197 Oceanography and Marine Biology: An Annual Review, 2006, 44, 197-276 © R. N. Gibson, R. J. A. Atkinson, and J. D. M. Gordon, Editors Taylor & Francis DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS — FROM HISTOLOGY TO ECOLOGY HEIKE WÄGELE 1 , MANUEL BALLESTEROS 2 & CONXITA AVILA 3 1 Rheinische Friedrich-Wilhelms-Universität, Institut für Evolutionsbiologie, An der Immenburg 1, 53121 Bonn, Germany and Zoologisches Forschungsmuseum Koenig, Adenauer Allee 160, 53113 Bonn, Germany E-mail: hwaegele@evolution.uni-bonn.de 2 Facultat de Biologia, Universitat de Barcelona, Av. Diagonal 645, 08028 Barcelona, Catalunya, Spain E-mail: mballesteros@ub.edu 3 CEAB-CSIC, c/Accés a la Cala Sant Francesc 14, 17300 Blanes, Girona, Catalunya, Spain E-mail: conxita@ceab.csic.es Abstract Opisthobranch molluscs are an extremely interesting group of animals, displaying a wide diversity in shape, colour and life strategies. Chemical ecology of this group is particularly appealing since most species have a reduced or absent shell and have developed chemical defences to avoid predation. New results on defensive glandular structures as well as a compilation of literature data in sea slugs (Opisthobranchia, Gastropoda, Mollusca) are presented in this review. Investigation of these structures is based on detailed analyses of the histology of many representative species of all major taxa of the Opisthobranchia. The results are correlated with previous and new findings of secondary metabolites in these animals and are set in a phylogenetic context. Addition- ally, information on food sources is given. Also, an hypothetical scenario relating chemical ecology to histology is proposed. This information will help future analyses to investigate defensive devices on a much more accurate basis and allow a better understanding of evolutionary processes, which are observed independently in many opisthobranch clades. Introduction Defensive strategies are manifold in Opisthobranchia and comprise cryptic appearance (Edmunds 1987, Wägele & Klussmann-Kolb 2005), formation of spicules (Cattaneo-Vietti et al. 1993, 1995), uptake of nematocysts from cnidarian prey (most recent literature: Gosliner 1994a, Martin & Walther 2002, 2003, Wägele 2004), incorporation of toxic metabolites from the prey, or even de novo synthesis of chemicals. Several reviews have covered the last topic of chemical ecology in molluscs (Karuso 1987, Cimino & Sodano 1989, Faulkner 1988, 1992, 2000, 2001, Pawlik 1993, Avila 1995, 2006, Cimino & Ghiselin 1998, Cimino et al. 2000, Stachowicz 2001, Amsler et al. 2001). Furthermore, some reviews have dealt with natural products from particular groups, such as porostome nudibranchs (Gavagnin et al. 2001), dorids and sacoglossans (Cimino et al. 1999, Cimino & Ghiselin 1998, 1999), or gastropods in general (Cimino & Ghiselin 2001), incorporating © 2006 by Taylor & Francis Group, LLC HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA 198 an evolutionary perspective in their analysis. In opisthobranchs, Faulkner & Ghiselin (1983) dis- cussed the importance of the acquisition of defensive chemicals during slug evolution, thus allowing the reduction of the shell (see also Wägele & Klussmann-Kolb 2005). This may have many ecological implications, such as the advantage of searching for new food sources, the exploitation of new habitats, and the development of mantle glands or structures, among others. Cimino & Ghiselin (1999) went even further in claiming that chemical defence is the driving force of opisthobranch evolution. Chemical defence is the main topic in molluscan chemical ecology, although it is by no means the only one. The importance of correctly demonstrating in situ activity against co-occurring predators has been a subject of repeated debate (Faulkner 1992, Avila 1995). However, many compounds are still assumed to have a defensive role without the supporting evidence of reliable ecological experiments. Ecological activity of the compounds has been evaluated in situ, against co-occurring predators for only a few species (Thompson 1960, Avila & Paul 1997, Johnson & Willows 1999, Marín et al. 1999, Avila et al. 2000, Becerro et al. 2001, Gosliner 2001, Iken et al. 2002, Rogers et al. 2002, Penney 2004). The methodological difficulties in carrying out in situ experiments or using co-occuring predators are probably responsible for the scarce information available. To overcome these problems, some studies used predators that do not occur in the same habitat (e.g., Mollo et al. 2005). On the other hand, there is also some literature that deals with parasites on opisthobranchs (Edmunds 1964; Arnaud 1978; Carefoot 1987; Huys 2001; Schrödl 2002, 2003; see also Rudman 2000a) but nothing is known about possible defensive strategies against these parasites. Since the review of the natural products of opisthobranch molluscs published 10 years ago (Avila 1995), many other articles have appeared that deal with opisthobranchs and which describe new interesting aspects of their chemistry (see Faulkner 2002 and previous reports; Blunt et al. 2005). Unfortunately, they cannot all be reviewed here. The geographic variation of natural products in Asteronotus cespitosus (Fahey & Garson 2002) and in Cadlina luteomarginata (Kubanek et al. 2000) has provided new insights into the field. Kubanek et al. (2000) suggested that in some nudibranchs, de novo biosynthesis may be modulated by habitat-specific external factors, thus working only when dietary compounds are not available. The authors suggested this represents an intermediate stage in the evolution of nudibranch chemical defences, between the probably primitive chemical sequestration from diet and the more evolved processes of de novo biosynthesis. The fact that some nudibranchs may only biosynthesise when dietary compounds are not available is an open question that needs to be tested in other species. Among nudibranchs, only C. luteomarginata and Dendrodoris grandiflora seem to possess both dietary sequestered compounds and biosynthetic chemicals (Cimino et al. 1985a, Avila et al. 1991a, Kubanek et al. 2000). Regarding the origin of these compounds, the number of biosynthetic compounds, compared with those obtained from the diet, continues to increase (Garson 1993, Cimino & Sodano 1994, Avila 1995, Faulkner 2002). The sesquiterpene aldehydes of the nudibranch Acanthodoris nanaimoensis are another example of de novo biosynthesis (Graziani & Andersen, 1996). Further studies on biosynthesis include Fontana et al. (1999a, 2003) and Jansen & de Groot (2004), and others reviewed by Garson (2001) and Cimino et al. (2004). Dietary chemicals are selected by a still unknown mechanism. Faulkner (1992) proposed two different mechanisms by which the selection of chemicals could be achieved, but this was never studied in detail. The sea hare Stylocheilus striatus accumulates very different metabolites when offered artificial diets (Pennings & Paul 1993). Fontana et al. (1994b) showed that in the laboratory a chromodoridid species was able to accumulate in the mantle glands compounds from a sponge that is not usually its prey in the field. These experiments would support the idea that the initial role of accumulation structures was that of excretion or autoprotection from the dietary chemicals and evolved later into a defensive mechanism. © 2006 by Taylor & Francis Group, LLC DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS 199 The available information on location and structure of the possible storage organs for chemical defences is scarce and mainly based on literature from the nineteenth to the early twentieth centuries (e.g., Blochmann 1883, Vayssière 1885, Perrier & Fischer 1911). The older literature was reviewed by Hoffmann (1939). More recent studies including histological structures are found, for example, in Edmunds (1966a,b), Thompson & Colman (1984), Thompson (1986), Gosliner (1994a), Wägele (1997), Kolb (1998), Brodie (2005) and Wägele & Klussmann-Kolb (2005). The couple Evelyn and Ernst Marcus, to whom we owe many thorough descriptions of opisthobranchs, very often included histological investigations when describing species, but only in very few cases do these cover defensive glands (also called repugnatorial glands) and then only in a rather sketchy way (e.g., Marcus & Marcus 1955; Marcus 1957, 1958, 1959). The same holds true for many descriptions from the Danish opisthobranch scientist Rudolph Bergh, which are not included here for the same reason. Recent and more extensive investigations on defensive glands are mainly confined to the mantle dermal formations (MDFs) in the doridoidean family Chromodorididae (García-Gomez et al. 1990, 1991; Cimino et al. 1993a; Avila & Paul 1997) and the glands of sea hares (Johnson & Willows 1999). Few investigations deal with epithelial structures or other glandular structures (e.g., Marín et al. 1991, Avila & Durfort 1996, Wägele 1997, Wägele & Klussmann-Kolb 2005). MDFs are suspected to store biochemicals from sponges, the food items of chromodorids. They are discussed as important key characters in the evolution of this particular family (Gosliner & Johnson 1994, Gosliner 2001, Wägele 2004) but, in fact, it is now known that other groups of opisthobranchs that do not forage on sponges also possess MDFs (see Wägele 1997, 2004 and this study). Finding MDFs in a bryozoan-consuming nudibranch (Limacia clavigera) (Wägele 1997) and in an algae- consuming sacoglossan (Plakobranchus ocellatus (see Wägele 2004)) renders invalid all the pre- vious assumptions of the mantle glands as an exclusive characteristic of the Chromodorididae. Until now, very few attempts have been made to relate knowledge on defensive chemicals to glandular structures known from histology (e.g., Marín et al. 1991 for Tethys fimbria, Marín et al. 1999 for Cephalaspidea). Avila (1993), Fontana et al. (1994b) and Avila & Durfort (1996) showed a preliminary relationship between some defensive glands and natural products for several species of nudibranchs. Actually, all the assumptions on location of chemicals are based on dissection and separation of body parts (e.g., MDFs, mantle border, etc.), and not on cytology or cytochemistry. This is the case in most of the located compounds, such as furanosesquiterpenes of Hypselodoris and Ceratosoma species, diterpenes of Chromodoris species, sesterterpenes of Glossodoris species, or sesquiterpenes of Dendrodorididae. This study tries to fill the gap in the knowledge of the relationship between glandular structures and defensive compounds by summarising histological studies on defensive glands or structures within Opisthobranchia and by tabulating published results on their secondary metabolites. Furthermore, the development of defensive glands, which are supposed to accumulate dietary chemicals in juvenile specimens of Hypselodoris species, was studied in order to ascertain their ontogeny. Material and methods To analyse the maximum information available on the defensive glands at histological, ecological and chemical levels, several species were selected from each group. Selection was based mainly on the availability of biological material for carrying out rigorous histological studies and also on existing data on ecology and chemistry for the species. However, this proved to be very difficult because very often data are incomplete. For example, data may be available on the chemistry but not on the histology and ecology of a species, and vice versa. Considerable effort has been made to include as many species as possible in the review so that it offers all the information available © 2006 by Taylor & Francis Group, LLC HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA 200 in the literature until June 2005. To reduce ambiguity, the taxonomic authorities of all species mentioned in the text are listed in Table 2. For histological analyses, many species were sampled during various expeditions all over the world in recent years, preserved in 4–6% formaldehyde/sea water and stored in 70% ethanol. After dehydration, the specimens were embedded in hydroxyethylmethacrylat (technique developed by Kulzer) (see Wägele 1997). Serial sections (2.5 μm) were stained with Toluidine blue, which specifically stains acid mucopolysaccharides red to violet, and neutral mucopolysaccharides blue. Some of the species investigated were very large and only smaller pieces could be studied histo- logically. However, this does not allow descriptions to be given of the wider occurrence of the glands, which have a very restricted distribution in the body. For comparison, a few basal pulmonate species are included. For analysis of the chemical composition of some structures (especially the mantle dermal formations), specimens of six species were embedded in Paraplast and sectioned (thickness of sections 5–6 μm). Different staining techniques were applied including two trichrome stains (Poinceau-Acidfuchsin-Azophloxin after Goldner, and Azocarmine-Aniline-Orange G after Heiden- hain) and a special staining technique for connective tissue (after Pasini). All methods are described in Böck (1989). Except where noted otherwise, staining records in the text and tables usually refer to Toluidine blue. Hypselodoris villafranca specimens for the ontogenetic studies were collected in Blanes and Tossa (Catalonia, Spain) in August 2003. Sizes of the juveniles ranged from 3–6 mm length. Some adults (15 mm) were also collected and studied to compare with the juveniles of the same popu- lations. They were fixed as described above. Results Description of glands Nearly all opisthobranch and pulmonate species investigated have more glands than just the repugnatorial or defensive glands and the foot in particular is highly glandular. These latter struc- tures, and others which are more likely involved in crawling (e.g., the tubular foot gland in pulmonates and some cephalaspideans), are not listed here, only those which might be of defensive value. The glandular structures can usually be assigned to certain types, some of which are already well known, others are newly described here. Defensive glandular structures are located in different areas of the animals. They can be located in the epidermis and are therefore part of the outer epidermis. They can lie subepidermally in the notum as single glandular structures or form distinct organs. Some lie in the notum, usually forming rather large organs. In a few cases, large glands are present in the visceral cavity. Table 1 and Figure 1 to Figure 9 give an overview of the types. Table 2 lists all the species investigated during the study and lists some types of glands found in particular species. The food and the chemical structure of the known secondary metabolites from the slug are also provided (Table 2). The glands are described and listed with regard to their location in the organism. Epidermal glandular structures, subepithelial glands, glands in the notum tissue and glands in the visceral cavity are distinguished (see Table 1). Glandular structures confined to the epidermis (Table 1, Table 2 Column 9) Single glandular cells (Table 1) Single glandular cells are mainly located in the notum epithelium and are widely spread. The contents of the vacuoles of the cells mainly stain dark violet, indicating acid mucopolysaccharides. Although morphological and histological complexity is rather low in these © 2006 by Taylor & Francis Group, LLC DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS 201 kinds of cells, a typical appearance of single glandular cells was noticed in many representatives of the Dendronotoidea (Figure 1A, Marionia blainvillea; see also Table 2 Column 9). Here the cuplike glandular cells are characterised by a huge vacuole, staining homogenously dark violet, indicating acid mucopolysaccharides. In other taxa, the contents of the vacuoles may be granular or even homogenous (Figure 1B, Dendrodoris nigra, arrow). This indicates the presence of different substances in the glandular cells. In Roboastra gracilis the glandular epithelium is characterised by numerous extremely tall violet-stained mucous cells with a granular appearance. (continued on page 227) Table 1 Overview of the different types of glandular structures arranged according to location, composition and staining properties Gland type Staining properties Violet staining — indicating acid mucopolysacharides Bluish staining indicating neutral mucopolysaccharides Nonstaining — indicating acidic or other substances Single gland cells in epidermis Cup cells (e.g., in many Dendronotoidea) (Figure 1A,B) Cells with a huge vacuole, contents staining homogeneously (Dendrodorididae) (Figure 1B) Spongy glands (Figure 1C) Single glands forming a layer Hypobranchial gland (Figure 1D) Subepithelial glands Single glandular cells of moderate size usually opening to the outside (Figure 4B at bottom) Bohadsch gland or opaline gland (Figure 2D,E) ‘Cellules spéciales’ (Figure 1F,G) Blochmann’s glands: some Cephalaspidea (Figure 2A,B) and Anaspidea (here known as ink gland or purple gland) (Figure 2C) Subepithelial acid glands (Pleurobranchoidea) (Figure 2G) Glandular organs lying in notum Marginal sacs of Arminidae (Figure 4A) Dorsal notum gland (Tylodinoidea) (Figure 3A–C) Interpallial gland (Scaphander) (Figure 3D,E) MDFs (Newnesia, Plakobranchus) (Figure 6A, 7F) MDF-like structures (Doriopsilla, Melibe, etc.) (Figure 6B–D, Figure 9A–F) Agglomeration of glandular cells (Thecacera, Cadlina) (Figure 4B,C) MDFs (Chromodorididae) (Figure 5A–F, Figure 6E–G, Figure 7A–F) Complex glands lying inside the body Median buccal gland (Bourne’s gland) (Pleurobranchoidea, Plocamopherus) (Figure 4D–F) © 2006 by Taylor & Francis Group, LLC HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA 202 Table 2 Compilation of available data on glandular structures, food and natural products. See notes on page 226. Column 1 2 3 456789 10 11 12 Higher taxon Genus and species, authorities Hypobranchial gland Spongy mantel glands Blochmann Glandular stripe MDF TYPE MDF-like structures Special defensive glands Food (references) Natural products (references) Previous histology (references) ACTEONOIDEA Hoffmann 1939 Acteonidae Acteon tornatilis Linneus, 1758 ++0000 Polychaeta (Rudman Web site Seaslugforum) Unknown Perrier & Fischer 1911, Hoffmann 1939, Wägele & Klussmann-Kolb 2005 Pupa solidula Linneus, 1758 ++0000 Polychaeta (Rudman Web site Seaslugforum) Unknown *Rudman 1972a Hydatinidae Hydatina physis Linneus, 1758 ++0000 Polychaeta (Rudman Web site Seaslugforum) Unknown Rudman 1972c CEPHALASPIDEA Hoffmann 1939 Aglajidae Chelidonura inornata Baba, 1949 ++0000 Turbellaria (Rudman Web site Seaslugforum) Unknown ** Chelidonura pallida Risbec, 1951 ++0+00 Congeners feed on polychaetes and turbellarians (Burn & Thompson 1998) Unknown Chelidonura tsurugensis Baba & Abe, 1959 + ? 0 + 0 0 Congeners feed on polychaetes and turbellarians (Burn & Thompson 1998) Unknown Wägele & Klussmann-Kolb 2005 © 2006 by Taylor & Francis Group, LLC 203 DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS Philinopsis cyanea (Martens, 1879) + 0 0 + 0 0 Cephalaspidea (Rudman Web site Seaslugforum, Yonow 1992) Unknown ** Haminoeidae Haminoea antillarum (d’Orbigny, 1841) + 0 + 0 0 0 Green algae (Rudman Web site Seaslugforum) Unknown ** Wägele & Klussmann-Kolb 2005, *Hoffmann 1939, *Marcus 1958, *Edlinger 1982 Haminoea callidegenita Gibson & Chia, 1989 + + + 0 0 0 Diatoms, detritus, pieces of Ulva, Cladophora (Gibson & Chia 1989, own studies) OC (Spinella et al. 1998, Alvarez et al. 1998, Izzo et al. 2000) ** Haminoea cymbalum (Quoy & Gaimard, 1833) ++0000 Green algae (Rudman Web site Seaslugforum) SQ (Poiner et al. 1989, Fontana et al. 2001) ** Haminoea orteai Talavera, Murillo & Templado, 1987 +0+00+ * Probably same food as other haminoids, namely turfing green algae (Burn & Thompson 1998) MO (Spinella et al. 1992b, 1992c, 1993, Marín et al. 1999) ** Bullidae Bulla vernicosa Gould, 1859 + + + ? 0 0 Green algae (Rudman Web site Seaslugforum) Unknown ** *Marcus 1957 (Bulla striata: discoidal glands above gill, open into mantle cavity) Smaragdinellidae Phanerophthalmus smaragdinus (Rüppell & Leuckart 1828) ++0+00 Green algae (Rudman 1972d) (Rudman Web site Seaslugforum) Unknown © 2006 by Taylor & Francis Group, LLC HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA 204 Table 2 (continued) Compilation of available data on glandular structures, food and natural products Column 1 2 3 456789 10 11 12 Higher taxon Genus and species, authorities Hypobranchial gland Spongy mantel glands Blochmann Glandular stripe MDF TYPE MDF-like structures Special defensive glands Food (references) Natural products (references) Previous histology (references) Smaragdinella cf calyculata (Broderip & Sowerby 1829) ++0+00 Herbivore (Rudman 1972d) PP OC (Szabo et al. 1996) Diaphanidae Newnesia antarctica Smith, 1902 ++0+2 * 0 ? Unknown Odhner 1926, Jensen 1996 Philinidae Philine alata Thiele, 1912 x + 0 ? 0 0 ?Foraminifera (Cedhagen 1996) Unknown *** *Guiart 1901, *Thompson 1960, 1986, 1988, *Rudman 1972b (P. auriformis) “fossette glandulare” Cylichnidae Scaphander lignarius Lineus, 1758 + + + ? 0 0 Interpallial gland Foraminifera, Annelida, Crustacea, Mollusca, Echinodermata, (Rudman Web site Seaslugforum) OC, IA? (Guiart 1901, Cimino et al. 1987a, 1989b) *** Perrier & Fischer 1911, Hoffmann 1939 Acteocina atrata Mikkelsen & Mikkelsen, 1984 + 0 0 ? 0 0 Foraminifera Unknown Sagaminopteron ornatum Tokioka & Baba, 1964 + 0 0 + 0 0 ? Unknown © 2006 by Taylor & Francis Group, LLC 205 DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS Siphopteron quadrispinosum Gosliner, 1989 + 0 0 + 0 0 ? Unknown Klussmann-Kolb & Klussmann 2003 Runcinidae Runcina adriatica Thompson, 1980 +00000 Unknown *Vayssiere 1883, *Hoffmann 1939, *Fernandez- Ovies 1983 SACOGLOSSA Hoffmann 1939 Plakobranchidae Elysia crispata (Mörch, 1863) 000000Many sub- epithelial glands Caulerpa, Halimeda (Jensen 1993) PP (Ireland et al., 1979, Ireland & Faulkner 1981, Ksebati 1985, Ksebati & Schmitz,1985, Gavagnin et al 1996, 1997a, 2000 (some as Tridachia crispata)) ** Wägele & Klussmann-Kolb 2005, *Marcus 1957 E. cauze Elysia ornata (Swainson, 1840) 0 00+0+ * Bryopsis sp. (Horgen et al. 2000, Jensen 1993) NC (Horgen et al. 2000) ** Elysia viridis (Montagu, 1804) 0 00+00 Codium vermilara, Bryopsis, Chaetomorpha Green algae (Jensen 1993, Gavagnin et al 1994, Trowbridge, 2004) PP (Gavagnin et al. 1992, 1994c) ** Thompson 1960, Wägele 1997 Plakobranchus ocellatus van Hasselt, 1824 000030 Udotea, Chlorodesmis (Jensen 1993) PP (Ireland & Scheuer 1979, Fu et al. 2000, Manzo et al. 2005) Kawaguti et al. 1966, Wägele & Klussmann-Kolb 2005 Thuridilla hopei (Verany, 1853) 000000Unusual contents of subepider- mal glands Derbesia tenuissima Green algae (Gavagnin et al. 1994c) DT (Gavagnin et al. 1992, 1993, 1994c) Oxynoidae Oxynoe viridis (Pease, 1861) +00000 Caulerpa (Jensen 1993) Unknown ** © 2006 by Taylor & Francis Group, LLC HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA 206 Table 2 (continued) Compilation of available data on glandular structures, food and natural products Column 1 2 3 456789 10 11 12 Higher taxon Genus and species, authorities Hypobranchial gland Spongy mantel glands Blochmann Glandular stripe MDF TYPE MDF-like structures Special defensive glands Food (references) Natural products (references) Previous histology (references) ANASPIDEA Blochmann 1883, Perrier & Fischer 1911, Klussmann-Kolb 2004 Akeridae Akera soluta (Gmelin, 1791) + + + + 0 0 Green algae (Rudman Web site Seaslugforum) Unknown ** *Perrier & Fischer 1911, *Hoffmann 1939, *Morton 1972 Aplysiidae Aplysia parvula Guilding in Mörch, 1863) 0 0 + ? 0 0 Opaline gland Green and red algae, Delisea pulchra, Laurencia filiformis, Portieria hornemannii MT DT SQ (Willan 1979, Fenical et al. 1979, Miyamoto et al. 1995, de Nys et al. 1996, Yamada & Kigoshi 1997, Higuchi et al. 1998, Rogers et al. 2000a,b, Ginsburg & Paul 2001, Jongaramruong et al. 2002) *Marcus & Marcus 1955, Klussmann-Kolb 2004 © 2006 by Taylor & Francis Group, LLC [...]... et al 1993, Dumdei 1994, Fontana et al 19 95, Dumdei et al 1997a, Kubanek et al 1997, 2000, Kubanek 1998 (but see also Avila 19 95) ) *Marcus 1 955 (Cadlina rumia) 0 Cadlina marginata MacFarland, 19 05 9 214 MDF-like structures 7 MDF TYPE 6 Glandular stripe 5 Blochmann 4 Spongy mantel glands Higher taxon Genus and species, authorities 3 Hypobranchial gland 2 Chromodorididae Glands in tubercles Ophlitaspongia... Cephalaspidea (e.g., Figure 2A, Haminoea antillarum, Figure 2B, Bulla vernicosa) and Anaspidea In Anaspidea this gland is called the ink gland and is composed of many Blochmann’s 228 © 2006 by Taylor & Francis Group, LLC DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS Figure 2 Histological sections of opisthobranch subepithelial glands (A) Haminoea antillarum Blochmann’s gland with duct composed of cuboidal... cerata (Doto, Eubranchus) Blochmann’s glands and ink gland (purple gland) (Table 1, Table 2 Column 5) Blochmann’s gland is a large single glandular cell lying subepithelially and characterised by a big nucleus The contents hardly stain The single gland has a duct composed of small cuboidal cells leading to the outside The glandular cell is surrounded by muscle fibres This glandular type is only present... Blochmann 1883, Hoffmann 1939, Wägele & Klussmann-Kolb 20 05 Hoffmann 1939 DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS © 2006 by Taylor & Francis Group, LLC Aplysia punctata Cuvier, 1803 © 2006 by Taylor & Francis Group, LLC 4 5 6 7 8 Blochmann Glandular stripe MDF TYPE MDF-like structures Higher taxon Genus and species, authorities 3 Spongy mantel glands 2 9 10 11 12 Special defensive glands... Compilation of available data on glandular structures, food and natural products 8 216 MDF-like structures 7 MDF TYPE 6 Glandular stripe 5 Blochmann 4 Spongy mantel glands Higher taxon Genus and species, authorities 3 Hypobranchial gland 2 ? ? ? ? + ? ? ? + ? 0 0 0 0 3 0 Hypselodoris fontandraui (Pruvot-Fol, 1 951 ) 0 0 0 0 0 0 Hypselodoris gasconi Ortea, 1996 Hypselodoris orsinii (Verany, 1846) ? ? ? ? + ? 0... 1966 Vayssiere 18 85, Wägele & Klussmann-Kolb 20 05 HEIKE WÄGELE, MANUEL BALLESTEROS & CONXITA AVILA Column 1 Hypobranchial gland Table 2 (continued) Compilation of available data on glandular structures, food and natural products Hoffmann 1939 0 0 0 0 0 Median buccal gland 0 0 0 0 0 0 Median buccal gland Porifera (Rudman Web site Seaslugforum) IA (Avila 1992, 1993, Thompson & Colman 1984) Berthellina... compound glands have larger vacuoles with granular and bluish stained contents They have been observed in several species, e.g., Cadlina luteomarginata and C laevis (Figure 2F) In the latter species, the glands are sunk deeply in the notum, and could also be assigned to the notum glands (see below) Glandular organs lying in the notum (Table 1, Table 2 Column 9) Dorsal mantle gland This gland is present... (B) Bulla vernicosa Blochmann’s gland (C) Aplysia parvula ink gland (composed of Blochmann’s glands) (D) Bursatella leachii opaline gland (gland of Bohadsch), note the large nucleus (arrow) (E) Clione limacina opaline glands (gland of Bohadsch), note the large nucleus (arrow) (F) Cadlina laevis compound glands lying in notum with outleading duct (G) Berthellina edwardsii acid glands in notum with opening... glands lying close together in the dorsal mantle cavity and opening above the gill (Figure 2C, Aplysia parvula) The ink gland exudes whitish or purple secretions The ink gland is considered to be only present in Anaspidea, but it is difficult to differentiate between the ink gland in the Anaspidea and the presence of the Blochmann’s glands in several members of the Cephalaspidea Subepithelial acid glands... 1997 DEFENSIVE GLANDULAR STRUCTURES IN OPISTHOBRANCH MOLLUSCS © 2006 by Taylor & Francis Group, LLC Notaeolidia gigas Eliot, 19 05 © 2006 by Taylor & Francis Group, LLC Table 2 (continued) Compilation of available data on glandular structures, food and natural products 8 224 MDF-like structures 7 MDF TYPE 6 Glandular stripe 5 Blochmann Facelinidae 4 Spongy mantel glands Higher taxon Genus and species, authorities . 197 Oceanography and Marine Biology: An Annual Review, 2006, 44, 19 7-2 76 © R. N. Gibson, R. J. A. Atkinson, and J. D. M. Gordon, Editors Taylor & Francis DEFENSIVE GLANDULAR STRUCTURES. data on glandular structures, food and natural products Column 1 2 3 456 789 10 11 12 Higher taxon Genus and species, authorities Hypobranchial gland Spongy mantel glands Blochmann Glandular stripe MDF. data on glandular structures, food and natural products Column 1 2 3 456 789 10 11 12 Higher taxon Genus and species, authorities Hypobranchial gland Spongy mantel glands Blochmann Glandular stripe MDF