Pathogens of Vertebrates and Plants as Pathogens of Their Acarine and
JOHN PAUL KRAMER
Section of Economic Entomology, Illinois Natural History Survey, Urbana, Illinois
I. Introduction . . . . 251
II. Viruses . . . . 252
III. Rickettsiae . . . . 254
IV. Bacteria . . . . 254
A. Pasteurella pestis (Lehmann and Neumann) . . . 254 B. Pasteurella tularensis (McCoy and Chapin) . . . . 257
C. Species of Salmonella . . . . 258
D. Spirochetes . . . . 259
V. Protozoa . . . . 259
A. Trypanosomatidae . . . . 259
B. Species of Plasmodium . . . . 262
C. Other Protozoa . . . . 264
VI. Helminths . . . . 265
A. Filarioidea .. .. 265
B. Other Helminths . . . . 266
VII. Discussion . . . . 267
References . . . . 268
Many microorganisms and helminths causing diseases of higher ani
mals and of plants multiply and/or undergo cyclic development in their acarine and insect vectors. Hence, these agents of disease are true parasites of their vectors. Are these parasites ever harmful to the vec
tors? In the present chapter I have attempted to consider this aspect 251
of the pathogen-vector relationship. Most of the evidence rests on mor
tality studies of populations of infected (parasitized) arthropods. In a few cases there is some evidence based on histological, physiological, and symptomatological data; all too frequently mortality studies have not included data of this type. Other pertinent data are fragmentary and disjunctive and often are immersed in reports which are only inci
dentally concerned with the harmful effects on the vectors. Recognizing the limitations of these data, only a few tentative generalizations have been drawn by this author. Finally, it must be mentioned that positive evidence has been emphasized in this discussion in order to make the reader aware of these microorganisms and helminths as insect pathogens.
I I . VIRUSES
It has been amply demonstrated that at least twenty vertebrate viruses and about ten plant viruses multiply in their arthropod vectors. Fa
miliar examples are the yellow-fever virus in the mosquito Aedes aegypti (Linnaeus) (Whitman, 1937), and the clover-club-leaf virus in the leaf hopper Agalliopsis novella (Say) (Black, 1950). As far as the viruses of vertebrates are concerned, no evidence of significant alteration on the cellular level has been found in the arthropod vectors in spite of the fact that many tissues of the vector can be rather heavily infected.
In addition, there is no evidence that such infections affect the overall well-being of the vector in any manner. T h e apparent harmlessness of these viruses to their vectors is illustrated in a study by La Motte (1960).
He found that the virus of Japanese Β encephalitis multiplies in the abdominal part of the midgut, salivary glands, ovaries, nervous tissue, and certain other tissues of adult Culex pipiens pipiens Linnaeus. Since the mosquito has little, if any, capability for replacing cellular elements severely damaged by an infection, one would expect to see major cellular changes if the virus caused any such changes. However, La Motte's detailed cytological studies on tissues of mosquitoes which were infected from 1 to 40 days prior to sacrifice, revealed no changes attributable to the virus infection. He also compared the longevity of infected and virus-free mosquitoes and found no differences.
Evidence concerning the effects of plant viruses on their vectors stands in sharp contrast to comparable evidence for vertebrate viruses.
T h a t a plant virus may in fact alter the tissues of its vector was suggested by Littau and Maramorosch (1956). They found that the nuclei of fat-body cells of Macrosteies fascifrons (Stäl) infected with aster-yellows virus were stellate with reticulate cytoplasm. In virus-free leafhoppers the nuclei of fat-body cells were more or less rounded with homogeneous cytoplasm. As yet there is no evidence that this virus is harmful to
M. fascifrons. Some relevant physiological data have been provided by Yoshii and Kiso (1957) for Geisha distinctissima (Walker), a plant- hopper vector of the virus causing dwarf disease of orange. They re
ported that oxygen consumption in the vector as well as in the host plant is reduced in the presence of the virus. T h e authors do not elaborate on the effects on the vector. However, this reduction in oxygen utilization strongly suggests a deleterious effect on the vector.
T h e first real evidence that a plant virus can shorten the life span of its arthropod vector was presented by Jensen (1958, 1959a, b ) . He found that the peach yellow leaf strain of western X-disease virus causes the premature death of its leafhopper vector Colladonus mon- ianus (Van Duzee). He compared the mean longevity of large groups of infected and virus-free individuals and found highly significant differ
ences. T h e mean longevity for the former was about 20 days and for the latter 51 days. By testing infected and noninfected leafhoppers which had fed on diseased plants, he also demonstrated that the ob
served reductions in longevity could not be attributed to the deranged physiology of the host plant. Jensen (1960) has also found that virus- infected C. montanus lay fewer eggs than do uninfected individuals.
Ehrhardt (1960) reported that oxygen consumption in Myzus per- sicae (Sulzer) was reduced from 2.95 milliliters per gram body weight per hour to 2.01, a reduction attributable to potato leaf roll virus. T h e insects were given an 8-hour acquisition feeding period on a virus- infected plant and then were held on host plants immune to the virus.
Although the insects were tested throughout an 80-hour period, the maximum reduction (approximately 30 percent) was reached within
30 hours on the immune host.
Watson and Sinha (1959) observed some interesting effects of the European wheat striate mosaic virus on its planthopper vector Delpha- codes pellucida Fabricius. Infective females that fed on infected plants as nymphs had 40 percent fewer progeny than those fed on healthy plants. Some embryos died in the egg at a late stage of develop
ment. This suggests that the virus was pathogenic to them. Additional evidence that homopterans which have acquired a plant virus by trans- ovarial transmission are harmed by a virus has been reported by Shinkai
(1960). He found that leafhoppers, Inazuma dorsalis (Motschulsky) (= Deltocephalus dorsalis Motschulsky), which have acquired the rice dwarf virus through the egg tend to die before attaining the adult stage.
These exciting discoveries, which clearly indicate that certain plant viruses harm their vectors, should stimulate further studies on other arthropods infected with virus pathogens of plants as well as similar studies on arthropods infected with virus pathogens of vertebrates.
I I I . RICKETTSIAE
Those arthropod-borne rickettsiae which cause diseases of man and other vertebrates multiply intensively in their natural vectors (see also Chapter 1 7 ) . Of special interest is the agent of epidemic typhus Rickett
sia prowazekii da Rocha-Lima which is pathogenic to its vector Pediculus humanus humanus Linnaeus. According to da Rocha-Lima (1916), who first described this harmful pathogen-vector relationship, and to Weyer (1960), Zdrodovskii and Golinevich (1960), and others, R. prowazekii, ingested with a blood meal, invades the epithelial cells of the gut.
Here the microorganisms multiply, and within a few days these cells, which are now packed with rickettsiae, burst and discharge their con
tents into the lumen of the gut. Most infected lice die within 12 days after an infective meal whereas uninfected lice may live for 30 to 60 days. Moribund lice turn reddish in color; this results from the escape of ingested blood from the gut through the damaged gut wall to the coelomic cavity. Such lice die within a few hours. Although death of the louse results primarily from the destruction of the gut epithelium, Weyer (1960) suggests that a toxin may also be involved.
Mooser and Castaneda (1932) traced the development of the agent of murine typhus R. typhi (Wolbach and Todd) ( = R. mooseri Monteiro) in its usual vector Xenopsylla cheopis (Rothschild) as well as in other fleas. They found that rickettsiae multiply in the gut epithelium and in cells of the Malpighian tubes of the flea. Unlike R. prowazekii in the louse, R. typhi causes no ill effects in the flea since fleas are able to re
generate damaged epithelium whereas lice cannot. In acarine vectors of other pathogenic rickettsiae, a generalized type of infection is not uncommon. For instance, Parker and Spencer (1926) found the agent of Rocky Mountain spotted fever, R. rickettsii (Wolbach), in the brain, muscles of the chelicerae, genital organs, and salivary glands as well as in the gut and Malpighian tubes of infected Dermacentor andersoni Stiles. Yet, as Philip (1958) notes, this and other rickettsial pathogens of vertebrates have no known harmful effects on their acarine vectors.
I V . BACTERIA
A. Pasteurella pestis (Lehmann and Neumann)
T h e voluminous literature concerned with the complex interrela
tionships of Pasteurella pestis, its flea vectors, and its vertebrate hosts reflects the tremendous importance of plague as a disease which has caused widespread mortality in human populations up to the twentieth century. Of special interest in the present discussion, however, is the fact that plague is a disease of fleas as well as of rodents and human beings.
T h a t the plague bacillus is carried by fleas was firmly established early in the present century. An account of the numerous studies which led to this discovery is beyond the scope of the present chapter, and the reader is referred to a concise review by Jellison (1959). Neverthe
less, several pioneering studies should be mentioned. Simond (1898) suggested that fleas probably transmit the plague organism. Zirolia
(1902) observing Pulex nutans Linnaeus, and Liston (1905) observing Xenopsylla cheopis, found that P. pestis can multiply in the stomach of
the flea. Bacot and Martin (1914) not only discovered the mechanism by which fleas usually transmit P. pestis, but they also noted that P.
pestis may harm the flea as well. A flea feeding upon the blood of an infected host ingests the plague bacilli which then may multiply in its proventriculus and stomach, sometimes becoming so numerous as to block the lumen of the esophagus as well as that of the proventriculus.
In the attempts of such a flea to feed, blood carrying some plague bacilli is regurgitated and injected back into the host. In the fleas the tough jellylike culture masses of P. pestis may be autolyzed after a few days, and the normal passage of blood is restored. On the other hand, fleas with this obstruction may die before the culture masses have lysed.
Bacot and Martin suggested that such fleas, being unable to feed, suc
cumb to death by desiccation, especially under conditions of high tem
perature and low atmospheric humidity.
Since the remarkable discovery of Bacot and Martin, mentioned above, scores of workers have observed the blocking phenomenon in a great number of flea species. In any species blockage is not constant, and hence it is difficult to make generalizations. T h e development of the proventricular block, however, seems to follow a different course in different fleas. For instance, in X. cheopis which is the classical vector of P. pestis, blockage may occur in a matter of days and about 50 percent of the individuals may eventually show blockage. In contrast, under similar conditions of temperature and humidity, it may take as long as two months for proventricular blockage to occur in most wild-rodent fleas, and comparatively few individuals may be so affected. Doubtless these variations in time and extent of blockage are due to subtle differ
ences in the morphology and physiology of various flea species. Whether or not blockage takes place depends also upon the temperature of the environment of the flea. For example, Kartman et al. (1958) state that temperatures in the range of about 20 to 22°C with high humidity favor the growth of P. pestis in the flea; temperatures of about 27°C with high humidity are harmful to both the ingested bacilli and the flea. In addition, these workers believe that blockage in the flea may depend also upon the number of bacilli ingested during its infective
feeding. T h e factors influencing the development of the proventricular block, including the temperature-humidity relationships, need further elucidation.
T h e lodgment and multiplication of the plague bacilli among the spinelike epithelial cells of the proventriculus of the flea constitute the mechanism of blockage. T h e bacillus apparently does not invade the tissues of the flea, and generally the deleterious action of the bacillus on the flea is thought to be purely mechanical, as originally suggested by Bacot and Martin (1914). Several workers, however, have presented evi
dence that indicates that other factors may be involved. For instance, Kartman et al. (1956) found that the survival time of starved P. pestis- free X. cheopis is considerably greater than that of other X. cheopis which have been permanently blocked by P. pestis. In all probability, the plague endotoxin also contributes to the death of the permanently blocked flea although this has not been demonstrated.
T h e plague-stricken flea has been described by Holdenried (1952).
These permanently blocked fleas gradually shrink while they are still alive. T h e abdominal segments telescope anteriorly into each other, and the alimentary canal and other abdominal organs are forced into the thorax. Such withered fleas die within 1 to 4 days after blockage has occurred. In contrast, well-fed healthy fleas may live for five months to a year or more (Burroughs, 1953). From an epidemiological standpoint, it is well to note that fleas which have lost their proventricular block, although they often harbor P. pestis, are also long lived. This and other aspects of the complex P. pestis-Rea relationship are discussed in great detail by Hirst (1953) and Pollitzer (1954).
Other insects and acarines which have been incriminated in the transmission of plague may also succumb to the effects of P. pestis.
Bacot (1915) and Cornwall and Menon (1917) found that a large pro
portion of bed bugs (Cimex lectularius Linnaeus), especially first-instar nymphs, die soon after feeding on infective blood. Sassuchin and T i k - homirova (1936), while studying the persistence of P. pestis in ticks, found that over 60 percent of the larvae and nymphs of Dermacentor silvarum Olen under investigation died when given an infective meal.
Nuttall (1897) studied P. pestis in adult house flies (Musca domestica Linnaeus) and concluded that plague infection was fatal for them, especially at temperatures around 30°C. Gosio (1925) observed that larvae of M. domestica and certain blow flies often ingest P. pestis while feeding on the dead bodies of infected rodents. Such larvae complete their development in a normal manner, though numerous plague bacilli can be found both in the ventriculus and in the feces. Only small num
bers of bacilli persist in the pupae. T h e adult flies emerging from these
are normal for a time, but soon develop large numbers of plague bacilli, and many die in 15 to 24 hours. Healthy flies in a control group lived about 7 days. As in the case of the flea, the way in which P. pestis overcomes these minor vectors is not entirely clear. Blockage as it occurs
in the flea is probably of little or no importance. In general, the afore
mentioned workers suggest that plague-stricken bed bugs, ticks, and flies die from a toxemia—a septicemia exerting a secondary effect.
B. Pasteurella tularensis (McCoy and Chapin)
Pasteurella tularensis is the etiological agent of tularemia, a disease of rodents, lagomorphs, and occasionally of man. Ticks, of prime im
portance in the present discussion, are probably the most notable vec
tors of P. tularensis. While some ticks may acquire P. tularensis by transovarial transmission, these acarines usually acquire the bacillus with a blood meal from an infected host. T h a t ingested bacilli may invade and multiply within the epithelial cells of the gut of Dermacentor an
der soni, a noted vector of P. tularensis, was shown by Francis (1927).
Burgdorf er and Owen (1956) also demonstrated this phenomenon in several species of Ornithodoros which are potential vectors of the tula
remia bacillus; they found that infected epithelial cells become swollen and distended and eventually rupture, discharging their contents into either the gut lumen or the body cavity of the tick. After a time the salivary glands, central ganglion, coxal organs, tissues of the genital and of the excretory systems are invaded by P. tularensis. Although the aforementioned workers did not comment on the effects of the bacterium on the tick, the general observations of Philip and Jellison (1934) strongly suggest that massive doses of B. tularensis ingested with a blood meal may be fatal to the tick. While studying Dermacentor variabilis
(Say) as a host of the tularemia bacillus, these workers found a high mortality among engorged ticks which had fed on fatally infected hosts.
Death was especially common among ovulating females which had not detached until the death of the host. Mortality was also high among the progeny of these females. No precise investigations on the longevity of P. tularensis- infected ticks with detailed histological studies of such ticks are known to the writer. T h e results of such investigations will probably show that at least certain strains of P. tularensis can be path
ogenic to some, if not all, species of ticks.
In at least two other potential vectors of the tularemia organism, infection has been clearly demonstrated by histological methods. Francis
(1927) found that P. tularensis infects the gut epithelium and occasion
ally the Malpighian tubes of Cimex lectularius. In a detailed study by Price (1957), it was found that P. tularensis invades and multiplies in
the midgut lumen and coelomic cavity and within the epithelial cells of the midgut of Pediculus humanus humanus. As long as the infection is limited to the gut, the louse is apparently unharmed, but once the bacteria gain entry to the coelomic cavity, death occurs within 7 days.
Uninfected lice and lice with gut infections live for at least 35 days.
C. Species of Salmonella
Certain bacteria of the genus Salmonella are responsible for out
breaks of acute, and sometimes fatal, gastroenteritis with or without bacteremia in man and other vertebrates. Several arthropods which have been incriminated in the dissemination of these bacteria may them
selves be fatally affected. Rodhain and van Oye (1941) found that the Salmonella which causes paratyphoid of pigeons survives for at least three months when ingested by the tick Ar gas reflexus (Fabricius). T h e bacteria did not seem to harm the ticks at comparatively low tempera
tures, but at 22 °C or higher death was rapid. When this occurred, the body of the tick became dark brown and swollen; its legs became reddish, indicating a diffusion of ingested blood, and probably the bacteria as well, into its coelomic cavity. Parker and Steinhaus (1943) found that Salmonella enteritidis (Gaertner) ingested with a blood meal persists in the tick D. andersoni for as long as 35 days. They also noticed that S.
enteriditis can be lethal to the tick. Mackerras and Pope (1948) found that S. adelaide Cleland [ = S. species (Type Adelaide) Kauffmann and White] and some closely related forms persist in the gut of Nauphoeta cinerea (Oliver) and other cockroaches for as long as 42 days. These authors accepted these findings as evidence that the gut of the cockroach is infected. While infected roaches showed no obvious debility, a higher mortality was found in the infected group than in a control group.
Eskey et al. (1949), while studying the transmission of S. enteritidis by fleas, found that X . cheopis and Nosopsyllus fasciatus (Bosc) may develop fatal S. enteritidis infections. In fleas diagnosed as infected, the stomach has a dark cloudy appearance following a blood meal; in nor
mal fleas the stomach usually is uniformly bright red after feeding. T h e esophagus of the infected flea is outlined by very fine dark specks. T h e posterior third of the body cavity of the infected flea contains brownish discolored areas of varying size and intensity. Such conditions are absent in the normal flea. In some instances infected N. fasciatus developed a
"bloody" diarrhea. Fleas showing these symptoms usually died within 24 hours. Excessive defecation was not observed in X. cheopis. Efforts of infected fleas to feed were prolonged, and this was attributed to a loss of muscle tone. About 75 percent of the infected fleas observed by Eskey and associates died within 30 days after an infective meal; other
infected fleas were dead by the fortieth day. As has been noted earlier, normal well-fed fleas typically live for many months. Alverdes and Bieling (1949), while studying the fate of various bacteria in Pediculus vestimenti Linnaeus ( = P. humanus humanus Linnaeus), found that S.
typhosa (Zopf), S. paratyphi (Kayser), and other colon bacteria invade and multiply within the stomach cells of the louse. Such infections lead to a detachment of the stomach lining from which the lice die.
Similar results were reported by Milner et al. (1957), who further noted that 90 percent of the lice which had ingested S. enteritidis died in 24 hours and all died within 48 hours. Although S. typhi, S. paratyphi, and other species were found to be similarly infectious for lice, they were not as rapidly lethal at S. enteritidis.
Some spirochetes causing diseases of man and other vertebrates are transmitted by anoplurans and ticks. T w o well-studied examples are Borrelia recurrentis (Lebert) and B. duttoni (Novy and Knapp) which cause relapsing fevers of man and are transmitted by the louse P. hu
manus humanus and ticks of the genus Ornithodoros, respectively. While some ticks are transovarially infected, ticks generally and lice without exception acquire the spirochete with a blood meal from an infected vertebrate. Within a short time the spirochetes penetrate the gut wall of the arthropod and enter the coelomic cavity, where, after a time, they actively multiply in the coelomic fluid. In ticks the spirochetes may gradually spread to various organs including the coxal glands and salivary glands. In lice the spirochetes may invade the neural ganglia and muscles (see Heisch and Harvey, 1962). Even among heavily infected ticks and lice there is, however, no evidence of appreciable injury attrib
utable to the spirochetes. On the other hand, at least two workers, Pirot and Bourgain (1945), speculate that Ornithodoros tholozani (Laboulbene and Megnin) infected with Spirochaeta persica Dschunkowsky [= Bor
relia persica (Dschunkowsky)] may not live as long as uninfected ticks.
Many trypanosomes of the genera Leishmania and Trypanosoma causing diseases of man and other vertebrates are transmitted by insects which feed on blood. For instance, T. cruzi Chagas, the agent of Chagas*
disease, is transmitted by Panstrongylus megistus (Burmeister) and other reduvids. In the course of the life cycle in the vertebrate and insect, these trypanosomes not only assume various forms but they also multiply,
often prodigiously. Of primary interest, however, is the fact that most insect vectors are not appreciably harmed by these flagellate infections.
For example, intensive studies on the interaction of tsetse flies (Glossina spp.) and T. rhodesiense Stephens and Fantham, as well as other typa- nosomes involved in African sleeping sickness, have revealed no ad
verse effects on infected flies. This is probably not too surprising since, as Buxton (1955) points out, these trypanosomes never penetrate into the body cavity of the fly; they are at no time intracellular and are not transovarially transmitted. In addition, they never seriously obstruct the alimentary canal of the fly. In the main these generalizations seem to apply to the T . cn/zs'-reduvid relationship as well. But Wood (1942) discovered among a series of Triatoma protracta (Uhler) that had fed on infected mice one dead bug in which the body fluid was teeming with T. cruzi. This apparently indicates that T. cruzi may at times naturally invade the body cavity of the bug, resulting in the death of the vector.
While studying the life history and morphology of the etiological agent of Indian kala-azar, Leishmania donovani (Laveran and Mesnil), as seen in sections of infected Phlebotomus argentipes Annandale and Brunetti, Shortt et al. (1926) made a very interesting observation. T h e y noticed that the lumen of the pharynx of heavily infected flies is often completely blocked with a solid plug of L. donovani recalling the phe
nomenon which occurs in fleas infected with the plague bacillus. Smith et al. (1940, 1941), noting that blockage may be partial as well as com
plete, found that the passage to the midgut at the esophagus was com
pletely blocked in about 20 percent of P. argentipes infected in the lab
oratory. Once a fly is completely blocked, it is unable to take a second blood meal although it will attempt to do so. Under laboratory condi
tions such flies die within a few days. Why fatal blockage develops in only a small percentage of infected flies is not known. This blocking phenomenon apparently does not occur in other species of sand flies which transmit other species of Leishmania although there may be con
siderable growth of the flagellates at the anterior part of the midgut in most infected flies.
Although Trypanosoma lewisi (Kent) is normally a nonpathogenic parasite of rats, in at least one instance it has been associated with an unspecific fever in man (Hoare, 1949). This trypanosome transmitted by various fleas actually penetrates and multiplies within the epithelial cells of the stomach of the flea. According to Wenyon (1926), the host cell is reduced to a mere membrane enclosing a mass of trypanosomes.
T h a t this damage to the stomach cells harms the flea was demonstrated by Garnham (1955). He compared the daily death rates in groups of young adult fleas ( X . cheopis) which had fed on an infected rat with
similar rates in other groups composed of young adults which had fed on an uninfected rat. T h e results of his study clearly show there was a heavy death rate among infected fleas as compared with the controls during the first 3 to 4 days following the initial feeding. But rates of mortality in the infected and uninfected groups after the fourth day were not appreciably different.
Trypanosoma melophagium (Flu) is a common parasite of sheep;
apparently it is harmless under normal conditions although, according to Hoare (1923), it might be harmful in debilitated animals. T h a t this trypanosome can be pathogenic to its insect vector was noted by Nelson (1956). He found that a large number of sheep keds, Melophagus ovi- nus (Linnaeus), die on sheep as a result of blockage of the posterior midgut by large masses of T. melophagium. Diseased keds have swollen abdomens and develop a reddish color which indicates an escape of in
gested blood from the gut into the coelomic cavity. Internally, the anterior midgut is distended with undigested blood while the lumen of the posterior midgut is solidly packed with flagellates.
Trypanosoma rangeli Tejera is a parasite of man and other verte
brates. While it does not appear to cause serious infections in verte
brates, Grewal (1957) found that T. rangeli is pathogenic for one of its reduvid vectors Rhodnius prolixus Stäl and for the bed bug Cimex lectularius as well. First-instar nymphs of R. prolixus that fed on in
fected mammals suffered considerable mortality during that and subse
quent instars. Bugs with heavy infections, generally involving the coe
lomic cavity, cannot molt. Infected bugs are sluggish, unnaturally light in color, and translucent. In one case only 41 of 120 infected first-instar nymphs reached the adult stage; these were long lived, and only one of
them had an infection in the coelomic cavity. Mortality was higher when nymphs were fed on animals with heavy infections. Trypanosoma rangeli was even more harmful to bed bugs; more than 80 percent of infected nymphal bugs died before reaching adulthood. T h e rest died after feeding three times at most. Macfie and Thompson (1929) studied a trypanosome (probably T. paddae Laveran and Mesnil) which para
sitizes birds and found that it invades and multiplies within the body cavity of its mite vector, Dermanyssus gallinae (De Geer), with great regularity. Heavily parasitized mites succumb to the infection.
Trypanosomes of the genus Phytomonas causing diseases of plants are transmitted by certain sap-feeding insects. For example, the coreid bug Chariesterus cuspidatus (Distant) transmits a species of Phytomonas which is pathogenic for certain herbs such as Euphorbia pilulifera Lin
naeus and E. hyperici)"olia Linnaeus (Strong, 1924). These trypanosomes multiply and undergo cyclic development in the alimentary tract of the
insect vector. Available evidence suggests that they do no harm to the insect.
B. Species of Plasmodium
Species of Plasmodium transmitted by female mosquitoes cause ma
laria in man and other vertebrates. T h e literature pertaining to the epidemiology of malaria is rich and attests to the extraordinary im
portance of these parasites in the welfare of man and animals up to the present day. Of initial importance in this discussion, however, is the fact that the parasite undergoes cyclic development and multipli
cation in the insect as well as in the vertebrate. Sexual forms of the parasite are ingested by a mosquito with a blood meal from an infective vertebrate. In the stomach of a susceptible mosquito, these forms unite in pairs forming ookinetes (motile zygotes) which invade the stomach wall and grow into oocysts. T h e cysts, protruding into the body cavity of the mosquito, eventually rupture and release great numbers of slender sporozoites which migrate to the salivary glands. T h e sporozoites are injected into another vertebrate when the mosquito takes a blood meal.
While the effects of plasmodia on vertebrates are comparatively well known, remarkably little is known regarding their effects on the mos
quito. Available data are both scanty and contradictory. Sergent (1919), Mayne (1920), Boyd (1940), and others while studying various mos- quito-plasmodium relationships have found no evidence that the general well-being of the mosquito is affected by the parasite. King (1929), using Plasmodium vivax (Grassi and Feletti), compared the longevity of infected and uninfected Anopheles quadrimaculatus Say but found no difference. He even failed to find marked reductions in the vitality of individuals with heavy infections in the stomach wall and salivary glands.
On the other hand, some workers have suggested that plasmodial infections may harm the mosquito. For instance, Ross (1910) states that Culex fatigans Weidemann ( = C. quinquefasciatus Say) infected with Proteosoma (= Plasmodium) die sooner than when not infected, but only slightly so. Sinton and Shute (1938), following experiments with Anopheles maculipennis var. atroparvus van Theil, concluded that se
vere P. vivax infections might shorten the life of mosquitoes in a debili
Buxton (1935) presented the first detailed study indicating that the longevity of a mosquito may be adversely affected by a plasmodial in
fection. He studied the effect of Proteosoma praecox Grassi and Feletti [= Plasmodium relictum (G. and F.)] on the survival of Culex fatigans.
At 30°C a series of infected insects showed a higher mortality on the
first day than uninfected controls; at 23°C the same difference was noted on the second day. On the seventh day mortality was also high in the infected group. These observed differences were statistically significant, and Buxton concluded that the early deaths were due to invasion of the stomach wall by the ookinetes and the later deaths probably due to the growth of the oocysts.
T h e findings of Thompson and Huff (1944) are of considerable interest. They allowed Aedes aegypti and Culex pipiens Linnaeus to feed upon an Iguana iguana rhinolopha Wiegmann and two specimens of Sceloporus undulatus (Latreille) infected with Plasmodium rhadinurum Thompson and Huff. All these mosquitoes (165 specimens) died within 24 hours after feeding, even though they were kept under the same con
ditions provided for stock colonies of mosquitoes. A group of C. pipiens which had fed on an uninfected 5. undulatus suffered no adverse ef
fects. These observations strongly suggest that P. rhadinurum is lethal for the mosquitoes in question. Garnham (1955) compared the daily death rates in a batch of newly emerged Aedes aegypti that were given daily opportunities to feed on healthy chicks with the same rates in another batch which fed on chicks infected with P. gallinaceum Brumpt.
No differences in death rates were found up to 27 days. He repeated this experiment using 1-week-old A. aegypti and found a higher mor
tality in the infected batch from the sixth through the ninth day. Since this is the interval during which the first oocysts rupture, he concluded that the higher mortality was probably due to this phenomenon. At the end of a fortnight, however, there was no marked difference in the number of survivors in each group. Ragab (1958) also compared the death rates of P. gallinaceum-iniected A. aegypti with uninfected con
trols but found no differences. In this case, 5-day-old mosquitoes which were maintained on raisins, sugar, and water after a single blood meal, were observed for 20 days.
In all probability, the pathogenicity of the plasmodial infection de
pends upon the numbers of parasites involved. Boyd and Stratman- Thomas (1933) believe that over 100 oocysts of P. vivax are harmful to many Anopheles quadrimaculatus. De Buck and Swellengrebel (1935) found greater mortality among heavily infected A. maculipennis Meigen in comparison to lightly infected individuals. They believe that salivary infections are harmful whereas intestinal infection alone is not. De Buck (1936) is of the opinion that infected A. maculipennis may not be able to survive infections of 300 to 400 oocysts. According to Garnham
(1961), workers of the Rockefeller Foundation have shown that espe
cially high oocyst infection in Anopheles is associated with a high death rate within a few days after an infective blood meal of P. gallinaceum.
Huff (1961) and Schmidt (1961) have found that A. freeborni Aitken and A. quadrimaculatus heavily infected with P. cynomolgi Mayer and P.
vivax, respectively, have a higher mortality rate than lightly infected or uninfected mosquitoes. T h a t plasmodial infections may also impair re
productive functions was demonstrated by Roubaud (1945). He found that heavy oocyst infections of P. relictum in Culex pipiens (designated C. autogenicus sternopallidus Roubaud) retard oviposition and also re
duce the number of eggs laid.
While infected salivary glands are somewhat misshapen and fragile, available histological evidence suggests that plasmodial infections pro
duce no gross lesions in the stomach of the mosquito. Nevertheless, it is reasonably certain that heavy plasmodial infections are prejudicial to the mosquito, especially under unfavorable conditions, such as starvation (see Boyd, 1949).
C. Other Protozoa
A multitude of sporozoans of uncertain affinities causing fatal infec
tions in vertebrates are transmitted by ticks and mites. Typically these protozoans (e.g., species of Babesia, Piroplasma, Haemogregarina, and others) are acquired by the vector with an infective blood meal, but some are also transmitted transovarially. These parasites generally un
dergo metacyclic changes in the arthropod; often the parasite invades and multiplies within several organs of the vector, e.g., epithelium of the gut, coelomic cavity, ovaries, and salivary glands. Although host cells are destroyed or injured, the damage inflicted does not seem to impair the well-being of the vector in most cases. On the other hand, several workers have suggested that heavy infections can be fatal to the arthropod. Miller (1908) noted that oocysts of Hepatozoon perniciosurn Miller [ = H. muris (Balfour)], a hemogregarine pathogenic for the white rat, when present in great density, kills its mite vector Laelaps echidninus Berlese [ = Echinolaelaps echidninus (Berlese)]. Brumpt (1938) found that Haemogregarina mauritanica Ed. and Et. Sergent, a parasite of a tortoise, was pathogenic to its tick vector Hyalomma syria- cum Koch; infected ticks could not feed properly, and more than 50 percent succumbed to the infection. Abramov (1955) noted that eggs of the tick Hyalomma plumbeum (Panzer) heavily infected with Piro
plasma caballi Nuttall [ = Babesia caballi (Nuttall)], an agent of piro- plasmosis of the horse, frequently fail to hatch. Riek (1961) found that a very high proportion of female ticks, Boophilus microplus (Canes- trini), which engorged on cattle heavily infected with either Babesia bigemina (Smith and Kilborne) or B. argentina (Lignieres), died within 7 days. In diseased ticks there is some alteration in the permeability of
the gut wall, and portions of the ingested blood diffuse into the coelomic cavity; fatally affected ticks turn reddish.
V I . H E L M I N T H S
Many filarial nematodes that cause diseases of man and other verte
brates are transmitted by blood-sucking arthropods of which the best known are mosquitoes, black flies (Simuliidae), biting midges (Cera- topogonidae), horse flies, and deer flies (Tabanidae). T h e nematode is taken up as a microfilaria by these vectors with a blood meal from an infective vertebrate. Typically the nematode penetrates the wall of the midgut and migrates to its site of development, which may be in the muscles, fat body, Malpighian tubes, or coelomic cavity, depending upon the species of worm involved. T h e nematode becomes immobile and grows to maturity in these areas. After reaching maturity, the worm once again becomes motile and migrates freely in the coelomic cavity of the arthropod. T h e nematode eventually emerges from the mouth
parts of the arthropod as the arthropod feeds on a vertebrate host. T h e effects of these nematodes on their arthropod vectors and related topics have been ably reviewed by Lavoipierre (1958) and summarized by Hawking and Worms (1961).
Noe (1901) presented the first detailed histological evidence show
ing that a vector is harmed by filarid infection. He found that Diro- filaria immitis (Leidy), the heartworm of dogs, and D. repens (Railliet and Henry) destroy the cytoplasm and cell membranes in the Malpigh
ian tubes of Aedes aegypti. T h e mortality of diseased mosquitoes is high. Phillips (1939), Travis (1947), Rosen (1955), and many others have reported similar phenomena in Aedes spp. and Anopheles spp. in
fected with D. immitis. Steward (1933) found that Onchocerca cervicalis Railliet and Henry, an agent of fistulous withers and poll evil of the horse, causes serious damage in the muscle fibers of its host, Culicoides nubeculosus (Meigen). Lebied (1950) found the same sort of damage in Simulium damnosum Theobald infected with O. volvulus (Leuckart), the agent of human onchocerciasis. Lewis (1953) noted that O. volvulus interferes with the formation of the peritrophic membrane in S. dam
nosum while Lavoipierre (1958) observed the same event in A. aegypti infected with D. immitis. In general, afflicted insects are sluggish and do not fly with ease. Escape of the infective larvae may cause injury to the mouthparts of the vector; Pratt and Newton (1946) and others have suggested that this phenomenon may shorten the life of the vector. At least one worker (Causey, 1939) has suggested that oviposition may be adversely affected in parasitized mosquitoes. Pistey (1959) noted that
two peaks of mortality occur among batches of Aedes taeniorhynchus (Wiedemann) and Anopheles quadrimaculatus Say infected with Diro- filaria tenuis Chandler. These occur during the second, eighth, and ninth days after an infective meal. Pistey and others have suggested that such high mortalities are caused by the migration of the larvae into the Malpighian tubes and by their escape therefrom, respectively.
Hawking and Worms (1961) consider that mortality in infected vectors is related to the number of larvae ingested with the infective blood meal. They state: "A few larvae have no effect, more larvae cause an increasing mortality, which is proportional to the number of larvae ingested; eventually, at a certain number of larvae, all the vectors (mos
quitoes) are killed." T h e i r generalization probably holds for all types of helminth infections in arthropods. According to the authoritative opinion of Lavoipierre (1958), the cause of death in heavily infected insects appears to be a result of extensive damage to the peri trophic membrane rendering the digestion of blood virtually impossible. Some other im
portant filarial nematodes which can be pathogenic to their arthropod vectors are: Loa loa (Cobbold), the African eye worm, in Chrysops silacea Austen (Connal and Connal, 1922); Wuchereria bancrofti (Cob- bold) , an agent of lymphangitis and elephantiasis in Aedes polynesiensis Marks (Rosen, 1955); and W. malayi Brug [ = Brugia malayi (Brug)] in Mansonia longipalpis van der Wulp (Wharton, 1957).
B. Other Helminths
Scores of other helminths which cause diseases of vertebrates are transmitted by acarines and insects. Compared with the Filarioidea, the effects of these helminths on their vectors are not well known. However, several workers have suggested that massive infections are fatal to the vector. For example, Johnston (1920) found a high mortality among larvae of muscoid flies (Musca domestica and others) heavily infected with the spirurids Habronema muscae (Carter) and H. megastoma (Ru- dolphi) which parasitize the fat body and Malpighian tubes of the mag
got and cause "summer sores" of the horse. Chen (1934) found that over 35 percent of larval Ctenocephalides felis (Bouche) which had in
gested large quantities of eggs of Dipylidium caninum (Linnaeus), died within 24 to 48 hours after an infective meal. A second period of high mortality occurred immediately before pupation, and a third during the pupal stage; the eggs of this tapeworm hatch in the ventriculus of the larval flea, migrate through the intestinal epithelium, and develop into cysticercoids in the coelomic cavity. T h a t a massive infection of developing tapeworms may also kill an acarine was suggested by Stun- kard (1939) in the case of oribatid mites (Galumna spp.) harboring
Moniezia expansa (Rudolphi). Möhler (1939) noted that heavily in
fected larval lamellicorn beetles often do not survive an infection by the acanthocephalid Macracanthorhynchus hirudinaceus Pallas, a parasite of the pig. Wehr and Lucker (1952) noted a similar phenomenon in the grasshoppers Melanoplus femurrubrum (De Geer) and M. differen- tialis (Thomas) infected with the globular stomachworm of poultry, Tetrameres americana Cram. In general the mobility of infected insects and acarines is seriously impaired; these debilitated arthropods are easily caught by predators.
V I I . DISCUSSION
In the foregoing survey we have seen that certain pathogenic arthro
pod-borne microorganisms and helminths produce pathogenic effects in their vectors. While our understanding of this aspect of the pathogen- vector relationship is far from complete, some generalizations can be made regarding the production of these effects. T h e pathogen may in
jure its vector in one or more of the following ways:
( 1 ) By sheer weight of numbers. Obviously there is a limit to the number of extraneous organisms that an arthropod can support in its body, yet remain unaffected. Excessive numbers of pathogens may be taken in with a meal (e.g., Dipylidium caninum by larval Ctenocepha- lides felis). Excessive numbers may also result from unrestrained mul
tiplication within the vector (e.g., Salmonella in Argas reflexus).
(2) By destruction of the vector's substance. T h i s includes damage in solid tissues (e.g., filarial nematodes in the mouthparts of the mos
quito) and damage at the cellular level (e.g., Rickettsia prowazekii in the gut epithelium of Pediculus humanus humanus).
(3) By causing a mechanical obstruction (e.g., Leishmania donovani in Phlebotomus argentipes and, in part, Pasteurella pestis in the flea).
(4) By the production of toxins (e.g., Rickettsia prowazekii in Pedic
ulus humanus humanus).
(5) By reducing the vector's resistance to predators (e.g., Tetrameres americana in grasshoppers).
This list does not exhaust the possibilities of ways in which the pathogen might injure the vector. But in the absence of real evidence, it would be unwise to suggest additional possibilities at this time.
Finally, it is clear that certain pathogens of higher animals and of plants may be pathogens of their vectors. Our knowledge and under
standing of insect diseases and the epidemiology of arthropod-borne diseases will be greatly enhanced by further elucidations of this much- neglected aspect of the pathogen-vector relationship.
Abramov, I. V. 1955. On the length of preservation of the causal agent of equine piroplasmosis (Piroplasma caballi) in the tick Hyalomma plumbeum Panzer 1795.
Veterinariya, 32, 42-46 (in Russian).
Alverdes, F., and Bieling, R. 1949. Untersuchungen über bakterielle Infektionen bei Kleiderläusen (Pediculus vestimenti). Z. Naturforsch., 4b, 150-157.
Bacot, A. W . 1915. Notes on the development of Bacillus pestis in bugs (Cimex lectularius) and their power to convey infection. / . Hyg., 14 (Plague Suppl. IV), 777-792.
Bacot, A. W., and Martin, C. J . 1914. Observations on the mechanism of the trans
mission of plague by fleas. / . Hyg., 13 (Plague Suppl. Ill), 423-439.
Black, L . M. 1950. A plant virus that multiplies in its insect vector. Nature, 166, 852-853.
Boyd, M. F. 1940. On the correlation between the incidence of stomach and gland infection in Anopheles quadrimaculatus infected with Plasmodium vivax. Am.
J. Trop. Med., 20, 129-131.
Boyd, M. F., ed. 1949. Epidemiology: factors related to the definitive host. In
"Malariology," Vol. I, pp. 608-697. Saunders, Philadelphia.
Boyd, M. F., and Stratman-Thomas, W. Κ. 1933. A controlled technique for the employment of naturally induced malaria in the therapy of paresis. Am. J. Hyg., 17, 37-54.
Brumpt, E . 1938. Formes evolutives d'Haemogregarina mauritanica chez la tique Hyalomma syriacum. Ann. parasitol. humaine et comparee, 16, 350-361.
Burgdorfer, W., and Owen, C. R. 1956. Experimental studies on argasid ticks as possible vectors of tularemia. / . Infectious Diseases, 98, 67-74.
Burroughs, A. L . 1953. Sylvatic plague studies. X . Survival of rodent fleas in the laboratory. Parasitology, 43, 35-48.
Buxton, P. A. 1935. T h e effect of Proteosoma upon the survival of Culex. Parasi
tology, 27, 547-550.
Buxton, P. A. 1955. Tsetse and trypanosomes. In "The Natural History of Tsetse Flies," pp. 592-653. Η. Κ. Lewis, London.
Causey, O. R. 1939. Development of the larval stages of Foleyella brachyoptera in mosquitoes. Am. J. Hyg., 30, 69-71.
Chen, Η. T . 1934. Reactions of Ctenocephalides felis to Dipylidium caninum. Z.
Parasitenk., 6, 603-637.
Connal, Α., and Connal, S. L . M. 1922. T h e development of Loa loa (Guyot) in Chrysops silacea (Austen) and in Chrysops dimidata (Van der Wulp). Trans. Roy.
Soc. Trop. Med. Hyg., 16, 64-89.
Cornwall, J . W., and Menon, Τ . Κ. 1917. On the possibility of the transmission of plague by bed-bugs. Indian J. Med. Research, 5, 137-159.
da Rocha-Lima, H. 1916. Beobachtungen bei Flecktyphusläusen. Arch. Schiffs- u.
Tropen-Hyg., 20, 17-31.
De Buck, Α. 1936. Some results of six years' mosquito infection work. Am. J. Hyg., 24, 1-18.
De Buck, Α., and Swellengrebel, Ν. H. 1935. On the seasonal longevity of Anopheles maculipennis in Holland with reference to their ability to act as malarial vectors.
Proc. Acad. Sei. Amsterdam, 38, 335-343.
Ehrhardt, P. 1960. Zum Sauerstoffverbrauch von Myzus persicae (Sulz.) vor und nach Aufnahme des Blattrollvirus. Entomol. Exptl. et Appl. 3, 114-117.
Eskey, C. R., Prince, F. M., and Fuller, F. B. 1949. Transmission of Salmonella
enteritidis by the rat fleas Xenopsylla cheopis and Nosopsyllus fasciatus. Public Health Repts. (U. S.), 64, 933-941.
Francis, E. 1927. Microscopic changes of tularaemia in the tick Dermacentor ander- soni and the bedbug Cimex lectularius. Public Health Repts. (U. S.), 42, 2763- 2772.
Garnham, P. C C. 1955. T h e comparative pathogenicity of protozoa in their ver
tebrate and invertebrate hosts. Symposium Soc. Gen. Microbiol. 5th pp. 191-206.
Garnham, P. C C. 1961. Personal communication.
Gosio, B. 1925. Über die Verbreitung der Bubonenpesterreger durch Insektenlarven.
Arch. Schiffs- u. Tropen-Hyg., 29, 134-139.
Grewal, Μ. S. 1957. Pathogenicity of Trypanosoma rangeli Tejera, 1920 in the in
vertebrate host. Exptl. Parasitol., 6, 123-130.
Hawking, F., and Worms, M. 1961. "Transmission of filarioid nematodes." Ann.
Rev. Entomol., 6, 413-432.
Heisch, R. B., and Harvey, A. E. C. 1962. T h e development of Spirochaeta duttoni and S. recurrentis in Pediculus humanus. Parasitology, 52, 77-88.
Hirst, L . F. 1953. "The Conquest of Plague," 478 pp. Oxford Univ. Press, London and New York.
Hoare, C. A. 1923. On a trypanosome occurring in British sheep and its transmission by the sheep-ked. Vet. ] . , 79, 271-274.
Hoare, C. A. 1949. T. lewisi in man. In "Handbook of Medical Protozoology," p.
216. Bailliere, Tindall & Cox, London.
Holdenried, R. 1952. Sylvatic plague studies. VIII. Notes on the alimentary and reproductive tracts of fleas, made during experimental studies of plague. / . Para
sitol., 38, 289-292.
Huff, C G. 1961. Personal communication.
Jellison, W . L . 1959. "Fleas and disease." Ann. Rev. Entomol., 4, 389-414.
Jensen, D. D. 1958. Reduction in longevity of leafhoppers carrying peach yellow leaf roll virus. Phytopathology, 48, 394 (abstr.).
Jensen, D. D. 1959a. Insects, both hosts and vectors of plant viruses. Pan-Pacific Entomologist, 35, 65-82.
Jensen, D. D. 1959b. A plant virus lethal to its insect vector. Virology, 8, 164-175.
Jensen, D. D. 1960. Pathogenicity of western X-disease virus of stone fruits to its leafhopper vector, Colladonus montanus Van Duzee. Verhandl. XI Intern. Kongr.
Entomol. Wien, 17 bis 27 August (in press).
Johnston, Τ . H. 1920. Flies as transmitters of certain worm parasites of horses.
Sei. and Ind. (Australia), 2, 369-372.
Kartman, L . , Prince, F. M., and Quan, S. F . 1956. Studies on Pasteurella pestis in fleas. Comparative plague-vector efficiency of Xenopsylla vexabilis and Xenopsylla cheopis. Bull. World Health Organization, 14, 681-704.
Kartman, L., Prince, F. M., Quan, S. F., and Stark, Η. E. 1958. New knowledge on the ecology of sylvatic plague. Ann. Ν. Y. Acad. Sei., 70, 668-711.
King, W . V. 1929. On the development of malaria parasites in the mosquito. Am.
J. Hyg., 10, 560-564.
La Motte, L . C 1960. Japanese Β encephalitis virus in the organs of infected mos
quitoes. Am. J. Hyg., 72, 73-87.
Lavoipierre, Μ. M. J . 1958. Studies on the host-parasite relationships of filarial nematodes and their arthropod hosts. II. T h e arthropod as a host to the nema
tode: a brief appraisal of our present knowledge, based on a study of the more important literature from 1878 to 1957. Ann. Trop. Med. Parasitol., 52, 326-345.
Lebied, B. 1950. "Une nouvelle theorie endemiologique. Sur le role de fonction du parasitisme X mecanisme du vol du vecteur comme facteur decisif de l'etablis- sement du foyer l'endemicite de l'Onchocercose et de filarioses en general." 54 pp.
Imprimerie Darantiere, Dijon, France.
Lewis, D. J . 1953. Simulium damnosum and its relation to onchocerciasis in the Anglo-Egyptian Sudan. Bull. Entomol. Research, 43, 597-644.
Liston, W. G. 1905. Plague, rats and fleas. / . Bombay Nat. Hist. Soc, 16, 253-274.
Littau, V. C., and Maramorosch, Κ. 1956. Cytological effects of aster-yellows virus on its insect vector. Virology, 2, 128-130.
Macfie, J . W. S., and Thomson, J . G. 1929. A trypanosome of the canary (Serinus canarius Kock). Trans. Roy. Soc. Trop. Med. Hyg., 23, 185-191.
Mackerras, I. M., and Pope, P. 1948. Experimental salmonella infections in Aus
tralian cockroaches. Australian J. Exptl. Biol. Med. Sei., 26, 465-470.
Mayne, B. 1920. Can the mosquito convey infection from a malaria patient under
going treatment? Does sporogony affect mosquito life? Public Health Repts.
(U. S.), 35, 1664-1669.
Miller, W . W . 1908. Hepatozoon perniciosum (n.g. n.sp.); a haemogregarine patho
genic for white rats; with a description of the sexual cycle in the intermediate host, a mite (Lelaps echidninus). Bull. Hyg. Lab. U. S. Public Health and Ma
rine Hosp. Serv. No. 46, 51 pp.
Milner, Κ. C , Jellison, W . L . , and Smith, B. 1957. T h e roll of lice in transmission of Salmonella. J. Infectious Diseases, 101, 181-192.
Möhler, J . R. 1939. "Report of the Chief of the Bureau of Animal Industry," 82 pp. U. S. Dept. Agr., Washington, D. C.
Mooser, H., and Castaneda, M. R. 1932. T h e multiplication of the virus of Mexican typhus fever in fleas. / . Exptl. Med., 55, 307-323.
Nelson, W. A. 1956. Mortality in the sheep ked Melophagus ovinus (L.) caused by Trypanosoma melophagium Flu. Nature, 178, 750.
Noe, G. 1901. Sul ciclo evolutivo della Filaria bancrofti (Cobbold) e della Filaria immitis (Leidy). Ricerche Lab. Anat. Norm. Univ. Roma, 8, 275-353.
Nuttall, G. H. F. 1897. Zur Aufklärung der Rolle welche die Insekten bei der Ver
breitung der Pest spielen. Ueber die Empfindlichkeit verschiedener Tiere für diesebel. Centr. Bakteriol. Parasitenk. Abt. I Orig., 22, 87-97.
Parker, R. R., and Spencer, R. R . 1926. Rocky Mountain spotted fever. Α study of the relationship between the presence of rickettsia-like organisms in tick smears and the infectiveness of the same ticks. Public Health Repts. (U.S.), 41, 461-469.
Parker, R . R., and Steinhaus, Ε . Α. 1943. Salmonella enteritidis: experimental transmission by the Rocky Mountain wood tick Dermacentor andersoni Stiles.
Public Health Repts. (U.S.), 58, 1010-1012.
Philip, C. B. 1958. Evidence of masking and latency in the fields of insect and helminth microbiology. Symposium on Latency and Masking in Viral and Rickett
sial Infections Proc. Conf. Univ. Wisconsin Med. School 1957, pp. 88-106.
Philip, C. B., and Jellison, W . L . 1934. T h e American dog tick, Dermacentor va
riabilis, as a host of Bacterium tularense. Public Health Repts. (U.S.), 49, 386-392.
Phillips, J . H. 1939. Studies on the transmission of Dirofilaria immitis in Massachu
setts. Am. J. Hyg., 29, 121-129.
Pirot, R., and Bourgain, M. 1945. Perte du pouvoir infectant a'Ornithodoros tholozani infecte congenitalement par Spirochaeta persica et surinfecte au Stade nymphal. Bull. soc. pathol. exotique, 38, 88-90.
Pistey, W. R. 1959. Studies on the mortality of mosquitoes infected with Dirofilaria tenuis Chandler. Exptl. Parasitol., 8, 596-608.
Pollitzer, R. 1954. "Plague," 698 pp. World Health Organization, Geneva, Switzer
Pratt, I., and Newton, W . L . 1946. T h e migration of infective larvae of Wuchereria bancrofti within the mosquito host and their rate of escape under laboratory conditions. / . Parasitol., 32, 272-280.
Price, R. D. 1957. A microscopic study of Pasteurella tularensis in the human body louse. Parasitology, 47, 435-446.
Ragab, H. A. A. 1958. Effect of the plasmodium on the transmitting mosquito host from the point of view of the longevity of the infected mosquito. / . Egyptian Med. Assoc., 41, 447-454.
Riek, R. F . 1961. Personal communication.
Rodhain, J . , and van Oye, E . 1941. Sur le role d' Argus reflexus dans la transmission du paratyphus des pigeons. Acta Biol. Belg., 1, 216-220.
Rosen, L . 1955. Observations on the epidemiology of human filariasis in French Oceania. Am. J. Hyg., 61, 219-248.
Ross, R. 1910. Possible effect of malaria on the anophelines. In "The Prevention of Malaria," 1st ed., pp. 197-198. John Murray, London.
Roubaud, E. 1945. Influence du developpement plasmodien sur la fecondite des moustiques notes. Bull. soc. pathol. exotique, 38, 300-304.
Sassuchin, D., and Tikhomirova, M. 1936. T h e preservation of Pasteurella pestis in the larvae and nymphs of the tick Dermacentor silvarum Olen. Vestnik Mikro- biol. Epidemiol. Parazitol. (Saratov), 15, 357-362 (in Russian).
Schmidt, L . H. 1961. Personal communication.
Sergent, E. 1919. Le Plasmodium relictum, agent pathogene du paludisme des oiseaux, ne donne pas une maladie mortelle au moustique transmetteur. Bull, soc. pathol. exotique, 12, 601-603.
Shinkai, A. 1960. Premature death of Inazuma dorsalis Motschulsky which received the rice dwarf virus through the egg. Ann. Phytopathol. Soc. Japan, 25, 42 (abstr.).
Shortt, Η. E., Barraud, P. J . , and Craighead, A. C. 1926. T h e life-history and mor
phology of Herpetomonas donovani in the sandfly Phlebotomus argentipes. Indian J. Med. Research, 13, 947-959.
Simond, P. L . 1898. L a propagation de la peste. Ann. inst. Pasteur, 12, 625-687.
Sinton, J . Α., and Shute, P. G. 1938. A report on the longevity of mosquitoes in relation to the transmission of malaria in nature. Rept. Public Health and Med.
Subjects, (London) Rept. No. 85, 1-45.
Smith, R. Ο. Α., Halder, Κ. C , and Ahmed, I. 1940. Further investigations on the transmission of kala-azar. Part II. T h e phenomenon of the 'blocked' sandfly.
Indian J. Med. Research, 28, 581-584.
Smith, R. Ο. Α., Halder, Κ. C , and Ahmed, I. 1941. Further investigations on the transmission of kala-azar. Part IV. T h e duration of life and other observations on 'blocked' flies. Indian J. Med. Research, 29, 783-787.
Steward, J . S. 1933. Onchocerca cervicalis (Rauhet and Henry 1910) and its develop
ment in Culicoides nubeculosus Mg. Rept. Inst. Animal Pathol. Univ. Cambridge, 3, 272-284.
Strong, R. P. 1924. Investigations upon flagellate infections. Am. J. Trop. Med., 4, 345-385.
Stunkard, H. W . 1939. T h e development of Moniezia expansa in the intermediate host. Parasitology, 30, 491-501.
Thompson, P. E., and Huff, C. G. 1944. Saurian malarial parasites of the United States and Mexico. / . Infectious Diseases, 74, 68-79.
Travis, Β. V. 1947. Relative efficiency of six species of mosquitoes from Guam, Μ. I., as developmental hosts for Dirofilaria immitis. J. Parasitol., 33, 142-145.
Watson, Μ. Α., and Sinha, R. C. 1959. Studies on the transmission of European wheat striate mosaic virus by Delphacodes pellucida Fabricius. Virology, 8, 139-163.
Wehr, Ε . Ε . , and Lucker, J . T . 1952. Insects and helminths. In "Insects: T h e Yearbook of Agriculture." pp. 169-179. U. S. Dept. Agriculture, Washington, D. C.
Wenyon, C. M. 1926. "Protozoology," Vol. I, p. 471. Bailliere, Tindall & Cox, London.
Weyer, F. 1960. "Biological relationships between lice (Anoplura) and microbial agents." Ann. Rev. Entomol., 5, 405-420.
Wharton, R. H. 1957. Studies on filariasis in Malaya: observations on the develop
ment of Wuchereria malayi in Mansonia (Mansonioides) longipalpis. Ann. Trop.
Med. Parasitol., 51, 278-296.
Whitman, L . 1937. T h e multiplication of the virus of yellow fever in Aedes aegypti.
J. Exptl. Med., 66, 133-143.
Wood, S. F . 1942. T h e persistence of Trypanosoma cruzi in dead cone-nosed bugs (Hemiptera, Reduviidae). Am. J. Trop. Med., 22, 613-621.
Yoshii, H., and Kiso, A. 1957. Studies on the nature of insect-transmission in plant viruses (II). Some researches on the unhealthy metabolism in the viruliferous plant hopper, Geisha distinctissima Wal., which is the insect vector of the dwarf disease of Satsuma orange. Virus (Osaka), 7, 315-320 (in Japanese).
Zdrodovskii, P. F., and Golinevich, Η. M. 1960. Rickettsioses of the blood-sucking arthropods. In "The Rickettsial Diseases," pp. 38-68. Pergamon, New York.
Zirolia, G. 1902. Der Pestbacillus im Organismus der Flöhe. Centr. Bakteriol.
Parasitenk. Abt. I Orig., 31, 687-688.