MFR PAPER 1146 spores. Besides the morphometries .of the spores, the various stages of the lIfe cycle, the mode of sporogony, the sites ofinfection, and the host specificity are Microsporidian Infections of of diagnostic importance. However, since some original descriptions are Amphipods with Special Reference vague and fail to provide adequate de­ to Host-Parasite Relationships: tail, a satisfactory review of all species recorded in amphipods cannot be pre­ A Review sented. Nevertheless, an attempt has been made to list all species described and to summarize specific features for H.-P. BULNHEIM their recognition (Table 1). The list is based on a survey presented by Lipa (1967), but includes several additions ABSTRACT-A survey of the 10 species of microsporidian~associa~~dwith and corrections. In several species the amphipod crustaceans is presented. Specific features for t~elr recognitIOn are dimensions of fresh spores are given, given on taxonomy, morphology, spore si~e, sit~s of InfectlO~, and host range. but in others it is doubtful whether size Some aspects of the host-parasite relationships are considered. In s.ev~ral refers to fixed or fresh spores. The microsporidians recorded from species, transovarian transfer ap~ears. to. be a major route of transmission. Previous results on microsporidlans indicate that they do not cause fatal amphipods belong to 10 species from 5 diseases in their amphipod hosts. A sex-determining influence on the progeny genera. Most host species belong to the of Gammarus duebeni afterinfection by Octosporea ef~e~inansorThelohanla genus Gammarus which occurs in herediteria is indicated. Both of these microspondlans are transm/~ted freshwater as well as brackish and through the eggs to the host's offspring which, in genera~, all de~elop Into marine habitats. Some additional data females. Some results and problems of this effect on sex ratio are discussed. for characterization ofthe microsporid­ ian genera (cf. Weiser, 1961) and species are brieflY presented below. INTRODUCTION of microsporidian species occurring in crustaceans. Moreover, the widely Microsporida are cytozoic parasites scattered literature supplies little or no Genus Nosema Nageli, 1857 with a wide host range, comprising all information on host-parasite relation­ The essential characteristic of this phyla of the animal kingdom from pro­ ships. Therefore, only scanty data are tozoans to mammals. They are impor­ genus is that only one spore is produced available for an assessment of their by each sporont. tant pathogens ofarthropods, especially pathological significance. insects, since they cause severe dis­ Nosema gammari van Ryckeghem This paper is confined to the micro­ eases in several members of this group. has been described from only one sporidian species parasitic in amphipod Compared with the numerous detailed specimen ofGammarus pulex, found in crustaceans, and presents a survey of investigations ofmicrosporidioses in in­ Belgium (van Ryckeghem, 1930). A dif­ their taxonomy, specific morphological sects, very few studies are devoted to fuse infection of the host muscles was characters, sites of infection, and host observed, but no further details on the microsporidian infections in crusta­ range. In addition, various aspects of ceans, and to the effects they have on life history have been reported for this the host-parasite relationships are con­ parasite. In England, Pixell-Goodrich their hosts. Since Kudo's review (1924), sidered. no comprehensive and critical report ~n (1929, 1956) noted Nosema sp. in G. the taxonomy and biology of the ml­ TAXONOMIC SURVEY pulex, but no detailed characteristics of crosporidians detected in crustaceans this species have been published. has been published, except for a survey Microsporidia are protozoan para­ Nosema kozhovi Lipa was recorded sites which are characterized by the recently presented by Sprague (1970a) (Lipa, 1967) in Brandtia lata lata formation of spores equipped with an on protozoan parasites in decapod collected on the shores of Lake Baikal extrusible polar filament. Their life Crustacea. Sprague recorded less than (Soviet Union). All tissues were in­ cycle commences with the liberation of two dozen microsporidian species, fected with especially heavy concentra­ a uninucleate or bi-nucleate sporoplasm mainly from marine hosts, with some tions in the gut epithelium, adipose tis­ from the spore with subsequent entry known to cause diseases in commer­ sue, and muscles. Parasitized animals cially important decapods. into a host cell. An intracellular multi­ had a milky-white appearance. Due to several inadequate descrip­ plicative phase (schizogony) is followed by the development of spores tions and some taxonomic confusion, it Genus The/ohania (sporogony). The resistant spores infect is difficult to estimate the exact number Henneguy, 1892 new hosts. Among the critelia employed for the This genus develops eight spores H.-P. Bulnheim is with the Biolo­ separation and identification of micro­ from a single pansporoblast and the gische Anstalt Helgoland (Zen­ sporidian species, the most significant spores may remain together within a trale), Hamburg, Germany (FRG). characters are shape and size of the common membrane. 39 Table 1.-Llst of mlcrosporldlan species parasitic In amphlpod crustaceans.

Microsporidian species Host species Sites of infection Size of spores References (I'm)

Nosema gammar; Gammarus pulex L. peri- and intermuscular 1.5 by 0.75 van Ryckeghem (1930) van Ryckeghem tissue Nosema kozhov; Brandtis Ista gut epithelium. adipose 3.3-3.9 by Lipa (1967) Lipa lata (Dybowski) tissue. muscles 2.1-2.2 (fresh) Thelohania mulleri Gsmmarus pulex L., muscles 4-5 by 2 Pfeiffer (1895). Stempell Gammarus chevreuxi (fresh) StempelI (1902). Leger Sexton and Hesse (1917). jirovec (1936). Pixell Goodrich (1929. 1956). Bulnheim (1971a) Thelohania mulleri var. Gammsrus pulex L. muscles 3 by 1.5 van Rycheghem (1930) minuta van Ryckeghem Thelohania vandeli Niphsrgus srygius muscles (?) 6-6.5 by Poisson (1924) Poisson Schiodte max. 3 Thelohan;a herediteria Gammarus duebeni muscles. ovaries 4.5·6 by Bulnheim (1969. 1971a) Bulnheim Lilljeborg 1.9·2.7 (fresh) Stempellia mulleri Gammarus pulex l.. abdominal muscles 4-5.5 by Pfeiffer (1895). Labbe (Pfeiffer) Gsmmsrus locusta (L). 2.5-3 (fresh) (1899). Stempell (1902), [syn.: Glugea mulleri Gammarus oceanicus Lliger and Hesse (1917). Pfeiffer (partim). Plistophors SegerstrAle. Gammsrus Debaisieux (1919.1928), mulleri (Pfeiffer). salinus Spooner, Zwolfer (1926a. 1926b). The/ohania giraudi Gammarus zaddachi Sexton, George-itCh (1929). Leger and Hesse. Plistophora Gammarus duebeni van Ryckeghem (1930). blochmanni ZwOller) Lilljeborg. Niphsrgus Butnheim (1971 b) ilidiensis Schafer Octosporsa gammari Gsmmarus pulex L excretory system, 4·6 by van Ryckeghem (1930). van Ryckeghem heart epithelium 1.2-2 Jirovec (1943) Octosporea effeminans Gammarus duebeni ovarial tissue, 4-10 by Butnheim (1967.1969. Bulnheim and Vavra Lilljeborg adipose tissue 15-2.5 (tresh) 1970). Burnheim and Vavra (1968) Bacillidium niphargi Niphargus stygius ? 8-9 by 2 Poisson (1924). (syn.: Mrazskia niphargi Schiodle Jirovec (1936) Poisson)

Thelohania mulleri Stempell, a para­ (Bulnheim, 1971a). Although the pos­ it must be transferred to the genus site ofG. pulex, was described in detail terior part of the body is more heavily Stempellia. The spores have an ovoid by Stempell (1902). Evidently the same parasitized than the anterior, infection shape (Fig. 2). S. mulleri has a wide host microsporidian was found in Gam­ of the host cannot be recognized mac­ range as demonstrated by several infec­ marus chevreuxi by Pixell-Good­ roscopically. The only record of this tion experiments (Bulnheim, 197Ib). rich (1929). The papers of Leger and species is from the River Elbe estuary in Therefore, it can be expected that this Hesse (1917), van Ryckeghem (1930), Germany. parasite may invade amphipods other Jirovec (1936) and Bulnheim (197Ia) than those listed in Table I. Host rec­ also deal with this species. Initially, Genus Stempellia ords derive from Germany (freshwater and euryhaline species), Belgium, and T. mulleri was confused with Leger & Hesse, 1922 Stempellia mulleri, as outlined in a sub­ Yugoslavia. S. mulleri can be easily sequent paragraph. The infected host In this genus, 4, 8, 16, or 32 spores recognized by the presence of one or displays a spotted, whitish, opaque col­ develop within one pansporoblast. more white tubular masses of parasites oring. Both the body muscles and the Stempellia mulleri (Pfeiffer) has a which are arranged in the abdominal muscles of the appendages become rather complicated taxonomic history. muscles of its hosts and separated from heavily infected. The spores are typi­ Pfeiffer (1895) described a species from one another by 2-3 mm. cally pyriform in shape, but anomalies G. pulex named Glugea mulleri, which of spore formation occasionally may is similar to S. mulleri. Later on it was Genus Octosporea Flu, 1911 occur with the development of four or named Plistophora mulleri (Pfeiffer) by even two spores that are significantly Labbe (1899) and T. mulleri (Pfeiffer) Species of the genus Octosporea larger than the others within a pan­ by Stempell (1902). Debaisieux (1919) have cylindrical spores which may be sporoblast. Host records derive from and Zwolfer (1926a) stated that the form slightly arched. The spore width is one­ Germany, England, and Belgium. discern. One species is to be regarded as third or less of the spore length. and all T. mulleri var. minuta van Ryck­ T. mulleri, the other as S. mulleri. The stages of the life cycle are binucleate. eghem is a smaller microsporidian than latter appears to be identical with the Octosporea gammari van Ryck­ S. mulleri, wi th the same characteristics descriptions of Thelohania giraudi eghem was detected in one specimen of of spores and sites of infection (van (Leger and Hesse, 19(7), G. mulleri G. pulex from the region of Louvain in Ryckeghem, 1930). Without re-exam­ descriptions of Thelohania giraudi Belgium. Van Ryckeghem (1930) ining both forms, it is difficult to decide (Leger and Hesse, 1971), G. mulleri noticed in this specimen a dual infection whether they represent distinct species. (Debaisieux, 1919, 1928) and Plistopho­ of 0 . gammari and T. mulleri. Jirovec Thelohania heredileria Bulnheim is ra blochmanni (Zwolfer, 1926a, 1926b). (1943) later observed the same micro­ clearly distingishable from T. mulleri by Georgevitch (1929) recognized this syn­ sporidian near Prague, Czechoslo­ its larger size and more cylindrical onymy and named the microsporidian vakia. It invades the excretory system spores (Fig. I). It invades the muscles in question P. mulleri (Pfeiffer). Ac­ and the tissue around the heart. and ovaries of female Gammarus cording to the numbers of spores pro­ Octosporea ejjemininans Bulnheim duebeni, but does not occur in males duced within one pansporoblast, and Vavra (Fig. 3) has been found in the 40 Figure 1.-The/ohanla heredlterl". Fresh spores from ["fected Gammarus dueben/. (Phase contrast, 2,OOOx). ovaries and adipose tissue of the assigned this microsporidian to the species will be discovered in this crus­ brackish-water species G. duebeni genus Bacillidium and named it B. tacean group. (Bulnheimand Vavra, 1968). This para­ niphargi. Unfortunately, no further site occurs only in females and, some­ biological data have been recorded on TRANSMISSION times, in intersexes. This parasite was this parasite. found in populations ofG. duebeni from In general, the infection of a suscep­ the River Elbe estuary in Germany and tible host is initiated by the ingestion of the Baltic Sea. Dual infections by this Unnamed Species spores. It is assumed that the digestive species and by T. herediteria have been fluids then cause the extrusion of the In the muscles and heart of Talitrus observed in a few cases (Bulnheim, polar filament and the discharge of the sp., Mercier (1906) observed a micro­ 1971b). sporoplasm which penetrates a host sporidian. Anders (1957) detected a mi­ cell. Transovarian transfer represents a crospolidian, whose taxonomic position Genus Bacillidium Janda, 1928 route of infection which is probably the could not be clearly identified, as­ major method of transmission of mi­ The genus Baeillidium is charac­ sociated with G. pulex subterraneus. crosporidians in amphipods studied terized by very long, rod-shaped He found this parasite in intersexual thus far. spores. In contrast to members of the specimens. Recent studies by the au­ An experimental infection of genus Mrazekia, they have no tails thor havedemonstrated thatGammarus laboratory-reared gammarids by uptake (Weiser. 1961). However, Sprague loeusta and Gammarus salinus may of spores with food was achieved in S. (1970b) pointed out that the genus also be attacked by Thelohania sp. mulleri (Bulnheim, 1971 b). Although Baeil/idium was falsely distinguished which have smaller spores than T. Zwolfer (I926a) failed to infect G.pulex from Mrazekia by comparison with a herediteria but similar morphology and in this way, Bulnheim (197Ib) transmit­ species incorrectly regarded as the type sites of infection. Whether or not they ted this species by feeding starved of the latter genus and is ajunior subjec­ represent a new species requires care­ gammarids with infected musculature tive synonym of Mrazekia. ful investigation and comparison from other specimens to demonstrate Bacillidium niphargi (Poisson) has with the known species of the genus the wide range ofpossible hosts for this been reported to occur in the subterra­ Thelohania. microsporidian. nean amphipod Niphargus stygius. It From these observations it is obvious In contrast to S. mulleri, which does was first named Mrazekia niphargi by that a considerable diversity of micro­ not invade the ovaries, several other Poisson (1924), but the spores did not sporidian species exists in amphipods, species have been shown to be trans­ possess tails. Jirovec (1936), therefore, and that many new microsporidian ferred through the eggs of their hosts. 41 This mode of transmission was record­ found in the oocytes. The propagation PATHOGENICITY ed in O. effeminans and T. herediteria of the parasites within the ooplasm pro­ (Bulnheim and Vavra, 1968; Bulnheim, ceeds until the formation of yolk Epizootic diseases such as micro­ 1971a). Further investigations and re­ granules takes place. When the eggs are sporidian infections may cause various examination provided evidence that released into the brood pouch and fer­ histopathological alterations, often re­ transovarian transfer also occurred in tilized, the parasites undergo a second sulting in an enormous hypertrophy. Thelohania sp. associated with other period of schizogonic multiplication However, no evidence of such pro­ representatives of the genus Gam­ which leads to a strong infiltration of the nounced pathological changes from marus: G. loellsla, G. salinus, and developing embryo by vegetative microsporidian infections in amphipods G. pulex. However, the taxonomic stages. has been provided. As a result of pro­ position of Thelohania sp. from the lat­ Attempts to achieve peroral transfer gressive multiplication of the parasites, teramphipods could not be clarified, but of the microsporidians O. effeminans the muscles become filled up with ripe the microsporidian found in G. pulex and T. heredileria to their host G. due­ spores, ultimately destroying the host was assigned to T. mulleri var. minula, beni did not succeed. Although fresh muscle fibers. In some gammerids in­ which was brieflly described by van and dried tissues contaminated by fected with members of the genera Ryckeghem (1930). spores were offered to the test animals, Nosema and Thelohania, Pixell­ In the microsporidians transferred an experimental infection could not be Goodrich (1929) observed yellow or transovarially, infection of the oocytes accomplished. The reasons for this fail­ brownish chitinoid nodules which con­ and multiplication by schizogony is in­ ure are not clear, but may be due to the stituted necrotic muscle fibers that were timately associated with the reproduc­ fact that extll.lsion of the filament from detached from the surrounding tissues. tive cycle of the female hosts. Their the spore cannot be instigated by chem­ These muscles were then attacked by ovaries are long paired tubes which con­ ical or mechanical stimuli in these phagocytes which also ingested spores. tain oogonia and three layers of species. Nevertheless, a natural infec­ Owing to the secretion of chitinoid sub­ different-sized oocytes. Generally, the tion by uptake ofspores scattered in the stance by these hemocytes, the areas oocytes are not infected before they are aquatic environment cannot be ex­ where the attack was most advanced arranged in the third layer in order to cluded. However, transovarian transfer exhibited the darkest brown color. undergo intensive cytoplasmic growth. of vegetative stages appears to be the A similar defense mechanism of the As a rule, only vegetative stages, most important and effective way of host appears to occur in G. pulex mainly binucleate schizonts, can be regularly transmitting an infection. infected by S. mulleri. The large masses

FIgure 2.-Stempema muller/. Fre'h 'poreo 'rom Infected Gammarus sallnus, .ome wIth extruded .poroplasm. (Phase contrast, 2,OOOx). 42 Figure 3.-octosporea e"emlnans. Fresh spores and sporonts together with 8 binucleate schizont (lett) from Intected Gammarus duebenl. (Phase contrast,2,OOOx). of parasites distributed within the ab­ not find any apparent pathogenic effects Except for a reduced resistance to dominal muscles are sometimes sur­ due to these microsporidians. S. mulleri temperature stress noticed in specimens rounded by a brownish envelope, as ob­ has no noticeable pathogenic effect on infected by T. herediteria, no further served by Zwolfer (I 926a). He also its hosts (Zwolfer, 1926a), as confirmed differences in the life functions tested noticed partially digested spores and by my own observations. Two micro­ have been revealed. Thus, the results sporoblasts at the periphery of such sporidian species, O. effeminans and T. obtained from studies on O. effeminans zones and suggested that the connective herediteria, associated with G. duebeni and T. herediteria document the rela­ tissue of the host might be responsible have no pathological effects. Infected tionships between parasite and host to for this encapsulation. Only severe in­ and noninfected specimens of G. be rather well balanced. fections, which lead to a complete duebeni have been reared for many gen­ breakdown of the muscles, can cause erations in the laboratory. Several life INFLUENCE ON this reaction by the host (Zwolfer, functions have been studied and com­ SEX DETERMINATION 1926a). Similar responses in tissues in­ pared, such as brood size, mortality of vaded other than muscles have not been embryos, juveniles and adult individu­ Another aspect of the host-parasite reported. als, growth intensity, onset of maturity, relationship to be considered is the With respect to the effects of the life span, molting frequency, and influence on the determination and in­ parasites on their hosts, some findings metabolic rates, with no significant dif­ heritance of sex. This effect, elucidated have been recorded which indicate that ferences observed between infected and by several studies on microsporidian in­ none of the microsporidian species healthy amphipods (Bulnheim and fections in the brackish-water crusta­ which infect amphipods cause fatal dis­ Vavra, 1968; Bulnheim, 197Ia). Results cean G. duebeni (Bulnheim, 1967, 1969, eases, and thus do not seriously affect of investigations on standard metabo­ 1970, 1971a, 1972a; Bulnheim and the life functions of their hosts. Lipa lism as a function of size in noninfect­ Vavra, (968), represents a peculiarity (1967) stated that specimens of B. lata ed G. duebeni juveniles and females without parallel among Microsporidia. lata infected by N. kozhovi display re­ compared with those infected by T. G. duebeni exhibits considerable de­ duced locomotory activity compared herediteria are presented in Figure 4 (cf. viations from the normal 1: I sex ratio. with healthy individuals. Reduced Bulnheim, 1972b for further experi­ Rearing experiments demonstrated capacity for locomotion and increased mental details). Despite the rather se­ females produced young of both sexes mortality was observed by Zwolfer vere infection of the host, only a slight and other females which give birth only (I926a) in G. pulex infected by T. reduction in the respiratory rate was to female offspring. Females of such mulleri. Stempell (1902), however, did established with increasing size. strains mated with males from strains of 43 different origin again produced broods erations (Bulnheim, 1969, 197Ia). For periods may have a pronounced consisting exclusively or predominantly this reason, males do not harbor these influence on sex ratio (Bulnheim, 1969, of females, but accompanied by a few parasites. 1972a). males or intersexes. Since this sex-ratio It appeared of interest to obtain in­ Considering the mode of the sex de­ condition was transferred through the formation on whether or not sex deter­ termining influence by O. effeminans maternal line, cytoplasmatic inheri­ mination could be established in other and T. heredileria, the assumption is tance was first assumed (Traut, 1962). amphipods infected with microsporid­ proposed that the microsporidians During an investigation conducted to ians. Therefore, the following am­ might affect the differentiation of the find the suggested extra-chromosomal phipods were studied: G. locusla, G. androgenic gland during postembryonic elements affecting sex determination, salinus, and G. pulex. They were all development. This gland, situated at the the occurrence of transovarially trans­ infected with Thelohania sp. whose vas deferens, is the source of the male ferred microsporidians was detected. taxonomic position at the species level, sex hormone in Malacostraca and con­ Since these were found almost exclu­ as previously mentioned, is still uncer­ trols the differentiation of primary and sively in females, but sometimes in in­ tain. Th elohania sp. are transferred secondary male sex characters, and if it tersexes, it was supposed that the transoval;ally and, thus, the young are does not develop its hormonal function parasites might be involved in the infected at birth before sexual differen­ the gonads develop into ovaries mechanism of sex determination. In tiation is initiated. In G .Iocus/Q and G. (Charniaux-Cotton, 1956, 1965). order to obtain definite proof of this as­ salinus, breeding experiments with Observations on infected intersexes sumption, the sex ratio of female prog­ specimens attacked by the microsporid­ with rudimentary androgenic glands eny from a noninfected strain was com­ ians were conducted in the laboratory, and. later on, from experimentally in­ pared with that from experimentally whereas parasitized individuals of G. fected males, demonstrate that this infected females. Females derived from pulex were collected in the field. In all organ or its anlage are not attacked by one brood of two noninfected strains cases studied, it became evident that the parasites. Therefore, it is probable were divided into two groups. The females as well as males are associated that any substances or byproducts the females of one group were infected by with microsporidians. Therefore, a sex­ microsporidians excrete during their inoculation of contaminated ovarial tis­ determining influence by Thelohania multiplication might inhibit the differen­ sue into the body cavity, while the other sp. on their hosts can be excluded. tiation of this gland. The idea that the group was not infected and served as a With regard to the particular host­ parasites might cause such inhibitory ef­ control. After pairing with males about parasite relationship detected in the two fects was supported by another finding. 2 months later, offspring from the two microsporidian species associated with As mentioned above, males of G. groups were reared and sexed. The re­ G. duebeni females, the question duebeni have not been shown to be sults of this experiment, listed in Table arises: what is the underlying parasitized by either O. effeminans or 2, clearly demonstrate that the experi­ mechanism ofthe host's response to the T. heredileria. Therefore, experimental mental infection, compared with the infection? The suggestion that the mi­ infection ofadult males was undertaken control, resulted in shifting the sex ratio crosporidians might be involved in in order to test whether it exerts an significantly toward females. The influencing genetic processes control­ influence on their sexual organization. female descendants of the experimen­ ling determination and inheritance of Since attempts at peroral transfer failed, tally infected females proved to be con­ sex in G. duebeni, which was initially an inoculation was accomplished by taminated and produced only unisexual taken into consideration, could not be transplantation of contaminated tissues offspring. confirmed. Detailed studies on the of females into the male body cavity. The microsporidian responsible for mode of sex determination in this am­ After several molts, the male test ani­ this sex-ratio condition was shown to be phipod revealed a lack of heteromor­ mals infected by O. effeminans exhibit­ O. effeminans (Bulnheim, 1967; Buln­ phic sex chromosomes. From the re­ ed some alterations in their external heim and Vavra, 1968). Later, another sults obtained by breeding experiments sex characters. It was found that the microsporidian, T. herediteria, was de­ with non-infected individuals, it can be size of the gnathopods, uropods, and tected in G. duebeni females, which af­ concluded that sex determination is antennae was gradually reduced and fects sex determination of its host in the governed by a balanced polygenic sys­ development of oostegites, which rep­ same way when transmitted via the eggs tem of sex genes, whereby environmen­ resent secondary sex characters of to the offspring through successive gen- tal factors such as different photo- females, was observed. Thus, the males attained an intersexual appearance with Table 2.-Results of breeding experlmenls (15'C,100f0. sellnlly) In Gammarus duebeni infected with Oclosporea respect to external characters. How­ effemJnans.' ever, the male gonads, although in­ No. of No. of No. of Sex ratio Mortality vaded by microsporidians, displayed no Strain couples broods juveniles ';>0 ('!oj structural changes. Uninfected da 9 555 224:231 18 This finding indicates that interfer­ controls db 25 1.066 215:665 16 94 intersexes ence of microsporidians with the male sex hormone produced by the an­ Infected da 3 9 458 393:10 12 amphipods db 7 25 650 568:0 12 drogenic gland might be responsible for 3 intersexes the sexual alterations observed. On the 1 Females divided from one brood of two noninfected strains (da. db) were divided into two groups. The females of the other hand, a species-specific effect of one group were experimentally infected by transplantation of contaminated ovarial tissue. whereas the other group served as a control to compare sex ralio of descendanls in bolh series. (Data from Bulnheim. 1967). the microsporidians upon their host 44 -

10- Reference should be made to host­ Chamiaux-Collon, H. 1956. Determinisme hor­ monal de la differenciation sexuelle chez les parasite interactions between some Crustaces. Annee BioI. 32:371-399. Thelohania sp. and mosquitoes. In ---::-----:-,-_. 1965. Hormonal control ofsex dif­ 5- ferentiation in invertebrates. In R. L. DeHaan Culex larsalis, and probably also in and H. Ursprung (editors). Organogenesis, p. other representatives of Culicidae, in­ 701-740. Holt, Rinehart. and Winston, N.Y. Debaisieux, P. 1919. Etudes sur les Micro­ fection by Thelohania sp. is fatal to sporidies II. Glugea danilewski L. Pfr. III. Glugea mulleri L. Pfr, Cellule 30: 153-183. male larvae. Sporogony only occurs in _____. 1928. Etudes cytologiques sur :2 male hosts which usually succumb with quelques Microsporidies. Cellule 38:387-450. "- E progressive infiltration by the parasites, Fisher, F. M., Jr., and R. C. Sanborn. E 1- 1964. Nosema as a source ofjuvenile hormone whereas females acquire benign infec­ in parasitized insects. BioI. Bull. (Woods Hole) 126:235-252. tions and harbor only schizogonic Georgevitch, J. 1929. Nouvelles recherches sur 0.5- stages which are transmitted transovar­ les Microsporidies. Contribution a la connais­ -- NON-INFECTED ?2 AND JUVENILES sance du cycle evolutif de Plis/ophora bloch­ ~~ AND JUVENILES INFECTED BY ially (Kellen and Wills, 1962; Kellen et manni Zwblfer. Arch. Protistenkd. 65: 124-150. Hazard, E. I., and J. Weiser. 1968. Spores of THELOHANIA HEREDITERIA ai., 1965). The same responses have Thelohanin in adult female Anopheles: De­ been reported in Anopheles sp. infected velopment and transovarial transmission, and with Thelohania legeri, which is carried redescription of T. legeri Hesse and T. obesa I I Illllt! 11 1111 1 I Kudo. J. Protozool. 15:817-823. 0.001 0.005 0.01 0.05 0.1 9 via the eggs to their progeny. In each Jiovec, O. 1936. Studien uber Microsporidien. Mem. Soc. ZooI. Tchecosl. (Prague) 4:5-79. generation t he infected female larvae ----c"---.".. 1943. Cnidosporidia cizopasici y Figure 4.-Relatlonship between oxygen-uptake develop into adults, while infected male naSich blesivc-'ch. Priroda 35: 150-152. rates (standard metabolism) and size (wet weight) Kellen, W. R., H. C. Chapman, T. B. Clark, andJ. of Gammarus duebeni99 and Juveniles infected by larvae die (Hazard and Weiser, 1968). E. Lindegren. 1965. Host-parasite relation­ Thetohanta heredlterla In comparison with 99 and In contrast 10 the situation found in the ships of some Thelohania from mosquitoes Juveniles free of mlcrosporidlans (15°C, 10"/.. S). (Nosematidae: Microsporidia). J. Invertebr. Consumption of 0, Is expressed by the regression progeny of G. duebeni females as­ Pathol. 7: 161-166. equations log y = log 24.35 + 0.57 log. (Infected Kellen, W. R., and W. Wills. 1962. The trans­ specimens) and log y = log 30.63 + 0.607 log. sociated wi th O. effeminans or T. ovarian transmission of Thelohania califarnica (noninfected specimens). There are no significant heredileria, the shift ofsex ratio in mos­ Kellen and Lipa in Calex tarsalis Coquille!. J. differences (p>0.1) between the slopes of the two Insect Pathol. 4:321-326. regression lines. quitoes is caused by selective mortality Kudo, R. 1924. A biologic and taxonomic study ofthe offspring during the larval stages. ofthe Microsporidia. III. BioI. Monogr. 9:77-344. Labbe, A. 1899. Sporozoa. In Das Tierreich. 5. cannot be excluded. This became obvi­ Lieferg., Dtsch. Zool. Ges., Berl. LITERATURE CITED Uger, L., et E. Hesse. 1917. Sur les Micro­ ous when T. heredileria, experimen­ sporidies de la Crevelle d'eau douce. C. R. tally transferred to G. Juebeni males, Anders, F. 1957. Uber die geschlechtsbeein­ Hebd. Soc. BioI. (Paris) 80: 12-15. ftussende Wirking von FarbaJlelen bei Lipa, J. J. 1967. Nosema kozhovi sp. n., a new did not induce any changes in either ex­ Gammarus palex ssp. sabterraneas (Schneider). microsporidian parasite of Brandtin lata lata ternal or internal sex characters. The Z. fur Induhl. Abstamm.-und Vererbungsl. (Crastacea, Gnmmaridae) of Baical Lake. Acta 88:291-332. Protozool. 5:93-96. assumption of a species-specific action Bulnheim, H.-P. 1967. Mikrosporidieninfection Mercier, L. 1906. Sur une microsporidie du und Geschlechtsbestimmung bei Gammaras Talitre. C. R. Hebd. Soc. BioI. (Paris) 61:90-91. is confirmed by observations with S. daebeni. ZooI. Anz., SuppI. 30(Verh. DIsch. Pfeiffer, L. 1895. Nachtrage zu: Die Protozoen mulleri in association with G. duebeni, ZooI. Ges. 1966):432-442. als Krankheitserreger. Korresp.-BI. Allg. arztl. 1969. Zur Analyse gesch­ Ver. (Thurirtgen) 24:74-93 (I), 117-122 (II). where neither a sex-determining lechtsbestimmender Factoren bei Gammaras Pixell-Goodrich, H. 1929. Reactions of Gam­ influence on the host nor a modification d/lebeni (Crustacea, Amphipoda). Zool. Anz., marus to injury and disease, with notes on some SuppJ. 32 (Verh. Dtsch. Zool. Ges. microsporidial and fungoid diseases. Q. J. Mi­ of sex characters occurs. 1968):244-260. crosc. Sci. 72:325-353. It _---:-:----:_. 1970. Einftuss von mikrosporidien 1956. Crayfish epidemics. should be mentioned that a hor­ aufbestimmung und vererbung des Geschlechts. Parasitology 46:480-483. monal involvement of a microsporidian Umsch. wiss. Tec. 70:782-783. Poisson, R. 1924. Sur quelques Microsporidies 1971a. Entwicklung, Uber­ parasites d'Arthropodes. C. R. Acad. Sci. has been detected in insects. In a study lragung und Parasil-Wirt-Beziehungen von (Paris) 178:664-666. on endocrinological implications of Thelohania herediterio sp. n. (Protozoa. Mi­ Ryckeghem, J. van. 1930. Les Cnidosporidies et crosporidia). Z. Parasit.. 35:241-262. autres parasites du Gammarus pulex. Cellule Tribolium larvae infected by Nosema _--:__--,-. 1971b. Uber den wirlskreis der 39:399-418. sp., Fisher and Sanborn (1964) demon­ mikrosporidie Stempellio miilleri (On the host Sprague, V. 1970a. Some protozoan parasites range of the microsporidian Stempellia miilleri). and hyperparasites in marine decapod Crus­ strated the ability of the parasites to [Engl. Summ.} Arch. Protistenkd. 113: 137-145. tacea. Am. Fish. Soc. Spec. Publ. 5:416-430. _____. 1972a. On sex-determining factors __--:--:--:. 1970b. Taxonomy of Micro­ produce a substance with juvenile hor­ in some euryhatine Gammaras species. In B. sporidia. J. Parasitol. (Part I) 56:327. mone activity in their hosts. Battaglia, (editor), Proc. 5th Europ. Symp. Mar. Stempell. W. 1902. Ueber TheJohania miilleri (L. BioI., Piccin, Padova, p. 115-130. Pfr.). Zool. Jahrb. Anal. 16:235-272. The various aspects which pertain to 1972b. Vergleichende Unter­ Traut, W. 1962. Zur Geschlechtsbestimmung bei the relationships between microsporid­ suchungen zur Atmungsphysiologie euryhaliner Gammaras daebeni Lillj. und verwandten Arlen Gammariden unter besonderer Beriick­ (Crustacea, Amphipoda). Z. wiss. Zool. ian infection and sex determination in sichtigung der Salzgehaltsanpassung. [Engl. 167: 1-72. G. duebeni cannot be discussed in full abstr.] Helgolander. wiss. Meeresunters. Weiser, J. 1961. Die Mikrosporidien als Para­ 23:485-534. siten der tnsekten. Monogr. Angew. Entomol. detail in this presentation. Additional --,--- . (In press.) Intersexuality in 17: 1-149. Gammaridae and its conditions. Publ. Stn. Zool. Zwolfer, W. I926a. PlislOphora bloehmanni, results obtained from these investiga­ Napoli. eine neue Microsporidie aus Gnmmaras pulex L. tions will be submitted in a forthcoming Bulnheim, H.-P., and J. Vavra. 1968. Infection Arch. Protistenkd. 54:261-340. by microsporidian Oetosporea effeminans sp. 1926b. Plistophora bloehmanni. publication. In addition, the interrela­ n., and its sex determining influence in the am­ II. (Bemerkungen zu einer Microsporidienarbeit tions found between environmental fac­ phipod Gammuflls daebeni. J. Parasitol. von P. Debaisieus.) Arch. Protistenkd. 54:241-248. 54:341-354. tors, multiplication of the microsporid­ ians, and sex differentiation of the host MFR Paper 1146. From Marine Fisheries Review, Vol. 37, Nos. 5-6, have not been outlined in this report, May-June 1975. Copies 01 this paper, in limited numbers, are available since recent studies provide detailed in­ lrom 083, Technical Information Cenler, NOAA, Washington, DC 20235. Copies of Marine Fisheries Review are available from the Superintendent formation on this subject (Bulnheim, 01 Documents, U.S. Government Printing altice, Washington, D.C. 20402 1969, In press). for $1.10 each. 4S