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The Colleteric Glands in Sacculinidae (Crustacea, Cirripedia, Rhizocephala): an Ultrastructural Study of Ovisac Secretion

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The Colleteric Glands in Sacculinidae (Crustacea, Cirripedia, Rhizocephala): an Ultrastructural Study of Ovisac Secretion Contributions to Zoology, 70 (4) 229-242 (2002) SPB Academic Publishing bv, The Hague The colleteric glands in Sacculinidae (Crustacea, Cirripedia, Rhizocephala): an ultrastructural study of ovisac secretion Sven Lange Department of Cell Biology and Anatomy, Zoological Institute, University of Copenhagen, Universitets- parken 15, DK-2100 Copenhagen Ø, Denmark. Present address: Institutefor Biodiversity and Ecosystem Dynamics (IBED), PO box 94766,1090 GT Amsterdam, The Netherlands Keywords:: Cirripedia, Rhizocephala, Sacculina carcini, Thoracica, colleteric gland, ovisac, Carcinus maenas Abstract Ovisacs and oviposition in S. carcini 235 Colleteric glands and ovisac secretion in H. dollfusi 238 Discussion 238 Ovisac secretion by the paired colleteric glands of Sacculina Functional morphology of colleteric glands in carcini and Heterosaccus dollfusi (Rhizocephala, Sacculinida) S. carcini and H. dollfusi 238 was documented and studied at the ultrastructural level. and masses Oviposition formation of branched egg Preparatory to oviposition, the epithelium of each colleteric in S. carcini- 239 The gland secretes one branched, elastic, transparent ovisac. Ovisacs in other Rhizocephala 239 ovisac wall consists of a reticulated inner zone, secreted first, Morphological comparison between Sacculinidae and a dense outer zone. After secretion, the ovisac detaches and Thoracica 240 from most of the secretory epithelium but remains anchored 241 proximally in the gland until oviposition ends. The exterior Acknowledgements Abbreviations 241 ovisac surface is predominantly smooth and impervious. References 241 Proximally, however, the surface is irregular and perforated. the the During oviposition eggs enter paired ovisacs, forcing the ovisacs throughthe ovipores into the maternal mantle cavity. Simultaneously the ovisac volume increases approximately Introduction 100 The like times. resulting paired egg masses, branched the and ventilated in the mantle ovisacs, are brooded cavity. Ovisacs that with the The are aberrant cirripedians that prevent developing embryos are lost prematurely Rhizocephala ventilation Within two current. days the egg masses solidify parasitise other crustaceans, mainly Decapoda. They and attach to retinacula in the mantle cavity cuticle. The ovisacs, have lost the typical cirripedian feeding structures now probably obsolete, are no longer discernible. The literature and instead absorb nourishment by means of a on colleteric glandmorphology implies that ovisacs are secreted branched root system, which penetrates by all Sacculinidaeand perhapsother Rhizocephalawith colleteric profusely & in both the the host’s interior The glands. Similarities secretory process andmorphology (Bresciani Hoeg, 2001). between the colleteric ofSacculinidae suggest homology glands part of the parasite engaged in reproduction is and the oviducal glands of Thoracica (Cirripedia) and bet- usually attached externally to the host abdomen. ween their products. This so-called externa is of simple architecture. It includes a visceral mass containing a voluminous and ovary typically two sperm-producing recep- Contents tacles. A mantle surrounds the visceral mass. Be- tween these structures lies a mantle cavity, which Introduction 229 functions as a brood chamber and communicates Materials and methods 230 with the ambient sea mantle Results 230 by a opening (Hoeg & Anatomy of the externae of S. carcini and Liitzen, 1985). 230 H. dollfusi Most recent studies on rhizocephalan reproduc- Anatomy of the colleteric glands in S. carcini 230 tion have focused on the sperm-producing tissue Ultrastructure of the gland cells in S. carcini 231 (reviewed by Hoeg 1991; Hoeg & Liitzen 1995), Ovisac secretion in S. carcini 232 Downloaded from Brill.com10/09/2021 04:32:24PM via free access 230 S. Lange - Ovisac secretion in Sacculinidae, Crustacea used. Most while the function of the female part of the repro- Only mature, reproducing parasites were were dissected and the colleteric glands fixed immediately after ductive organs remains insufficiently understood. collection.Samples forTEM were fixed in modified trialdehyde addition to the In ovary, most species possess paired (Lake 1973), postfixed in osmium tetroxide for 1 to 2 hours, secretory oviducts, conventionally called colleteric embedded in Epon, ultrathin-sectioned and contrasted in uranyl Gland varies and has glands. design considerably acetate and lead citrate. Ultra sections were made on a LKB constitute of the been well-studied, as they one ultramicrotome and examined in a JEOL electron microscope fixed in Bouin few anatomical landmarks of importance for iden- (JLM-100 SX). Other glands were fixative, embedded in paraffin and sectioned for light microscopy. In tification and separation of species. Being flat or order to observe the oviposition and to obtain colleteric glands in shallow secretory epithelial pads some groups, during and immediately after this event a technique developed in other the glands are represented by simple sacs. by Delage (1884) was successfully applied (Fig. 1A). Crabs In two families (Clistosaccidae, Sacculinidae) the hosting S. carcini were strapped to a coarse nylon net by 0.5 glands possess richly branchedsecretory blind-sacs mm metal wire. The host was placed with its dorsal side against to immobilise (Hoeg & Liitzen 1985). the nylon net with special care taken chelipeds and legs to prevent the host from damagingits parasite. Finally Rhizocephala usually produce several broods in the abdomen was strapped down exposing the parasite to in succession (Hoeg & Liitzen 1985). A study of Sac- situ observation under dissection microscope while keeping the culina carcini Thompson, 1836 showed that the water. host and parasite in sea Since oviposition usually occurs colleteric gland epithelium undergoes a secretory 48-72 hours after nauplii-release,host animals could be strapped cycle, synchronously with the oocyte development, down well before oviposition. Ca. 48 hours after releasea window mantle ofthe in preparation to oviposition (Delage 1884). Delage (5x5 mm) was cut through the parasite enabling of ofthe colleteric and directobservation one two glands ovipores. concluded that each colleteric gland secretes an Hosts suffered no loss of appetite and the individual parasites ovisac that the when into envelops eggs they pass survived vivisection for more than 24 hours. Egg masses were the conclusion that has been mantle cavity, a ques- preserved at various times during and after oviposition (Figs. tioned authors from his time to the by many own 1B, C, D). Empty ovisacs were examined with interference con- present. trast optics (Nomarski). Comparative anatomy makes it obvious that the colleteric glands can best be compared to the ovi- ducal glands of the non-parasitic Cirripedia. Recent Results ultrastructural studies have shown that the ovisacs produced by these glands are important during I. Anatomy of the externae of S. carcini and H. oviposition and fertilisation (Walley 1965; Klepal dollfusi et al. 1977; Walker 1977, 1980). It was decided in this to the structure muscular mantle new perspective reinvestigate The bag-like externa consists of a of the colleteric and their secretion. S. carcini glands surrounding a visceral mass (Fig. 1). The visceral was chosen in order to check Delage’s results to- contains voluminous and mass one ovary paired wards modern and because this technique oviducts with colleteric glands situated superficially the text-book in represents typical Rhizocephala. the lateral surfaces, one on each side (orienta- tion in Paired explained legend to Fig. 1). recep- tacles normally housing dwarf males and paired Materials and methods ovipores all open into the mantle cavity, delim- ited by the mantle. The mantle cavity, which may S. carcini parasitising the common shore crab Carcinus maenas contain of branched communi- a pair egg masses, (L., 1758) were collected in August and September 1993 from cates with the sea through the mantle opening. eel-traps in the western part of Limfjorden, Denmark at 4 to 5 from mussels in m, or as by-catch commercial vessels fishing II. Anatomy of the colleteric glands in S. carcini the same area. Additional sacculinised crabs were collected in Gullmarsfjorden, Sweden, from ell-traps in August-October 1995 and and observed in water. of another kept running sea Specimens Seen from the outside the colleteric gland occu- sacculinid, Heterosaccus dollfusi Boschma, 1960 infesting the pies an oval- or heart-shaped 2x3 mm area dis- swimming crab Charybdis longicollis Leene, 1938 were collected tinguished from the surrounding ovary by a lighter with a beam-trawl in the Mediterranean off Palmahim, Israel, and clearer appearance in live as well as in pre- at 35 m in May 1994. Downloaded from Brill.com10/09/2021 04:32:24PM via free access - Contributions to Zoology, 70 (4) 2002 231 I. from The ofthe C. the Fig. Experimental set-up (modified Delage, 1884). immobilisation host, maenas, exposes sac-like parasite, orientation of S. carcini. 1A-D; Steps in the oviposition (explained in text). The conventional the sacculinid externa: The stalk and the The the visceral mass with mantle opening occur posteriorly and anteriorly respectively. mesentery connecting the mantle, marks the left side. However, this orientation lacks firm dorsal region. Consequently, the externae are seen from the anatomical evidence (see Hoeg& Liitzen 1985). Drawn by Beth Beyerholm. is minute served material. The ovipore a opening while rough endoplasmatic reticulum
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