Mesograzers in Posidonia Oceanica Meadows: an Update of Data on Gastropod-Epiphyte-Seagrass Interactions
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Article in press - uncorrected proof Botanica Marina 52 (2009): 439–447 ᮊ 2009 by Walter de Gruyter • Berlin • New York. DOI 10.1515/BOT.2009.054 Mesograzers in Posidonia oceanica meadows: an update of data on gastropod-epiphyte-seagrass interactions Esperanca¸ Gacia1,*, David Costalago2, Patricia characteristic assemblages on leaves of P. oceanica, Prado1, Diana Piorno1 and Fiona Tomas3 whereas leaf sheaths and rhizomes shelter species from the leaves and others from nearby infralitoral communi- 1 Centre d’Estudis Avanc¸ ats de Blanes, CSIC, Ctra. ties (macroalgal, coraligenous; Templado 1984a). Acce´ s Cala St. Francesc 14, 17300 Blanes, Spain, Seagrass leaf-associated gastropods generally feed on e-mail: [email protected] the epiphytic component, ingesting the biofilm com- 2 Centre Mediterrani d’Investigacions Marines i posed of bacteria and diatoms, as well as various algal Ambientals, CSIC, Passeig Marı´tim de la Barceloneta, groups and animals (Van Montfrans et al. 1982, Kitting 37-49, 08003 Barcelona, Spain 1984, Mazzella et al. 1992). Gastropods have traditionally 3 Institut Mediterrani d’Estudis Avanc¸ ats, CSIC, been assigned to different feeding guilds (Purchon 1968) c/Miquel Marque` s 21, 07190 Esporles, Palma de coupled to the morphology of the feeding apparatus Mallorca, Spain (radula) that constrains acquisition of food material and * Corresponding author indirectly modulates the feeding resources for grazers (Steneck and Watling 1982) via selection of different food types (Peduzzi 1987, Mazzella and Russo 1989, Jerna- Abstract koff and Nielsen 1997). These trophic abilities underlie our traditional understanding of feeding habits and die- Information on dietary habits of mesograzers in Posido- tary preferences of molluscs; for example, the diet of the nia oceanica seagrass meadows is scarce and restricted herbivorous snail is based on the size, shape and tough- to a few species. Here we provide data on the most likely ness of a single algal species (Steneck and Watling 1982, food sources for eight gastropod species inferred from Mazzella et al. 1992). Thus, trophic strategies of sea- stable isotope data. We observed very similar isotopic grass-associated gastropods are diverse and difficult to signals for all species regardless of trophic guild cate- approach at the community level, but they can be rele- gory, indicating similar consumption behaviour with a vant to the dynamics of the whole system (Phillippart main diet contribution from epiphytes. We also review the 1995, Hughes et al. 2004). state of knowledge on gastropod-epiphyte-seagrass Stable isotope analysis is an indirect method for iden- interactions, with particular emphasis on the scarcity of tifying food pathways within complex ecosystems (Fry studies derived from Mediterranean systems. Laboratory et al. 1987). In general, carbon (C) isotopes are used to experiments showed that under moderately nutrient- identify the most likely carbon source of individual organ- enriched conditions, two species of gastropods (Bittium isms (Fry and Sherr 1984), whereas nitrogen (N) isotopes reticulatum and Jujubinus striatus) were controlling epi- are typically used to identify the trophic position of these phyte biomass at high grazer densities, with no conse- organisms within the food web (Fry et al. 1987). The nitro- quences for seagrass performance. Finally, the results of gen isotopic signature at the consumer level can also be a long-term in situ fertilisation experiment showed that used to define foraging sites for organisms and the com- the d15N signal for seagrass, epiphytes and gastropods positions of their diets relative to differences in N inputs reflects experimentally induced eutrophication, thus cas- (Shriver et al. 2002, Weiss et al. 2002, Carmichael et al. cading up nutrient effects throughout the food web. 2004, Vizzini and Mazzola 2004), and thus is a useful tool for tracking eutrophication phenomena (McClelland et al. Keywords: epiphytes; gastropods; grazing; nutrients; 1997). Posidonia oceanica; stable isotopes. In Posidonia oceanica seagrass meadows, data on the relative contribution of different food sources have been investigated for macroherbivores (i.e., fish and sea Introduction urchins) using direct analyses of gut contents (Kempf 1962, Verlaque 1981), integrative stable isotope app- Seagrass meadows shelter an important diversity of flora roaches (e.g., Havelange et al. 1997, Jennings et al. and fauna (Hemminga and Duarte 2000). One important 1997, Vizzini and Mazzola 2004, 2006, Tomas et al. 2006, component of this diversity is the vagile fauna, a group among others), or a combination of both (Pinnegar and associated with seagrass blades and comprising small Polunin 2000). Unfortunately, information on dietary hab- animals (crustaceans, molluscs, polychaetes) with its of mesograzers is scarce, and for gastropods it is reduced mobility. In Posidonia oceanica (L.) Delile mea- restricted to manipulative experiments designed to dows, gastropod molluscs are among the most important assess dietary preferences of Gibbula and Jujubinus spp. elements of this vagile fauna in terms of both species associated with P. oceanica (Peduzzi 1987, Mazzella and richness (Mazzella and Russo 1989, Gambi et al. 1991) Russo 1989) and isolated data on stable isotopic com- and numbers of individuals (Ledoyer 1968, Kikuchi and positions for a few species from the Bay of Calvi (Dauby Peres 1977, Templado et al. 2004). Gastropods form 1989, Lepoint et al. 2000). Meadows of Zostera marina L. Brought to you by | Csic/Ctre D Estudis Avancats 2009/84 Authenticated | 161.111.254.106 Download Date | 10/3/12 10:17 AM Article in press - uncorrected proof 440 E. Gacia et al.: Gastropod-epiphyte-seagrass interactions in Posidonia oceanica have been studied more comprehensively, with direct Trophic behaviour assessment using stable isotopes microscopic observation of seagrass leaf scars after grazing (Van Montfrans et al. 1982, Neckles et al. 1993) We collected gastropods of different species (minimum and, most recently, a combination of stable isotopes and length 15 mm) from the Fenals Posidonia oceanica fatty acid biomarkers for several gastropod species meadow (Figure 1) and inferred food diet from the stable (Kharlamenko et al. 2001, Alfaro et al. 2006). isotopic composition. Individuals were left for 24 h in Interactions between grazers and epiphytes result in seawater tanks to eliminate faeces and then stored fro- reductions in epiphyte biomass, increases in production zen. To sort the snails, the shells were broken and the and a shift in species composition (see the review by bodies extracted, making sure that there were no pieces Jernakoff et al. 1996). For gastropods, direct data on of shell left. Gastropods were rinsed in distilled water, grazing activity are scarce but there is experimental work dried (24 h, 608C) and ground to a fine powder. Samples showing epiphyte control by gastropods on Thalassia were sealed in glass vials for further isotope analysis. All testudinum Banks et Sol. ex Koenig from Florida (Fran- species were collected in summer 2004. kovich et al. 2003, Peterson et al. 2007), Zostera species Isotope abundances were measured on a continuous- from North America and Hong Kong (Neckles et al. 1993, flow isotope radiomass spectrometer Delta C (Thermo Nelson 1997, Fong et al. 2000) and Posidonia sinuosa Finnigan, Bremen, Germany) coupled to a Flash 1112 elemental analyser (Thermo Finnigan) through a Conflo III Cambridge et Kuo from Western Australia (Jernakoff and interface. Carbon and nitrogen were analysed in dual Nielsen 1997). In the Mediterranean Sea, although sea- isotope mode. Samples of reference material (internal grasses can accumulate large amounts of epiphytes standards) were used to calibrate the system and com- (Cebria´ n et al. 1999, Tomas et al. 2005), particularly the pensate for drift with time. Experimental precision, based long-lived Posidonia oceanica, we do not know of any on the standard deviation of replicates of the internal study on potential control of seagrass epiphyte biomass standard, was 0.5‰ for both isotopes. The isotope ratios communities by mesograzers. Regulation of epiphyte are expressed relative to the PeeDee Belemnite (PDB) overgrowth by grazers is particularly relevant under high standard for C and to N in air for N. Isotope ratios were nutrient conditions and may result in enhancement of 2 calculated as: seagrass productivity and/or survival. Hughes et al. (2004) compiled data on the impact of nutrients and 13 15 sw x= the effects of grazers in 35 meadows worldwide. They d Cord N (Rsample /R standard -1) 1000 mention only one reference for the Mediterranean Sea, viz. epiphyte overgrowth on the seagrass Cymodocea where R is the corresponding 13C/12Cor15N/14N ratio. nodosa (Ucria) Ascherson, but no information on inter- All analyses were performed at the Serveis Cientı´fico- action with grazers is provided. More recently, studies on Te` cnics (University of Barcelona). P. oceanica have shown that nutrient inputs cause an increase in epiphyte biomass and a shift in species com- Interaction between meso-herbivores, epiphytes and position (Prado et al. 2008) and promote macrograzer Posidonia oceanica under laboratory conditions pressure under experimental (Prado 2007) and anthro- pogenic nutrient input gradients (Kirkman and Young To examine the interactions among gastropods, epi- 1981, Ruı´z et al. 2001). However, there is still no infor- phytes and the seagrass Posidonia oceanica, we used mation on whether