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Comparative Electron Microscopic Study of the Stomach of Orchestia Cavimana and Arcitalitrus Sylvaticus (Crustacea: Amphipoda)

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Comparative Electron Microscopic Study of the Stomach of Orchestia Cavimana and Arcitalitrus Sylvaticus (Crustacea: Amphipoda) JOURNAL OF MORPHOLOGY 259:340–346 (2004) Comparative Electron Microscopic Study of the Stomach of Orchestia cavimana and Arcitalitrus sylvaticus (Crustacea: Amphipoda) Jasna Sˇ trus1* and Volker Storch2 1Department of Biology, University of Ljubljana, 1001 Ljubljana, Slovenia 2Zoologisches Institut, D 69120 Heidelberg, Germany ABSTRACT The functional morphology of stomachs of and also from that of other Mysidacea, Euphausia- the European semiterrestrial amphipod Orchestia cavi- cea, and Decapoda. Terrestrial isopods are well mana and of the Australian terrestrial species Arcitalitrus known for their complex stomach morphology. Dif- sylvaticus was studied by electron microscopy. The stom- ferences in the structure and function of the stom- ach of the two amphipod species is divided longitudinally achs in amphibious and terrestrial isopods were de- into a spacious dorsal food channel and two ventral filtra- ˇ tion channels. Additionally, a prominent helically oriented scribed by Strus et al. (1995). Studies by Coleman circulation channel is situated on each lateral side of the (1992) show that the stomachs of amphipods in gen- stomach, forming a semicircular channel separated from eral have a basic pattern, which in certain groups the food channel by spines. The food channel conveys could be related to food strategies. He described the coarse food particles directly into the midgut through a setation of lateralia as an important character that funnel. The filtration channels receive fine material fil- might indicate phylogenetic proximity among the tered through primary and secondary filters. Material families he examined. Comparative anatomical forced through the secondary filters by the pressure of the study of the stomach of hyperid amphipods laterally located inferolateralia eventually reaches the openings of the midgut glands. Washing of filters and (Coleman, 1994) showed that its structure is soaking of ingested food items with enzymes probably is strongly aberrant and the filtering capacity is re- achieved by a forward stream of digestive juice from the duced. It was proposed that the foregut morphology midgut glands and conveyed through the circulatory chan- could be helpful in amphipod classification. nels. The specializations of the stomach of the two species Since the amphipod stomach has been studied of Amphipoda investigated are described and compared to mainly in aquatic species, a study of a semiterres- the pertinent structures of Mysidacea and Isopoda. J. trial species, Orchestia cavimana, and a truly ter- Morphol. 259:340–346, 2004. © 2004 Wiley-Liss, Inc. restrial species, Arcitalitrus sylvaticus, was under- taken. O. cavimana has proliferated along European KEY WORDS: Orchestia cavimana; Arcitalitrus sylvati- cus; amphipods; stomach; electron microscopy river banks, starting from southeast Europe (Kin- zelbach, 1972; Fischenich, 1979). Our investigations showed that one reason for their success is that they feed indiscriminately on a range of food items. As Morphology of peracaridean alimentary systems interpreted from the ultrastructure of the R-cells of has attracted the attention of several crustacean the midgut glands, this species can metabolize cel- biologists (Schmitz and Scherrey, 1983; Schmitz, lulose (Storch and Burkhardt, 1984, 1986) better 1992; Wa¨gele et al., 1981; Wa¨gele, 1992; Coleman, ˇ than terrestrial isopods (Beck and Friebe, 1981), 1994; Strus et al., 1995; De Jong-Moreau, 1998). although the amphipods have been less successful However, our understanding of the most complex ecologically. Most semiterrestrial Amphipoda are re- part of the alimentary canal, the stomach, is still insufficient from the ultrastructural and functional as well as phylogenetic viewpoints. Only a few work- ers (Icely and Nott, 1984; Storch, 1987, 1989; Storch Contract grant sponsor: Deutsche Forschungsgemeinschaft; Con- ˇ tract grant number: DFG Sto 74/4 and 11; Contract grant sponsor: and Strus, 1989; Kobusch, 1998) have used electron Slovenian Ministry of Education, Science and Sport; Contract grant microscopy to analyze the peracaridean stomach. number: MSˇ ZSˇ PO-0525. The structure of the stomachs was studied in differ- ent species of Mysidacea and it was shown that the *Correspondence to: Jasna Sˇ trus, Department of Biology, Univer- morphology of the stomach is characteristic of the sity of Ljubljana, Vecˇna pot 111, 1001 Ljubljana, Slovenia. genus and not related to the ecology of the species E-mail: [email protected] (De Jong, 1996; De Jong-Moreau and Casanova, 2001). In Lophogastrida the fine structure of the stomach differs within genera of the same suborder DOI: 10.1002/jmor.10216 © 2004 WILEY-LISS, INC. EM STUDY OF AMPHIPOD STOMACH 341 stricted to fairly narrow niches. Landhoppers, truly terrestrial species of the family Talitridae, inhabit the leafmold of tropical and cold-temperature forests (Hurley, 1968). Where they are present, talitrids form an important element of the leaf-litter fauna, e.g., in the wetter forests of Australia and other regions of the southern hemisphere. About 120 spe- cies live independently of water bodies (Friend and Richardson, 1986). Most of these are as terrestrial as woodlice; their diet is generally unspecialized and consists principally of decayed plant material. The purpose of the current research was to de- scribe the complexity of the stomachs of the two ecologically different amphipod species and compare it to the stomachs of other peracaridean crusta- ceans. MATERIALS AND METHODS Orchestia cavimana Heller, 1865, was collected from the banks of river Rhine in Germany, and Arcitalitrus sylvaticus Haswell, 1978, was sampled from rotten logs at Mt. Tomah in New South Wales, Australia. Dissections of the stomachs were conducted under a binocular dissecting microscope. Complete unopened and opened stomachs were prepared for light and electron microscopy. For electron microscopy, whole stomachs and isolated parts were fixed in 3.5% glutaraldehyde in So¨rensen phosphate buffer (pH 7.5) for2hat4°C.Thefixed material was repeatedly rinsed in buffer, postfixed in buffered 1% osmium tetroxide, and dehy- drated through a graded series of ethanol. For scanning electron microscopy, opened stomachs were critical point-dried, sputter- coated with gold, and examined with a Cambridge SEM S4-10 microscope. The samples for transmission electron microscopy were embedded in Araldite. Semithin sections were stained with methylene blue-Azure II after Richardson et al. (1960). Ultrathin Fig. 1. a: Schematic presentation of amphipod stomach based sections were stained for 5 min with uranyl acetate and lead on micrographs of the foreguts in Orchestia cavimana and Arci- citrate (Reynolds, 1963). They were examined in a Zeiss EM 9-S2 talitrus sylvaticus. b: Gross morphology of the stomach in O. electron microscope. cavimana. The food channel (FC) is filled with food, the filtering channel (FiC) situated ventrally drives filtrate to the secondary filter (SF) region. Circulation channel (CC) is free of food parti- RESULTS cles. Scale bar ϭ 150 ␮m. Abbreviations for Figures 1–3: C, cardiac chamber; E, esophagus; F, funnel; IL, inferolateralia; IM, The following description of the stomach is inferomedianum; L, lateralia; PF, primary filter; P, pyloric cham- based on freshly dissected specimens, serial sec- ber; SF, secondary filter. tions, and scanning electron microscopic prepara- tions. Although we have selected to follow the descriptive scheme of Kanneworff and Nicolaisen the publications of Agrawal (1965) and Schmitz and (1969) and Icely and Nott (1984), phylogenetic Scherrey (1983). A longitudinal section of the stom- considerations require a terminology that may ach of Arcitalitrus sylvaticus shows that it is subdi- eventually make it possible to understand homol- vided into cardiac, pyloric, and funnel regions (Fig. ogies among the Peracarida. The anatomical no- 2a). However, to better understand the functioning menclature is based primarily on the work of of the stomach the subdivision into food, filtering, Scho¨nichen (1899), Scheloske (1976), and Licˇar (1977), who performed detailed studies on the and circulation channels should be taken into ac- anatomy of the isopod stomach. count (Fig. 1b). Coarse food particles are transported The sac-like stomach of Orchestia cavimana and through the food channel running along the roof of Arcitalitrus sylvaticus comprises about one-third of the stomach and are eventually conveyed to the the alimentary canal and extends from the esopha- midgut. Fluid may pass through complicated ventral gus to the funnel region (Fig. 1a,b) which protrudes filtration channels (Fig. 3a) leading to the midgut into the midgut. The whole stomach is lined by a glands where it is absorbed. In the midgut glands, cuticle of variable thickness and structure. Several digestive enzymes are produced and transported by folds project into the lumen, thus making cross- the circulatory channels which begin on each ven- sections difficult to interpret, as can be seen from trolateral side, surround the stomach helically, and 342 J. Sˇ TRUS AND V. STORCH Fig. 2. a: Longitudinal sec- tion of the stomach in Arcital- itrus sylvaticus consisting of the cardiac (C), pyloric (P), and fun- nel (F) regions with lateralia (L), inferolateralia (IL) and filtering compartments (PF, primary fil- ter; SF, secondary filters). SEM. Scale bar ϭ 150 ␮m. b: Parallel rows of filtering setae of paired secondary filter. Scale bar ϭ 10 ␮m. c: Filtering setae of the pri- mary filter (PF) along the an- teromedianum (A). Scale
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