This article was downloaded by: [Mount Allison University 0Libraries] On: 16 April 2013, At: 20:29 Publisher: Taylor & Francis Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK Ophelia Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/smar19 Feeding ecology of platynereis dumerilii (audouin & milne-edwards) in the seagrass posidonia oceanica system: The role of the epiphytic flora (Polychaeta, nereididae) Maria Cristina Gambi a b , Valerio Zupo a , Maria Cristina Buia a & Lucia Mazzella † a a Stazione Zoologica “A. Dohrn” di Napoli, Laboratorio di Ecologia del Benthos, Punta S. Pietro, Ischia, Napoli, Italy b Italy Phone: +39 81 5833513 Fax: +39 81 5833513 E-mail: Version of record first published: 19 Dec 2011. To cite this article: Maria Cristina Gambi , Valerio Zupo , Maria Cristina Buia & Lucia Mazzella † (2000): Feeding ecology of platynereis dumerilii (audouin & milne-edwards) in the seagrass posidonia oceanica system: The role of the epiphytic flora (Polychaeta, nereididae), Ophelia, 53:3, 189-202 To link to this article: http://dx.doi.org/10.1080/00785326.2000.10409449 PLEASE SCROLL DOWN FOR ARTICLE Full terms and conditions of use: http://www.tandfonline.com/page/terms-and-conditions This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. The publisher does not give any warranty express or implied or make any representation that the contents will be complete or accurate or up to date. The accuracy of any instructions, formulae, and drug doses should be independently verified with primary sources. The publisher shall not be liable for any loss, actions, claims, proceedings, demand, or costs or damages whatsoever or howsoever caused arising directly or indirectly in connection with or arising out of the use of this material.
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This article was downloaded by: [Mount Allison University 0Libraries]On: 16 April 2013, At: 20:29Publisher: Taylor & FrancisInforma Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House,37-41 Mortimer Street, London W1T 3JH, UK
OpheliaPublication details, including instructions for authors and subscription information:http://www.tandfonline.com/loi/smar19
Feeding ecology of platynereis dumerilii (audouin &milne-edwards) in the seagrass posidonia oceanicasystem: The role of the epiphytic flora (Polychaeta,nereididae)Maria Cristina Gambi a b , Valerio Zupo a , Maria Cristina Buia a & Lucia Mazzella† aa Stazione Zoologica “A. Dohrn” di Napoli, Laboratorio di Ecologia del Benthos, Punta S.Pietro, Ischia, Napoli, Italyb Italy Phone: +39 81 5833513 Fax: +39 81 5833513 E-mail:Version of record first published: 19 Dec 2011.
To cite this article: Maria Cristina Gambi , Valerio Zupo , Maria Cristina Buia & Lucia Mazzella† (2000): Feeding ecology ofplatynereis dumerilii (audouin & milne-edwards) in the seagrass posidonia oceanica system: The role of the epiphytic flora(Polychaeta, nereididae), Ophelia, 53:3, 189-202
To link to this article: http://dx.doi.org/10.1080/00785326.2000.10409449
PLEASE SCROLL DOWN FOR ARTICLE
Full terms and conditions of use: http://www.tandfonline.com/page/terms-and-conditions
This article may be used for research, teaching, and private study purposes. Any substantial or systematicreproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form toanyone is expressly forbidden.
The publisher does not give any warranty express or implied or make any representation that the contentswill be complete or accurate or up to date. The accuracy of any instructions, formulae, and drug doses shouldbe independently verified with primary sources. The publisher shall not be liable for any loss, actions, claims,proceedings, demand, or costs or damages whatsoever or howsoever caused arising directly or indirectly inconnection with or arising out of the use of this material.
ABSTRACT The feeding ecology and the ecological role of the herbivorous polychaete Plo.tynereis dwne'lilii (Audouin & Milne-Edwards) (Nereididae) in the epiphytic community of the Mediterranean seagrass ·Posidonia oceanica (L.) Delile was investigated under natural and laboratory conditions. Experiments were devised to define the preferred items, their consumption rate and degree of assimilation of chlorophylls. Results of faecal pellets analyses, food-choice experiments and photosynthetic pigment analyses demonstrated that P. dllmmlii feeds preferentially on erect filamentous algae. Worms of length above 10 mm may graze also on living tissue of Posidonia leaves, when starved. This behaviour has rarely been reported for invertebrates, and especially for polychaetes in Posidonia ecosystems. Small individuals had a lower feeding rate on large macroalgae (e.g., Cystosei-ra), but higher digestive efficiency. Platynereis dllmmlii thus feeds preferentially on erect micro- and macroalgae which are more easily cut by the jaws of its eversible pharynx. This selective herbivore thus has a special microniche, with respect to other mesograzers inhabiting the Posidonia meadows.
Mesograzers are defined as small-sized herbivores living in the seaweeds on which they feed (Hay et al. 1988). They are abundant in macroalgal communities on hard bottoms (Brawley 1992) and on the canopies of marine phanerogams (Hutchings 1982; Scipione et al. 1996), and play an important role in the food
webs of these systems as links to the highest trophic levels (Hawkins et al. 1992; Orth & van Montfrans 1984). Habitat selection and feeding preferences of mesograzers coincide, and represent a compromise between the structural complexity of the plants (algae or seagrasses), selected respect to size and crypsis potential, and plant toughness and palatability, which is related to their morpho-functional features and energy require men ts (Brawley 1992) . Mesograzers play a minor role in the direct consumption of seagrass living tissues. However, they are important consumers of the algal epiphytic community on the leaves and of detritus entrapped in the periphyton (Orth & van Montfrans 1984; Mazzella & Zupo 1995). Furthermore, the epiphytic algal forms show a variety of morpho-functional guilds (Littler & Littler 1980; Hudon & Legendre 1987), which have implications for their availability as potential food for invertebrate grazers (Steneck & Watling 1982; Mazzella et al. 1994).
The leaves of the Mediterranean seagrass Posidonia oceanica (L.) Delile support a highly diversified and complex plant-epiphytic community, exhibiting typical successional stages, with the maximum diversity and biomass in summer, mainly in shallow water stands (Mazzella et al. 1989, 1994; Buia 1989). Most of this production is transferred to secondary consumers through the grazing pathway, due to mesograzers (Mazzella et al. 1992; Mazzella & Zupo 1995) mainly represented by molluscs, and crustaceans (Scipione et al. 1996). The
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Fig. 1. A, a typical early colonization phase of the plant epiphytic community on a Posidonia oceanica leaf characterized by prostrate diatoms of the genus Cocconeis, and a young specimen of Fosliella/Pneophyllum (scale bar; 0.1 mm). B, a specimen of the epiphytic erect alga Sphace-
laria sp. on a Posidonia leaf (s.b.; I mm).
role of the epiphytic flora of P oceanica in the feeding ecology of mesograzers has been studied for some species of gastropod molluscs (Mazzella & Russo 1989), amphipod (Scipione & Mazzella 1992) and decapod crustaceans (Zupo 1994) .
The polychaete Platynereis dumerilii (Audouin & Milne-Edwards) (Nereididae) represents a typical mesograzer, commonly associated with seaweeds, mainly brown algae, from shallow hard bottoms (Bedford & Moore 1985; Giangrande 1988). It is also very common in seagrass meadows, such as Posidonia, Zostera and Cymodocea (Lanera & Gambi 1993; Gambi et al. 1995) in the Mediterranean Sea. A study on polychaete distribution in a P oceanica bed off the Island of Ischia (Gulf of Naples), revealed that P dumerilii is frequent in shallow water (1-5 m) during late spring and summer (Gambi et al. 1992; Gambi & Lanera 1992), mainly represented by relatively small or juvenile specimens
(Gambi, pers. observ.). P dwnerilii is semelparous, reproducing in late summer by epitoky and possessing a pelagic stage with a planktotrophic larva (Pfannenstiel et al. 1987; Grant 1989; Giangrande 1989). Worms live inside semi-permanent mucous tubes, that are generally attached to macroalgal thalli (Bedford & Moore 1985). Like congeneric species, P dumerilii generally feeds close to the tube entrance, to which worms attach small pieces of algae. Such typical behaviour is known as "algal gardening" (Casanova & Coulon-Roso 1967; Woodin 1977; Cram & Evans 1980; Branch et al. 1992).
Aspects of the trophic behaviour and ecology of P dumerilii have been studied under laboratory conditions (Cram & Evans 1980; Evans & Downie 1986; Gambi & Di Meglio 1996). However, data on this species from both seaweeds (Bedford & Moore 1985) and seagrass meadows Qacob & Pierson 1979) are limited, and are lacking as far as P oceanica beds are concerned. This research, which is part of a wider project aimed at a better definition of the grazing pathways involved in energy transfer through the Posidonia system, is focused on the feeding ecology of P dllrnerilii in Posidonia meadows. The aims are to characterize the natural diet of this species, evaluate its faecal pellet production and assimilation efficiency, as well as to discuss the adaptive significance and the ecological implications of its trophic behaviour.
RESULTS
Posidonia epiphytic comm1Lnity
The plant epiphytic community on the Posidonia leaves offered was characterized by two main morpho-functional groups of species: encrusting and erect algal forms. The encrusting assemblage was characterized by the dominance of both diatoms (mainly of the genus Cocconeis) , and encrusting coralline algae of the Fosliella/ Pneophyllw1! spp. group (Fig. lA) (coverage between 25 and 90%) and Myrionema orbietLlare (coverage between 1 and 60%). The coverage of the encrusting species, before exposure to worm grazing, varied between 32 and 100% with a mean of 64.6±17 .3% (N = 24) on the upper leaf side, while the lower leaf side had lower values, ranging from 11 to 80% with a mean of 36.6±16.8% (N = 24).
The erect epiphytic community was characterized by a complex association of micro- and macro algae , representing the mature stage of
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FEEDING ECOLOGY OF P. DUMERlUI IN POSIDONIA ECOSYSTEM 191
Table 1: List of the plant epiphytes identified in the Posidonia oceanica leaves, and in the fecal pellets of the polychaete Platynereis dumlffilii in natural diet and laboratory grazing conditions.
Other items broken frustules of diatoms filamentous algae (unident. remains) Coralline algae (unident. remains) Posidonia oceanica (L.) Delile (fragments) Coccolitophorids Spores (unidentified) Amorphous material Mucous
+ ~ presence; - ~ absence.
Posidonia leaves
+ + + + + + + + + + + + + + + + + + + + +
+ + + + + + + + + + + + + + + + + + +
+ +
P. dumerilii faecal pellets (natural diet on Posidonia)
+ +
+
+ + +
+ + +
+
+ + +
+ +
P. dumerilii faecal pellets (laboratory
grazing)
+
+ + + + + + + + + + +
+
+ + +
+
+ + +
+
+ + +
+ +
+ + + +
+ + +
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Fig. 2. A, S.E.M. micrograph of a typical faecal pellet of Plat)>nere-is d-urnerilii under natural diet (Posidonia meadow)· conditions. B, S.E.M. micrograph of a typical faecal pellet of P. dumerilii in laboratory feeding conditions (erect epiphytes); note the presence of the thin, mucous film (peri trophic membrane) enveloping the faecal material. C and D, S.E.M. micrographs of items found in faecal pellet material of Platynerei.s dumerilii under natural diet (PosidDnia meadow) conditions: C, frustules of VariOllS species of benthic diatoms; D, fragment of a
coralline alga; (s. b. of all micrographs: 0.1 mm)
Fig. 3. S.E.M. micrographs showing the traces of grazing of Plalynerei.s dumerilii on epiphytes of Posidonia leaves under laboratory feeding conditions. A and B, traces of grazing on coralline algae (Fosliella/Pneophyllum) ; C, traces of grazing on erect filamen taus algae (Spha celaria sp.); D, traces of grazing on Posidonia living leaf tissue. Note the 'half-moon' shape of the bite marks; (s.b. of all
micrographs= 0.1 mm) .
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FEEDING ECOLOGY OF P. DUlVIERILII IN POSIDONIA ECOSYSTEM 193
Fig. 4. Stereo microscope picture showing the grazing of a large specimen of P. dllmerilii on the edge of a Posidonia leaf, characterized by an encrusting epiphytic community. Note the 'half-moon' shape of the bites (arrows).
the Posidonia epiphytic assemblage (Mazzella et al. 1989; 1994). Among the diatoms, besides the genus Cocconeis, which dominates with several species, the genera Amphora, Gmmmatophora and Synedra were also frequent. The macro algae were dominated by erect filamentous forms, mainly brown algae, such as Sphacelaria ciTTosa (Fig. IB) (coverage between 6 and 65%) and A-udovinella daviesii (coverage between 3 and 10%), but the encrusting corallinaceous forms were also quite abundant, especially Fosliella/Pneoph."lllum with coverage ranging from 5 to 80%. The coverage of erect and encrusting epiphytes on the upper side of leaf blades, before feeding by the worms, varied between 35 and 100% with a mean of 68.6±23.6.0% (N =
11), while lower and more variable values were observed on the lower leaf side, ranging from 15 to 70% with a mean of30.1±16.1 % (N = 10).
A complete list of the plant taxa found as epiphytes on the Posidonia leaves is given in Table 1.
Faecal pellet analyses
Faecal pellets collected under natural conditions and in laboratory experiments were quite irregular in size. They were cylindrical in shape, with a compact consistency (Fig. 2A) . Most of the pellets were covered by a thin, mucous film (Fig. 2B) that constitutes the per-
itrophic membrane, as observed in other polychaetes (Fretter & Graham 1976).
Only a few faecal pellets were produced immediately after collection of worms in the Posidonia bed (natural diet), as most of the worms had empty guts. The pellets contained a variety of plant items (Table 1): mostly diatoms and coralline algae (Fig. 2C and 2D). However, small fragments of both macro algae and Posidonia leaves were also frequently observed in the pellets of worms of different sizes. The most abundan t genera of epiphytic diatoms found in the faecal pellets were Synedra, Rhabdone-ma, Lychmophora, Navicula, Grammatophora, Amphora, Diploneis. Some of these taxa are free living on the leaf surface (e.g., Amphora, Navicula, Synedra), or are colonial species (e.g., Lychmophora) which can be easily detached by the grazing activity of the worm or can be ingested with other epiphytized items.
The analysis of faecal pellets deriving from grazing under laboratory conditions revealed a larger variety of plant items (Table 1), dominated by macroalgal tissues, regardless of worm size. The analysis of the pieces of Posidonia grazed by worms revealed no significant differences in epiphyte composition and coverage with respect to the ungrazed controls, both for the upper (t= 0.279, p = 0.79) and the lower (t= 0.099, p= 0.92) leaf sides. This pattern was con-
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Table 2A. Sequential analysis of the binary food choice experiments lasting 24 hours (12 in light and 12 in dark conditions).
Table 2B. Sequential analysis of the binary food choice experiments under 12 hours of continuous dark or light conditions.
tested items Dark Light conditions conditions
Posidonia erect epiph. Posidonia encrusting epiph. s. s. Posidonia erect epiph. Dictyota dichotoma n.s. n.s. Posidonia erect epiph. Stypocaulon scapariurl! n.s. n.s. Posidania erect epiph. Cystoseim crinita n.s. n.s. Ulva rigida Dietyota diehotoma n.s. s. Die/yota diehotoma Cystoseim crinita n.s. n.s. Ulva rigida Cystoseim Clinita s. s. Cowllina elongala (5) Posidonia encrusting epiph. s. n.s.
s.= significant at 95% n.s.= not significant at 95% The plant items significantly preferred are those on the left column
firmed also when single items (e.g., Sphacelaria cirrosa) were considered separately. The mean epiphyte coverage of grazed leaves ranged between 40 and 100% (mean 71.1±18.0%), and between 15 and 80% (mean= 30.9±19.8%) in the lower leaf side. The grazed leaves showed, however, clear feeding marks on both encrusting (Fig. 3A and 3B) and erect filamentous macro algae (Fig. 3C), as well as on Posidonia living tissues (Fig. 3D and Fig. 4). These marks had often a typical half-moon shape (Fig. 4), and those on Posidonia tissues were limited to samples grazed by larger worms (size 3 category, >15 mm length). The fluorescence microscopy analysis revealed traces of undigested chlorophylls in the faecal pellets produced.
macroalgae) tested during the experiments belonged to five different morpho-functional guilds (Table 2). The results of the statistical tests for each food choice experiment are reported in Table 2A (p=0.95; 24 hours experiments) and Table 2B (p= 0.95; 12 hours experiments in continuous light or dark conditions).
In all the experiments, no significant different effect of worm size on food choice was detected. In both sets of experiments, Posidonia with erect epiphytes was preferred significantly to Posidonia with encrusting epiphytes or without epiphytes (Table 2A; Fig. 5). The food choice experiments showed that Posidonia with erect epiphytes was preferred only over Stypocattlon scoparittm, but not over Dictyota, Cystoseira or Wva thalli. Posidonia leaves without epiphytes, or with coralline encrusting algae were only preferred when less attractive items,
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FEEDING ECOLOGY OF P. DUMERILII IN POSIDONIA ECOSYSTEM 195
IZZZl Cystoseira :-g > 60 ... gardening '6 c ~tube
~ 0 40 N=50
20
0
3 2 3 2
Size category
Fig. 5. Two examples of binary food choice experiments under 12 hours of continuous dark or light conditions: A, erect vs encrusting epiphytes; B, erect epiphytes vs Cystoseira. Note the "gardening" behaviour occurring, in both
choice experiments, only during dark conditions. 'lube" ~ specimens remain inside their tubes, no food choice.
such as macro algae characterized by high toughness (Caulerpa prolifera or Stypocaulon seaparium), were offered (Table 2).
When Posidonia leaves with encrusting epiphytes or without epiphytes were offered, relatively large portions of living Posidonia leaf tissues were occasionally eaten, especially along the cut edges of the leaf (Fig. 4). This behaviour was observed in some larger P dumerilii (> 10 mm length). The grazed leaves showed very dearly the bite marks with typical 'halfmoon'shape (Fig. 4).
Comparisons between the experiments under continuous light or dark conditions revealed a high consistency of the food choices
with the previous 24 hours experiments. During light condition experiments a dear tendency for the specimens to remain inside their tubes was observed, regardless of the worm's size (Fig. 5). Under light conditions, the 'gardening" behaviour was almost absent, while it was recorded in about 5% of the specimens during dark experiments. The 'gardening" behaviour of P dumerilii occurred with many different algal forms and also with epiphytized Posidonia leaves. This behaviour was also correlated to the size of individuals, being more frequent in specimens of size categories 3 and 2 (Fig. 5).
Fig. 6. Daily production of faecal pellets of Platynerei.s dumerilii fed on different plant foods, as a function of worm size. CollUnns represent means, bars represent standard deviations of 5 specimens for each size category.
Faecal pellet production and pigment analysis
Mean daily production of faecal pellets by individuals, under different dietary regimes across the three considered sizes, indicated that plant consumption was related to both worm size and food type. Erect epiphytic algae generated highest faecal pellet output, along with Cystaseira and encrusting algae (Fig. 6). Size 1 worms showed such high variability that the differences in consumption of various items were not significant. Size 2 worms showed a well de-
fined pattern of feeding activity, with faecal pellet production about twice as high with erect epiphytes as with encrusting ones. Cystoseira, however, was preferred to erect epiphytes, at least during the first two days of the experiment. Size 3 worms also showed a similar trend, except for Cystoseira at 1 st day (Fig. 6).
Pigment contents (chlorophyll a, band c and phaeopigments) of the faecal pellets which derived from various treatments showed no significant differences among worm sizes (p>O.05), or among the days of the experiment (p>O.05).
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FEEDING ECOLOGY OF P DWVIERIllI IN POSIDONIA ECOSYSTEM 197
Table 3. Values of the pigment contents (pm pigm./mg faecal pellet cP) in the faecal pellets of Platynereis dwnerilii of different size categories and under different treatments.
Fig. 7. Percentages of the undigested chlorophyll a (A) and of chlorophyll c (B) content in the faecal pellets of Plalynereis dumerilii, according to worm size and experimental treatments.
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Therefore, the results of the 4-day treatments were grouped to obtain an average production allowing comparisons of different plant items and worm sizes (Table 3). Size 1 worms generally exhibited lower pigment contents per weight units of faecal pellets. Chlorophyll a content was consistently higher in individuals feeding on erect algae, followed by the Cystaseim treatment. Chlorophyll b showed very low values in faecal pellets, testifying that Posidonia tissues were scarcely represented in the diet. Chlorophyll c was detectable only in the treatment with erect algae, where the component of brown algae was dominant, while it was not detectable in the treatment with encrusting algae. In this latter, in fact, Corallinaceae dominated and the diatom component was too low to be measured by spectophotometry. Chlorophyll c was relatively high in Cystoseim treatment from small-sized worms. As regards to phaeopigments, faecal pellets of small-sized worms fed on erect algae contained lower amount of phaeopigments than larger worms (Table 3). Small individuals fed on Cystoseim, however, produced higher amounts of phaeopigrnents than larger worms. The highest amounts of phaeopigments were produced by individuals of sizes 2 and 3 fed on erect algae (Table 3).
Values of the undigested chlorophyll a were higher for the erect algae treatment and lower for the encrusting one, regardless of worm size (Fig. 7A). Smaller worms produced faecal pellets with lower chlorophyll a values, indicating a higher digestive efficiency, compared witl1 larger worms. A similar picture was revealed by the undigested chlorophyll c values (Fig. 7B), although in this case small worms showed higher ·values. On the whole, values of undigested chlorophylls, for the erect algae treatments, ranged between 40 and 60% (indicating a digestion efficiency between 60-40%), while for the Cystoseira treatment the undigested values were more variable, ranging between 85 and 15%, and for the encrusting algae between 15 and 5% (Fig. 7). These results indicate high efficiency of digestion. However, the data regarding encrusting algae, may be biased by low consumption rates.
DISCUSSION
Present observations on feeding behaviour and food choice of P. dumerilii confirm the typical mesograzer habit of the species. The erect Posidonia epiphytes, which were dominated in our experiments by brown, branched algae of the
genus Sphacelaria, have a relatively high structural complexity, and they appear more palatable than the encrusting coralline algae or the Posidonia leaf tissues. The present work demonstrates that P. dumerilii, when grazing, prefers erect epiphytes (both micro- and macro algae) . This pattern may be related to the morphology of the feeding apparatus of P. dumerilii. The species, in fact, has an reversible pharynx armed with a pairs of jaws (Fauchald & Jumars 1979) that are more suitable for cutting, rather than for scraping encrusting materials. To this respect P. dumerilii has a distinctive role from other mesograzers. A previous study dealing with feeding ecology of mollusc gastropods of the genus Gibbula on P. oceanica meadows showed that these animals prefer the encrusting algal component of the epiphytic community (Mazzella & Russo 1989), which is more easily removed by their radular apparatus. A similar research on crustacean amphipods, pointed out their preference for various morpho-functional forms of epiphytic diatoms, scraped by the action of their antennae (Scipione & Mazzella 1992). Therefore, P. dumerilii and the other mesograzers studied seem to exploit different components of the epiphytic community, according to their morphological features and sizes, thus increasing their microniche differentiation and reducing competition for food ",>jth other grazers.
It is worthwhile to stress the capability of larger P. dumerilii (> 10 mm length) to feed on living Posidonia leaf tissues, even though this behaviour occurred only when worms were forced to graze upon less attractive plant items, such as the coralline algae. This peculiar behaviour is consistent with the observation ofJacob & Pierson (1979) on P. dumerilii living inside the flower spathes of the seagrass Zostera marina. Therefore, P. dumerilii appears to be one of the few species of invertebrates able to graze directly on living Posidonia tissues. Seagrass tissues, in fact, are rarely consumed by direct grazers, due to the fact that they are particularly tough and unpalatable for their high content of structural carbohydrates (mainly lignin) (Mazzella et al. 1992), and for the presence of anti-grazing compounds (Cariello & Zanetti 1979). A few other polychaete species, belonging to the Eunicidae, borers into Posidania scales (bases of old leaves persisting along the rhizome) (Cuidetti et al. 1997) have been documented as being capable of grazing on living Posidonia tissues in natural conditions (Cambi et al. 2000). Finally, the typical 'half-
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FEEDING ECOLOGY OF P. DUMERIIJI IN POSIDONIA ECOSYSTEM 199
moon' shaped bite marks of P dumerilii have also been observed by Bedford & Moore (1985) on the thalli of brown algae of the genus Laminana, and are still related with the shape and function of the jaws
Under light conditions individuals of P dumerilii are less active, and remain generally inside their tubes. Like in other Nereididae, also in P dumerilii feeding requires the partial or total exit of the worm from the tube (Cram & Evans 1980). During such searching for food, the worms are more vulnerable to potential predators. The "gardening" behaviour has been considered to be an adaptation to reduce the risks of predation (Woodin 1977). The prolonged occurrence of P dumerilii inside the tubes, and the avoidance of "gardening" during light conditions may therefore be explained as an anti-predatory behaviour, as also hypothesized for other species of Nereididae (Roe 1975). These results suggest that, also in the field, P dumerilii could forage more actively at night.
Faecal pellet production, for larger worms (size categories 2 and 3), is higher for specimens fed on erect algae than for worms feeding on encrusting algae. Only small individuals (size 1) seemed to have comparable faecal pellet production when feeding on different plant items, with micro algae as a constant component of their diet. Diatoms seem to be fed as a whole with the macro algae they epiphytize. However, a selective choice, especially in the case of small individuals, must be taken into account, when we consider that the species assemblage, identified in the faecal pellets, is different from that found on Posidonia leaves, being colonial forms not tightly attached to the substrate (Lychmophora, Navicula) more ab1.mdant than prostrate ones (e.g., Cocconeis spp.), which are dominant on the leaves.
Platynereis dwnerilii seems therefore capable of utilizing any plant material which is easy to cut by means of its pharyngeal jaws. A selection is made mainly on less corticated macroalgae. The consumption of plant material is function of worm size. It increases in larger worms, which can consume larger items, that are probably unaccessible for small specimens. Small individuals shifted their diet to microphytes, when forced to graze on tough materials. However, in spite of their lower rate of feeding, small-sized worms showed a higher digestive efficiency, demonstrated by the lower percentages of undigested chlorophyll a.
The feeding pattern of P dumerilii in P ocean-
ica meadows seems to be limited more by the anatomy of its feeding apparatus rather than by the quality of available food. In fact, the large variety of plant items ingested suggests a certain degree of fceding adaptability, especially in large individuals. This species is able to use all the plant materials present on the Posidonia leaves, but erect epiphytes are preferred to all the other items. Posidonia tissues are scarcely utilized and small individuals feed mainly on microalgae, finding other plant materials difficult to cut.
The pattern of occurrence of P dumerilii in Posidonia meadows, with higher abundances on the leaf stratum and during the summer season, is consistent with the pattern of epiphyte production, which reach the highest development in summer, especially in shallow water (Mazzella et al. 1989). A similar pattern of cooccurrence has been observed in Posidonia for another mesograzer, the decapod Hippolyte inermis, for which a clear relationship between epiphyte availability, and shrimp diet and life cycle was evidentiated (Zupo, 1994).
The data on P dumerilii, as well as those of the other mesograzers studied, demonstrate once more the link between the structural diversity offered by plant epiphytes of the P oceanica ecosystem, and the functional diversity of its associate invertebrates.
MATERIAL AND METHODS
Specimens of P dumerilii were collected by SCUBA diving at Castello Aragonese (Island of Ischia, Gulf of Naples), along a shallow rocky shore (0-3 m depth), characterized by an algal community dominated by brown (Cystoseira crinita Duby and Stypocaulon scopanum (L.) Ki.i.tzing), and by green (Cladophora sp.) algae, and in a nearby shallow P oceanica meadow. In the hard bottom worms were sampled by collecting and shaking the algae; while in the Posidonia meadow worms were sampled from the leaf stratum by means of a hand-towed net (Russo et al. 1985), and also by collection of Posidonia shoots and visual analysis of the leaf blades. All samples were collected during late morning hours, so the possibility of a day-cycle in the feeding, and therefore in the gut fullness, of the worms was not tested. Specimens of P dumerilii sampled were separated into three size categories, based on their body length: viz. size 1 «9 mm); size 2 (9-15 mm); size 3 (>15 mm). Worms were reared in Petri dishes and kept at a constant temperature of 19°C. Water
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in Petri dishes was renewed daily using filtered and aerated seawater. In order to avoid intraspecific aggressive behaviour, common in nereidpolychaetes (Reish & Alosi 1968), all the experiments were done on isolated individuals. All the worms used for our experiments were in the atokous stage (no mature gametes). Various experiments were devised:
Identification of natural diet (Posidonia meadow)
Specimens of P dumerilii collected in the shallow P oceanica meadow were immediately isolated in Petri dishes after collection and were observed every hours until faecal pellets were produced. The faecal pellets were immediately removed and analysed at the microscope in order to identify the items ingested in natural conditions. Matelial was also fixed for the scanning electron microscopy (S.E.M.) analysis in order to identify the diatoms; faecal pellets were dehydrated in ethanol, critical-point dried with CO2 and coated with carbon and gold before observation with a Philips 505 instrument.
Effects of grazing on the epiphytic community
Small pieces of Posidonia leaves (1 cm length), epiphytized by encrusting or erect algae, were offered to worms that have been starved for two days. The pieces of Posidonia leaves used in the feeding experiments were examined before grazing initiated in order to identify the major algal epiphytes and determine their percent of coverage. The same pieces were examined again for traces of grazing activity, after 2 days of worm feeding, to detect changes in composition and coverage of epiphytes. In all the analyses, both sides of each leaf (upper and lower) were examined separately, as the epiphytic community differs between the two leaf sides (Casola et aL 1987). The Student's test was performed to evaluate statistical difference in coverage data before and after the grazing experiments. The feeding experiments were performed on worms of different sizes reared in a thermostatic chamber at 19°C and with a day length of 12 hours. Faecal pellets were removed daily and divided into sub-samples used for observation by optical microscopy, fluorescence microscopy, or fixed and processed for S.E.M. as illustrated above.
Food choice experiments
These experiments were done utilizing various
species of macroalgae and differently epiphytized Posidonia leaves. The tested macroalgae were Cystoseim crinita Duby, Dictyota dichotoma (Hudson) Lamouroux, Ulva rigida C. Agardh, Stypocaulon scoparium (L) Ki.itzing, Flabellia petiolata (Turra) Nizamuddin, Caulerpa prolifera (Forsskal) Lamouroux and Co-rallina elongata Ellis & Solander. The first set of experiments lasted 24 hours, with a light-dark cycle of 12 hours. The animals were checked at 2, 4, 6, 12 and 24 hours intervals, by recording their position inside the offered plant items, and the occurrence of the "gardening" behaviour, characterized by the presence of the worm in one of the items and the attachment of the other item at the tube.
The second set of experiments was done to study the behavioural differences between light and dark conditions. A binary food choice experiment was tested after 12 hours of continuous light, and then after a period of starvation of 1 day, the same food choice was tested after 12 hours of continuous dark conditions. In each experiment, pieces of the various plant items (ca. 1 cm long) were offered in binary choices to P dumerilii individuals; smaller pieces of the same items (ca. 0.5 cm long) were offered to small worms (size 1 category). The items were placed at equal distances from each worm, that was generally inside its mucous tube. Different combinations of binary food choices were performed with the selected plant items, for a total of30 experiments, 14 of which lasted 24 hours, and 16 lasted 12 hours under continuous light (8) or dark (8) conditions. Each binary choice experiment was done on about 50 individuals, in a single triaL The results of all binary food choice experiments were tested using the graphical method of the Sequential Analysis (Lison 1961).
Faecal pellet production and digestion efficiency
Based on the results of the previous qualitative observations, quantitative evaluation of the amount of material ingested, the weight of faecal pellets produced and the efficiency of digestion were restricted to the preferred plant items. Each experiment lasted 4 days. Five worms of each size category were reared individually in Petri dishes filled with filtered sea water containing a small portion of the plant items under test. Faecal pellets were removed daily using a Pasteur pipette under a dissection microscope, ·and the water renewed. The faecal
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FEEDING ECOLOGY OF P DUlvIERlL1I IN POSIDONIA ECOSYSTEM 201
pellets produced by individuals belonging to the same size group were pooled, and blotted with filter paper. Five ml 90% buffered acetone solution was added, and samples stored at about sac. Finally, the solutions were centrifuged, faecal pellets were removed, washed in distilled water, dried (soac, 24 hours) and weighed, in order to assess the amount of material egested throughout the experiment.
The chlorophyll a, band c contents in the supernatant was analysed by spectrophotometry, and evaluated by spectrophotometric equations Qeffrey & Humphrey 1975). When the absorbance was too low to be detected by spectrophotometry, the solution was analysed using a fluorometer, in order only to estimate the content of chlorophyll a (Lorenzen 1967). The solution was then acidified, adding two drops of 50% hydrochloric acid (HCl), and re-analysecl, in order to calculate the content in phaeopigments according to Lorenzen (1967).
The pigment content of the fresh algae used for grazing experiments was measured at appropriate absorbance using spectrophotometric analyses, after grinding in chilled 90% acetone solution, and centrifuging. Dry weight (80 a C, 24 hours) of the plant material was determined in order to refer pigment concentrations to weight units. The differences between values for pigments in fresh algal items and those in the faecal pellets were calculated, and the values expressed as percentages of the undigested chlorophyll contents. This procedure allowed to evaluate the digestion efficiency of worms with respect to the chlorophylls, but does not take into account the degradation of the whole organic matter of the ingested food.
Acknowledgements. We wish to thank Dr Maria A Di Meglio for collaboration in data collection and laboratory rearing of Platynereis d"Umerilii. The Electron Microscopy Service of the Stazione Zoologica of Naples provided the technical support for the S.E.M. micrographs. Two anonymous referees provided constructive comments that improved the paper. This project has been funded by the European Community (Environmental projects, ref. EV4V-039B, and STEP-0063C).
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