optimum temperature for feeding varied with the species, season, and between the tropics and the arctic. Feeding of S. erythrocephalum was most intense at 1.5”-27°C in the Volga delta and at 12’-27’C for S. venustum, S. ornatum, and S. pusillum in the arctic. Maximum activity of S. pusillum began at 12’C and of S. venustum at 15’C. Biting occurred at temperatures as low as 6°C in the arctic and 9°C at the Volga delta. The optimum light intensity was more than twice as high in the arctic as in the south. Zahar (1951) reported feeding by S. ornatum throughout the day in Scotland and stated it was most intense when the relative humidity was high and the temperature was loo-26.7”C. Edwards (1920) found it fed especially “on warm, rather still days, chiefly in the afternoon sun.” Several reports state that flies are active throughout the day if it is cloudy, and that they prefer the shaded part of the host on which to feed (Edwards et al., 1939; Breev, 1950; Davies, 1952; Ogata, 1954; Peterson, 1956; Wolfe and Peterson, 1960). The preference for feeding in the evening may be associated with the prevailing lower light intensity (Jenkins, 1948; Davies, 1955; Peterson and Wolfe, 1958; Anderson and De Foliart, 1961). The tendency for fair people to be bitten more than dark people in the early morning and evening and for darker people to be bitten more during the day suggests the effect of light on feeding (Wolfe and Peterson, 1960). These authors believe changing light is a major factor controlling diurnal rhythm. Available data indicate the cessation of feeding of simuliids with darkness although there are exceptions. Peterson (1956) recorded biting of some species at night at high

460

PARASITOLOGICAL

altitudes in Utah. Bennett and Fallis (unpublished observations) noted that engorged S. aureum and Cnephia mnithophilia came off birds as late as 9 P.M. E.S.T. in Algonquin Park. Presumably these flies were on the birds before dark as in repeated trials no proof of them going to the birds after dark was obtained. Bennett (1960) recovered more flies from woodland birds late in the evening than earlier, whereas most S. rugglesi were taken from ducks between 4 and 7 P.M. E.S.T. Collections of simuliids in rather high numbers in light traps in Scotland by Davies and Williams (1962) and by Frost (1949) and Fox (1953), as cited by Davies and Williams, suggest that some species show more crepuscular or night activity than suspected hitherto. It would be of interest to know whether the flies entered the light traps throughout the dark period or more at the beginning and end of it. Activity and feeding is interrupted in strong winds (Edwards, 1920; Edwards et al., 1939; Underhill, 1940, 1944; Ogata, 1954; Peterson and Wolfe, 1958; Wolfe and Peterson, 1960; Anderson and DeFoliart, 1961). Underhill (1940) noticed little feeding of S. nigroparvum below 50 and above 80% RH.* Davies (1952) observed less activity of S. venustum below 40% RH, especially if the temperature was above 80°F. Wolfe and Peterson (1960) reported feeding of S. venustum at 29-95% RH and a noticeable decrease if it was raining. Rubtzov (1939) found most activity at 75-9070 RH. Anderson and DeFoliart (1961) report little effect of humidity on the ornithophilic species studied. Underhill (1939, 1940) found S. nigroparvum feeding at a 4000 feet altitude and reported an increase with a drop in barometric pressure, especially if the humidity was high; the more rapid the change the greater the effect. Few engorged flies were taken when the pressure was high. Peterson (1956, 1959a) reports field observations on biting of some * RH = relative humidity.

REVIEWS

flies at different altitudes in Utah. C. mutata, S. arcticum, S. tuberosum, S. hunteri, and S. vittatum seldombit man below 1000 feeet, although S. vittatum is known to bite cattle and horsesfreely at lower altitudes. Climatic influences on feeding may depend on factors associatedwith individual flies, as Davies (1955, 1957a) found more old S. ornatum fed during the late evening than did young individuals. Lewis (1960a,b) noted an increase in the number of parous females of S. damnosumand S. neavei among those flies feeding at midday. Rubtzov (1951), from a study of simuliids in Central Asia and farther north, found the flies were more aggressivein the north where he thought their need for a blood meal was more acute. Sailer (1953) concluded from observations of the samespecies in Alaska that feeding behavior differed in the summer and autumn. He noticed also that S. venustum was biting man in one locality but not in another. He related this to the absence of humans in the one locality and their availability as hosts for at least 700 years in the other locality. XI.

SUMMARY

Few generalizations on feeding behavior of simuliids are warranted becauseof insufficient data for most speciesand conflicting reports on some. Some, especially ornithophilic species, show definite feeding preferences; others have more “catholic tastes.” These feeding preferences could be important in the transmission of parasites and could affect their prevalence and distribution as much as the specificity of the parasites for particular flies. The frequency of feeding, longevity, and flight range of the flies as well as the size and rate of digestion of the meal likewise determine their importance as vectors of parasites. Factors responsiblefor the attraction of flies to various animals are largely unknown. Odor appears especially significant but visual and tactile stimuli are almost certainly important. The dominanceof any one stimulus may vary

FEEDING

BEHAVIOR

throughout the feeding cycle and differ from fly to fly. The nature of the bite appears similar for all species although there are noticeable differences in the reactions to bites. Perhaps the reaction depends as much on the animal bitten as on the species of fly. Biting activity, although differing from species to species, is influenced by light intensity, temperature, barometric pressure, vegetation that provides shade that affects the light and temperature, and by the color and odor of the animal. Some of these factors may tend to attract flies to the animal and may be related only indirectly to biting. Experimental studies to evaluate the importance of these and other factors in the biting activity of all species of simuliids is needed. REFERENCES ABREU, M. M. M. DE ARAUJO. 1960. Contribuicao para o estudo dos Simuliidae de Angola (Diptera: Nematocera). Algunsdados sobre a sua ecologia, biologia e relacoes corn a epidemiologia da oncocercose. Anais do Znstituto de Medicina Tropical 17, 113-171. ABREU, M. M. M. DE AURAUJO. 1961. Simulideos angolanos (Diptera: Simuliidae). Anais do Instituto de Medic&a Tropical 18, 77-91. ABUSALIMOV, N. S. 1947. Blood-sucking midges of Azerbaijan. Veterinarija 7, 41-42 (in Russian), from Review of Applied Entomology (B) 26, 173 (1948). ANDERSON, J. R., AND DEFOLIART, G. R. 1961. Feeding behavior and host preferences of some black flies (Diptera: Simuliidae) in Wisconsin. Annals of Entomological Society of America 64, 716-729. ANDERSON, J. R., LEE, V. H., VADLAMUDI, S., l%~SON, R. P., AM) DEFOLIART, G. R. 1961. Isolation of eastern encephalitis virus from Diptera in Wisconsin. iUosquito News 21, 244-248. ANDERSON, J. R., TRAINER, D. O., AND DEFOLIART. G. R. 1962. Natural and experimental transmission of the waterfowl parasite, Levcocytozoon simondi M. and L. in Wisconsin. Zoonoses Research 1, 155-164. ANDERSON, J. R., AND VOSKUIL, G. H. 1963. A reduction in milk production caused by the feeding of black flies (Diptera: Simuliidae) on dairy cattle in California, with notes on the feeding activity on other animals. Mosquito News 23, 128-131.

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ANDERSON, R. C. 1956. The life cycle and seasonal transmission of Ornithofilaria fallisensis Anderson, a parasite of domestic and wild ducks. Canadian Journal of Zoology 34, 485-525. AUSTEN, E. E . 1906. “Illustrations of British Blood-Sucking Flies,” pp. l-74. British Museum, London. AUSTEN, E. E. 1909. “African Blood-Sucking Flies,” Chapter III (“Simuliidae”), pp. 23-35. British Museum (Natural History), London. AUSTEN, E. E. 1921. A contribution to knowledge of the blood-sucking Diptera of Palestine, other than Tabanidae. Bulletin of Entomological Research 12, 107-124. BALFOUR, A. 1906. Biting and noxious insects other than mosquitoes. Second Report of the Wellcome Research Laboratories Khartoum, pp. 29-50. BANG, B. 1918. Kvaegymg som Aarsag til Sygdom (Simuliids as a cause of disease). Maunedsshrift for Syrlaeger, Copenhagen 30, l-32, from Review of Applied Entomology (B) 7, 172 (1919). BARANOV, N. 1934. Golubacka musica u godini Simulium reptans columbacsense in the year 1934. Veterinaria Archiv Zagreb 4, 48 (in Serbian with Russian summary), from Review of Applied Entomology (B) 22, 203 (1934). BARANOV, N. 1935. K posnavanju golubafke mulicae II. (Contribution to the knowledge of Simulium reptans columbaczense.) Veterinaria Archiv 6, 58-140 (in Serbian), from Review of Applied Entomology (B) 23, 161-162 (1935). BARANOV, N. 1937. K posnavanju goluba?ke musice V. (Studij epidemiologije golubafke muSice na inveziji g. 1936). [Contribution to the knowledge of the Golubatz fly V. (Study of the epidemiology of the fly in 1936.)1 Veterinaria Archiv 7, 229-276 (in Serbian), from Review of Applied Entomology (B) 25, 249-250. BARNLEY, G. R. 1958. Control of Simulium vectors of onchocerciasis in Uganda. Proceedings of the Tenth International Congress of Entomology 2, 535-537. BENINC, A. L. 1924. Arbeiten Biologische Volga Station (Simuliids of the lower Volga) 7, 8489 (in Russian), from Review of Applied Entomology (B) 12, 140 (1924). BENNETT, G. F. 1960. On some ornithophilic bloodsucking Diptera in Algonquin Park, Ontario, Canada. Canadian Journal of Zoology 38, 377389. BENNETT, G. F. 1961. On the specificity and transmission of some avian trypanosomes. Canadian Journal of Zoology 39, 17-33. BENNETT, G. F. 1963. Use of Ps2 in the study of a population of Simulium rugglesi (Diptera:

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Simuliidae) in Algonquin Park, Ontario. Cafcadian Journal of Zoology 41, 831-840. BEQUAERT, J. 1938. The black flies or Simuliidae of the Belgian Congo. American Journal of Tropical Medicine Supplement 18, 116-138. BERZINA, A. N. 1953. Attack by simuliids on man in nature. Parazitologicheskii Sbornik, Akademiya Nauk S.S.S.R. Zoologicheskii Institut. 15, 353-385. B~AGI, F. F., Rum, R. F., TAY, J., AND PORTILLA, J. 1958. Simuliztm gonzalezi coma posible transmisor de la onocercosis. Medicina 38, 169-171, from Review of Applied Entomology (B) 50, 267 (1962). BLACKLOCK, D. B. 1926a. The development of Onchocerca volvulus in Simulium damnosum. Annals of Tropical Medicine and Parasitology 20, l-48. BLACKLOCK, D. B. 1926b. The further development of Onchocerca volvulus (Leuckart) in Simulium damnosum Theob. Annals of Tropical Medicine and Parasitology 20, 203-218. BLACKLOCK, D. B. 1927. The insect transmission of Onchocerca volvzdus (Leuckart, 1893), the cause of worm nodules in Africa. British Medical Journal 1, 129-133. BRADLEY, G. H. 1935. Notes on the Southern buffalo gnat Eusimulium pecuarum (Riley) (Diptera: Simuliidae). Proceedings of the Entomological Society of Washington 37, 60-64. BREEV, K. A. 1950. The behaviour of blood-sucking Diptera and Bot-Mes when attacking reindeer and the responsive reactions of reindeer. I. The behaviour of blood-sucking Diptera and Bot-flies when attacking reindeer. Parazitologicheskii Sbornik 12, 167-198 (in Russian), from Review of Applied Entomology (B) 42, 67-68 (1954). BROWN, P. W., ALLAN, R. M., AND SHANKS, P. L. 1956. Rabbits and myxomatosis in north-east Scotland. Scottish Agriculture 35, 204-207, from Review of Applied Entomology (B) 45, 166 (1957). BROWN, S. G. 1960. Observations on Simulium neavei Roubaud, with special reference to a focus of Onchocerciasis in the Belgian Congo. Bulletin of Entomological Research 51, 9-16. BRYANT, J. 1935. Endemic retino-choroiditis in the Anglo-Egyptian Sudan and its possible relationship to Onchocerca volvulus. Transactions of the Royal Society of Tropical Medicine and Hygiene 28, 523-532. BUCKLEY, J. J. C. 1934. On the development in Culicoides furens Poey, of Filaria (1Mansonella) ozzardi Manson 1897. JournaE of Helminthotogy 12, 99-118.

REVIEWS in relation J. A. 1952. The insect vector to myxomatosis in Australia. Journal Department of Agriculture West Australia 3, 819-821, 823, 825, 827-829; from Review of Applied Entomology (B) 42, 77 (1954). CAMERON, A. E. 1918. Some blood-sucking flies of Saskatchewan. Agricultural Gazette of Canada 5, 556-561, from Review of Applied Entomology (B) 6, 178-179 (1918). CAMERON, A. E. 1922. The morphology and biology of a Canadian cattle-infesting black fly, Simulium simile Mall. (Diptera: Simuliidae) . Dominion of Canada, Department of Agriculture Bulletin Number 5, I-26. Studies on Scandinavian black CARLSSON, G. 1962. flies. Opuscula Entomologica Supplementurn, Entomologiska Sallskapet, Lund, 279 pp. CNREA, J., AND DINULESCU, G. 1924. Ravages causes par la mouche de Goloubatz en Roumanie; ses attaques contre les animaux et contre l’homme. Annals of Tropical Medicine and Parasitology 18, 323-342. CRISP, G. 1956. “Simulium and Onchocerciasis in the Northern Territories of the Gold Coast,” 171 pp. London British Empire Society for the Blind, London; from Review of Applied Entomology (B) 45, 191 (1957). CROSSKEY, R. W. 1954a. Infection of Simulium damnosum with Onchocerca volvulus during the wet season in Northern Nigeria. Annals of Tropical Medicine and Parasitology 46, 152-159. CROSSKEY, R. W. 1954b. Onchocerciasis in Galma Valley Area, Northern Nigeria. West African Medical Journal 3, 75-79, from Review of Applied Entomology (B) 44, 137 (1956). CROSSKEY, R. W. 1955. Observations on the bionomics of adult Simulium damnosum Theobald (Diptera, Simuliidae) in Northern Nigeria. Annals of Tropical Medicine and Parasitology 49, 142-153. CROSSKEY, R. W. 1958. The body weight in unfed Simulium damnosum Theobald, and its relation to the time of biting, the fat body and age. Annals of Tropical Medicine and Parasitology 52, 149-157. CROSSKEY, R. W. 1959a. Aspects of black-fly control and entomology in the new world in relation to the Simulium problem in Nigeria. Bulletin of the World Health Organization 21, 727-736. CROSSKEY, R. W. 1959b. Personal communication. CROSSKEY, R. W. 1962. Observations on the uptake of human blood by Simulium damnosum: The engorgement time and size of the bloodmeal. Annals of Tropical Medicine and Parasitology 56, 141-148. BUTTON,

FEEDING BEHAVIOR OF FEMALE R. W., AND CROSSKEY, M. E. 1958. Filarial infection in Simulium griseicolle Becker. Nature 181, 713. DALIHAT, H. T. 1949. New species of Simuliidae (Diptera) from Guatemala. I. Annals of En-

CROSSKEY,

tomological

Society

of

America

1955. Behaviour of young and old of the black-fly, Simulium ornatum Mg. 176, 979-980. 1957a. A study of the blackfly Simulium ornatum Mg. (Diptera) with particular reference to its activity on grazing cattle. Bul-

DALMAT,

America

48, 537-545.

H. T. 1952. Longevity and further tight range studies on the blackflies (Diptera, Simuliidae), with the use of dye markers. Annals of

letin

Entomological

Society

of America

46, 23-37.

H. T. 195’4. Ecology of Simuliid vectors of Onchocerciasis in Guatemala. American Midland Naturalist 62, 175-196. DALMAT, H. T. 1955. Black flies (Diptera, Simuliidae) of Guatemala and their role as vectors of Onchocerciasis. Smithsonian Miscellaneous Collection 126, 425 pp. DALMAT, H. T., AND GIBSON, C. L. 1952. A study of flight range and longevity of black flies (Diptera, Simuliidae) infected with Onchocerca volvu1us.

Annals

of

Entomological

Society

of

America 46, 605-612. DAMPF, A. 1933. Concentration of microfilariae by the salivary secretions of blood sucking insects. Science 77, 20-21, from Review of Applied Entomology

(B)

21, 65 (1933).

D. M. 1952. The population and activity of adult female black flies in the vicinity of a stream in Algonquin Park, Ontario. Canadian Journal of Zoology 80, 287-321. DAVIES, D. M. 1953. Longevity of black flies in captivity. Canadian Journal of Zoology 31, 304312. DAVIES, D. M., AND PETERSON, B. V. 1956. Observations on the mating, feeding, ovarian development, and oviposition of adult black flies (Simuliidae, Diptera) . Canadian Journal of Zoology 84, 615-655. DAVIES, D. M., AND PETERSON, B. V. 1957. Black flies over lakes (Simuliidae, Diptera). Annuls of

Entomological

of

Research

48, 407-424.

DAVIES, L. 1957b. A study of the age of females of Simulium ornatum Mg. (Diptera) attracted to cattle. Bulletin of Entomological Research

DALMAT,

DALMAT,

463

DAVIES, L. females Nature DAVIES, L.

42, 538-553.

H. T. 1950. Studies on the flight range of certain Simuliidae, with the use of aniline dye marker. Annals of Entomological Society of

SIMULIIDAE

46, 535-552.

DAVIES, L. 1961. Ecology of two Prosimulium species (Diptera) with reference to their ovarian cycles. Canadian Entomologist 93, 1113-1140. DAVIES, L., AND WILLIAMS, C. B. 1962. Studies on black flies (Diptera: Simuliidae) taken in a light trap in Scotland. I. Seasonal distribution, sex ratio and internal conditions of catches. Transactions of London

of the Royal

Entomological

Society

114, l-20. DAVIES, L., DOWNE, A. E. R., WEITZ, B., AND WILLIAMS, C. B. 1962. Studies on black flies (Diptera, Simuliidae) taken in a light trap in Scotland. II. Blood-Meal identification by precipitin tests. Transactions of the Royal Entomological Society of London 114, 21-27. DAVIS, H. G., AND JAMES, M. T. 1957. Black flies attracted to meat bait. Proceedings of tke Entomological Society of Washington 69, 243244.

DAVIES,

G. R. 1951. A comparison of several repellants against black flies. Journal of ECO-

DEFOLIART,

nomic

Entomology

44, 265-266.

DEFOLIART, G. R., AND PETERSON,B. V. 1960. New North American Simuliidae of the genus Cnephia Enderlein (Diptera) . Annals of Entomological Society of America 63, 213-219. DE HOOGHE, M. 1934. Contribution B I’&ude de I’onchocercose humaine dans le vele. Annales de la Societd Belge de Medecine Tropicale 14, 153180, from Review of Applied Entomology (B) 23, 212 (1935).

D. M., PETERSON, B. V., AND WOOD, D. M. 1962. The black flies (Diptera: Simuliidae) of Ontario. Part I. Adult identification and distribution with description of six new species.

B. 1930. On the Ethiopian Simuliidae. Bulletin of Entomological Research 21, 185-200. DE MEILLON, B. 1957. Bionomics of the vectors of onchocerciasis in the Ethiopian Region. Bulletin of the World Health Organization 16, 509-

Proceedings of the Entomological Ontario, 1961 9!2, 70-154.

DEM’YANCHENKO,

Entomological

Society

of

America

60, 512-514.

DAVIES,

Society

of

D. M., AND SYME, P. D. 1958. Three new Ontario black tlies of the genus Prosimulium (Diptera: Simuliidae). Part II. Ecological observations and experiments. Canadian Entomol-

DAVIES,

ogist

90, 744-759.

DE

MEILLON,

522.

G. F. 1960. I. Features of infestation of farm animals with simuliid flies. II. Toxic action of simuliid fies on foal and lamb. Trudy Nauchno-Issledovatel’skogo Veterinarnogo Znstituta. Minsk 1, 105-109, 116-131 (in Russian), from Veterinary Bulletin 82, 302-303

464

PARASITOLOGICAL

(1962) and Review of Applied Entomology (B) 60, 141 (1962). DOROGOSTAJSKIJ, U. Y., RUBTZOV, I. A., AND VLA1935. Notes on the taxonomy, SENKO, N. M. biology and geographical distribution of blackflies in East Siberia. Magazin de Parasitologie de Music Zoologique Acadtmie des Sciences U.S.S.R. 5, 107-204 (in Russian with English summary). DOWNE, A. E. R. 1957. Precipitin test studies on rate of digestion of blood meals in black flies (Diptera: Simuliidae). Canadian Journal of Zoology 35, 459-462. DOWNE, A. E. R., AND MORRISON, P. E. 1957. Identification of blood meals of blackflies (Diptera: Simuliidae) attacking farm animals. MOSquito News 17, 37-40. DRUMMOND, F. H. N. 1933. West Australian Simuliidae. Journal of the Royal Society of West Australia 18, 1-12, from Review of Applied Entomology (B) 23, 69-70 (1935). DRY, F. W. 1921. Trypanosomiasis in the absence of tsetses and a human disease carried by Simulium in Kenya Colony. Bulletin of Entomological Research 12, 233-238, from Review of Applied Entomology (B) 10, 16-17 (1922). no BUYSSON, H. 1921. Observations sur les Moeurs du Simulium cinereum Macq. (Dipt.). Miscellanea Entomologie Uzds 26, 65-66, from Review of Applied Entomology (B) 9, 154 (1921). DUKE, B. 0. L. 1962a. Simulium aureosimile Pomeroy, a possible vector of Onchocerca volvulus. Annals of Tropical Medicine and Parasitology 66, 255-263. DUKE, B. 0. L. 196213. Studies on factors influencing the transmission of Onchoceriasis. I. The survival rate of Simulium damnosum under laboratory conditons and the effect upon it of Onchocerca volvulus. Annals of Tropical Medicine and Parasitology 66, 130-135. DUKE, B. 0. L. 1962c. Studies on factors influencing the transmission of onchocerciasis. II. The intake of Onchocerca volvulus microfilariae by Simulium damnosum and the survival of the parasites in the fly under laboratory conditons. Annals of Tropical Medicine and Parasitology 66, 255-263. DUNBAR, R. W. 1959. The salivary gland chromosomes of seven forms of black flies included in Eusimulium aureum Fries. Canadian Journal of zoology 37, 495-525. DYCE, A. L., AND LEE, D. J. 1962. Blood-sucking flies (Diptera) and Myxomatosis transmission in a mountain environment in New South Wales. II. Comparison of the use of man and rabbit as

REVIEWS

bait animals in evaluating vectors of myxomatosis. Australian Journal of Zoology 10, 84-94. EDGAR, S. A. 1953. A field study of the effect of black fly bites on egg production of laying hens. Poultry Science 32, 779-780. EDWARDS, F. W. 1915. On the British species of Simulium. I. Adults. Bulletin of Entomological Research 6, 23-42. EDWARDS, F. W. 1920. On the British species of Simulium. II. Early stages with corrections and additions to Part I. Bulletin of Entomological Research 11, 211-246. EDWARDS, F. W. 1921. New species of palaearctic Simuliidae in the British Museum (Diptera, Nematocera). Annals and Magazine of Natural History London 6, 141-143, from Review of Applied Entomology (B) 9, 52 (1921). EDWARDS, F. W., OLDROYD, H., AND SMART, J. 1939. “British Blood-Sucking Flies,” pp. l-156. London British Museum (Natural History). ENDERLEIN, G. 1921. Das System der Kriebelmiicken (Simuliidae) . Deutscke Tieriirztlicke Wockensckrift 29, 197-200, from Review of Applied Entomology (B) 9, 104 (1921). ENDERLEIN, G. 1924. Die Simuliiden Bulgariens und ihre SchPden im Jahr 1923. Zoologiscker Anzeiger 61, 11-12, from Review of Applied Entomology (B) 13, 57 (1925). ENDERLEIN, G. 1934. Aussereuropaische Simuliiden aus dem Wiener Museum. Sitzungsberichte Gesellschaft Naturforschender Freunde, Berlin, No. 4-7, 190-195; from Review of Applied Entomology (B) 23, 91 (1935). FAIN, A. 1950. Simulies nouvelles du RuandeUrundi. Revue de Zoologie et de Botanique Africa&es 43, 101-123, from Review of Applied Entomology (B) 41, 29 (1953). FALLIS, A. M., AND BENNETT, G. F. 1958. Transmission of Leucocytozoon bonasae Clarke, to ruffed grouse (Bonusa umbellus L.) by the black flies Simulium latipes Mg. and Simulium aureum Fries. Canadian Journal of Zoology 33, 533-539. FALLIS, A. M., AND BENNETT, G. F. 1961. Sporogony of Leucocytozoon and Haemoproteus in Simuliids and Ceratopogonids and a revised classification of the Haemosporidiida. Canadian Journal of Zoology 39, m-228. FALLIS, A. M., AND BENNETT, G. F. 1962. Observations on the sporogony of Leucocytozoon mirandae, L. bonasae, and L. fn’ngillinarum (Sporozoa: Leucocytozoidae) Canadian Journal of zoology 40, 395-400. FALLIS, A. M., ANDERSON, R. C., AND BENNETT, G. F. 1956. Further observations on the transmission and development of Leucocytozoon simondi. Canadian Journal of Zoology 34, 389-404.

FEEDING

BEHAVIOR

OF

A. M., DAVIES, D. M., AND VICKERS, M. A. 1951. Life history of Leucocytozoon simondi Mathis and Leger in natural and experimental infections and blood changes produced in the avian host. Canadian Journal of Zoology 29, 305-328. FIGUEROA, C. S. 1917. DOS nuevos simulidos de Chile. Boletin de Museo National de Historia Natural, Chile 10, 28-35, from Review of Applied Entomology (B) 11, 135 (1923). FITCH, C. P. 1918. Animal parasites affecting equines. Journal of American Veterinary Medi-

FALLIS,

cal Association

63, 312-330.

FITCH, H. S., SWENSON,F. S., AND TILLOTSON, D. F. 1946. Behavior and food habits of the redtailed hawk. The Condor 48, 205-237. FLOCH, H., AND ABONNENC, E. 1946a. Simulidb de la Guadeloupe. Publications de l’lnstitut Pasteur Guyane 130, 6 pp., from Review of Applied Entomology (B) 38, 113 (1950). FLOCH, H., AND ABONNENC, E. 1946b. Simulides de la Guyane francaise. Publications de l’lnstitut Pasteur Guyane 196, 20 pp., from Review of Applied Entomology (B) 99, 113 (1950). FREDEEN, F. J. H. 1958. Black flies (Diptera: Simuliidae) of the agricultural areas of Manitoba, Saskatchewan and Alberta. Proceedings of the Tenth

International

Congress

of Entomology

3, 819-823. FREDEEN, F. J. H. 1961. A trap for studying the attacking bebaviour of black flies, Simulium arcticum Mall. Canadian Entomologist 92, 73-78. FREEMAN, P., AND DE MEILLON, B. 1953. “Simulidae of the Ethiopian Region,” 224 pp., London British Museum (Natural History) ; from Review of Applied Entomology (B) 42, 15-16 (1954). FRIEDERICHS, K. 1921a. Zur Kriebelmiickenfrage. Deutsche Tieriirztliche Wochenschrift 29, 171173, from Review of Applied Entomology (B) 9, 104 (1921). FRIEDERICHS, K. 1921b. Untersuchungen ueber Simuliiden (Teil II). Zeitschrift fiir angewandte Entomologie 8, 31-92, from Review of Applied Entomology (B) 9, 212-213 (1921). FRIEDERICHS, K. 1925. Beobachtungen an Simuliiden in Ost-Java. Archiv fiir Schiffs-und Tropenhygiene 29, 119-125, from Review of Applied Entomology (B) 13, 181 (1925). FROHNE, W. C., AND SLEEPER, D. A. 1951. Reconnaissance of mosquitoes, punkies and blackflies in Southern Alaska. Mosquito News 11, 209-213. FULLER, H. S. 1940. Black-flies bite woodchuck. Bulletin 36,

155.

of the Brooklyn

Entomological

Society

FEMALE

SIMULIIDAE

465

GALLI-VALERIO, B. 1923. Beobachtungen iiber Culiciden nebst Bemerkungen iiber Tabaniden und Simuliiden. Centralblatt fiir Bakteriologie Parasitenkunde und Znfektionskrankeiten 99, 38-40, from Review of Applied Entomology (B) 11, 80-81 (1923). GALLI-VALERIO, B . 1932. Observations sur les Culitides les TabanidCs et les SimulidCs. Zentralblatt fiir Bakteriologie I. Originale 125, 485-490, from Review

of

Applied

Entomology

(B)

20,

79

(1932). GARSIDE,J. S., AND DARLING, H. S. 1952. Death of turkeys from attack by Simulium griseicolle Becker in northern Sudan. Bulletin of Entomological

Research

42, 583-584.

GEOR&ITCH, J. 1909. Sur nouveau, Critkidiu simuliue, (Simulium

un Trypanosome n.sp. d’une Simulie de la Serbie septen-

columbacensis) rendus des Seances cietd de Biologie 87, 480-482.

trionale. Comptes

de la So-

J. 1923. Nouvelles recberches sur la mouche de Goloubatz. Comptes Rendus Hebdomadaires des Seances Acaddmie des sciences (Paris) 178, 1500-1502, from Review of Applied Entomology (B) 11, 139 (1923). GIBBINS, E. G. 1934. Further studies on Ethiopian Simuliidae. Transactions of the Entomological GEORGI~VITCH,

Society

of London

82, 51-97.

GIBBINS, E. G. 1935. Mbwa flies. Uganda Journal 2, 272-279, from Review of Applied Entomology (B) 29, 184 (1935). GIBBINS, E. G. 1937. Simuliidae of the Buganda, eastern and western provinces of Uganda. B,ulletin

of Entomological

Research

28, 289-309.

GIBBINS, E. G. 1938. The mouth parts of the female in Simulium damnosum Theobald, with special reference to the transmission of Onchocerca volvulus (Leuckart). Annals of Tropical Medicine and Parasitology 32, 9-20. GIBBINS, E. G. 1941. Notes on Ethiopian Simuliidae. East African Medical Journal 18, 210-218, from Review of Applied Entomology (B) 30, 97 (1942). GIBSON, C. L. 1955. Consideraciones sobre la alimentacion de Simulidos antropofilicos en huespedes humanos y animales, con referencia a estudios de la transmision de la oncocercosis humana en Guatemala. Revista Zbdrica de Parasitologia Tomo Extraordinairia March, 307-311. GIBSON, C. L., AND DALMAT, H. T. 1952. Three new potential intermediate hosts of human onchocerciasis in Guatemala. American Journal of Tropical Medicine and Hygiene 1, 848-851. GLICK, P. A. 1939. The distribution of insects, spiders and mites in the air. Technical Bulletin of the

United

States

Department

of Agriculture

466

PARASITOLOGICAL

673, 150 pp., from Review of Applied Entomology (B) 26, 42 (1940). GNEDINA, M. P. 1950. Contribution to the biology of the nematode Onchocerca gutterosa Neumann, 1910, parasitising cattle. Doklady Akademia Nauk SSSR 70, 169-171 (in Russian), from Review of Applied Entomology (B) 40, 49 (1952). 1954. Acute and GUDGEL, E. F., AND GRAUER, F. H. chronic reactions to black fly bites (Simulium fly). Archives of Dermatology and Syphilology 70, 609-615. GUTZE~ICH, A. V. 1939. On the blood-sucking Diptera in Transbaikal Region (East Siberia). Travaux Acadtmie militaire mddicin Kiroff Armte Rouge 19, 39-47 (in Russian), from Review of Applied Entomology (B) 34, 41 (1946). HALL, M. C., AND WIGDOR, M. 1918. Notes on the acanthocephalid and arthropod parasites of the dog in North America. Journal of the American Veterinary Medical Association 53, 493-500. HARGREAVES, H. 1925. Annual Report of the Government Entomologist, Uganda. Annual Report of the Department of Agriculture, 21-28, from Review of Applied Entomology (B) 13, 167 (1925). The blackflies of British ColumHEARLE, E. 1932. bia (Simuliidae, Diptera). Proceedings of the Entomological Society of British Columbia 29, 5-19. HISSETTE, J. 1932. Memoire sur I’Onchocerca volvulus “Leuckart” et ses manifestations oculaires au Congo Belge. Annales de la Societt Belge de Medtcine Tropicale 12, 433.529, from Review of Applied Entomology (B) 21, 85 (1933). HOCKING, B. 1953. The intrinsic range and speed of flight of insects. Transactions of the Royal Entomological Society of London 104, 233-345. HOCKING, B., AND HOCKING, J. M. 1962. Entomological aspects of African onchocerciasis and observations on Simulium in the Sudan. Bulletin of The World Health Organization 2’7, 465-472. HOCKING, B., AND PICKERING, L. R. 1954. Observations on the bionomics of some northern species of Simuliidae (Diptera). Canadian Journal of Zoology 32, 99-119. HOCKING, B., AND RICHARDS, W. R. 1952. Biology and control of Labrador black flies (Diptera: Simuliidae). Bulletin of Entomological Research 43, 237-257. HOFFMAN, C. C. 1930. Los Simulidos de la region onchocercosa de chiapas (con descripcibn de nuevas especies). Anales de Institute de Biologia Universidad National, Mexico 1, 293-306, from Review of Applied Entomology (B) 19, 113 (1931).

REVIEWS

C. C., AND VARGAS, L. 1931. Nuevas communicaciones acerca de la Onchocercosis de chiapas. Revista Mexicana de Biologia 9, 127147, from Review of Applied Entomology (B) 20, 113 (1932). HUGHES, M. H., AND DALY, P. F. 1951. Onchocerciasis in the southern Gold Coast. Transactions of the Royal Society of Tropical Medicine and Hygiene 45, 243-252. HUNTER, S. J. 1913. Pellagra and the sand-fly. Journal of Economic Entomology 6, 96-101. IONESCXJ-BRAILA, G., AND DINULESCU, G. 1939. La mouche de Golubatz (Simulium reptans L.) et son action pathoghne. Bulletin of the Ofice International des Epizootics Paris 12, 276-303, from Review of Applied Entomology (B) 40, 70 (1940). JAMNBACK, H. 1952. The importance of correct timing of larval treatments to control specific blackflies (Simuliidae). Mosquito News 12, 7778. JENKINS, D. W. 1948. Ecological observations on the blackflies and punkies of Central Alaska. Mosquito News 6, 148-154. JENNINGS, A. H. 1914. Study of two years study of insects in relation to pellagra. Journal of Parasitology 1, 10-21. JOBBINS-POMEROY, A. W. 1916. Notes on five North American buffalo gnats of the genus Simulium. United States Department of Agriculture Bulletin 329, l-48, from Review of Applied Entomology (B) 4, 81-82 (1916). JOHNSON, E. P., UNDERHILL, G. W., Cox, J. A., AND THRELKELD, W. L. 1938. A blood protozoon of turkeys transmitted by Simulium nigroparvum (Twinn). American Journal of Hygiene 27, 649655. JONES, C. M., AND RICHEY, D. J. 1956. Biology of the black flies in Jasper County, South Carolina, and some relationship to a Leucocytozoon disease of turkeys. Journal of Economic Entomology 49, 121-123. JONES, R. H. 1961. Some observations on biting flies attacking sheep. Mosquito News 21, 113-115. JORDAN, P., AND GOATLY, K. D. 1962. Bancroftian filariasis in Tanganyika: A quantitative study of the uptake, fate and development of microfilariae of Wuchereria bancrofti in Culex fatigans. Annals of Tropical Medicine and Parasitology 66, 173187. KERSHAW, W. E. 1958. The population dynamics of infection with Onchocerca volvulus in the vector Simulium damnosum. Proceedings of the Tenth International Congress of Entomology 3, 499-501. KING, H. H. 1908. Report on economic entomolHOFFMAN,

FEEDING

ogy. Third Laboratory,

Report of Khartoum,

the

BEHAVIOR

Wellcome

OF FEMALE

Research

pp. 201-248. Report of the entomological

KING, H. H. 1911. section. Fourth Report

of the Wellcome

Research

pp. 95-105. KIRK, R. 1947. Observations on onchocerciasis in the Bahr-El-Ghazal province of the Sudan. Annals of Tropical Medicine and Parasitology 41, 357-364. KNAB, F. 191.5. Some new neotropical Simuiiidae. Laboratory,

Khartoum

Bulletin KNOWLTON,

Journal KNOWLTON,

(B),

of Entomological

Research

6, 279-282.

G. F. 1935. Simuiiids annoy livestock. of Economic Entomology 28, 1673. G. F., AND MADDOCK, D. R. flies in Utah. Journal of Economic

do Institute

Biologic0

(Sao Paulo,

Brazil)

11, 189-195, from Review of Applied Entomology (B) 29, 188 (1941). LEE, D. J., DYCE, A. L., AND O’GOWER, A. K. 19.57. Blood-sucking flies (Diptera) and myxomatosis transmission in a mountain environment in New South Wales. Australian Journal of Zoology 6, 355-401. LEON, N. 1909. Le Simulium columbaczense de Roumanie. Centralbkztt fur Bakteriologie, Abteilung (Originale) 1, 659-660. LE Roux, P. L. 1929. Onchocerciasis of cattle with special reference to its possible life-cycle and control. Pan-African Agricultural and Veterinary Conference, Pretoria, 1929. Papers of the Veterinary Section, pp. 107-112, from Review of Applied Entomology (B) 18, 213 (1930). LEWIS, D. J 1948. The Simuliidae of the AngloEgyptian Sudan. Transactions of the Royal Entomological Society of London 99, 475-496. LEWIS, D. J. 1953. Simulium damnosum and its relation to onchocerciasis in the Anglo-Egyptian Sudan. Bulletin of Entomological Research 43, 597-644. LEWIS, D. J. 1957. Simuiiidae and their relation to onchocerciasis in the Sudan. Bulletin of the World Health Organization 16, 671-674. LEWIS, D. J. 1958. Some aspects of the study of Simulium damnosum. Proceedings of the Sixth International

Congresses

on

Tropical

Medicine

and Malaria 2,305-314. LEWIS, D. J. 1960a. Observations on the Simulium

467

neavei complex at Anami in Tanganyika. Bulof Entomological Research 61, 95-113. LEWIS, D. J. 1960b. Observations on Simulium damnosum in the southern Cameroons and Liberia. Annals of Tropical Medicine and Parasitology 64, 208-223. LEWIS, D. J. 1962. Some recent observations on African Simuliidae. Proceedings of the Eleventh International Congress of Entomology 3, 131134. LEWIS, D. J., AND GARNEAM, P. C. C. 1960. The Simuiiidae (Diptera) of British Honduras. Bulletin

letin

1944. Ento-

Snipe mology 37, 119. LANDAU, R. 1962. Four forms of Simulium tuberosum (Lundstr.) in southern Ontario; a salivary gland chromosome study. Canadian Journal of .%ology 46, 921-940. LANE, J., AND PORTO, C. E. 1940. Simuiideos de regiao Neotropica. III. Descrica de novas especies dos generos “‘Similium” e “Eusimulium.” Arquivos

SIMULIIDAE

of Entomological

Research

60, 703-710.

R. 1962. Simuhidae and their relation to human onchocerciasis in northern Venezuela. Bulletin of the World Health Organization 27, 449-464. LOEWENTHAL, L. J. A. 1943. Cutaneous changes in onchocerciasis. Annals of Tropical Medicine and LEWIS,

D.

J.,

AND

Parasitology

IBA%EZ

DE

ALDECOA,

37, 147-148.

R. 1942. Stand der Simuliidenforschung und Beitrag zur Immunititsfrage. The present position of Simuiiids and a contribution to the question of immunity. Deutsche Tieriirztliche Wochensckrift 60, 274, from Review of Applied Entomology (B) 31, 84-85 (1943). LOWTHER, J. M. 1962. Personal communication. LUTZ, A. 1917. Terceira contribucao para o Conhecimento das Especies brazileiras do Genero Simultim 0 Pium do Norte (Simulium amazonicum). Memoire do Institute de Oswald0 Cruz 9, 63-67, from Review of Applied Entomology (B) 6, 129 (1918). LOHMANN,

LUTZ,

A., DE SOUZA

ARAUJO,

H.

C., AND

DA

FONSECA,

0. 1918. Viajem scientific no Rio Parana e a Assuncion corn Volta por Buenos Aires, Montevideo e Rio Grande. Memo&s Institute Oswald0 Crux 10, 104-173, from Review of Applied Entomology LUTZ,

(B)

8, 2.5-26

(1920).

A. 1922. Zoologia Medica-Nematocercos hematophagos nLo pertincendo aos Cuhcideos (Blood-sucking Nematocera other than Culicids) . A Folka Medica Rio de Janeiro 3, 89-92, from Review of Applied Entomology (B) 10, 199-200 (1922).

MCCARTHY,

P.

H.

1961.

Austrosimulium

pestilens,

a source of severe irritation to marsupials. Australian Veterinary Journal 37, 334. MACKERRAS, M. J., AND MACKERRAS, I. M. 1948. Simuhidae (Diptera) from Queensland. Australian Journal of Scientific Research, Series B 1, 231-270. MCKIEL, J. A., AND WEST, A. S. 1961. Nature and causation of insect bite reactions. Pediatric Clinics of North America 8, 795-816.

468

PARASITOLOGICAL

MCMAEON, J. P. 1940. Onchocerca volvulus and its vector in South Kavirondo district of Kenya. Transactions of the Royal Society of Tropical Medicine and Hygiene 34, 65-83. MCMAHON, J. P. 1947. Simuliidae of Kenya. East African Me.dical Journal 24, 51-56, from Review of Applied Entomology (B) 39, 21 (1951). MALMCH, J. R. 1914. American black flies and buffalo gnats. United States Agricultural Bureau of Entomology, Technical Series 26, l-72, from Review of Applied Entomology (B) 2, 167 (1914). MARR, J. D. M. 1962. The use of an artificial breeding-site and cage in the study of Simulium damnosum Theobald. Bulletin of the World Health Organization 27, 622-629. MIESSNER, H. 1916. Zahlreiche Todesf%lle beim Rind in der Leineniederung, veranlasst durch Simulium reptans. Deutsche Tieriirztliche Wochenschrift 24, 183-185. from Review of Applied Entomology (B) 4, 126 (1916). MILLAR, J. L., AND REMPEL, J. G. 1944. Livestock losses in Saskatchewan due to black flies. Canadian Journal of Comparative Medicine and Veterinary Science a, 334-337. MUMFORD, E. P., AND ADAMSON, A. M. 1934. Entomological researches in the Marquesas Islands. Memoires Societi de Biogeographie, Paris 4, 21% 234, from Review of Applied Entomology (B) 23, 201 (1935). NELSON, G. S., AND PESTER, F. R. N. 1962. The identification of infective filarial larvae in Simuliidae. Bulletin of the World Health Organization 27, 473-481. NICHOLSON, H. P. 1945. The morphology of the mouthparts of the non-biting blackfly, Eusimulium dacotense D. & S. as compared with those of biting species, Simulium venusturn Say (Diptera: Simuliidae). Annals of the Entomological Society of America 38, 281-297. NICHOLSON, H. P., AND MICKEL, C. E. 1950. The black flies of Minnesota (Simuliidae). University of Minnesota Agriculture Experiment Station Technical Bulletin 192, l-64. OGATA, K. 1954. Studies on the diurnal rhythm of biting activity in Simulium venusturn Say. Japanese Journal of Applied Zoology 19, 136-141. OGATA, K., HARADA, S., AND NAKAMURA, M. 1956. Ecological studies on the black flies, Simulium aokii Takahasi, 1941. Japanese Journal of Sanitary Zoology 6, 100-110. O’ROKE, E. C. 1934. A malaria-like disease of ducks. University of Michigan School of Forestry Conservation Bulletin 4, 44 pp. PETERSEN, A. 1924. Bidrag til de Danske Simuliers naturhistorie. Danske Videuskabernes selskab

REVIEWS Skrifter Naturvideuskabelig og mathematisk afgeling, 8th series 6, 187 pp., from Review of Applied Entomology (B) 12, 170 (1924). PETERSON, B. V. 1956. Observations on the biology of Utah black flies (Diptera: Simuliidae) . Canadian Entomologist 33, 496-507. PETERSON, B. V. 1959a. Observations on mating, feeding, and oviposition of some Utah species of black flies (Diptera: Simuliidae). Canadian Entomologist 91, 147-155. PETERSON, B. V. 1959b. Notes on the biology of some species of Utah black flies (Diptera: Simuliidae). Mosquito News 19, 86-90. PETERSON, B. V. 1962. Cnephia abdita, a new black fly (Diptera: Simuliidae) from eastern North America. Canadian Entomologist 94, 96102. PETERSON, D. G., AND WOLFE, L. S. 1958. The biology and control of black flies (Diptera: Simuliidae) in Canada. Proceedings of the Tenth International Congress of Entomology 3, 551564. POMEROY, A. W. J. 1922. New species of African Simuliidae and further studies of the early stages. Bulletin of Entomological Research 12, 457-463. RATCLIFFE, F. N. 1955. Review of myxomatosis in Australia, 1950-1955. Journal of the Australian Institute of Agricultural Science 21, 130-133, from Review of Applied Entomology (B) 46, 207 (1957). A. P. 1947. An REMPEL, J. G., AND ARNASON, account of three successive outbreaks of the black fly Simulium arcticum, a serious livestock pest in Saskatchewan. Scientific Agriculture 27, 428-445. R%TRLY, A. 1925. Les calamites naturelles en Hongrie de 930 & 1876. Mater&x Etude des Galamitt% 1, 373-378, 2, 77-78, from Review of Applied Entomology (B) 13, 154 (1925). RIVOSECCHI, L., AND COLUZZI, M. 1962. Tre Simulidi (Simuliztm aureum Fries (S.L.), (Simulium erythrocephalum De Geer, Simulium reptans L.) the en Italia pungono l’uomo. Parassitologia 4, 181-190. ROTHFELS, K. H. 1956. Black flies: siblings, sex and species grouping. Journal of Heredity 47, 113-122. ROOT, F. M. 1922. Notes on mosquitoes and other blood-sucking flies from Puerto Rico. American Journal of Hygiene 2, 394-405, from Review of Applied Entomology (B)13, 23 (1925). RUBTZOV, I. A. 1939. Factors of outbreaks of the black flies. Travaux Acaddmie Militaire MLdecin Kiroff Armt!e Rouge 19, 177-207 (in Russian), from Review of Applied Entomology (B) 34, 42-43 (1946).

FEEDING

BEHAVIOR

OF

RUBTZOV, I. A. 1951. Contribution to the biology and ecology of the midges (Simuliidae) of Central Asia. Parasitologicheskii Sbornik 13, 3% 342 (in Russian), from Review of Applied Entomology (B) 49, 68 (1954). RUBTZOV, I. A. 1956. Fauna of the U.S.S.R. insects (Diptera). Black flies (family Simuliidae). Zoologicheski

instituta

Akademiya

Nauk

SSSR

6, l-860

(in Russian), from Tropical Diseases Bulletin 68, 754 (1961). SAILER, R. I. 1953. The blackfly problem in Alaska. Mosquito News lS, 232-235. SANDERSON,E. D. 1910. Controlling the blackfly in the White Mountains. Journal of Economic Entomology

9, 27-29.

SCHMIDT, M. 1916. Durch die Kolumb&ser Miicken hervorgerufene Erkrankungen. Deutsche Tieriirztliche Wochenschrift Hannover 24, 247-248, from Review of Applied Entomology (B) 4, 158 (1916). SCEWETZ, J. 1930. Sur quelques diptkres hCmatophages du Congo. Bulletin de la Societi de pathologic exotique 23, 987-994, from Review of AppZied Entomology (B) 19, 82 (1931). SENIOR-WHITE, R. 1922. Notes on Indian Diptera. Memoirs

Department

of Agriculture

of India.

Entomological

Series 7, 3-4, 83-169; from Review of Applied Entomology (B) 11, 98 (1923). SHEWELL, G. E. 1955. Identity of the black fly that attacks ducklings and goslings in Canada (Diptera: Simuliidae). Canadian Entomologist 87,

345-349.

SHEWELL, G. E. 1957. Interim report on distribution of the black flies (Simuliidae) obtained in the Northern insect survey. Defence Research Board Tecknical Reports 7, l-3 + 47 maps. SEEWELL, G. E., AND FREDEEN,J. F. H. 1958. Two new black flies from Saskatchewan (Diptera: Simuliidae). Can&an Entomologist 99, 733-738. SICIDMORE, L. V. 1932. Leucocytozoon smithi infection in turkeys and its transmission by Simulium occidentale Townsend. Zentralblatt fiir Bakteriologie Originale

und

Parasitenkunde

Abteilung

1.

136, 329-335. SMART, J. 1934. Notes on the biology of Simulium pictipes Hagen. Canadian Entomologist 99, 6265. SMART, J. 1935. The internal anatomy of the black-fly Simulium ornatum Mg. Annals of Tropical Medicine and Parasitology 29, 161-170. SMART, J. 1936. Notes on Simuliidae occurring at Fortingal, Perthshire. Scottish Naturalist 217, 22-26, from Review of Applied Entomology (B) 24, 118 (1936). SMART, J. 1943. Simuliztm feeding on ivy flowers.

FEMALE

469

SIMULIIDAE

76, 20-21, from Review (B) 91, 148 (1943).

Entomologist Entomology

of Applied

SORT, J. 1944. The British Simuliidae with keys to the species in the adult, larval and pupal stages. Scientific Publications of the Freshwater Biological

Association

of the British

Empire

9,

l-57. SOMMERMAN, K. M. 1958. Two new species of Alaskan Prosimulium, with notes on closely related species. Proceedings of the Entomological Society of Washington 80, 193-202. SOMMERMAN, K. M., SAEER, R. I., AND ESSELBOUGH, C. 0. 1955. Biology of Alaskan black flies (Simuliidae, Diptera). Ecological Monographs 25, 345-385. STEWARD, J. S. 1931. A note on Sin&urn species attacking horses and cattle in Hereford&ire. Report of the Institute University of Cambridge

of Animal

Pathology,

2, 194-197. STEWARD, J. S. 1937. The occurrence of Onchocerca gutterosa Neumann in cattle in England, with an account of its life history and development in Simulium ornatum Mg. Parasitology 29, 212-218. STOKES, J. H. 1914. A clinical, pathological and experimental study of the lesions produced by the “black fly” Simulium venuskm. Jolrmal of Cutaneous

Diseases

92, 751-769,

STONE, A. 1952. The Simuliidae ceedings

of the Entomological

830-856.

of Alaska. ProSociety

of Wash-

ington 64, 69-96. STONE, A., AND JAMNBACK, H. A. 1955. The black flies of New York State (Diptera: Simuliidae). Bulletin

of the New

York

State

Museum

949,

l-444. STRONG,R. P., SANDGROUND,J. H., BEQUAERT, J. C., AND Murjoz OCHOA, M. 1934. Onchocerciasis with special reference to the Central American form of the disease. Contribution of the Department versity Entomology

of

Tropical

Medicine,

Harvard

Uni-

6, 175-224, from Review of Applied (B) 23, 172-173 (1935). SWAN, D. C. 1937. Insects and other invertebrates of economic importance in south Australia during the period July 1934 to June 1936. Journal of the Department of Agriculture, tralia 40, 717-731, from Review Entomology (B) 29, 225 (1937).

So&h Ausof Applied

SYME, P. D., AND DAVIES, D. M. 1958. Three new Ontario black flies of the genus Prosimulium (Diptera: Simuliidae) Part I. Descriptions, morphological comparisons with related species and distribution. Canadian Entomologist 99, 697-719. TAYL.OR,F. H. 1944. Sandflies. Australian Museum Magazine 8, 210-213, from Review of Applied Entomology (B) 92, 141 (1944).

470

PARASITOLOGICAL

TESKEY, H. J. 1960. Survey of insects affecting livestock in southwestern Ontario. The Canadian Entomologist 92, 531-544. TRAVIS, B. V. 1949. Studies of mosquitoes and other biting-insect problems in Alaska. Journal of Economic Entomology 42, 451-457. TRAVIS, B. V., SMITH, A. L., AND MADDEN, A. H. 1951. Effectiveness of insect repellents against black flies. Journal of Economic Entomology 44, 813-814. TWINN, C. R. 1933. The blackfly Simulium venusturn Say, and a protozoon disease of ducks. Canadian Entomologist 65, l-3. TWINN, C. R. 1952. A review of studies of bloodsucking flies in northern Canada. Canadian Entomologist 34, 22-28. TWINN, C. R., HOCKING, B., MCDUFFIE, W. C., AND CROSS, H. F. 1948. A preliminary account of the biting flies at Churchill, Manitoba. Canadian Journal of Research (D) 26, 334-357. UNDERHILL, G. W. 1939. Two simuliids found feeding on turkeys in Virginia. Journal of Economic Entomology 32, 765-768. UNDERHIJL, G. W. 1940. Some factors influencing feeding activity of Simuliidae in the field. Journal of Economic Entomology 33, 915-917. UNDERHILL, G. W. 1944. Blacktlies found feeding on turkeys in Virginia, (Simulium nigroparvum Twinn and Simulium slossonae Dyar and Shannon). Virginia Polytechnic Institute of Agriculture, Experiment Station Technical Bulletin 34, l-32. USOVA, Z. V., AND KULIKOVA, Z. P. 1958. The activity of black flies (Diptera: Simuliidae) in Karelia. Entomologi Olvozrenie 37, 751-762, from translation notes. 1941. Recherches sur I’onchoVAN DEN BERGHE, L. cercose au Congo belge. Premiere Memoire. La transmission d’onchocerca volvulus par des simulies. Altnales de la SocietC Belge de Mtdecine Tropicale 21, 63-67, from Review of Applied Entomology (B) 3, 27 (1944). WALKER, G. P. 1927. A blackfly (Simulium bracteatum) fatal to goslings. Canadian Entomologist 63, 123. WANSON, M. 1950. Contribution a 1’8tude de I’Onchocercose africaine humaine. Annales de la Societk Belge de MLdicine Tropicale 30, 667-863, from Review of Applied Entomology (B) 41, 201-202 (1953).

REVIEWS

WANSON, M., AND LEBEID, B. 1948. Note sur le cycle gonotrophigue de Simulium damnosum. Revue de Zoologie et de Botanique Africaines 41, 66-82, from Review of Applied Entomology (B) 41, 13 (1953). WANSON, M., HENRARD, C., AND PEEL, E. 1945. Onchocerca volvulus Leuckart. Indices d’infection des simulies agressives pour l’homme. Cycle de developpement chez Simulium damnosum Theobald. Recueil de Travaux de Sciences Mtditales au Congo Belge 4, 122-138, from Review WEBSTER, F. M. 1914. Natural enemies of Simulium: Notes. Psyche 21, 95-99, from Review of Applied Entomology (B) 2, 177 (1914). WEHR, E. E. 1962. Studies of leucocytozoonosis of turkeys, with notes on schizogony, transmission, and control of Leucocytozoon smithi. Avian Diseases 6, 195-210. WENK, P. 1962. Anatomie des Kopfes von Wilhelmia equina L. (Simulidae syn. Melusinidae, Diptera). Zoologische Jabrbiicher. Abteilung fiir Anatomie und Ontogenie der Tiere 30, 81-134. WENK, P., AND SCHLBRER, G. 1963. Wirtsorientierung und Kopulation bei blutsaugenden Simuliiden (Diptera). Zeitschrift fiir Tropenmedizin und Parasitologie 14, 177-191. WELLMAN, F. C. 1908. Notes on some Angolan insects of economic or pathological importance. Entomological News 19, 224-230. WILHELMINI, J., AND SALING, TH. 1928. Stand und Aufgaben der Simuliidenforschung. Zeitschrift fiir Wissenschaftliche Zoologie 132, 329-354, from Review of Applied Entomology (B) 17, 71 (1929). WOLFE, L. S., AND PETERSON, D. G. 1959. Black flies (Diptera: Simuliidae) of the forests of Quebec. Canadian Journal of Zoology 37, 137159. WOLFE, L. S., AND PETERSON, D. G. 1960. Diurnal behaviour and biting habits of black flies (Diptera: Simuliidae) in the forests of Quebec. Canadian Journal of Zoology 33, 489-497. WOOD, D. M. 1963. Two new species of Ontario black flies. Proceedings of the Entomological Society of Ontario (1962) 63, 94-98. WV, Y. F. 1931. A contribution to the biology of Simulium (Diptera). Michigan Academy of Science, Arts and Letters (1930) 13, 543-599. ZAHAR, A. R. 1951. The ecology and distribution of black flies (Simuliidae) in south-east Scotland. Journal of Animal Ecology 20, 33-62.