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Microsporidian Infections of Amphipods with Special Reference

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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
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  • 192 396 397 398 399 400 401 402 403 404 405 406 407 408 409 410

    192 396 397 398 399 400 401 402 403 404 405 406 407 408 409 410

    192 201 Geography Appendix III 396 Yellow Sea 397 China 398 Ryukyu (=Loo Choo, = Lu-Chu, =Liu-Chiu) 399 [Boreal Pacific and Atlantic] 400 [Tropical Atlantic Ocean] 401 Mindelo quadrant, 15-30° N, 15-30° W or eastward to Africa, 200+ m 402 Atlantis quadrant, 15-30° N, 30-45° W, 200+ m 403 Vema quadrant, 15-30° N, 45-60° W, 200+ m 404 Sargasso quadrant, 15-30° N, 60-75° W but only east of Caribbean islands, 200+ m 405 406 Venezuela quadrant, 09-21° N, 61-83° W, but always south and west of Greater Antilles and north and east of American continent 407 Tortugas quadrant, 20-31° N, 82-100° W, 200+ m 408 Leone quadrant, 0-15° N, 15-30° W, 200+ m 409 Doldrum (Demerara) quadrant, 0-15° N, 30-45° W, 200+ m 410 [Atlantic Eurylatitudinal] 411 Guyana (Demerara) quadrant, 0-15° N, 4 5-60° W, 200+ m 412 Guinea quadrant, 0-15° S, 15° E-0°, 200+ m 413 Chain quadrant, 0-15° S, 0-15° W, 200+ m 414 Romanche (Chain) quadrant, 0-15° S, 15-30° W, 200+ m 415 Rocas (Pernambuco) quadrant, 0-15° S, 30-45° W, 200+ m 41*6 Valdivia quadrant, 15-30° S, 15° E-0°, 200+ m 417 Trade (Rio Grande) quadrant, 15-30° S, 0-15° W, 200+ m 418 Ridge (Almeida Columbia) quadrant, 15-30° S, 15-30° W, 200+ m 419 Hotspur (Santos) quadrant, 15-3,0° S, 30-51° W, 200+ m 420 [Cosmopolitan marine] 421 [Pantropical] 422 [Marine Cosmopolitan in latitudes below 60°] 423 [Cosmopolitan in latitudes below 45°] 424 [North Atlantic] 425 [South Atlantic] 426 [North and South Atlantic] 427 [Tropical to Boreal E.
  • Dictyocoela Microsporidia Diversity and Co-Diversification with Their Host, a Gammarid Species Complex (Crustacea, Amphipoda)

    Dictyocoela Microsporidia Diversity and Co-Diversification with Their Host, a Gammarid Species Complex (Crustacea, Amphipoda)

    Quiles et al. BMC Evol Biol (2020) 20:149 https://doi.org/10.1186/s12862-020-01719-z RESEARCH ARTICLE Open Access Dictyocoela microsporidia diversity and co-diversifcation with their host, a gammarid species complex (Crustacea, Amphipoda) with an old history of divergence and high endemic diversity Adrien Quiles1,2, Rémi A. Wattier1, Karolina Bacela‑Spychalska2, Michal Grabowski2 and Thierry Rigaud1* Abstract Background: Although the processes of co‑evolution between parasites and their hosts are well known, evidence of co‑speciation remains scarce. Microsporidian intracellular parasites, due to intimate relationships with their hosts and mixed mode of transmission (horizontal but also vertical, from mother to ofspring), may represent an interesting biological model for investigating co‑speciation. Amphipod crustaceans, especially gammarids, are regular hosts of microsporidian parasites, in particular the Dictyocoela spp., which have so far been found limited to these amphipods and are known to use a vertical mode of transmission. The amphipod genus Gammarus has a diversifcation history spanning the last 50–60 Mya and an extensive cryptic diversity in most of the nominal species. Here, we investigated the degree of co‑diversifcation between Dictyocoela and Gammarus balcanicus, an amphipod with high degrees of ancient cryptic diversifcation and lineage endemism, by examining the genetic diversity of these parasites over the entire geographic range of the host. We hypothesised that the strong host diversifcation and vertical transmission of Dictyocoela would promote co‑diversifcation. Results: Using the parasite SSU rDNA as a molecular marker, analyzing 2225 host specimens from 88 sites covering whole host range, we found 31 haplogroups of Dictyocoela, 30 of which were novel, belonging to four Dictyocoela species already known to infect other Gammarus spp.