Susceptibility of mosquitoes to avian malaria

PARASITOLOGICAL

EXPERIMENTAL

PARASITOLOGY

REVIEWS

16, 107-132 (1965)

Susceptibility

of Mosquitoes

to Avian

Malarial

Clay G. Huff Department

of Parasitology,

Naval Medical

In the 65 years that have lapsed since Ronald Ross discovered the mosquito transmission of a malarial parasite of birds, much research has been done upon avian malaria. An inclusive account of this research would fill a large book. Recently, a review by the writer (1963) of the experimental work done in the past 5-7 years in this field covered 65 pages. Other reviews and books have summarized the extensive work on chemotherapy, exoerythrocytic stages, immunology, and other aspects of general malariology. This review summarizes the literature on the susceptibility of mosquitoes to avian malaria and discusses factors contributing to susceptibility. Previously (Huff, 1954) a preliminary listing and account of this material was given a limited circulation. The response to this account was very gratifying. I want to thank all persons who have called my attention to omissions and errors in this preliminary list. They have made possible a more nearly complete coverage of the wide range of publications in which results of this kind have appeared. However, in spite of assiduous searching of the literature on my part and the aid of those who had read the earlier account, it is probable that some records have been overlooked. I have not attempted to include all refer1 From Bureau of Medicine and Surgery, Navy Department, Research Task MR 005.09-1030, Subtask No. 2. The opinions and assertions contained herein are those of the author and are not to be construed as official or reflecting the views of the Navy Department or the Naval service at large.

Research Institute,

Bethesda, Maryland

ences to mosquito infectivity to avian malaria. The species Plasmodium cathemerium and Plasmodium gallinaceum have been, for example, so intensively studied in Culex pipiens and Aedes aegypti, respectively, that it would not be feasible to include all references to them. I have in all instances attempted to include references to (a) the first demonstration of susceptibility of a species of mosquito to a particular species of parasite, (b) all papers in which the results differed sufficiently from others to be of interest, and (c) new combinations of vertebrate host, parasite, and mosquito. Although several references to susceptibility of a species of mosquito to an unidentified Plasmodium are included in the tables, I have excluded such references as Ross (1898) and Daniels (1899)) in which it was not possible to identify either the parasite or the mosquito. The most comprehensive summary of this type was made by Vargas (1949). However, he omitted from his summary all anopheline mosquitoes and references to experiments in which the results were negative. As the present review will show, a high percentage of positive results has been obtained in the species of Anopheles which have been tested for susceptibility to avian malaria. Moreover, negative findings have value in guiding investigators in their research for species most suitable to their experiments. As will be indicated in the discussion section, many factors influence the growth of a particular species of parasite in a given species of mosquito. For this reason, the avian host from which the 107

108

HUFF

parasite was isolated or upon which the mosquitoes to be tested were fed has been given whenever this information was available. Likewise, the total numbers of mosquitoes dissected, the number which contained oocysts, the number in which the salivary glands contained sporozoites, and the number of actual transmissions effected are given in all instances in which this information was supplied. All new records not previously published from the reviewer’s laboratory are listed under reference “Huff (unpublished) .”

names of species in which contradictory results were recorded. In subsequent summaries these species are included among the susceptible group and not in the insusceptible group. Total numbers of species shown to be susceptible and of those found to be susceptible for each species of parasite are also shown in this table. The results are numerically summarized in Table III according to genera of mosquitoes which contain species known to be susceptible to one or more of the species of parasites. Further analysis of these tabulations will be REVIEW OF KNOWN DATA made in the discussion section. Table IV lists the species of avian PlasmoAs many of the data pertinent to this paper as possible were extracted from original arti- dium for which no susceptible mosquitoes cles and placed in Table I. Arrangement of have been found. As will be noted, 12 of these these data was made according to (1) sys- species are of questionable status. Nine of the tematic position of the mosquito, (2) species 17 species generally considered to be of good of parasite, (3) vertebrate host which was taxonomic status have been demonstrated to utilized, (4) infection or lack of it expressed be capable of developing in one to 34 species in numbers of mosquitoes in which oocysts or of mosquitoes. Only 3 of the remaining 8 sporozoites were found or by which transmis- species have been recorded as having been sions were made, and (5) reference from tested for infectivity to mosquitoes, and in which the information was obtained. The each of these not more than 2 individual mosscientific names of the mosquitoes are listed quitoes were tested. according to current usage; where the name DWXSSION used by the investigators differs from current The records relative to the susceptibility of usage, the former is placed in parentheses. Although the mosquito now known as Aedes mosquitoes to avian malaria given here are aegypt; was known in the earher Iiterature as extensive in number, geographically wideStegomyia fasciata, the latter name was spread, and variable as to content. In nearly omitted from the tables. Wherever numerical all of them the presence or absence of oocysts results were recorded in the original paper on the stomach is indicated, and in a large these are shown in columns 4-6, the number proportion the incidence of infection is given of positive results being the numerator and for the particular parasite in a given host. It the total number used the denominator. If the should be emphasized that the recording of results were listed only qualitatively they are negative results does not necessarily signify recorded as + or -. The fractions employed insusceptibility in the mosquito host. Several in column 6 (transmissions) refer to the num- instances are indicated by asterisks in Table ber of attempts at transmission rather than II in which the same species of mosquito was reported as susceptible and insusceptible to a the number of mosquitoes employed. The results in Table II are grouped accord- species of parasite in different references. The ing to species of parasite so that it can be seen presence of oocysts on the stomach of a mosreadily which species have been found to be quito which fed upon a bird with one of the species of avian parasites is proof of the sussusceptible or insusceptible to a particular species of Plasmodium. Asterisks precede the ceptibility of the mosquito. In the absence of

Mosquito

cathemerium elongatum (= praecox) cathemerium elongatum elongatum elongatum fallax fallax gallinaceum gallinaceum gallinaceum hexamerium lopkurae lopkurae lopkurae

relictum relictum relicturn relicturn gallinaceum gallinaceum relicturn relictum gallinaceum cathemerium gallinaceum relicturn (praecox) sp.

Plasmodium

0 Transmitted to sparrow. b Sturnus 2). vulgaris. c Passer domesticus. d In canary isolated from house finch. * Avian host unknown; mosquitoes were field caught.

punctipennis punctipennis quadrimaculatus quadrimaculatus quadrimaculatus quadrimaculatus quadrimaculatus quadrimaculatus quadrimaculatus quadrimaculatus quadrimaculatus quadrimaculatus quadrimaculatus quadrimaculatus quadrimaculatus

(franciscanus)

freeborni freeborni hyrcanus hyrcanus sinensis hyrcanus sinensis macirlipennis pseudopunctipennis

freeborni freeborni

CYllCianS

Anopheles (Anopheles) crucians crucians crucians

canary canary canary canary duck sparrow chicken pigeon chicken chicken chicken duck chick duck duck

chicken canary *

starling” sparrow” canary sparrowC chicken chicken sparrowe canaryd chicken

11/63 1931327 9/17 O/3 26/56 7/29

O/8

o/13 O/l 13/120 O/47 o/21 o/20 4/51

S/50 18/4.3 o/15 3/27 60% 6/42 18/32 7/62 O/l o/14 O/8 z/205

Oocysts

TABLE and Insusceptibility

Host

List of Data on the Susceptibility

-t

•t

o/15

5162

+

+ + O/15 o/27 +

Sporozoites

I of Mosquitoes

+c

+

O/3

Sa

+”

-P

3/4

2/3

111

Transmission

1

to Sfiecies of Avian PIasmodium

Huff, 1927 Huff, 1927 Micks, McCollum, 1953 Micks, 1949 Micks, 1949 Micks, 1949 Huff et al., 1950 Huff et al., 1950 Haas, Akins, 1947 Eyles, 1952 Cantrell, Jordan, 1949 Huff (unpublished) Coggeshall, 1940, 1941 Hurlbut, Hewitt, 1941 Hurlbut, Hewitt, 1942

Hunninen, 1951 Hunninen, 1951 Hunninen et al., 1950 Hunninen et al., 1950 Eyles, 1960 Eyles, 1952 Hunninen, 1951 Mok, 1951 Russell, Menon, 1942 Tanaka, 1946 Weathersby, 1962 Reichenow, 1932 Reeves et al., 1954

Reference

sp. gallinaceum sp. gallinaceum sp. gallinaceum gallinaceum cathemerium elongatum gallinaceum gallinaceum gallinaceum gallinaceum heroni heroni relictum sp.

circumflexurn

Anopheles (Myzomyia) annularis (= fuliginosis) culicifacies culicifacies fluviatilis jluviatilis jeyporiensis jeyporiensis ludlowii maculatus maculates splendidus stephensi stephensi stephensi subpictus subpictus subpictus (= rossi)

Culiseta annulata (= Theobaldia annadata)

cathemerium

gallinaceum relicturn relicturn relictum cathemerium

Anopheles (Nysorrhynchus) albimanus albimanus albimanus albimanus norestensis

strodei

lophurae relictum relicturn relicturn relicturn relicturn

Plasmodium

Anopheles (Anopheles) quadrimaculatus quadrimaculatus quadrimaculatus quadrimaculatus quadrimaculatus quadrimaculatus

Mosquito

( ?)

canary

sparrow chicken sparrow chicken sparrow chicken chicken canary canary chicken chicken chicken chicken Ardeola gvayi Ardeola grayi sparrow sparrow

20/20

o/2

7/?

-

o/33 7

-

o/40

o/2

o/7 o/40 o/10

-

o/2

O/28

o/2 o/2

l/4

Brachyspiza pileata

30/49 l/51 26/60 73% 48/93 28/159

+

+ + +

o/53 4/60 + + +

Sporozoites

I (continued) Oocysts

53/B 40/43 51/61 80% s/41

TABLE

chicken starlingb sparrowC sparrowC “Tico-tico”

duck canary sparrowe sparrow” sparrowC starlingb

Host

+

Sa +a

+” -tn

+c

O/l

3/4

Transmission 1

Reichenow,

1932

James, 1902 Russell, Menon, 1942 James, 1902 Russell, Menon, 1942 James, 1902 Russell, Mohan, 1942 Russell, Menon, 1942 Russell, 1931 Reichenow, 1932 Hunninen, 1953 Russell, Menon, 1942 Russell, Mohan, 1942 Russell, Menon, 1942 Basu, 1938 Basu, 1938 Mayne, 1928 James, 1902

Lucena, 1938

Eyles, 1960 Hunninen, 1951 Hunninen, 1951 Hunninen, 1953 Barreto, 1943

Jeffrey, 1944 Hunninen et al., 1950 Hunninen et al., 1950 Hunninen, 1953 Hunninen, 1951 Hunninen, 1951

Reference

t: 0

f Redwing

(Molothrus a. ater) strain. blackbird (Agelaius p. phoeniceus) strain.

gallinaceum gallinaceum galdinaceum cathemeriume cathemeriumf cathemerium circumflexume circumflexumf elongatum elongatum (praecox)

Aedes (Aedimorphus) jamesi jamesi stokesi vexans vexans vexans vexans vexans vexans vexans

C Cowbird

cathemerium

Psorophora ferox (= sayi) chicken chicken chicken canary canary canary canary canary canary canary

canary

chicken l/l

o/10 O/7

o/30

+ 15/15 213

o/19

517

-

-

4/5

canary

circumjlexumf

gallinaceum

+

canary

1927

Jordan,

1938

1938

1938

Russell, Menon, Mohan, 1955 OkapaIa, 1958 Herman, 1938 Herman, 1938 Huff, 1927 Herman, 1938 Herman, 1938 Micks, 1949 Huff, 1927

Huff,

Cantrell,

Herman,

Herman,

Herman,

1938

1942

1945

Herman,

1945

-

Jordan,

1932

1932

Sergent, Sergent, 1918

Cantrell,

Reichenow,

Reichenow,

Reference

+

Transmission

circumflexume

canary

cathemeriume

l/22

2114

o/7

Sporozoites

I (continued) Oocysts

+

canary

relicturn

TABLE

cathemeriumf

chicken

canary

relicturn

gallinaceum

canary

Host

elongatum

(praecox)

Plasmodium

Mansonia perturbans

annulata (E Theobaldia annulata) annulata (= Theobaldia annulata) inornata (E Theobaldia innorata) longiareolata (= Theobaldia spathipalpis) melaneura (= Theobaldia melaneurus) melaneura (= Theobaldia melaneurus) melaneura (= Theobaldia melaneurus) melaneura (= Theobaldia melaneurus)

Culiseta

Mosquito

c t

gallinaceum gallinaceum relictum SP.

gallinaceum elongatum fallax gallinaceum lophurae gallinaceum gallinaceum cathemerium gallinaceum gallinaceum gallinaceum gallinaceum cathemerium gallinaceum gallinaceum cathemerium elongatum (= praecox) elongatum elongatum elongatum fallax gallinaceum

gallinaceum cathemerium cathemeriumf circumftexuma elongatum (praecox) gallinaceum

Aedes (Finlaya) albolatoralis atropalpus atropalpus atropalpus atropalpus chrysolineatus geniculatus japonicus japonicus pallirostris pseudotaeniatus pseudotaeniatus togoi togoi togoi triseriatus triseriatus triseriatus triseriatus triseriatus triseriatus triseriatus

Aedes (Ochlerotatus) campestris canadensis canadensis canadensis canadensis canadensis

Plasmodium

Aedes (Aedimorphus) vexans vexans vexans vexans

Mosquito

chicken canary canary canary canary chicken

chicken chicken canary canary canary canary duck pigeon chicken

chicken chicken chicken chicken

chicken duck pigeon chicken duck chicken chicken

chicken chicken canary *

Host

TABLE

O/4 2/23

IS/16 012s

18/33 + O/51 016 l/3 Z/82 l/27 S/20 s/12

4/10 -

2/2 2/6 + +

O/S2 4/7 78/87 12/12 +

+

20/21 + l/12 28/172

Oocysts

+

+

20/46 +

l/4 + +

+ + + 2/2

Sporozoites

I (continued)

-(2

-

+

+

-

4/s

2/s

20/23

Transmission

1

Cantrell, Jordan, Huff, 1927 Herman, 1938 Herman, 1938 Huff, 1927 Cantrell, Jordan,

1949

1945

Russell, Menon, 1942 Micks, 1949 Huff, et al., 1950 Trembley, 1946 Laird, 1941 Russell, Mohan, 1942 Roubaud et al., 1939 Tanaka, 1946 Weathersby, 1962 Russell, Mohan, 1942 Russell, Mohan, 1942 Mohan, 1955 Tanaka, 1946 Weathersby, 1962 Inoki, 1951 Huff, 1927 Huff, 1927 Huff, 19.30 Micks, 1949 Micks, 1949 Huff et at., 1950 Cantre!l, Jordan, 1945

Cantrell, Jordan, 1945 Russell, Menon, 1942 Rosen, Reeves, 1954 Grundman et al., 1952

Reference

E Iu

canary canary * chicken ? canary canary canary canary canary canary canary canary chicken chicken

SP. relicturn sp. gallinaceum gallinaceum

relictum relicturn cathemerium cathemeriume cathemeriumf circumfEexume circumjlerumf elongatum (praecox) gallinaceum gallinaceum

cathemerium elongatum (praecox) elongatum elongatum elongatum elongatum fallax fallax fallax fallax

Aedes (Stegomyia) aegypti aegypti aegypti aegypti aegypti aegypti aegypti aegypti aegypti aegypti canary canary canary canary duck sparrow canary chicken chicken duck

canary canary canary canary canary canary chicken

Host

cathemeriume cathemerkmf cathemerium circumflexume circumjlexumf elongatum (= praecox) gallinaceum

Plasmodium

Aedes (Ochlerotatus) cantator cantator cantator cantator cantator cantator cantator communis (= Culex nemorosus) dorsalis dorsalis lepidus lepidus mariae (= Acartomyia mariae) nigromaculis sollicitans sollicitans sollicitans sollicitans sollicitans sollicitans stimulans trivittatus

Mosquito

TABLE

l/36 O/55 O/168 o/30 O/65 O/89 36/49 30/172 o/45 4/36

o/12 6/10 4/7

O/3 o/12

l/13 48/355 + +

+

6/10

O/6

o/37

+

-I-

+

+

Sporozoites

I (continued) oocysts

+

+ + -(

+

+

+

+

-(

-

( (

6

112

416

2

Transmission

)

1

1945

Huff, 1927 Huff, 1927 Micks, 1949 Reichenow, 1932 Micks, 1949 Micks, 1949 Huff (unpublished) Huff (unpublished) Huff et al., 1950 Hluff (unpublished)

Sergent, Sergent, 1918 Rosen, Reeves, 1954 Huff, 1927 Herman, 1938 Herman, 1938 Herman, 1938 Herman, 1938 Huff, 1927 Cantrell, Jordan, 1945 Cantrell, Jordan, 1945

Koch, 1899 Rosen, Reeves, 1954 Grundrnan et al., 1952 Cerqueira, Paraense, 1945 Paraense, 1945

Herman, 1938 Herman, 1938 Huff, 1927 Herman, 1938 Herman, 1938 Huff, 1927 Cantrell, Jordan,

Reference

9 Colinus v. virginianus.

aegypti aegypti aegypti aegypti aegypti aegypti aegypti aegypti aegypti aegypti aegypti aegypti aegypti aegypti aegypti aegypti aegypti aegypti albopictus albopictus albopictus albopictus albopictus albopictus

aegypti

Aedes (Stegomyia) aegyfiti aegypti aegyfiti aegypti aegypti aegypti aegypti aegypti aegypti

Mosquito

fallax fallax gallinaceum gallinaceum gallinaceunz gallinaceum gallinaceum gallinaceum gallinaceum gallinaceum heroni heramerium hexamevium juxtanucleare lophurae lophurae lophurae lophurae relicturn (inconstans) relicturn (praecox) relicturn relicturn relictum relictum (pigeon strain) relicturn (pigeon strain) vaughani vaughani cathemerium circumflexurn fallax fallax fallax fallax

fallax

Plasmodium

canary canary gosling guinea fowl pigeon

pigeon pigeon turkey chicken chicken chicken chicken guinea fowl quails chicken chicken Ardeola grayi canary duck chicken chicken chicken duck duck canary canary canary canary canary canary pigeon canary robin

Host

TABLE

o/31 19/20 7/36 9/10 191/261

6/115 O/56

+ + 35/39 43/46 57/63 80/133 o/140 O/158 9/318 21/55 O/18 28/169 2/16 57/501

l/110 43/224 73/232 loo/loo

Oocysts

11/115

+ +

+

Sporozoites

I (continued)

)

+ + +

+ ( 3/10 1

+ + ( w3

Transmission Huff et al., 1950 Huff (unpublished) Huff (unpublished) Brumpt, 1935 Brumpt, 1936 Russell, Mohan, 1942 Inoki, 1951 Huff (unpublished) Huff (unpublished) Cantrell, Jordan, 1949 Mohan, 1955 Basu, 1938 Huff (unpublished) Huff (unpublished) Paraense, 1944 Coggeshall, 1940 Huff, 1940 Laird, 1941 Jeffery, 1944 Huff, 1927 Neumann, 1908 Sergent, Sergent, 1918 Sergent, Sergent, 1907 Sergent, 1940 Redmond, 1944 Redmond, 1944 Huff (unpublished) Manwell, 1947 Tanaka, 1946 Huff (unpublished) Huff (unpublished) Huff (unpublished) Huff (unpublished) Huff et al., 1950

Reference

E P

gallinaceum gallinaceum gallinaceum gallinaceum cathemerium gallinaceum gallinaceum gallinaceum gallinaceum

Armigeres annulipalpis aureolineatus kuchingensis magnus obturbans obturbans obturbans obturbans subalbatus

Plasmodium

fallax fallax gallinaceum gallinaceum gallinaceum gallinaceum gallinaceum gallinaceum gallinaceum gallinaceum gallinaceum gallinaceum hexamerium lophurae lophurae lophurae lophurae lophurae lophurae vaughani gallinaceum eallinaceum gallinaceum gallinaceum gallinaceum

Mosquito

Aedes (Stegomyia) albopictus albopictus albopictus albopictus albopictus albopictus albopictus albopictus albopictus albopictus albopictus albopictus albopictus albopictus albopictus albopictus albopictus albopictus albopictus albopictus pseudalbopictus scutellaris unilineatus vittatus vittatus

chicken chicken chicken chicken

chicken chicken chicken chicken

quails turkey chicken chicken chicken chicken chicken chicken chicken chicken gossling turkey duck canary duck duck duck duck turkey canary chicken chicken chicken chicken chicken

Host

TABLE

+ 5/15 381/398 23/42

17/17 227/398 25/44

+ +

+ + + +

+

7/73

+ + + + f

103/108 364/1410 o/10 2/359 O/56 + + + f 18/71

530/547 12/16

467/547 14/20 20/20 + 88/101 23/49 24/30 o/35 o/25

+

+ +

Sporozoites

+ -I-

2X/302

2/2

Oocysts

I (continued1

6/6

3/3

1

S/6

+ + + ( 25/38 >

+

-I+ (

Transmission

Russell, Menon, 1942 Russell, Mohan, 1942 Russell, Mohan, 1942 Russell, Menon, 1942 Tanaka, 1946 Russell, Mohan, 1942 Mohan, 1955 Russell, Menon, 1942 Weathersby, 1962

Huff (unpublished) Huff (unpupblished) Brumpt, 1936 Inoki, 1951 Russell, Mohan, 1942 Russell, Menon, 1942 Weathersby, 1962 Cantrell, Jordan, 1949 Dasgupta, Ray, 1956 Mohan, 1955 Huff (unpublished) Huff (unpublished) Huff (unpublished) Huff (unpublished) Huff et al., 1947 Laird, 1941 Jeffery, 1944 Huff (unpublished) Huff (unpublished) Huff (unpublished) Russell, Mohan, 1942 Russell, Mohan, 1942 Russell, Mohan, 1942 Russell, Mohan, 1942 Mohan, 1955

Reference

pipiens pipiens pipiens pipiens pipiens pipiens pipiens pipiens pipiens pipiens pipiens pipiens pipiens pipiens pipiens pipiens pipiens pipiens pipiens pipiens pipiens pipiens pipiens pipiens

pipiens

bitaeniorhynchus bitaeniorhynchus bitaeniorhynchus bitaeniorhynchus bitaeniorhynchus bitaeniorhynchus gelidus mimeticus mimeticus mimeticus (= mimuloides)

Culex (Culex)

Mosquito

cathemerium galliltaceum gallinaceum gallinaceum relicturn (praecox) relicturn relicturn (praecox) gallinaceum gallinaceum gallinaceum cathemerium cathemeriume cathemeriumf circumflexum~ circumflexumf circumfEexum elongatum elongatum elongatum elongatum elongatum elongatum elongatum elongatum fallax gallinaceum gallinaceum hexamevium hexamerium hexamerium hexamerium (= oti) lophurae lophurae lophurae nucleophilum

Plasmodium

canary canary canary canary canary duck sparrow chicken chicken chicken canary canary duck canary duck duck chick canary

chicken chicken chicken canary canary canary canary canary canary

“sparrow”

chicken chicken chicken

Host

TABLE

O/25 O/26 l/167

O/65

o/120

21/398 l/72 o/72

11/723 o/59 + 12/47

o/30

O/418 O/9 + 21/21 + o/12 l/35 75/169

6/7 -

-(5

+ +

+

1412 1

O/418 o/11

+

Sporozoites

I (continued) Oocysts

-(5

)

-(5

+ + +

+ -

+ +c2 + ( l/2 -(2

O/3

Transmission

)

>

)

) )

Tanaka, 1946 Russell, Mohan, 1942 Singh, Mohan, 1955 Weathersby, 1962 Russell, Mohan, 1942 Singh, Mohan, 1955 Russell, Mohan, 1942 Russell, Mohan, 1942 Russell, Menon, 1942 Russell, Menon, 1942 Huff, 1927 Herman, 1938 Herman, 1938 Herman, 1938 Herman, 1938 Reichenow, 1932 Raffaele, 1936 Micks, 1949 Reichenow, 1932 Huff, 1930 Huff, 1927 Wolfson, 1946 Micks, 1949 Micks, 1949 Huff et al., 1950 Brumpt, 1936 Cantrell, Jordan, 1945 Manwell, 1947 Huff (unpublished) Huff (unpublished) Manwell, 1947 Laird, 1941 Jeffery, 1944 Coggeshall, 1940 Manwell, 1947

Reference

E Q\

(pigeon strain)

relicturn

relictum

relicturn% relicturn” relictum~~ relictumh relictum7b relicturn matutinum relictum matutinum rouxi rouxi SP. SP. vaughani

pipiens

pipiens

pipiens @ens pipiens pipiens pipiens pipiens pipiens pipiens pipiens pipiens pipiens pipiens

h See text for explanation.

(pigeon strain)

relicturn

pipiens

(pigeon strain)

(pigeon strain) (pigeon strain)

(pigeon strain)

(inconstans) (iflconstans) (praecox) (penguin strain)

Plasmodium

relicturn relicturn relicturn relicturn relictum relicturn relictum relicturn relictum relicturn relictum relictum relictum relictum relic&m

Culex (Culex) pipiens pipiens pipiens pipiens pipiens pipiens pipiens pipiens pipiens pipiens pipiens pipiens pipiens pipiens pipiens

Mosquito

TABLE

2/39 +

+ + 34/108 +

-

+

+

+a

+a

+ -

+

f(

15/116 +

-t +

+

3

Transmission

+

Sporozoites

I (continued) Oocysts

canary ?/I2 canary 28/30 canary 85/104 canary 11/11 canary 9/116 canary 104/111 canary + Columba guinea canary pigeon sparrowc 60/61 sparrowc 80% sparrowc 25/108 starlinga 45/68 Streptopelia humilis Streptopelia senegalensis Streptopelia chinensis Zenaidura macroura l/179 pigeon canary o/547 o/290 canary 21/346 pigeon 18/286 canary canary canary + canary canary canary + * l8/99 canary O/36

Host

)

1948

1948

1948

Huff, 1948 Huff et al., 1959 Huff et al., 1959 Huff et al., 1959 Huff et al., 1959 Huff et al., 1959 Manwell, 1940 Manwell, 1947 Huff, 1932 Manwell, 1947 Ruge, 1901 Grundman et al., 1952 Manwell, 1947

Huff,

Huff,

Huff,

Huff, 1927 Reichenow, 1932 Neumann, 1908 Rodhain, 1939 Hunninen, et al., 1950 Sergent, 1940 Redmond, 1944 Huff, 1948 Sergent, Sergent, 1907 Redmond, 1944 Hunninen, 1951 Hunninen, 1953 Hunninen, et al., 1950 Hunninen, 1951

Reference

quinquefasciatus

i Larus novae-hollandai. j To sparrows and gulls.

quinquefasciatus quinquefasciatus quinquefasciatus quinquefasciatus quinquefasciatus quinquefasciatus quinquefasciatus quinquefasciatus quinquefasciatus quinquefasciatus

matutinum

relictum relictum relicturn relicturn

rouxi

(capistrani) (inconstans)

(praecox)

relicturn relicturn

gallinaceum gallinaceum gallinaceum gallinaceum heroni juxtanucleare

fallar

elongatum elongatum elongatum elongatum

quinquefasciatus quinquefasciatus quinquefasciatus quinquefasciatus quinquefasciatus quinquefasciatus quinquefasciatus

Brachyspiza pileata canary canary canary duck pigeon chicken chicken chicken chicken Ardeola grayi chicken canary canary canary canary gulli canary canary

( ?)

oryzornis

Fringilla kawarahiwa canary canary canary

(praecox)

relicturn

relicturn cathemerium cathemerium cathemerium cathemerium

pallens

pipiens

(praecox)

chicken Oryzivova

canary canary canary

Host

dictum

relicturn cathemerium gallinaceum

vaughani relicturn

Plasmodium

pipiens pipiens quinquefasciatus quinquefasciatus quinquefasciatus quinquefasciatus

berbericus pallens pallens pallens

pipiens pipiens pipiens pipiens pipiens pipiens

Culex (Culex)

Mosquito

TABLE

l/16 36/72 + 2/13S O/78

2/2

+ 3/232 7/15

o/791

O/j O/78 + o/47 l/12

32/100 28/34 S/15 4/7 10148

O/36 100/100 48/100 62187 O/42 -

OocYsts

36/72 +

+

11/138

+

+

+

O/48

Suorozoites

I (continued)

+ + ( +i +

+

-(3

+

1

2/3 )

O/7

Transmission

1934 1953

Huff, 1927 Micks, 1949 Raffaele, 1934 Micks, 1949 Huff et al., 1950 Brumpt, 1936 Russell, Mohan, 1942 Russell, Menon, 1942 Vargas, Beltran, 1941 Basu, 1938 Paraense, 1944 Russell, 1932 Huff, 1927 Romana et al., 1946 Rosen, Reeves, 1954 Lawrence, Bearup, 1961 Huff, 1937 Huff, 1932

Katahira, 1929 Roubaud, Mezger, Micks, McCollum, Huff, 1927 Tanaka, 1946 Lucena, 1938

Huff (unpublished) Roubaud, Mezger, 1934 Roubaud, Mezger, 1934 Tanaka, 1946 Weathersby, 1962 Katahira, 1929

Reference

&

Mosquito

L Strain from Humboldt’s z Transmitted to pigeon.

Culex (C&x) quinquefasciatus quinquefasciatus restuans restuans salinarius salinarius salinarius salinarius salinarius stigmatosoma stigmatosoma stigmatosoma tarsalis tarsalis tarsalis tarsalis tarsalis tarsalis tarsalis tarsalis tarsalis tarsalis tarsalis tarsalis tarsalis tarsalis tarsalis tarsalis tarsalis tarsalis tarsalis tarsalis territans

penguin.

sp. sp. elongatum lophurae cathemerium elongatum (praecox) gallinaceum relicturn (inconstans) rouxi relicturn relictum sp. cathemerium circumflexurn elongatum elongatum fallax gallinaceum hexamerium ‘relicturn relicturn relicturn relictum (lPl)h relictum (lP2)h relictum (lBl)l~ relicturn relictum (IP) h relictum (lB)h rouxi sp. sp. vaughani cathemerium

Plasmodium

canary canary

canary canary canary canary canary canary pigeon pigeon canary * *

canary canary canary canary* turkey chicken canary *

canary duck canary canary chicken canary canary canary * *

sparrow *

Host

TABLE

26/31 41/80 4/23 160/1978 54/409 o/112 9/14

86/8X 20/24 191/269 134/166 34/59

26/155 3/7 Z/208 3/18 + 17/48 19/21 o/120

3/22 6/6 o/14 12/123’

w

23/26 13/679 4/182 2/4 3/5

Oocysts

99/1965

+

86/88

+

81148

S/662 +

Sporozoites

I (continued)

213 3/5

) )

( 6124 ) ( lo/lo )

( (

+z

+ + +

+

+ +

+

Transmission James, 1902 Reeves, et al., 1954 Micks, 1949 Laird, 1941 Huff, 1927 Huff, 1927 Cantrell, Jordan, 1945 Huff, 1927 Huff, 1932 Rosen, Reeves, 1954 Reeves et al., 1954 Reeves et al., 1954 Huff, 1932 Huff (unpublished) Huff, 1932 Huff, Shiroishi, 1962 Huff (unpublished) Huff (unpublished) Huff (unpublished) Reeves et al., 1954 Rosen, Reeves, 1954 Huff, 1932 Huff et al., 1959 Huff et al., 1959 Huff et al., 1959 Schinazi, Ball, 1956 Huff et al., 19.59 Huff et al., 1959 Huff, 1932 Reeves et al., 1954 Grundmann et al., 195’2 Huff (unpublished) Huff, 1927

Reference

cathemerium cathemerium 7eJictum (capistrani) gallinaceum

cathemeriumf circumflexumf relictum cathemerium gallinaceum

Culex (Lutzia) fuscanus fuscanus fuscanus raptor

Culex (Neoculex) apicalis apicalis apicalis (= hortensis) hayashii hayashii

Plasmodium

elongatum (praecox) relicturn (inconstans) rouxi relictum (praecox) cathemerium gallinaceum relicturn (praecox)

Mosquito

Culex (Culex) territans tervitans territans theileri tritaeniorhynchus tritaeniorhynchus whitmorei

chicken

canary canary canary

canary canary chicken

chicken

canary canary canary canary

Host

TABLE

-

O/8

2/3 l/l O/9

-

s/5 3/4 l/12 + 7/13 O/16 +

Oocysts

o/13

+

o/19

Sporozoites

I (continued)

+

-

-(2

o/2

Transmission

1

1942 Herman, 1938 Herman, 1938 Sergent, Sergent, 1918 Tanaka, 1946 Weathersby, 1962

Tanaka, 1946 Nono, 1932 Nono, 1932 Russell, Menon,

Huff, 1927 Huff, 1927 Huff, 1932 Russell, Mohan, 1942 Tanaka, 1946 Weathersby, 1962 Russell, Mohan, 1942

Reference

SUSCEPTIBILITY

OF MOSQUITOES

oocysts on the stomach, susceptibility to the parasite may be indicated by the presence of sporozoites in the salivary glands. Ability to transmit a parasite is proved only by production of infection in a susceptible bird by the bite of the mosquito. Under conditions of laboratory experiment such a demonstration does not necessarily incriminate it as being a natural vector, since under natural conditions the mosquito may for one or more reasons not come into close contact with the infected or susceptible bird. It is well to keep all of these factors in mind when interpreting the listings in the tables of this review. Many factors are influential in producing infections of a given parasite in a species of mosquito. Granting that environmental conditions such as temperature are favorable for the extrinsic development of the parasite, these factors fall into the two categories: (1) those concerning the mosquito, and (2) those concerning the parasite. The age of the adult mosquito and the state of nutrition have been shown by Terzian et al. (1956) to affect significantly the susceptibility of A. aegypti to P. gallinaceum. It has been abundantly shown by many authors that the susceptibilities of species, varieties, and strains of mosquitoes vary widely in the same species of parasite. The genetic factors affecting susceptibility were first shown by Huff (1929) to be subject to change by selection. By selecting progenies from infected and uninfected females of C. pipiens, he demonstrated an increase and decrease in susceptibility in respective strains to Plasmodium cathemerium. Subsequently (Huff, 193 1) it was shown that the same results held for Culex quinquefasciatus, and also that the inheritance of susceptibility of C. pipiens to P. cathemerium appeared to depend upon a simple, recessive trait. Several other examples of experimental change of susceptibility were later described. Trager (1942) produced by selection a strain of A. aegypti more susceptible to Plasmodium lophurae than the parent strain, and Micks (1949) similarly enhanced the susceptibility of C.

TO

AVIAN

MALARIA

121

pipiens to Plasmodium elongatum. A more complete study of the genetic aspects of susceptibility of A. aegypti to P. gallinaceum was recently made by Ward ( 1963). Starting with a strain of this mosquito which had a very high susceptibility to P. gallinaceum, he was able after 26 generations of selection to reduce its susceptibility by 98%. He attributed most of the genetic variation in this system to the effect of a single genetic factor which lacked dominance. The factors associated with the parasite which may influence the susceptibility of the mosquito to it include (1) inherent ones and (2) the influence of its environment previous to ingestion by the mosquito, namely, that of the vertebrate host upon the sexual stages. The inherent factors appear at the species, subspecies, and the geographic and laboratory strain levels. The differences in susceptibility of a species of mosquito to different species of Plasmodium are too well known to require discussion. However, one example may be mentioned of the same type of difference between subspecies. The subspecies Plasmodium relicturn matutinum was shown to be less infectious to Culex fatigans than other strains of the species relicturn (Huff, 1937). Examples of the differences of susceptibility of a species of mosquito to strains of different geographic origin are found in the work of Ward ( 1963). When we turn from the inherent characters of the parasite which determine whether it is capable of infecting a species of mosquito, we find evidence that the same species of parasite (1) may produce widely different numbers of gametocytes in different species of birds and even in different individual birds of the same species, (2) may differ qualitatively in the gametocytes in respect to their ability to infect mosquitoes, and (3) may regularly produce, during the course of infection in an individual bird, gametocytes qualitatively different in their capabilities for producing oocysts in the mosquito (Huff and Marchbank, 1955). An analysis of the factors in the

HUFF

122

Species of Mosquitoes

Mosquitoes reported susceptible

Species of Plasmodium cathemerium

Hartman,

TABLE II Found to be Susceptible or Insusceptible Plasmodium from Birds

1927

Aedes aegypti *Aedes sollicitans Anopheles norestensis .inopheles quadrimaculatus Anopheles strodei Culex bitaeniorhynchus *Culex fuscanus Culex pipiens Culex pallens Culex quinquefasciatus Culex salinarius Culex tarsalis Culex territans Culex tritaeniorhynchus *Culiseta melanura

Total spp. circumflexurn

Total elongatum

Total fallax

1931

Culex larsalis Cz4liseta annulata Czlliseta circumflexurn

3

spp. Huff,

1930

*Aedes *Culer *Culex Culex Culex Culex Culex

spp.

triseriatus pipiens quinquefasciatus restuans salinarius tarsalis territans

7

Schwetz, 1930

Total

Mosquitoes reported insusceptible Aedes albopictus Bedes canadensis Aedes cantator Aedes japonicus *Aedes sollicitans Aedes togoi Aedes triseriatus Aedes vexans Anopheles hyrcanus sinensis Anopheles ludlowii Anopheles punctipennis Arm. obturbans Culex apicalis *Culex fuscanus Culex hayashii *Culiseta melanura Psorophora ferox 14

15

Kikuth,

‘@Aedesaegypti Aedes albopictus Aedes atropalpus Aedes triseriatus *Anopheles quadrimaculatus Culex quinquefasciatus Culex tarsalis

spp.

* Reported

to the Various Species of

7 both susceptible and insusceptible.

Bedes Aedes Aedes Aedes Aedes Culex Culex

albopictus canadensis cantator sollicitans vexans apicalis pipiens

*

Aedes aegypti Aedes atropalpus Aedes canadensis Aedes cantator Aedes sollicitans *Aedes triseriatus Aedes vexam Anopheles maculatus Anopheles punctipennis Anopheles quadrimaculatus *Culex pipiens *Culex quinquefasciatus Culiseta annulata 10 *dedes aegypti *Anopheles quadrimaculatus Culex pipiens

1

SUSCEPTIBILITY

OF MOSQUITOES

TABLE Species of Plasmodium gallinaceum

Total

Brumpt,

1935

Total

Total

Aedes aegypti Aedes albolatoralis Aedes albopictus Aedes atropalpus Aedes campestris Aedes canadensis Aedes cantator Aedes chrysolineatus Aedes geniculatus Aedes jamesi Aedes japonicus Aedes lepidus Aedes pallirostris Aedes pseudalbopictus Aedes pseudotaeniatus Aedes scutellaris Aedes stimulans Aedes stokesi Aedes togoi Aedes triseriatus Aedes trivittatus Aedes unilineatus Aedes vexans Aedes vittatus Anopheles albimanus Anopheles freeborni Anopheles quadrimaculatus Arm. annulipalpus Arm. aureolineatus Arm. kuchingensis Arm. magnus Arm. obturbans Arm. subalbatus Culex salinarius Culex tarsalis Culiseta inornata Mansonia perturbans

Anopheles culicifacies Anopheles fluviatilis Anopheles hyrcanus Anopheles jeyporiensis Anopheles maculatus Anopheles splendidus Anopheles stephensi Culex bitaeniorhynchus Culex hayashii Culex mimeticus Culex pallens Culex pipiens Culex quinquefasciatus Culex raptor Culex tritaeniorhynchus

15 Anopheles stephensi Anopheles subpictus Aedes aegypti

1

spp.

spp.

Mosquitoes reported insusceptible

1935

juxtanucleare \‘ersiana & Gomeo, 1943 Total

II (Continued)

Mosquitoes reported susceptible

Culex quinquefasciatus

spp. Huff.

123

MALARIA

37

spp.

heroni Basu, 1938

hexamerium

TO AVIAN

3 Aedes aegypti Aedes albopictus Anopheles quadrimaculatus Culex pipiens Culex tarsalis

0 Culex quinquefasciatus 1

5 Aedes aegypti 1

HUFF

124 TABLE

Mosquitoes reported susceptible

Species of Plasmodium lophurae

Coggeshall,

1938

Aedes aegypti *Aedes albopictus Aedes atropalpus Anopheles quadrimaculatus *C&x pipiens Culex

Total

II (Continued)

Culex quinquefasciatus Culex salinarius

Aedes aegypti Aedes dorsalis Aedes mariae Aedes vexans Anopheles albimanus Anopheles quadrimaculatus *Anopheles crucians Anopheles freeborni Anopheles subpictus Culex apicalis Culex bitaeniorhynchus Culex fuscanus Culex gelidus Culex pipiens Culex pipiens berbericus *Culex pipiens pallens Culex quinquefasciatus Culex salinarius Culex stigmatosoma Culex tarsalis Culex territans Culex theileri Culex whitmorei Culiseta annulata Culiseta longiareolata

Total

spp. Huff,

Total

Aedes aegypti (pigeon strain) Aedes nigromaculis *Anopheles crucians Anopheles maculipennis *Culex pi&ens pallens

25 1937

Culer pipiens Culex quinquefasciatus

3

Aedes aegypti

spp.

1

vaughani Novy and MacNeal 1908

Unidentified

2

3

spp.

relictum Grassi and Feletti, 1891

matutinum

0

6

Culew pipiens Culex tarsalis Culex territans

Total

*dedes albopictus *Culex pipiens

restuans

spp.

rouxi

Total

Mosquitoes reported insusceptible

spp. species

Aedes Aedes Cr4lex Czllex 0 Aedes communis Aedes dorsalis Aedes vexans Anopheles pseudeopunctipennis Culex pipens

aegypti albopictus pipiens tarsalis 4

Anopheles dnopheles Anopheles Anopheles

annularis culicifacies fluviatilis subpictus

SUSCEPTIBILITY

OF MOSQUITOES TABLE

125

MALARIA

II (Continued)

Mosquitoes reported susceptible

Species of Plasmodium

TO AVIAN

Mosquitoes reported insusceptible

Culex quinquefasciatus Culex stigmatosoma Culex tarsalis Total

8

spp.

avian host which influence the infectivity of the gametocyte for the mosquito was made by Huff et al. (1958). The relative effects of strain of parasite, vertebrate host, manner of transmission, and species of mosquito upon the susceptibilities of the mosquitoes tested were described by Huff et al. (1959). They gave the results of experimental feedings of C. pipiens and Culex tarsalis on two strains of P. relicturn isolated from domestic pigeons in different regions. The findings pertinent to this discussion are graphically shown in Fig. 1. In this figure P and B represent the two strains of parasite 0.05%

63.9%

G. piplens

C. torsofis

I PIGEON

I PIGEON

0%

71.0%

0%

00.7%

Gpipiens C. h~rsofis C. pipiens C torsalis I I I CANARY CANARY CANARY

\I

\/

I CANARY

I/

‘p\‘r/lpz SOUL El

A

PIGEON

/-\

PIGEON

II

C.pip:ens 6.1%

C. tdrsolis 51.2%

‘7\

CANARY

CANARY

II C. pip!ens

C.dsolis

6.3%

57.6%

FIG. 1. Scheme showing the percentage of susceptible individual Culex pipiens and C. tarsalis in two strains of Plasmodium relicturn isolated from pigeons (P and B). Strains IP, lP1, and 1B were established by blood inoculations; strains lP2 and lB1 were the result of inoculations of sporozoites (see Table I and discussion in text).

4

isolated from pigeons; the designations IP, lP1, and 1B identify strains established by subinoculation of blood to pigeons and canaries, while lP2 and 1Bl identify strains established by sporozoite transmission. These results indicated that C. tarsalis is more susceptible to strain P than to strain B regardless of vertebrate host or manner of transmission to these hosts. Contrariwise, these results show that C. pipiens is more susceptible to strain B than to strain P. There is some indication that C. tarsalis was somewhat more susceptible to both strains when transmitted by mosquitoes rather than by blood inoculation to the vertebrate hosts, although it was not possible to test this matter statistically because it was not discovered until one of the strains had been lost. Corradetti et al. (1960) elevated P. relicturn var. matutinum Huff, 1937 to the specific status P. matutinum Huff, 1937 on the basis of study of four strains from four different species of host, in the United States (Planesticus migratorius, Hylocichla mustelina, and Passer domesticus), and in Italy (Turdus iliacus). If the taxonomic change proposed by these Italian authors and the suggestion of Huff et al. (1959) that both strains of P. relicturn isolated from pigeons in the United States (strains B and P) probably belong to matutinum be accepted, it will be necessary in Table I to place all entries listed under “P. relicturn, pigeon strain” under “P. matutinum Huff,” and to refer to the above analysis as dealing with the species matutinum rather than to relicturn. When all the variables used to determine the susceptibility of mosquitoes to malarial parasites are considered, we see that the data

126

HUFF

in Table I are rather crude. In fact, these relationships are so complex that the question may legitimately be raised as to whether a true measure of either the susceptibility of the mosquito or the infectiousness of the parasite can in most instances be expressed. Nevertheless the listing in Table I of the salient findings of the papers that deal with susceptibility of mosquitoes should serve a useful purpose in indicating what has been and what still needs to be done. In the early history of malariology it was shown that malaria in man is transmitted uniquely by anopheline mosquitoes and that the culicine mosquitoes transmit malaria of birds. This antinomy which came to be widely accepted was more tacit than proved. Intensive epidemiological studies that have been made on human malaria show that invariably malaria is accompanied by “anophelism.” The other assumption, i.e., that culicine mosquitoes are always the vectors of avian malaria, was not the result of extensive experimentation. Mayne (1928) was the first to demonstrate that an Anopheles mosquito could transmit avian malaria. The list has grown until, of the 19 species of Anopheles listed here, 8 have been found to be susceptible to some species of avian Plasmodium. In several instances sporozoites were observed, and experimental transmission by Anopheles was effected. I am not aware of any report of a proved natural infection capable of transmission to other birds, but there seems to be no reason for believing that natural transmission does not occur by Anopheles mosquitoes. The species of anophelines known to be susceptible to avian malaria are distributed over the three subgenera: Anopheles, Nyssorhynchus, and Myzomyia. The parasite known to infect some species of Anopheles are: P. cathemerium, P. fallax, P. gallinacewm, P. lophurae, and P. relicturn.

Table I shows that, of the 74 species of mosquitoes which have been tested for susceptibility to any species of avian Plasmodium, 58 or 78% have been susceptible to one or more species of the parasites used.

Only one report has been made of the susceptibility of a culicine mosquito to human malaria. Williamson and Zain ( 1937) obtained experimental infection of laboratory bred Culex bitaeniorhynchus fed upon patients with mixed infections of P. vivax and P. falciparum and of P. malariae and P. falciparum. They reported sporozoites of both species from the salivary glands of this Culex but did not test their infectivity on human subjects. Although epidemiological evidence is against a belief in the ability of culicines to serve as natural vectors of human malaria, it must be admitted that the attempts to infect them experimentally have not been done on anything like the scale upon which anophelines have been tested for susceptibility to avian malaria. There is no good reason for assuming that culicines are all insusceptible to human malaria. In fact, susceptibility of a low degree to human malaria could exist in many of the culicines without having these mosquitoes play an important part in malarial transmission. Frequently in the history of medical entomology, beliefs have been held in the strict specificity of a given infectious agent for a known species of insect; however, further investigation has usually revealed other vectors. Early control work in yellow fever assumed that only A. aegypti could serve as its vector. Now a multitude of species is known to be susceptible. Once a species of insect had been incriminated, the scientific public appears to have given all other species the benefit of the accepted practice of assuming them innocent until proved guilty. This practice cannot be considered as commendable since it has often been responsible for delaying the testing of possible vectors. Very pertinent to the above discussion regarding human malaria are the data given by Warren and Wharton (1963) on susceptibility of culicine mosquitoes to simian malaria. They summarize the work done by others and by themselves in tabular form, and give references to the data included. Development to the oocyst stage of subspecies of Plasmodium cynomolgi was found in Culex vishnui, Culex

SUSCEPTIBILITY

OF MOSQUITOES

tritaeniorhynchus, Aedes butleri, and Mansonia uniformis. The presence of sporozoites of Plasmodium knowlesi in Aedes reginae and of a transmission of this species by Armigeres subalbatus are open to some question. However, Warren and Wharton cite a personal communication from Ramakrishnan stating that devolopment to the sporozoite stage of Plasmodium cynomolgi was obtained in Aedes pseudomediofasciatus. Of the 31 recognized genera of mosquitoes, some are so poorly studied that the adult feeding habits of the species within them are unknown. About 20 genera are known to be blood-sucking. Some of the species such as Culex apicalis are believed to feed on coldblooded animals ; others appear to prefer birds, while others seek out mammals. It appears likely that feeding preferences are determined by several factors such as the kinds and numbers of vertebrates available, location of these animals, the ecological influences which bring them into proximity, and genetic changes within the mosquitoes. In this respect, TABLE Relation

between Number

TO

AVIAN

127

MALARIA

Professor Corradetti in Rome has kindly permitted me to mention an unpublished work of his in which he obtained good evidence that selection of progenies of Culex which had fed upon birds or mammals resulted in an increased index of adaptation to the blood of the kind of host upon which they had fed, He now takes advantage of this finding by routinely making selections of this type when planning research involving a particular vertebrate host. In the present review, references have been found to tests of the susceptibility of species of avian malaria in only 7 of the 20 genera containing species which suck blood. As shown in Table III all of these except Psorophora contain species which are susceptible to one or more species of avian malaria. Even this exception is based upon the examination of only one mosquito. It seems significant that susceptibility of species to avian malaria has been found in such a high percentage of genera tested. It would seem safe to predict that susceptible species of mosquitoes will be III

of Species of MosquitoesSusceptible to Avian Plasmodium and the Total Number

of Species Tested Genera of mosquitoes

Species of Plasmodium cathemerium

Anopheles 3/6”

circumflexurn elongatum

o/3

jallax

l/l

gallinaceum

3/9

juxtanucleare lophurae

Culiseta

ManSO?Zi

l/l

Psorphora o/1

Aedes

2/7

Armigenes

7/10

O/l

O/5

l/3

30

O/l

l/7

6/6

41

213

87

3/s

77

4/J l/l

l/l

23/23

6/6

O/l 3/3

l/l

Total Genera susceptible to all parasites tested (%)

5/b 13/26

50

46

2/2

l/l

t-O&

relicturn

Culex

Mosquitoes susceptible to each species of parasite (%)

2/2 617

4/5 l/l

85

Q Numbers of susceptible species in the numerators;

O/l

34/57

59

2/2

100

3/5

60 92

ll/ll

b/7

85

total numbers in the denominators.

36/49

73

128

HUFF

TABLE IV Species of Plasmodium of Birds for Which NO Susceptible Mosquitoes Have Been Found P. durae Herman, 1941 P. formosanum Manwell, 1962 P. hexamerium Huff, 1935 P. hufi Muniz, Soares, and Batista, 1951 P. nucleophilum Manwell, 1935 P. pinottii Muniz and Soares, 1953 P. polare Manwell, 1934 P. vaughani Novy and MacNeal, 1908 P. *biziurae Gilruth, Sweet, and Dodd, 1910 P. *columbae Carini, 1912 P. *grassii Labbe, 1894 P. *lutzi Lucena, 1939 P. *major Raffaele, 1930 P. *mujoris Laveran, 1902 P. *malariae raupachi Parcvanidze, 1914 P. *paddae Brumpt, 1935 P. *passeris Johnston and Cleland, 1909 P. *subimmaculatus Grassi and Feletti, 1890 P. *subpraecox Grassi and Feletti, 1892 P. *wasielewskii Brumpt, 1910 * Species of questionable

status.

found in a considerable proportion of the blood-sucking genera which as yet remain unstudied. Less we fall into the same error as in the above-cited case of assuming that only culitine mosquitoes could transmit avian malaria, it would appear that the possibilities of transmission of some of these species of Plasmodium by other blood-sucking orthorrhaphous diptera such as the Ceratopogonidae, Psycodidae, Simuliidae, and Tabanidae should be investigated. In addition to the well-known ability of species of Simuliidae to transmit Leucocytozoon, it has now been shown that transmission of both Haemoproteus and LEUcocytozoon can be effected by species of Culicoldes (Fallis and Bennett, 1960, 1961a, 1961b for Haevnoproteus; Akiba, 1960 for Leucocytozoon). It is likely that very few attempts have been made to transmit avian malaria (Plasmodium) by any of the bloodsucking Diptera except the Culicidae. Because of the fact that studies have been made on such a small proportion of the known avian malarial parasites and of the known blood-sucking species of mosquitoes, any gen-

eralizations upon the known data should be made with great caution. With this qualification the following tentative statements are made : 1. The systematically close relationship between Aedes and Armigeres is reflected in their susceptibility to P. gallinaceum. 2. The susceptibility of species of Aedes to P. fallax, P. gallinaceum, and P. lophurae reflects the known close relationship of these three parasites. 3. The close relationship between P. relicturn and P. cathemerium is reflected in the relatively high susceptibility of Culex to both of them. 4. Plasmodium elongatum would appear to be more closely related to the relictum-cathemerium group than to the fallax-gallinaceumlophurae group of parasites. If the large gaps in our knowledge were filled in by more extensive study of the interrelationship between blood-sucking mosquitoes and the species of Plasmodium which parasitize birds, it appears likely that we could reach a better understanding of the evolution and speciation of both the Plasvnomodidae and the Culicidae. The best working hypothesis at present seems to be that the association of malarial parasites and Culicidae has been a long one during which speciation occurred in each. No very strict lines of specificity of any group of these parasites for a group of their mosquito hosts can be drawn at this time. ACKNOWLEDGMENT

I want to express my gratitude to Dr. A. B. Weathersby for his suggestions regarding nomenclature and systematics of the mosquitoes. REFERENCES

K. 1960. Studies on the Leucocytozoon found in the chicken in Japan. II. On the transmission of L. caulleryi by Culicoides arakawae. Japanese Journal of Veterinary Science 22, 309317. BARRETO, P. 1943. SBbre a infecf5o experimental do A.(N) norestensis pelo Plasmodium cathemerium. An. paulis. med. e cir. 46(2), 142. AKIBA,

SUSCEPTIBILITY

OF MOSQUITOES

BASU, B. C.

1938. Studies on a malarial infection in a paddy bird. Journal of the Malaria Institute

of India 1, 273-284. BRUMPT, E. 193.5. RCceptivitC

de divers

oiseaux

domestiques et savages au parasite (Plasmodium gallinaceum) du paludisme de la poule domestique. Transmission de cet hematozoaire par le moustique Stegomyia jasciata. Comptes Rendus Hebdomadaires des Seances de l’tlcademie des Sciences 203, 750-52. BRUMPT, E. 1936. Etude experimentale du Plasmodium gollinaceum parasite de la poule domes-

tique. Transmission de ce germe par Stegomyia jasciata et Stegomyia albopicta. Annales de Parasitologie Humaine et Comparee 14, 597-620. CANTRELL, W., AND JORDAN, H. B. 1945. New mosquito hosts for Plasmodium gallinaceum. Journal of Parasitology 31, 55-56. CANTRELL, W., AND JORDAN, H. B. 1949. Relative susceptibility of ABdes aegypti, Ai;des albopictus, Aides can&e& and Anopheles quadrimaculatus to Plasmodium gallinaceum. Journal of Xnjectious Diseases 66, 170-172. CERQUEIRA, N. L., AND PARAENSE, W. L. 1945.

Uma nova especie de Aedes, transmissora de Plasmodium gallinaceum. Memdrias do Institute Oswald0 Crux 42, 11-15. COGGESHALL, L. T. 1940. The infection of Anopheles quadrimaculutus with monkey malaria parasite, Plasmodium cynomolgi and with an avian parasite, Plasmodium lophurae. Journal of Parasitology 26 (Suppl.), 44-45. COGGESHALL,L. T. 1941. Infection of Anopheles quadrimaculatus, with a monkey malaria parasite, and with Plasmodium lophurae, an avian malaria parasite. American Journal of Tropical Medicine 21, 524-530.

TO

AVIAN

129

MALARIA

albimanus to primate and avian malaria?,. Mosquito News 20, 368-371. FALLIS, A. M., AND BENNETT,G. F. 1960. Description of Haemoproteus canachites nsp. and sporogony in Culicoides. Canadian Journal of Research (Zoology) 26, 455-464.

FALLIS, A. M., AND BENNETT, G. F. 1961a. Ceratopogonidae as intermediate hosts for Haemoproteus and other parasites. Mosquito News 21, 21-28. FALLIS, A. M., AND BENNETT, G. F. 1961b. Sporogony of Leucocytozoon and Haemoproteus in simuliids and ceratopogonids and a revised classification of the Haemosporidiida. Canadian 39, 215-228. Journal of Research (Zoology) GRUNDMANN, A. W., NEWSON, H. D., AND WARNOCK,

R. G. 1952. Non-human malaria in mosquitoes and the English sparrow, Passer domesticus Linn., in the vicinity of Salt Lake City, Utah. Mosquito News 12, 53-57. HAAS, V. H., AND AKINS, H. 1947. Transmission of Plasmodium gallinaceum by Anopheles quadrimaculatus. Journal of the National Malaria Society 6, 244-245. HE~.MAN, C. M. 1938. Mosquito transmission of avian malaria parasites (Plasmodium circumflexurn and P. cathemerium). American Journal of Hygiene 27, 345-350.

HUFF, C. G. 1927. Studies on the infectivity of Plasmodia of birds for mosquitoes with special reference to the problem of immunity in the mosquito. American Journal of Hygiene 7, 706734.

HUFF, C. G. 1929. The effects of selection upon susceptibility to bird malaria in Culex pipiens Linn. Annals of Tropical Medicine and Parasitology

23, 427-439.

CORRADETTI, A., NERI, I., AND SCANGA, M. 1960. Segnalazione in Italia di Plasmodium praecox var. matutinum in Turdus iliacus, e separazione di quest0 Plasmodio da Plasmodium praecox come specie distinta: Plasmodium matutinum Huff, 1937. Parassitologia 2, 333-343. DANIELS, C. W. 1899. On the transmission of Fro-

HUFF, C. G. 1930. Plasmodium elongatum n.sp., an avian malarial organism with an elongate gametocyte. American Journal of Hygiene 11, 385-391. HUFF, C. G. 1931. The inheritance of natural immunity to Plasmodium cathemerium in two species of Culex. Journal of Preventive Medicine

teosoma to birds by the mosquito. Proceedings of Royal Society (London), Ser. B 64, 443-454. DASGUPTA, B., AND RAY, H. N. 1956. Aedes albopictus as vector of Plasmodium gallinaceum. Bulletin of the Calcutta School of Tropical Medicine 4, 63. EYLES, D. E. 1952. Studies on Plasmodium gattinaceum. IV. A comparison of the susceptibility of Aedes aegypti, Anopheles quadrimaculatus and Anopheles jreeborni. American Journal of Hygiene 66, 71-77. EYLES, D. E. 1960. Susceptibility of Anopheles

6, 249-259. HUFF, C. G. 1932. Further infectivity

experiments mosquitoes and bird malaria. American Journal of Hygiene 16, 751-754. HUFF, C. G. i937. A new variety of Plasmodium relicturn from the robin. Journal of Parasitology with

23, 400-404. HUFF, C. G. 1940.

Quantitative

studies

on size,

variability and growth rates of oocysts of different strains of avian malaria. American Journal of Hygiene 32, 71-80. HUFF, C. G. 1948. Natural immunity and suscepti-

130

HUFF

bility of doves and pigeons to exoerythrocytic and erythrocytic stages of Plasmodium relic&m. Proceedings of 4th Znzternational Congress of Tropical Medicine and Malaria, 602-606. HUFF, C. G. 1954. A review of the literature on susceptibility of mosquitoes to avian malaria with some unpublished data on the subject. Naval Medical Research Institute Research Report 12, 619-644. HUFF, C. G. 1963. Experimental research on avian malaria. In “Advances in Parasitology” (B. Dawes, ed.), pp. l-65. Academic Press, New York. HUFF, C. G., AND MARCHBANK, D. F. 1955. Changes in infectiousness of malarial gametocytes. I. Patterns of oocyst production in seven host-parasite combinations. Experimental Parasitology 4, 256-270. HUFF, C. G., AND SRIROISHI, T. 1962. Natural infection of Humboldt’s penguin with Plasmodium elongatum. Journal of Parasitology 48, 495. HUFF, C. G., COULSTON, F., LAIRD, R. L., AND PORTER, R. J. 1947. Pre-erythrocytic development of Plasmodium lophurae in various hosts. Journal of Infectious Diseases 81, 7-13. HUFF, C. G., MARCHBANK, D. F., SAROFF, A. H., SCRIMSHAW, P. W., AND SHIROISHI, T. 1950. Experimental infections with Plasmodium fallax Schwetz isolated from the Uganda tufted guinea fowl Numida meleagris major Hartlaub. Journal of the National Malaria Society 9, 307-319. HUFF, C. G., MARCHBANK, D. F., AND SHIROISHI, T. 1958. Changes in the infectiousness of malarial gametocytes. II. Analysis of the possible causative factors. Experimental Parasitology 7, 399417. HUFF, C. G., MARCHBANK, D. F., AND SRIROISHI, T. 1959. Susceptibility and resistance of avian and mosquito hosts to strains of Plasmodium relic&m isolated from pigeons. Journal of PYOtozoology 6, 46-51. HUNNINEN, A. V. 1953. Comparative development of Plasmodium relicturn oocysts in Anopheles quadrimaculatus, A. albimanus and Culex pipiens. Journal of Parasitology 39, 28-32. HUNNINEN, A. V., YOUNG, M. D., AND BURGESS, Q. W. 1950. The infection of anopheline mosquitoes by native avian malaria. Journal of the National Malaria Society 9, 145-150. HUNNINEN, A. V. 1951. Comparative susceptibility of four anopheline mosquitoes to Plmmodium relicturn. Journal of the National Melaria Society 10, 216-223. HURLBUT, H. S., AND HEWITT, R. 1941. Sporozoites of Plasmodium lophurae, an avian malaria parasite, in Anopheles quadrimaculatus.

United States Public Health Report 56, 13361337. HURLBUT, H. S., AND HEWITT, R. 1942. The transmission of Plasmodium lophurae, an avian malaria parasite by Anopheles quadrimaculatus. United States Public Health Report 57, 1891.. 1892. INOKI, S. 1951. Studies on the exoerythrocytic schizogony of the malarial parasite. Exoerythrocytic forms of the bird malarial parasites. Medical Journal of Osaka University 2, 61-73. JAMES, S. P. 1902. Malaria in India. Scientific Memoranda by Offices of Medical and Sanitation Departments, Government of India New Series No. 2. JEFFERY, G. M. 1944. Investigations on the mosquito transmission of Plasmodium lophurae Coggeshall 1938. American Journal of Hygiene 40, 251-263. KATAHIRA, J. 1929. Beitrag zur Kenntnis uber Vogelmalaria (Proteosoma praecox) . Formosan Medical Journal 292, l-67 (In Japanese, with German summary). KOCH, R. 1899. Uber die Entwickelung der Malariaparasiten. Zeitschrift fur Hygiene 23, l-24. LAIRD, R. L. 1941. Observations on mosquito transmission of Plasmodium lophurae. American Journal of Hygiene 34C, 163-167. LAWRENCE, J. J., AND BEARUP, A. J. 1961. A new host for Plasmodium relictum: the silver gull (Larus novae-hollandiae Stephens). Indian Journal of Malariology 15, 11-19. LUCENA, D. 1938. Malaria aviaria. IV. Infec@o experimental do Culex fatigans Wiedemann, 1828 e do Anopheles strodei Root, 1926 pelo Plasmodium cathemerium Hartman. Revista de Biologia e Hygiene 9, 47-50. MANWELL, R. D. 1940. Life-cycle of Plasmodium relicturn var. matutinum. American Journal of Tropical Medicine 20, 859-866. MANWELL, R. D. 1947. Failure of Aedes aegypti and Culex pipiens to transmit Plasmodium vaughani. Journal of Parasitology 33, 167-169. MANWELL, R. D. 1962. A new species of avian Plasmodium. Journal of Parasitology 9, 401-403. MAYNE, B. 1928. An anopheline mosquito as host for the parasites of bird malaria. Indian Journal of Medical Research 16, 557-558. MICKS, D. W. 1949. Investigations on the mosquito transmission of Plasmodium elongatum Huff. Journal of the National Malarial Society 8, 206-218. MICKS, D. W., AND MCCOLLUM, V. 1953. The infection of Anopheles quadrimaculatus, a human malaria vector, with Plasmodium catheme&m, an avian malaria parasite. American

SUSCEPTIBILITY

OF MOSQUITOES

Journal of Tropical Medicine and Hygiene 2, 930-932. MOHAN, B. N. 1955. Comparative susceptibility of some Aedes mosquitoes to Plasmodium gallinaceum. Indian Journal of Malariology 9, 75-79. MOK, F. F. 1951. Transmission of Plasmodium relictum Grassi & Feletti by Anopheles jreeborni Aitken. Science 113, 485. NEUMANN, R. 0. 1908. Die ubertragung von Plaspraecox auf Kanarienvijgel durch modium Stegomyia jaxiata und die Entwicklung der Parasiten im Magen und der Speicheldriisen dieser Stechmiicke. Archiv fur Protistenkunde 13, 23-69. NONO, A. M. 1932. Avian malaria studies. VI. Susceptibility of Lutzia juscana (Wiedemann) Edwards to avian malaria. Philippine Journal of Science 49, 225-229. OKPALA, I. 1958. Transmission of Plasmodium gallinaceum through Aedes stokesi. West African Medical Journal 7, 195-196. PARAENSE, W. L. 1944. InfecgLo experimental do Culex quinquejasciatus pelo Plusmodium juxtanucleare. Memdrias do Institute Oswald0 Cruz 41, 535-540. PARAENSE, W. L. 194.5. A transmissLo de Plasmod&m gallinaceum pelo Aedes (Ochlerotatus) lepidus. Memdrias do Institute Oswald0 Cruz 42, 81-84. RAFFAELE, G.

1934. Un ceppo italiano di Plasmodium elongatum. Rivista di Malariologia 13, 332-337. RAFFAELE, G. 1936. I1 doppio ciclo schizogonico di Plasmodium elongatum. Rivista di Malariologia 15, 309-317. REDMOND, W. B. 1944. Mosquito transfer of the pigeon strain of Plasmodium relicturn. Journal of Infectious Diseases 74, 184-188. REEVES, W. C., HEROLD, R. C., ROSEN, L., BROOKMAN, B., AND HAMMON, W. McD. 1954. Studies on avian malaria in vectors and hosts of encephalitis in Kern County, California. II. Infections in mosquito vectors. American Journal of Tropical Medicine and Hygiene 3, 696-703. REICHENOW, E. 1932. Die Entwicklung von Proteosoma circumflexurn in Theobaldia annulata nebst Beobachtungen iiber das Verhalten anderer Vogelplasmodien in Miicken. Jenaische Zeitschrijt Naturwissenschajt 67, Festschrift Ludwig Plate: 434-451. a Plasmodium relicRODHAIN, J. 1939. L’infection turn chez les pingouins. Annales de Parasitologic Humaine et Comparte 17, 139-157. ROMANA, C., GIL, J., HEREDIA, R., AND RACEDO, P. 1946. Paludismo de aves argentinas. Anales de1 Institute de Medicina Regional 1, 309-316.

TO AVIAN

131

MALARIA

ROSEN, L., AND REEVES, W. C. 1954. Studies on avian malaria in vectors and hosts of encephalitis in Kern County, California. III. The comparative vector ability of some of the local culicine mosquitoes. American Journal of Tropical Medicine and Hygiene 3, 704-708. ROSS, R. 1898. Report on the cultivation of Proteosoma Labbe in grey mosquitoes. Indian Medical Gazette 33, 401-448. R~UBAUD, E., COLAS-BELCOUR, J., AND MATHIS, M. 1939. Transmission de Plasmodium gallinaceum par Aedes geniculatus. Bulletin de la Societt de Pathologie Exotique 32, 28-30. ROUBAUD, E., AND MEZGER, J. 1934. Sur la sensibilitC au pauldisme des oiseaux (Plasmodium relic&m) des divers peuplements raciaux du moustique commun, Culex pipiens, L. Comptes Rendus Academic de Sciences 199, 170-172. RUGE,

R.

1901.

Untersuchungen

iiber

das deutsch

Proteosoma. Zentralblatt jiir bakteriologie parasitenkunde und infektionskrankheiten 29, 187191.

RUSSELL, P: F. 1931. Anopheles mosquitoes and avian malaria. American Journal of Tropical Medicine 11, 145-146. RUSSELL, P. F. 1932. Avian malaria studies. V. Plasmodium capistrani sp. nov., an avian malaria parasite in the Philippines. Philippine Journal of Science 48, 269-289. RUSSELL, P. F., AND MENON, P. B. 1942. On the transmission of Plasmodium gallinaceum to mosquitoes. American Journal of Tropical Medicine 22, 559-563. RUSSELL, P. F., AND MOHAN, B. N. 1942. Some mosquito hosts to avian plasmodia with special reference to Plasmodium gallinaceum. Journal of Parasitology 28, 127-129. SCHINAZI, L. A., AND BALL, G. H. 1956. Changes in infectivity of Plusmodium relicturn for avian hosts. Experimental Parasitology 6, 541-550. SERGENT, ED., AND SERGENT, ET. 1907. lhudes sur les hematozoaires d’oiseaux. Annales de Z’lnstitut Pasteur 21, 251-280. SERGENT, ED., AND SERGENT, ET. 1918. Sur le paludisme des oiseaux du au Plmmodium relicturn (vel Proteosoma). Annales de l’lnstitut Pasteur 32, 382-389. SERGENT, ET. 1940. Paludisme des oiseaux. Receptivite des moustiques a I’infection du Plasmodium relicturn. Archives de l’lnstitut Pasteur d’dlgerie 18, 2 14-215. SINGH, JASWANT, AND MOHAN, B. N. 1955. SUSceptibility of Culel: (Culex) bitaeniorhynchus Giles, 1901, to Plasmodium relicturn but not to Plasmodium gallinaceum and Plasmodium f&iparum. Indian Journal of Malariology 3, 71-74.

132

HUFF

B. 1946. Two new Japanese species of mosquitoes as hosts of avian malaria. Japanese Journal of Clinical and Experimental Medicine 23, 420-422. TATE, P., AND VINCENT, M. 1934. The susceptibility of autogenous and anautogenous races of C&x pipiens to infection with avian malaria (Pkzsmodium relicturn). Parasitology 26, 512-522. TERZIAN, L. A., STAFILER, N., AND IRREVERRE, F. 1956. The effects of aging, and the modifications of these effects, on the immunity of mosquitoes to malarial infection. Journal of Zmmunology 76, 308-3 13. TRAGER, W. 1942. A strain of mosquito, Aedes aegypti, selected for susceptibility to the avian malaria parasite Plasmodium lophurae. Journal of Parasitology 26, 457-465. TREMBLEY, H. L. 1946. Aedes atropalpus (Cog.), a new mosquito vector of Plasmodium gallinaceum Brumpt. Journal of Parasitology 32, 499501. VARGAS, L. 1949. Culicine and Aedine mosquitoes and the malaria infections of lower animals. In TANAKA,

“Malariology” (M. F. Boyd, ed.), Chapter 22, pp. 5’26-535. Saunders, Philadelphia, Pennsylvania. VARGAS,L., AND BELTRAN, E. 1941. Culex quinquefascia&s, a new vector of Plasmodium gallinaceum. Science 94, 389-390. WARD, R. A. 1963. Genetic aspects of the susceptibility of mosquitoes to malarial infection. Experimental Parasitology 13, 328-341. WARREN, McW., AND WHARTON, R. H. 1963. The vectors of simian malaria: identity, biology, and geographical distribution. The Journel of Parasitology 46, 892-904. WEATHERSBY, A. B. 1962. Susceptibility of certain Japanese mosquitoes to Plasmodium gallinaceum and Plasmodium berghei. Journal of Parasitology 46, 607-609. WILLIAMSON, K. B., AND ZAIN, M. 1937. A presumptive culicine host of human malaria parasites. Transactions of the Royal Society of Tropical Medicine and Hygiene 31, 111-114. WOLFSON, F. 1946. Plasmodium elongatum in the Pekin duck. American Journal of Hygiene 44, 268-272 (Cites transmission by Manwell).