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Grazing effect of two Gibbula species (Mollusca, Archaeogastropoda) on the epiphytic community of Posidonia oceanica leaves
Aquatic Botany, 35 (1989) 357-373 Elsevier Science Publishers B.V., Amsterdam - - Printed in The Netherlands
357
GRAZING E F F E C T OF TWO G I B B U L A S P E C I E S (MOLLUSCA, A R C H A E O G A S T R O P O D A ) ON THE E P I P H Y T I C C O M M U N I T Y OF P O S I D O N I A O C E A N I C A LEAVES
LUCIA MAZZELLA and GIOVANNI F. RUSSO
Stazione Zoologica "Anton Dohrn" di Napoli, Laboratorio di Ecologia del Benthos, 80077 Ischia (NA) (Italy) (Accepted for publication 13 April 1989)
ABSTRACT Mazzella, L. and Russo, G.F., 1989. Grazing effect of two Gibbula species (Mollusca, Archaeogastropoda) on the epiphytic community of Posidonia oceanica leaves. Aquat. Bot., 35: 357-373. The temporal and spatial patterns of the molluscs Gibbula ardens (L., 1758 ) and G. umbilicaris (Von Salis, 1793), which inhabit beds of Posidonia oceanica (L.) Delile indicated that these species occupy well-differentiated niches. To understand better this niche differentiation, the effect of the grazing activity of the two Gibbula species (Mollusca, Archaeogastropoda) on the epiphytic community (micro- and macroflora} of P. oceanica leaves was studied by scanning electron microscopy (SEM). The epiphytic community differs along the leaf axis according to leafage: the basal (youngest) part is colonized by bacteria and diatoms, ageing tissues by encrusting soft and calcareous algae, and the tips (oldest part ) by an upright layer on the encrusting layer. The large variety of periphyton components growing on the leaves represents a diversified food source for the herbivorous molluscs. G. ardens seems to prefer bacteria and diatoms, and seldom feeds on calcareous encrusting algae; G, umbilicaris seems to feed preferentially on erect macroalgae and seldom on soft encrusting species. Feeding habits are in accordance with species spatial arrangement along the leaves and the spatio-temporal distribution in the meadow.
INTRODUCTION
Herbivores represent an important fraction of the animal communities of seagrass systems (Ledoyer, 1962; Lewis and Hollingworth, 1982; Scipione and Fresi, 1984; Scipione, 1989) and hence it is important to establish their functional role. In spite of their conspicuous presence in these ecosystems, herbivores play a minor role in the direct consumption of plant production, the plant being converted through the so-called detritus food chain (Ott and Maurer, 1977; Yelimirov et al., 1981 ). However, herbivores are the principal consumers of the algal epiphytic community of the seagrass blade, whose contribution to 0304-3770/89/$03.50
© 1989 Elsevier Science Publishers B.V.
358 the overall production of the system is of paramount importance (van der Ben, 1971; Penhale, 1977; van Montfrans, Orth and Vay, 1982; Orth and van Montfrans, 1984; Heijs, 1985). In the ecosystem of Posidonia oceanica (L.) Delile, the algal epiphytic population is rich and diversified and, in relation to season and depth, can constitute a high percentage of the total biomass (Mazzella et al., 1982; Mazzella and Ott, 1984). In general, a more diversified community is present in all seasons in shallow stands than in the deep ones (Mazzella et al., 1989). Molluscs, and in particular Prosobranchs, are one of the principal algal consumers on rocky bottoms and in seagrass systems (see reviews by Orth and van Montfrans, 1984; Vadas, 1985). Several studies have been devoted to Prosobranch community ecology in P. oceanica prairies (Idato et al., 1983; Russo et al., 1983-84, 1984, 1985; Templado, 1984), however little is known concerning the trophic behaviour of the Mediterranean species and their influence on the structure of the epiphytic community. Furthermore, most studies on the effect of herbivorous molluscs concern macro-grazing, the importance of micro-grazing being underestimated. The present paper concerns the feeding habits of two Gastropod species belonging to the Trochidae family: Gibbula ardens (L., 1758) and Gibbula umbilicaris (von Salis, 1793). In the P. oceanica prairie off Lacco Ameno d'Ischia (Gulf of Naples), the species mostly co-occur in shallow stands, although G. umbilicaris dominates in summer and is generally found down to a depth of 5 m, while G. ardens is dominant in winter and is occasionally found in deeper stands (down to 30 m) (cf. Russo et al., 1984; G.F. Russo, unpublished data, 1985). According to Spada (1971), G. ardens is confined to the upper part of P. oceanica leaves, while G. umbilicaris is more widespread. Templado (1984), on the contrary, found G. umbilicaris on the foliar stratum and G. ardens at the rhizome level. The spatial arrangement of these species along the leaf axis is probably related to food availability and therefore to the colonization pattern of the micro- and macroflora that settles on the leaves (Mazzella, 1983; Novak, 1984; Casola et al., 1987). The qualitative approach used in this paper sheds some light on two aspects of the grazer-epiphyte relationship: the degree of selectivity among the microand/or macroflora exercised by the herbivores, and the impact of grazing on the whole algal community of the leaf blade. This study is a first step towards identifying and evaluating the different pathways of energy flow at low trophic levels in the herbivore food chain of a seagrass system. METHODS Gibbula umbilicaris and G. ardens specimens and plant shoots were collected at the end of May 1985 in a shallow stand (1 m depth) of the P. oceanica prairie off Lacco Ameno d'Ischia (Gulf of Naples). The specimens were placed in an aquarium and left for 5 days without food. Faecal pellets egested during this
359
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period, and therefore derived from the natural diet, were removed daily and fixed in alcohol for examination under the scanning electron microscope (SEM). To study the epiphytic colonization pattern along the leaf axes, two leaves, one old and one young, of a shoot were selected. A 1-cm long and ~ 1cm wide (depending on the width of the leaves) piece was cut out at the basal part and at each 10 cm along the leaves thereafter. The pieces so cut were fixed in alcohol for SEM examination. After the starving period, specimens of both mollusc species were placed in an aquarium containing Posidonia shoots and their spatial arrangement along the leaves was recorded. For grazing experiments old leaves, divided into three 8-cm long portions,
360 were used: (i) basal young tissue without macroscopic algal cover; (ii) intermediate tissue with primary cover formed by encrusting algae; (iii) apical old tissue with a full spectrum of epiphytes, including erect algae. Two pieces of the same type of tissue were suspended in a gauze-covered jar containing one mollusc specimen. The set of six jars (two mollusc species × three types of leaf tissue ) was replicated three times, for a total of 18 jars. All the jars were placed in an aquarium with running sea water (Fig. 1 ). Specimens were left to feed on the selected Posidonia pieces for 5 days. Faecal pellets were removed daily and fixed for SEM. On the sixth day, the leaf portions were removed from the jars and two 1-cm long segments of each piece were fixed in alcohol and both sides were examined under the SEM. RESULTS
Leaf epiphytic community Both sides of the basal part (very young tissue) of leaf blades were almost exclusively colonized by bacteria (Fig. 2A), with some rare diatoms, principally belonging to the genus Cocconeis (Fig. 2B). A few germination discs of encrusting algae (cf. Chamberlain, 1983) of the genera Fosliella and PneophyUum (Fig. 2C) were also found. This feature was observed within the first 20 cm of the ligula (the septum that separates the base from the photosynthetic tissue of the leaves ) of both the innermost (youngest) and outermost (oldest) leaves. The cover of encrusting calcareous algae (Fosliella and PneophyUum) increased with the distance from the ligula and several diatoms (mostly Coccoo neis) colonized the bare leaf surface, principally in the proximity of the edges of encrusting macrophytes (where they are probably protected from the micromovements of the water). This feature was more evident on ageing tissues (at ~ 40 cm from the base), with diatoms mainly settled among the macrophyte thalli on the available leaf surface (e.g., Cocconeis, Fig. 3A), or inserted under the edges of the crust (e.g., Fragilaria and Amphora, Fig. 3B ). On young Posidonia leaves, this pattern was the last stage observed in summer. On ageing leaves of the shoot, the encrusting algal community occupied almost the whole apical portion of the leaf surface. At this stage, a more diversified diatom flora, differing in the shape and size of the frustules (e.g., Striatella, Fragilaria, Cocconeis, Amphora, Navicula ) , had settled on the macrophyte thalli, mainly in the microcavities of calcareous algae (Fig. 3C). The macroflora colonization of the internal side of the blade differed from that of the external side. On the side less exposed to light and water movement, only a primary encrusting cover was seen, while on the other side there was a secondary erect layer growing on the primary layer. Towards the tip, the first erect structures to appear on the leaves were ascocysts and zoidocysts (vege-
Fig. 2. Colonization pattern in young tissues of P. oceanica leaves. (a) Bacttrial colonies [size bar (s.b.) = 10/xm ]; (b) diatom cells of Cocconeis scutellum Ehrenberg settled on the leaf surface (s.b. = 10 pm); (c) germination discs of encrusting red algae Fosliella and Pneophyllurn (s.b. = 0.1 mm ); (d) germination disc of Pneophyllum lejolisii (Rosanoff) Chamberlain with Cocconeis cells (s.b. = 0.1 mm ).
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Fig. 3. (a), (b) Old portion of young P. oceanica leaves. (a) Red calcareous algae surrounded by frustules of Cocconeis and Fragilaria {s.b. = 0.1 mm); (b) colonies of bacteria settled on the leaf surface and diatoms (Fragilaria) distributed along the crust edge of red calcareous algae (s.b.-- 10 pm). (c) Intermediate portion of old P. oceanica leaves: bacteria and diatoms (Cocconeis and Fragilaria ) settled on calcareous red algae (s.b. -- 10/~m).
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Fig. 4. Old portions of P. oceanica leaves. Algal erect layer: (a) vegetative and reproductive (ascocysts and zoidocysts) filaments ofMyrionema orbiculare (s.b.=0.1 mm); (b) erect layer with the species Giraudia sphacelarioides (G) and erect filaments of M. orbiculare (M) (s.b. = 1 mm ); (c) diatoms (Nitzschia) entrapped among the erect algal filaments (s.b. = 1/tm).
Fig. 5. Grazing effect of G. ardens on different leaf portions of P. oceanica leaves. (a) Grazing traces on bacterial colonies (s.b. = 10 ttm) and (b) on germination disc of encrusting calcareous alga (s.b. -- 0.1 mm); (c) broken frustules of the diatom Cocconeis (s.b. = 10 ]~m); (d) Gibbula radular tracks on the leaf surface (s.b. = 0.1 mm ); (e) grazing traces on a calcareous alga and (f) on the "soft" M. orb iculare (s.b. = 0.1 m m ) .
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tative and reproductive filaments) of the encrusting alga Myrionema orbiculare J. Agardh (Fig. 4A). At~60 cm from the base and on the side with the highest light exposure (usually, but not always, the external side), there was a dense growth of erect algae, mostly of Castagnea cylindrica Sauvageau, C. irregularis Sauvageau and Giraudia sphacelarioides Derb~s et Solier {Fig. 4B). Among the upright layer, the diatom flora consisted mainly of species of the genera Mastogloia and Nitzschia (Fig. 4C).
Effect of Gibbula ardens grazing On very young tissues, the grazing of G. ardens was evident from traces of removal of the bacterial colonies (Fig. 5A ) and of algal germination discs (Fig. 5B).
Fig. 6. Faecal pellet of G. ardens. (a) General structure of the faecal pellet (s.b.=0.1 mm); (b) broken frustules of diatoms included in the remaining material of the faecal pellet (s.b. = 10/~m).
Fig. 7. Grazing effect of G. umbilicaris on different tissue of P. oceanica leaves. (a) Young and intermediate leaf portions with unattached bacteria and diatoms (Fragi/aria and Cocconeis) (s.b. = 0.1 mm); (b) broken crusts of a red calcareous alga (s.b. = 0.1 mm) and (c) of M. orbiculare (s.b. =0.1 mm): (d) old part of the leaf with erect layer grazed by the mollusc (s.b. = 1 mm).
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Fig. 8. Faecal pellet of G. umbilicaris. (a) G e n e r a l feature w i t h several u n b r o k e n d i a t o m frustules ( s.b. = 0.1 m m ); ( b ) r e m a i n s of ingested macroalgae ( s .b. = 0.1 m m ).
Leaf tissues bearing mainly diatoms and calcareous algae often showed remains of Cocconeis frustules (Fig. 5C); radular tracks, made by the teeth on the leaf surface, were also observed (Fig. 5D ). The algal crusts, represented by Fosliella and PneophyUum thalli, showed clear breaking marks where cells of epi- and even hypothallium had been removed (Fig. 5E). More often, there were broken frustules of diatoms that had been removed by the grazer from the encrusting thalli. On older tissues, where the encrusting soft alga M. orbiculare covered most of the leaf surface, its erect filaments (vegetative and reproductive) were preferentially grazed. The prostrate part of the thallus was seldom grazed. In the latter case, remains of walls of the basal cells were evident (Fig. 5F). Traces of grazing by G. ardens were negligible on the oldest tissues.
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The faecal pellets were elongated, semicircular in transversal section, showing two ruts at the basis and a brain-like feature on the top (Fig. 6A). They were composed of an amorphous matrix of packed feeding remains, among which broken frustules of diatoms could be distinguished (Fig. 6B ). No differences in composition were observed between faecal pellets derived from a natural diet and those derived from "forced" grazing in aquaria.
Effect of Gibbula umbilicaris grazing Even without a microscope, a marked reduction of erect macroflora could be observed on Posidonia leaves grazed by G. umbilicaris. Scanning electron microscope observations showed that young leaf portions, exclusively colonized by microflora (bacteria and diatoms), were practically unaffected by grazing activity (Fig. 7A). Clear traces of grazing were observed on the primary layer that was formed of encrusting macrophytes. Calcareous FoslieUa and PneophyUum and soft Myrionema often showed traces of rasping by the mollusc; this was evident from the broken crusts and the damaged basal cells (Fig. 7B-C ). The encrusting cover had been totally removed from the leaf surface in some areas, where tracks of radular teeth could also be observed (Fig. 7D ). Diatoms living on this algal stratum remained mostly intact. On the oldest portions of the leaves, the secondary algal stratum, consisting of filaments (ascocysts and zoidocysts) of encrusting algae and erect macrophytes, were clearly reduced by grazing activity (Fig. 7E ). The faecal pellets were coarser, but similar in shape to those of the congeneric species (Fig. 8A). Among the packed feeding remains, macrophyte thalli and filaments from the upright epiphytic layer (Fig. 8B ) were easily identified. Many diatoms were present and most had intact frustules (Fig. 8A). Also in this species, there appeared to be no difference between faecal pellets derived from natural diets and those from experimental diets. DISCUSSION
The epiphytic colonization observed along the P. oceanica leaf is principally controlled by biological factors such as the growth rhythm (age) of the host plant and the life cycle of the epiphytes (Casola et al., 1987). These factors also affect microclimatic conditions, which in turn affect algal spatial arrangement. The result is a succession of vegetal epiphytic populations, from the leaf bases to the top, and a diversified micro- and macroflora. This situation is paramount in determining the spatial arrangement of herbivores, especially of creeping forms such as molluscs and, on a wider scale, in determining their presence. In fact, the occurrence of herbivorous species depends on the characteristics of the single algal species, e.g., the size, the shape and the toughness (Steneck and Watling, 1982; Russo, 1986 ), and on the struc-
370 ture of the whole community (see Hudon and Legendre, 1987, for microphytes; Lubchencko and Cubit, 1980, for macrophytes). Gibbula ardens grazes mainly on the algae characteristic of the first stage of colonization. This species removes bacteria and small adherent diatoms, mainly of the genus Cocconeis, from the bare leaf surface and from the primary encrusting layer. Large diatoms, such as Striatella spp., are left untouched. The large amount of broken diatom frustules in the faecal pellets confirms that the microphytes are the principal component of the diet of this species, although encrusting algae are also broken and presumably ingested. The secondary erect algal layer of the last successional stage is practically unaffected by the grazing activity of this species. The feeding activity of G. umbilicaris is opposite to that observed for G. ardens (Fig. 9). G. umbilicaris removes the secondary layer from the apical parts of the leaves and the faecal pellets contain the remains of the filamentous erect structures. The encrusting algae, including calcareous species, are seldom ingested, judging from the remains in the faecal pellets. Microphytes are only slightly grazed from each portion of the leaves. The presence of many intact cells of different size and shape in the faecal pellets suggests that the grazed diatoms seem to be poorly digested by the mollusc. The zonation along the leaf axes of the different food sources utilized by the two species is in agreement with the spatial arrangement of the specimens observed in aquarium, i.e., G. ardens distributed preferentially towards the base and G. umbilicaris towards the tip. These observations confirm the data reported by Templado (1984) and are in contrast with the in situ observations of Spada (1971). On a wider scale, the successional stages of the epiphytic community observed along the P. oceanica leaves differ according to season and depth (Battiato et al., 1982; Cinelli et al., 1984; Mazzella et al., 1989). The full spectrum of epiphytes was, in fact, recorded only in the shallow waters during the summer season, and was associated with the highest abundance of G. umbilicaris (Russo et al., 1984). In addition, the dominance of G. ardens in winter and its occasional presence in deeper stands of the prairie fits well with the contemporary and almost exclusive presence of the primary epiphytic covering on the leaf blades. In conclusion, G. ardens and G. umbilicaris can use a wide range of algal food (bacteria, small and large diatoms, soft and calcareous macrophytes, erect algae), although each of them feeds preferentially on organisms characterizing a different and well-defined stage (first and last, respectively) in the succession of the epiphytic community zoned along the P. oceanica leaves (Fig. 9). This difference in feeding habits explains well the species' occurrence during the year and their arrangement along the Posidonia leaves.
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zione Zoologica "Anton Dohrn" di Napoli for their invaluable help in conducting the SEM examinations; thanks are also due to the Photo- and Light Optics Laboratory. REFERENCES Battiato, A., Cinelli, F., Cormaci, M., Furnari, G. and Mazzella, L., 1982. Studio preliminare della macrofiora epifita della Posidonia oceanica (L.) Delile di una prateria di Ischia (Golfo di Napoli) (Potamogetonaceae, Helobiae). Nat. Sicil., S. IV, VI {suppl.), 1: 15-27. Casola, E., Scardi, M., Mazzella, L. and Fresi, E., 1987. Structure of the epiphytic community of Posidonia oceanica leaves in a shallow meadow. P.S.Z.N.I: Mar. Ecol., 8: 285-296. Chamberlain, Y.M., 1983. Studies in the Corallinaceae with special reference to FoslieUa and PneophyUum in the British Isles. Bull. Br. Mus. (Nat. Hist.) Bot., 11: 291-463. Cinelli, F., Cormaci, M., Furnari, G. and Mazzella, L., 1984. Epiphytic macroflora of Posidonia oceanica (L.) Delile leaves around the island of Ischia (Gulf of Naples). 1st International Workshop on Posidonia oceanica beds, C.F. Boudouresque, A. Jeudy de Grissac and J. Olivier {Editors), G.I.S. Posidonie Publ. Fr., pp. 91-99. Heijs, F.M.L., 1985. Some structural and functional aspects of the epiphytic components of four seagrass species {Cymodoceoideae) from Papua New Guinea. Aquat. Bot., 23: 225-247. Hudon, C. and Legendre, P., 1987. The ecological implications of growth forms in epibenthic diatoms. J. Phycol., 23: 434-441. Idato, E., Fresi, E. and Russo, G.F., 1983. Zonazione verticale della fauna vagile di strato foliare in una prateria di Posidonia oceanica (L.) Delile: I Molluschi. Boll. Malacol. Milano, 19: 109120. Ledoyer, M., 1962. Etude de la fauna vagile des herbiers superficiels de Zosterac~es et quelques biotopes d'algues littorales. Rec. Trav. Stn. Mar. Endoume-Marseille Fasc. Hors Ser. Suppl., 39: 117-235. Lewis, J.B. and Hollingworth, C.E., 1982. Leaf epifauna of the seagrass Thalassia testudinum. Mar. Biol., 71: 41-49. Lubchenco, J. and Cubit, J., 1980. Heteromorphic life histories of certain marine algae as adaptations to variations in herbivory. Ecology, 61: 676-687. Mazzella, L., 1983. Studies on the epiphytic diatoms of Posidonia oceanica (L.) Delile leaves. Rapp. Comm. Int. Mer M~dit., 28(3): 127-128. Mazzella, L. and Ott, J.A., 1984. Seasonal changes in some features of Posidonia oceanica (L.) Delile leaves and epiphytes at different depths. 1st International Workshop on Posidonia oceanica beds, C.F. Boudouresque, A. Jeudy de Grissac and J. Olivier (Editors), G.I.S. Posidonie Publ. Fr., 1: 119-127. Mazzella, L., Wittmann, K.J. and Fresi, E., 1982. La comunit~ epifita e suo ruolo nella dinamica dell'Ecosistema Posidonia. Atti del Convegno delle U.O. Sottoprogetti Risorse Biologiche ed Inquinamento Marino, Roma, November 1981, pp. 215-224. Mazzella, L., Scipione, M.B. and Buia, M.C., 1989. Spatio-temporal distribution of algal and animal communities in a Posidonia oceanica (L.) Delile meadow. P.S.Z.N.I: Mar. Ecol., 10: 107131. Novak, R., 1984. A study in ultra-ecology: Microorganisms on the seagrass Posidonia oceanica (L.) Delile. P.S.Z.N.I.: Mar. Ecol., 5: 143-190. Orth, R.J. and van Montfrans, J., 1984. Epiphyte-seagrass relationship with an emphasis on the role of micrograzing: a review. Aquat. Bot., 18: 43-69. Ott, J.A. and Maurer, L., 1977. Strategies of energy transfer from marine macrophytes to consumer level: the Posidonia oceanica example. In: B.F. Keegan, P.O. Ceidigh and P.J.S. Boaden (Editors) ,Biology of Benthic Organisms, Pergamon Press, Oxford. pp. 493-502.
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Penhale, P., 1977. Macrophyte-epiphyte biomass and productivity in an eelgrass (Zostera marina) community. J. Exp. Mar. Biol. Ecol., 26: 211-224. Russo, G.F., 1986. Evoluzione ed adattamenti trofici nei Prosobranchi: spunti per una analisi funzionale del popolamento malacologico di una prateria a Posidonia oceanica dell'isola d'Ischia. Nova Thalassia, 8 (Suppl. 3 ): 643-644. Russo, G.F., Fresi, E., Vinci, D. and Chessa, L.A., 1983-84. Malacofauna di strato foliare delle praterie di Posidonia oceanica (L.) Delile intorno all'isola d'Ischia (Golfo di Napoli): analisi strutturale del popolamento estivo in rapporto alia profondith ed alla esposizione. Nova Thalassia, 6: 655-661. Russo, G.F., Fresi, E., Vinci, D. and Chessa, L.A., 1984. Mollusks syntaxon of foliar stratum along a depth gradient in a Posidonia oceanica (L.) Delile meadow: seasonal variability. 1st International Workshop on Posidonia oceanica Beds. C.F. Boudouresque, A. Jeudy de Grissac and J. Olivier (Editors), G.I.S. Posidonie Publ., Fr., 1: 311-318. Russo, G.F., Fresi, E., Buia, M.C. and Vinci, D., 1985. Malacofauna delle praterie a Posidonia oceanica (L.) Delile della zona di Capo Passero (Sicilia Sud-orientale): analisi comparativa con i popolamenti dell'isola d'Ischia. Oebalia, 11NS:319-324. Scipione, M.B., 1989. Comportamento trofico dei Crostacei Anfipodi in alcuni sistemi bentonici costieri. Atti XIX congresso della Scieth Italiana di Biologia Marina, Oebalia. Scipione, M.B. and Fresi, E., 1984. Distribution of Amphipod Crustaceans in Posidonia oceanica (L.) Delile foliar stratum. 1st International Workshop on Posidonia oceanica Beds. C.F. Boudouresque, A. Jeudy de Grissac and J. Olivier (Editors), GIS Posidonie publ., Fr., 1: 319-329. Spada, G., 1971. Contributo aUa conoscenza della malacofauna della biocenosi a Posidonia oceanica (L.) lungo le coste italiane. Conchiglie, Milano, 8 (9-10 ): 125-135. Steneck, R.S. and Watling, L., 1982. Feeding capabilities and limitation of herbivore molluscs: a functional group approach. Mar. Biol., 68: 299-319. Templado, J., 1984. Moluscos de las praderas de Posidonia oceanica en las costas del cabo de Palos (Murcia). Invest. Pesq., 48: 509-526. Vadas, R.L., 1985. Herbivory: In: M.M. Littler and D.S. Littler (Editors), Handbook of Phycological Methods: Ecological Field Methods. Macroalgae. Cambridge University Press, Cambridge, pp. 532-572. Van Montfrans, J., Orth, R.J. and Vay, S.A., 1982. Preliminary studies of grazing by Bittium uarium on eelgrass periphyton. Aquat. Bot., 14: 75-89. Van der Ben, D., 1971. Les ~piphytes des feuilles de Posidonia oceanica Delile sur les cotes franqaises de la M6diterrande. Mem. Inst. R. Sci. Belg., 168: 1-101. Velimirov, B., Ott, J.A. and Novak, R., 1981. Microorganisms on macrophyte debris : biodegradation and its implication in the food web. Kiel. Meeresforsch., 5: 33-334.
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GRAZING E F F E C T OF TWO G I B B U L A S P E C I E S (MOLLUSCA, A R C H A E O G A S T R O P O D A ) ON THE E P I P H Y T I C C O M M U N I T Y OF P O S I D O N I A O C E A N I C A LEAVES
LUCIA MAZZELLA and GIOVANNI F. RUSSO
Stazione Zoologica "Anton Dohrn" di Napoli, Laboratorio di Ecologia del Benthos, 80077 Ischia (NA) (Italy) (Accepted for publication 13 April 1989)
ABSTRACT Mazzella, L. and Russo, G.F., 1989. Grazing effect of two Gibbula species (Mollusca, Archaeogastropoda) on the epiphytic community of Posidonia oceanica leaves. Aquat. Bot., 35: 357-373. The temporal and spatial patterns of the molluscs Gibbula ardens (L., 1758 ) and G. umbilicaris (Von Salis, 1793), which inhabit beds of Posidonia oceanica (L.) Delile indicated that these species occupy well-differentiated niches. To understand better this niche differentiation, the effect of the grazing activity of the two Gibbula species (Mollusca, Archaeogastropoda) on the epiphytic community (micro- and macroflora} of P. oceanica leaves was studied by scanning electron microscopy (SEM). The epiphytic community differs along the leaf axis according to leafage: the basal (youngest) part is colonized by bacteria and diatoms, ageing tissues by encrusting soft and calcareous algae, and the tips (oldest part ) by an upright layer on the encrusting layer. The large variety of periphyton components growing on the leaves represents a diversified food source for the herbivorous molluscs. G. ardens seems to prefer bacteria and diatoms, and seldom feeds on calcareous encrusting algae; G, umbilicaris seems to feed preferentially on erect macroalgae and seldom on soft encrusting species. Feeding habits are in accordance with species spatial arrangement along the leaves and the spatio-temporal distribution in the meadow.
INTRODUCTION
Herbivores represent an important fraction of the animal communities of seagrass systems (Ledoyer, 1962; Lewis and Hollingworth, 1982; Scipione and Fresi, 1984; Scipione, 1989) and hence it is important to establish their functional role. In spite of their conspicuous presence in these ecosystems, herbivores play a minor role in the direct consumption of plant production, the plant being converted through the so-called detritus food chain (Ott and Maurer, 1977; Yelimirov et al., 1981 ). However, herbivores are the principal consumers of the algal epiphytic community of the seagrass blade, whose contribution to 0304-3770/89/$03.50
© 1989 Elsevier Science Publishers B.V.
358 the overall production of the system is of paramount importance (van der Ben, 1971; Penhale, 1977; van Montfrans, Orth and Vay, 1982; Orth and van Montfrans, 1984; Heijs, 1985). In the ecosystem of Posidonia oceanica (L.) Delile, the algal epiphytic population is rich and diversified and, in relation to season and depth, can constitute a high percentage of the total biomass (Mazzella et al., 1982; Mazzella and Ott, 1984). In general, a more diversified community is present in all seasons in shallow stands than in the deep ones (Mazzella et al., 1989). Molluscs, and in particular Prosobranchs, are one of the principal algal consumers on rocky bottoms and in seagrass systems (see reviews by Orth and van Montfrans, 1984; Vadas, 1985). Several studies have been devoted to Prosobranch community ecology in P. oceanica prairies (Idato et al., 1983; Russo et al., 1983-84, 1984, 1985; Templado, 1984), however little is known concerning the trophic behaviour of the Mediterranean species and their influence on the structure of the epiphytic community. Furthermore, most studies on the effect of herbivorous molluscs concern macro-grazing, the importance of micro-grazing being underestimated. The present paper concerns the feeding habits of two Gastropod species belonging to the Trochidae family: Gibbula ardens (L., 1758) and Gibbula umbilicaris (von Salis, 1793). In the P. oceanica prairie off Lacco Ameno d'Ischia (Gulf of Naples), the species mostly co-occur in shallow stands, although G. umbilicaris dominates in summer and is generally found down to a depth of 5 m, while G. ardens is dominant in winter and is occasionally found in deeper stands (down to 30 m) (cf. Russo et al., 1984; G.F. Russo, unpublished data, 1985). According to Spada (1971), G. ardens is confined to the upper part of P. oceanica leaves, while G. umbilicaris is more widespread. Templado (1984), on the contrary, found G. umbilicaris on the foliar stratum and G. ardens at the rhizome level. The spatial arrangement of these species along the leaf axis is probably related to food availability and therefore to the colonization pattern of the micro- and macroflora that settles on the leaves (Mazzella, 1983; Novak, 1984; Casola et al., 1987). The qualitative approach used in this paper sheds some light on two aspects of the grazer-epiphyte relationship: the degree of selectivity among the microand/or macroflora exercised by the herbivores, and the impact of grazing on the whole algal community of the leaf blade. This study is a first step towards identifying and evaluating the different pathways of energy flow at low trophic levels in the herbivore food chain of a seagrass system. METHODS Gibbula umbilicaris and G. ardens specimens and plant shoots were collected at the end of May 1985 in a shallow stand (1 m depth) of the P. oceanica prairie off Lacco Ameno d'Ischia (Gulf of Naples). The specimens were placed in an aquarium and left for 5 days without food. Faecal pellets egested during this
359
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period, and therefore derived from the natural diet, were removed daily and fixed in alcohol for examination under the scanning electron microscope (SEM). To study the epiphytic colonization pattern along the leaf axes, two leaves, one old and one young, of a shoot were selected. A 1-cm long and ~ 1cm wide (depending on the width of the leaves) piece was cut out at the basal part and at each 10 cm along the leaves thereafter. The pieces so cut were fixed in alcohol for SEM examination. After the starving period, specimens of both mollusc species were placed in an aquarium containing Posidonia shoots and their spatial arrangement along the leaves was recorded. For grazing experiments old leaves, divided into three 8-cm long portions,
360 were used: (i) basal young tissue without macroscopic algal cover; (ii) intermediate tissue with primary cover formed by encrusting algae; (iii) apical old tissue with a full spectrum of epiphytes, including erect algae. Two pieces of the same type of tissue were suspended in a gauze-covered jar containing one mollusc specimen. The set of six jars (two mollusc species × three types of leaf tissue ) was replicated three times, for a total of 18 jars. All the jars were placed in an aquarium with running sea water (Fig. 1 ). Specimens were left to feed on the selected Posidonia pieces for 5 days. Faecal pellets were removed daily and fixed for SEM. On the sixth day, the leaf portions were removed from the jars and two 1-cm long segments of each piece were fixed in alcohol and both sides were examined under the SEM. RESULTS
Leaf epiphytic community Both sides of the basal part (very young tissue) of leaf blades were almost exclusively colonized by bacteria (Fig. 2A), with some rare diatoms, principally belonging to the genus Cocconeis (Fig. 2B). A few germination discs of encrusting algae (cf. Chamberlain, 1983) of the genera Fosliella and PneophyUum (Fig. 2C) were also found. This feature was observed within the first 20 cm of the ligula (the septum that separates the base from the photosynthetic tissue of the leaves ) of both the innermost (youngest) and outermost (oldest) leaves. The cover of encrusting calcareous algae (Fosliella and PneophyUum) increased with the distance from the ligula and several diatoms (mostly Coccoo neis) colonized the bare leaf surface, principally in the proximity of the edges of encrusting macrophytes (where they are probably protected from the micromovements of the water). This feature was more evident on ageing tissues (at ~ 40 cm from the base), with diatoms mainly settled among the macrophyte thalli on the available leaf surface (e.g., Cocconeis, Fig. 3A), or inserted under the edges of the crust (e.g., Fragilaria and Amphora, Fig. 3B ). On young Posidonia leaves, this pattern was the last stage observed in summer. On ageing leaves of the shoot, the encrusting algal community occupied almost the whole apical portion of the leaf surface. At this stage, a more diversified diatom flora, differing in the shape and size of the frustules (e.g., Striatella, Fragilaria, Cocconeis, Amphora, Navicula ) , had settled on the macrophyte thalli, mainly in the microcavities of calcareous algae (Fig. 3C). The macroflora colonization of the internal side of the blade differed from that of the external side. On the side less exposed to light and water movement, only a primary encrusting cover was seen, while on the other side there was a secondary erect layer growing on the primary layer. Towards the tip, the first erect structures to appear on the leaves were ascocysts and zoidocysts (vege-
Fig. 2. Colonization pattern in young tissues of P. oceanica leaves. (a) Bacttrial colonies [size bar (s.b.) = 10/xm ]; (b) diatom cells of Cocconeis scutellum Ehrenberg settled on the leaf surface (s.b. = 10 pm); (c) germination discs of encrusting red algae Fosliella and Pneophyllurn (s.b. = 0.1 mm ); (d) germination disc of Pneophyllum lejolisii (Rosanoff) Chamberlain with Cocconeis cells (s.b. = 0.1 mm ).
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Fig. 3. (a), (b) Old portion of young P. oceanica leaves. (a) Red calcareous algae surrounded by frustules of Cocconeis and Fragilaria {s.b. = 0.1 mm); (b) colonies of bacteria settled on the leaf surface and diatoms (Fragilaria) distributed along the crust edge of red calcareous algae (s.b.-- 10 pm). (c) Intermediate portion of old P. oceanica leaves: bacteria and diatoms (Cocconeis and Fragilaria ) settled on calcareous red algae (s.b. -- 10/~m).
363
Fig. 4. Old portions of P. oceanica leaves. Algal erect layer: (a) vegetative and reproductive (ascocysts and zoidocysts) filaments ofMyrionema orbiculare (s.b.=0.1 mm); (b) erect layer with the species Giraudia sphacelarioides (G) and erect filaments of M. orbiculare (M) (s.b. = 1 mm ); (c) diatoms (Nitzschia) entrapped among the erect algal filaments (s.b. = 1/tm).
Fig. 5. Grazing effect of G. ardens on different leaf portions of P. oceanica leaves. (a) Grazing traces on bacterial colonies (s.b. = 10 ttm) and (b) on germination disc of encrusting calcareous alga (s.b. -- 0.1 mm); (c) broken frustules of the diatom Cocconeis (s.b. = 10 ]~m); (d) Gibbula radular tracks on the leaf surface (s.b. = 0.1 mm ); (e) grazing traces on a calcareous alga and (f) on the "soft" M. orb iculare (s.b. = 0.1 m m ) .
366
tative and reproductive filaments) of the encrusting alga Myrionema orbiculare J. Agardh (Fig. 4A). At~60 cm from the base and on the side with the highest light exposure (usually, but not always, the external side), there was a dense growth of erect algae, mostly of Castagnea cylindrica Sauvageau, C. irregularis Sauvageau and Giraudia sphacelarioides Derb~s et Solier {Fig. 4B). Among the upright layer, the diatom flora consisted mainly of species of the genera Mastogloia and Nitzschia (Fig. 4C).
Effect of Gibbula ardens grazing On very young tissues, the grazing of G. ardens was evident from traces of removal of the bacterial colonies (Fig. 5A ) and of algal germination discs (Fig. 5B).
Fig. 6. Faecal pellet of G. ardens. (a) General structure of the faecal pellet (s.b.=0.1 mm); (b) broken frustules of diatoms included in the remaining material of the faecal pellet (s.b. = 10/~m).
Fig. 7. Grazing effect of G. umbilicaris on different tissue of P. oceanica leaves. (a) Young and intermediate leaf portions with unattached bacteria and diatoms (Fragi/aria and Cocconeis) (s.b. = 0.1 mm); (b) broken crusts of a red calcareous alga (s.b. = 0.1 mm) and (c) of M. orbiculare (s.b. =0.1 mm): (d) old part of the leaf with erect layer grazed by the mollusc (s.b. = 1 mm).
368
Fig. 8. Faecal pellet of G. umbilicaris. (a) G e n e r a l feature w i t h several u n b r o k e n d i a t o m frustules ( s.b. = 0.1 m m ); ( b ) r e m a i n s of ingested macroalgae ( s .b. = 0.1 m m ).
Leaf tissues bearing mainly diatoms and calcareous algae often showed remains of Cocconeis frustules (Fig. 5C); radular tracks, made by the teeth on the leaf surface, were also observed (Fig. 5D ). The algal crusts, represented by Fosliella and PneophyUum thalli, showed clear breaking marks where cells of epi- and even hypothallium had been removed (Fig. 5E). More often, there were broken frustules of diatoms that had been removed by the grazer from the encrusting thalli. On older tissues, where the encrusting soft alga M. orbiculare covered most of the leaf surface, its erect filaments (vegetative and reproductive) were preferentially grazed. The prostrate part of the thallus was seldom grazed. In the latter case, remains of walls of the basal cells were evident (Fig. 5F). Traces of grazing by G. ardens were negligible on the oldest tissues.
369
The faecal pellets were elongated, semicircular in transversal section, showing two ruts at the basis and a brain-like feature on the top (Fig. 6A). They were composed of an amorphous matrix of packed feeding remains, among which broken frustules of diatoms could be distinguished (Fig. 6B ). No differences in composition were observed between faecal pellets derived from a natural diet and those derived from "forced" grazing in aquaria.
Effect of Gibbula umbilicaris grazing Even without a microscope, a marked reduction of erect macroflora could be observed on Posidonia leaves grazed by G. umbilicaris. Scanning electron microscope observations showed that young leaf portions, exclusively colonized by microflora (bacteria and diatoms), were practically unaffected by grazing activity (Fig. 7A). Clear traces of grazing were observed on the primary layer that was formed of encrusting macrophytes. Calcareous FoslieUa and PneophyUum and soft Myrionema often showed traces of rasping by the mollusc; this was evident from the broken crusts and the damaged basal cells (Fig. 7B-C ). The encrusting cover had been totally removed from the leaf surface in some areas, where tracks of radular teeth could also be observed (Fig. 7D ). Diatoms living on this algal stratum remained mostly intact. On the oldest portions of the leaves, the secondary algal stratum, consisting of filaments (ascocysts and zoidocysts) of encrusting algae and erect macrophytes, were clearly reduced by grazing activity (Fig. 7E ). The faecal pellets were coarser, but similar in shape to those of the congeneric species (Fig. 8A). Among the packed feeding remains, macrophyte thalli and filaments from the upright epiphytic layer (Fig. 8B ) were easily identified. Many diatoms were present and most had intact frustules (Fig. 8A). Also in this species, there appeared to be no difference between faecal pellets derived from natural diets and those from experimental diets. DISCUSSION
The epiphytic colonization observed along the P. oceanica leaf is principally controlled by biological factors such as the growth rhythm (age) of the host plant and the life cycle of the epiphytes (Casola et al., 1987). These factors also affect microclimatic conditions, which in turn affect algal spatial arrangement. The result is a succession of vegetal epiphytic populations, from the leaf bases to the top, and a diversified micro- and macroflora. This situation is paramount in determining the spatial arrangement of herbivores, especially of creeping forms such as molluscs and, on a wider scale, in determining their presence. In fact, the occurrence of herbivorous species depends on the characteristics of the single algal species, e.g., the size, the shape and the toughness (Steneck and Watling, 1982; Russo, 1986 ), and on the struc-
370 ture of the whole community (see Hudon and Legendre, 1987, for microphytes; Lubchencko and Cubit, 1980, for macrophytes). Gibbula ardens grazes mainly on the algae characteristic of the first stage of colonization. This species removes bacteria and small adherent diatoms, mainly of the genus Cocconeis, from the bare leaf surface and from the primary encrusting layer. Large diatoms, such as Striatella spp., are left untouched. The large amount of broken diatom frustules in the faecal pellets confirms that the microphytes are the principal component of the diet of this species, although encrusting algae are also broken and presumably ingested. The secondary erect algal layer of the last successional stage is practically unaffected by the grazing activity of this species. The feeding activity of G. umbilicaris is opposite to that observed for G. ardens (Fig. 9). G. umbilicaris removes the secondary layer from the apical parts of the leaves and the faecal pellets contain the remains of the filamentous erect structures. The encrusting algae, including calcareous species, are seldom ingested, judging from the remains in the faecal pellets. Microphytes are only slightly grazed from each portion of the leaves. The presence of many intact cells of different size and shape in the faecal pellets suggests that the grazed diatoms seem to be poorly digested by the mollusc. The zonation along the leaf axes of the different food sources utilized by the two species is in agreement with the spatial arrangement of the specimens observed in aquarium, i.e., G. ardens distributed preferentially towards the base and G. umbilicaris towards the tip. These observations confirm the data reported by Templado (1984) and are in contrast with the in situ observations of Spada (1971). On a wider scale, the successional stages of the epiphytic community observed along the P. oceanica leaves differ according to season and depth (Battiato et al., 1982; Cinelli et al., 1984; Mazzella et al., 1989). The full spectrum of epiphytes was, in fact, recorded only in the shallow waters during the summer season, and was associated with the highest abundance of G. umbilicaris (Russo et al., 1984). In addition, the dominance of G. ardens in winter and its occasional presence in deeper stands of the prairie fits well with the contemporary and almost exclusive presence of the primary epiphytic covering on the leaf blades. In conclusion, G. ardens and G. umbilicaris can use a wide range of algal food (bacteria, small and large diatoms, soft and calcareous macrophytes, erect algae), although each of them feeds preferentially on organisms characterizing a different and well-defined stage (first and last, respectively) in the succession of the epiphytic community zoned along the P. oceanica leaves (Fig. 9). This difference in feeding habits explains well the species' occurrence during the year and their arrangement along the Posidonia leaves.
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zione Zoologica "Anton Dohrn" di Napoli for their invaluable help in conducting the SEM examinations; thanks are also due to the Photo- and Light Optics Laboratory. REFERENCES Battiato, A., Cinelli, F., Cormaci, M., Furnari, G. and Mazzella, L., 1982. Studio preliminare della macrofiora epifita della Posidonia oceanica (L.) Delile di una prateria di Ischia (Golfo di Napoli) (Potamogetonaceae, Helobiae). Nat. Sicil., S. IV, VI {suppl.), 1: 15-27. Casola, E., Scardi, M., Mazzella, L. and Fresi, E., 1987. Structure of the epiphytic community of Posidonia oceanica leaves in a shallow meadow. P.S.Z.N.I: Mar. Ecol., 8: 285-296. Chamberlain, Y.M., 1983. Studies in the Corallinaceae with special reference to FoslieUa and PneophyUum in the British Isles. Bull. Br. Mus. (Nat. Hist.) Bot., 11: 291-463. Cinelli, F., Cormaci, M., Furnari, G. and Mazzella, L., 1984. Epiphytic macroflora of Posidonia oceanica (L.) Delile leaves around the island of Ischia (Gulf of Naples). 1st International Workshop on Posidonia oceanica beds, C.F. Boudouresque, A. Jeudy de Grissac and J. Olivier {Editors), G.I.S. Posidonie Publ. Fr., pp. 91-99. Heijs, F.M.L., 1985. Some structural and functional aspects of the epiphytic components of four seagrass species {Cymodoceoideae) from Papua New Guinea. Aquat. Bot., 23: 225-247. Hudon, C. and Legendre, P., 1987. The ecological implications of growth forms in epibenthic diatoms. J. Phycol., 23: 434-441. Idato, E., Fresi, E. and Russo, G.F., 1983. Zonazione verticale della fauna vagile di strato foliare in una prateria di Posidonia oceanica (L.) Delile: I Molluschi. Boll. Malacol. Milano, 19: 109120. Ledoyer, M., 1962. Etude de la fauna vagile des herbiers superficiels de Zosterac~es et quelques biotopes d'algues littorales. Rec. Trav. Stn. Mar. Endoume-Marseille Fasc. Hors Ser. Suppl., 39: 117-235. Lewis, J.B. and Hollingworth, C.E., 1982. Leaf epifauna of the seagrass Thalassia testudinum. Mar. Biol., 71: 41-49. Lubchenco, J. and Cubit, J., 1980. Heteromorphic life histories of certain marine algae as adaptations to variations in herbivory. Ecology, 61: 676-687. Mazzella, L., 1983. Studies on the epiphytic diatoms of Posidonia oceanica (L.) Delile leaves. Rapp. Comm. Int. Mer M~dit., 28(3): 127-128. Mazzella, L. and Ott, J.A., 1984. Seasonal changes in some features of Posidonia oceanica (L.) Delile leaves and epiphytes at different depths. 1st International Workshop on Posidonia oceanica beds, C.F. Boudouresque, A. Jeudy de Grissac and J. Olivier (Editors), G.I.S. Posidonie Publ. Fr., 1: 119-127. Mazzella, L., Wittmann, K.J. and Fresi, E., 1982. La comunit~ epifita e suo ruolo nella dinamica dell'Ecosistema Posidonia. Atti del Convegno delle U.O. Sottoprogetti Risorse Biologiche ed Inquinamento Marino, Roma, November 1981, pp. 215-224. Mazzella, L., Scipione, M.B. and Buia, M.C., 1989. Spatio-temporal distribution of algal and animal communities in a Posidonia oceanica (L.) Delile meadow. P.S.Z.N.I: Mar. Ecol., 10: 107131. Novak, R., 1984. A study in ultra-ecology: Microorganisms on the seagrass Posidonia oceanica (L.) Delile. P.S.Z.N.I.: Mar. Ecol., 5: 143-190. Orth, R.J. and van Montfrans, J., 1984. Epiphyte-seagrass relationship with an emphasis on the role of micrograzing: a review. Aquat. Bot., 18: 43-69. Ott, J.A. and Maurer, L., 1977. Strategies of energy transfer from marine macrophytes to consumer level: the Posidonia oceanica example. In: B.F. Keegan, P.O. Ceidigh and P.J.S. Boaden (Editors) ,Biology of Benthic Organisms, Pergamon Press, Oxford. pp. 493-502.
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Penhale, P., 1977. Macrophyte-epiphyte biomass and productivity in an eelgrass (Zostera marina) community. J. Exp. Mar. Biol. Ecol., 26: 211-224. Russo, G.F., 1986. Evoluzione ed adattamenti trofici nei Prosobranchi: spunti per una analisi funzionale del popolamento malacologico di una prateria a Posidonia oceanica dell'isola d'Ischia. Nova Thalassia, 8 (Suppl. 3 ): 643-644. Russo, G.F., Fresi, E., Vinci, D. and Chessa, L.A., 1983-84. Malacofauna di strato foliare delle praterie di Posidonia oceanica (L.) Delile intorno all'isola d'Ischia (Golfo di Napoli): analisi strutturale del popolamento estivo in rapporto alia profondith ed alla esposizione. Nova Thalassia, 6: 655-661. Russo, G.F., Fresi, E., Vinci, D. and Chessa, L.A., 1984. Mollusks syntaxon of foliar stratum along a depth gradient in a Posidonia oceanica (L.) Delile meadow: seasonal variability. 1st International Workshop on Posidonia oceanica Beds. C.F. Boudouresque, A. Jeudy de Grissac and J. Olivier (Editors), G.I.S. Posidonie Publ., Fr., 1: 311-318. Russo, G.F., Fresi, E., Buia, M.C. and Vinci, D., 1985. Malacofauna delle praterie a Posidonia oceanica (L.) Delile della zona di Capo Passero (Sicilia Sud-orientale): analisi comparativa con i popolamenti dell'isola d'Ischia. Oebalia, 11NS:319-324. Scipione, M.B., 1989. Comportamento trofico dei Crostacei Anfipodi in alcuni sistemi bentonici costieri. Atti XIX congresso della Scieth Italiana di Biologia Marina, Oebalia. Scipione, M.B. and Fresi, E., 1984. Distribution of Amphipod Crustaceans in Posidonia oceanica (L.) Delile foliar stratum. 1st International Workshop on Posidonia oceanica Beds. C.F. Boudouresque, A. Jeudy de Grissac and J. Olivier (Editors), GIS Posidonie publ., Fr., 1: 319-329. Spada, G., 1971. Contributo aUa conoscenza della malacofauna della biocenosi a Posidonia oceanica (L.) lungo le coste italiane. Conchiglie, Milano, 8 (9-10 ): 125-135. Steneck, R.S. and Watling, L., 1982. Feeding capabilities and limitation of herbivore molluscs: a functional group approach. Mar. Biol., 68: 299-319. Templado, J., 1984. Moluscos de las praderas de Posidonia oceanica en las costas del cabo de Palos (Murcia). Invest. Pesq., 48: 509-526. Vadas, R.L., 1985. Herbivory: In: M.M. Littler and D.S. Littler (Editors), Handbook of Phycological Methods: Ecological Field Methods. Macroalgae. Cambridge University Press, Cambridge, pp. 532-572. Van Montfrans, J., Orth, R.J. and Vay, S.A., 1982. Preliminary studies of grazing by Bittium uarium on eelgrass periphyton. Aquat. Bot., 14: 75-89. Van der Ben, D., 1971. Les ~piphytes des feuilles de Posidonia oceanica Delile sur les cotes franqaises de la M6diterrande. Mem. Inst. R. Sci. Belg., 168: 1-101. Velimirov, B., Ott, J.A. and Novak, R., 1981. Microorganisms on macrophyte debris : biodegradation and its implication in the food web. Kiel. Meeresforsch., 5: 33-334.