EFFECTS OF SEA URCHIN GRAZING ON A POSIDONIA OCENICA MEADOW

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1 Actes du 3 ème Symposium méditerranéen sur la végétation marine (Marseille, mars 2007) Stefania COPPA 1,2, Ivan GUALA 1, Maura BAROLI 1, Monica BRESSAN 2, Serena COMO 1, Giuseppe PIERGALLINI 1, Giovanni DE FALCO 1,3 1 Fondazione IMC - International Marine Centre - Onlus, Loc. Sa Mardini, Torregrande, Oristano, ITALY 2 Università di Padova, ITALY 3 IAMC-CNR - Istituto Ambiente Marino Costiero, Sezione di Oristano, ITALY s.coppa@imc-it.org EFFECTS OF SEA URCHIN GRAZING ON A POSIDONIA OCENICA MEADOW IN THE GULF OF ORISTANO (WESTERN SARDINIA, ITALY) Abstract Although the interactions between grazers and Posidonia oceanica have been largely investigated, there are still controversial views about the importance of Paracentrotus lividus. This study investigates the effects of different densities of P. lividus on P. oceanica at leaf and shoot scale. The experiment was conducted in September 2005 and May 2006 on a shallow meadow in the Gulf of Oristano (western Sardinia, Italy). In the field, P. lividus individuals were included within cages, according to five different densities: 0, 8, 20, 40 and 80 individuals m -2. It was predicted that (i) under the cages, number and length of leaves, number of shoots and epiphyte biomass would decrease as an effect of sea urchins and that (ii) these effects would be higher at high than at low densities of sea urchins. The number of leaves and epiphyte biomass per surface unit did not change in response to sea urchin grazing, while a response was found in green and brown tissue as well as in the number of broken leaves. The number of shoots completely grazed by P. lividus varied for densities higher than 8 ind. m -2 ; it peaked at the highest densities of sea urchins (i.e. 80 ind m -2 ) exceeding the 45% of the total number of shoots initially present. The importance of this variable to quantify the grazing effect of P. lividus on the meadow is emphasized. Keywords: Posidonia oceanica, grazing, Paracentrotus lividus, epiphytes, caging experiment. Introduction The echinoid Paracentrotus lividus (Lamarck, 1816) is the most common grazer of the Mediterranean Sea (Palacin et al., 1997; Tomas et al., 2004) and one of the main consumers of the seagrass Posidonia oceanica (Valentine & Heck, 1991). Generally, P. lividus density within P. oceanica meadows ranges from 0 to 6 individuals m -2 (Tomas et al., 2005a; Tomas et al., 2005b; Baroli et al., 2006) even though higher densities and overgrazing events have been frequently described (Kirkman & Young, 1981; Tomas et al., 2005 a). P. lividus at densities of ind. m -2 can remove large patches of the meadow with considerable effects on seagrass biomass and production (Valentine & Heck, 1991; Valentine & Heck, 1999). Verlaque and Nedelec (1984) observed the complete loss of a P. oceanica meadow caused by sea urchins m -2. The same authors assessed ind. m -2 to be the critical density beyond which the consumption overcomes the production of the plant. A severe reduction of seagrass shoot density, up to 50% over six months, was reported due to sea urchin grazing, where individuals ranged between 11 and 30 ind. m -2 (Ruiz, 2000). On the contrary, other authors indicated that sea urchins grazing seems to be a factor of minor importance for the control of P. oceanica production (Cebrián et al., 1996), generally regulated by bottom-up factors as light, temperature and nutrients (Alcoverro et al., 1995). This hypothesis is supported by the evidence that seagrasses are not a preferential source of food for herbivores because of their high C/N ratios, their high content in cellulose and the presence of chemical deterrents (McMillan et al., 1980; Verges et al., 2006). The seagrass unpalatability suggests the potential 56

2 Proceedings of the 3 rd Mediterranean symposium on marine vegetation (Marseilles, March 2007) central role of epiphytes as an alternative or additional food resource for many herbivores (Duarte, 1995; Alcoverro et al., 1997) and in some systems, the interaction between herbivores and seagrass appears to be mediated, at least in part, by epiphytes (Tomas et al., 2005 a). P. lividus seems to feed preferentially on the distal portions of seagrass leaves (Nédelec & Verlaque, 1984; Tomas et al., 2005 a) and particularly on the old leaves where the highest epiphytic biomass occurs (Alcoverro et al., 1997). Removing relatively small amounts of leaf standing biomass, P. lividus feeds large amounts of epiphytes, and this behaviour could be part of an efficient feeding strategy due to the higher palatability of epiphytes than the host plant (Nédelec & Verlaque, 1984; Alcoverro et al., 1997). The aim of this work was to estimate, by means of field manipulative experiments, the critical density of P. lividus affecting a P. oceanica meadow, as well as investigating the grazing activity and its patterns both on leaf and shoot scale. In particular, we tested whether (i) leaf number and length, shoot number and epiphyte biomass per surface unit decreased in the cages as an effect of sea urchins inclusion and whether (ii) such response was dependent on different densities of sea urchins. Materials and methods The study site was located in the Gulf of Oristano ( N; E) along the western coast of Sardinia (Italy) (Fig. 1). The Gulf, extending for 150 Km 2 and 15 m depth in the middle, is colonized for 70% by a wide P. oceanica meadow (Cancemi et al., 1997; Cancemi et al., 2000). Seagrass shoot density was assessed by taking 10 replicate measurements using a 50x50 quadrat. EXPERIMENTAL CAGES Fig. 1: Sampling site. The experiment was carried out in September 2005 and May Fifteen quadrats (50 x 50 cm) were haphazardly selected at 5 m depth and surrounded with an hardware cloth (2.5 cm mesh and 70 cm high) fixed to the substrate with iron bars. Adult sea urchins (diameter ranging from 45 to 55 mm) were introduced inside these cages at different densities (0, 8, 20, 40 and 80 ind. m -2, thereafter I 0, I 8, I 20, I 40, I 80 ). Each density was replicated three times. Moreover, 3 quadrats (50 x 50 cm), without net were also considered as reference (C) to test for possible artefact effects, due to the presence of cages. Each experiment was limited to a one month period due to the considerable sampling effort required to maintain constant densities of sea urchins within cages. Because of high sea urchins mortality due to gastropods (i.e. Trunculariopsis trunculus) predation, inspections to 57

3 Actes du 3 ème Symposium méditerranéen sur la végétation marine (Marseille, mars 2007) verify the continuous presence of selected density were carried out three times per week. Each time, all sea urchins within I 8, I 20, I 40 and I 80 were counted and, if necessary, replaced. To achieve this, P. oceanica shoots inside the cages were handled to find sea urchins buried among them. To test for possible effects of this manipulation, for the experiment carried out in September, a procedural control (PC) was used. It consisted of three replicate cages without sea urchins where the same operations required to ensure the maintenance of the experimental conditions were simulated. At the end of both experiments three P. oceanica shoots were randomly collected from each quadrat and the following variables were measured for each shoot: (i) number of leaves > 5 cm (old and intermediate), (ii) length of old leaves (cm, distinguishing the green from the brown tissue), (iii) the Coefficient A (CoA) due to P. lividus grazing and (iv) the biomass of epiphytes per leaf surface (mg DW cm -2 ); moreover, (v) the number of shoots completely grazed (Fig. 2) was counted and the ratio with the total number of shoots was calculated for each quadrat. Analyses of variance (ANOVAs) were performed on these grazing variables to test for possible differences between I 0 and other sea urchins density (I 8 I 20 I 40 I 80, separately) and to evaluate if the grazing effects varied in time (September 05 vs. May 06). The artefact effect due to the cage was tested comparing C vs. I 8, that was the density closer to the natural one. The comparison between I 0 and PC, to test for possible effects of the manipulation, was carried out only for the first experiment (September 2005). Cochran s test was performed to test for homogeneity of variances and data were transformed when necessary. Post hoc comparisons, by mean of the Student-Newman-Keuls test (SNK), Fig. 2: Shoot were carried out in case of significant differences in the ANOVA. completely grazed by P. lividus. Results P. oceanica density resulted to be shoots m -2 (mean standard error). No significant difference, comparing either I 0 vs. PC and C vs. I 8, was evident for each of the considered variables. Also, epiphyte biomass per leaf surface and number of leaves per shoot did not change either between densities or between times. On the contrary, the analyses of variance showed significant differences, in the number of shoots completely grazed, starting from the density of 20 ind. m -2 ; any significant difference was pointed out between September and May. Sea urchins effect on the green leaf tissue was evident only for 80 ind. m -2, while for the brown part of the leaves the threshold was lower with significant differences starting from the density of 20 ind. m -2 ; the length of brown tissue varied also between times, with values significantly higher in September than in May. With reference to the Coefficient A, all the densities varied significantly from the control for both sampling times with higher values in May. Discussion The contrasts C vs. I 8 and PC vs. I 0 pointed out that neither the presence of cages nor the operator disturbance had significant effects on all the considered variables. The variable that better describes the effect of P. lividus on P. oceanica is the number of shoots completely grazed. As expected, the grazing effect is amplified according to increasing sea urchin densities, with the higher value due to 80 ind. m -2 ; this density, in one month, is able to reduce beyond 45% the initial number of shoots. Overall, the results highlighted that the density beyond which the effects of grazing are evident, should range between 9 and 20 ind. m

4 Proceedings of the 3 rd Mediterranean symposium on marine vegetation (Marseilles, March 2007) Tab. 1 - Mean values (± standard error; n = 3 for the number of shoots completely grazed and n = 9 for all other variables) of the six variables for each treatment and times. Treatments significantly different from the control (C) are represented in bold: * p < 0.05; ** p <0.01; *** p< Time Treatment Shoots completely grazed (%) Number of leaves Green tissue (cm leaf -1 ) Brown tissue (cm leaf -1 ) Epiphytes (mg DW cm -2 ) CoA due to P. lividus September '05 May '06 I ± ± ± ± ± ± 0.00 CP 0.34 ± ± ± ± ± ± 0.00 C ± ± ± ± ± 0.03 I ± ± ± ± ± ± 0.04 * I ± 2.68 * 5.56 ± ± ± 2.94 * 0.29 ± ± 0.04 ** I ± 2.65 ** 5.33 ± ± ± 1.80 * 0.25 ± ± 0.05 * I ± 3.72 * 4.67 ± ± 2.03 *** 1.73 ± 1.07 * 0.27 ± ± 0.08 * I ± ± ± ± ± ± 0.05 C 4.73 ± ± ± ± ± ± 0.06 I ± ± ± ± ± ± 0.04 * I ± 0.87 * 4.33 ± ± ± 0.52 * 0.30 ± ± 0.06 ** I ± 2.54 ** 4.78 ± ± ± 0.10 * 0.22 ± ± 0.07 * I ± 5.32 * 5.00 ± ± 2.32 *** 0.00 ± 0.00 * 0.17 ± ± 0.06 * Tomas et al. (2005a) did not record any difference in the number of shoots due to the sea urchin inclusion; however, their experimental densities were 5 and 15 ind. m -2, lower than the critical one (20 ind. m -2 ) we found to have an effect on P. oceanica; on the other hand 15 ind. m -2 are commonly detected on nearby meadows (S. Coppa, personal observation) without any evident detrimental effect perceived. For the Mediterranean, a complete lost of shoots due to P. lividus grazing is seldom reported, because most of literature documents mainly on sea urchin activity at the leaf scale. Nevertheless, other studies dealing with different latitudes, showed that other sea urchin species, in particular conditions can influence meadows density. For example, Maciá (2000) showed that Litechinus variegatus (10-20 ind. m -2 ) had a significant effect on shoot density of Thalassia testudinum along the Florida coasts. Moreover, this author found that sea urchins affected meadow density according to season: in summer sea urchin activity was lower than winter (the critical threshold correspond to 20 and 10 ind. m -2, respectively). In contrast, the present results did not show any significant differences on the number of grazed shoots between September 2005 and May 2006, even if more temporal replicates would be necessary to demonstrate a seasonal grazing pattern. With reference to the length of green tissue, higher values were found in May 2006, but this effect is probably imputable to the leaf cycle (Mazzella et al., 1986) rather than the grazing activity of sea urchins. Sea urchin influence is evident only at the higher density, indicating that P. oceanica does not seem to be particularly attractive, as suggested by McMillan et al. (1980) and Verges et al. (2006). On the contrary, the brown tissue was more extended in September, also in this case in relation to its seasonal variations rather than the sea urchin grazing (Mazzella et al., 1986). Moreover, the grazing on this tissue portion was already evident for density of 20 ind. m -2 ; hence, brown tissue is more affected by grazing than the green one, probably in relation to the higher colonization rate of epiphytes as observed by Nédelec & Verlaque (1984), Alcoverro et al. (1997) and Tomas et al. (2005a). Data on the bites of P. lividus on tips of the leaves (Coefficient A) indicated that grazing effect was already evident at natural density. The coefficient A showed also that grazing was significant higher in May, thus suggesting a more remarkable activity of sea urchins during the spring. 59

5 Actes du 3 ème Symposium méditerranéen sur la végétation marine (Marseille, mars 2007) A central role, in the interaction grazers-seagrasses, can be largely ascribed to epiphytes as both green and brown tissues covered by epiphytes are preferred (Boudouresque & Verlaque, 2007 and references therein). Keuskamp (2004) found that the grazers mostly affect the filamentous algae. Alcoverro et al. (1997) demonstrated that grazing is one of the factors that contribute to the temporal variability of the epiphyte biomass and that herbivores can be determinant in defining local differences between meadows. Tomas et al. (2005a) pointed out a clear effect of sea urchin density on epiphyte abundance and suggested epiphytes as the most limiting resource for sea urchins in P. oceanica systems. Our findings did not indicate any significant difference in the epiphyte biomass, calculated per surface unit, due to different sea urchin densities. This suggests that, even if P. lividus grazing on epiphytes affects the highly colonised leaf portions (Alcoverro et al., 1997; Boudouresque & Verlaque, 2007), it does not occur independently to leaves consumption. It is noteworthy that completely grazed shoots were found also within the non-caged plots, characterized by natural sea urchins density and within I 0, probably due to sea urchin grazing before cage installation. This should indicate that, also in natural conditions, P. lividus uses two grazing modalities: a complete grazing of the shoot, probably starting from the base of the leaves or, alternatively, the choice of the more palatable portions of the leaves. This hypothesis seems to be confirmed by the absence of effects on the number of leaves per shoot in all treatments. In conclusion, although the short duration of the experiment could have missed the detection of some grazing effects, especially at lower urchin densities, this research highlighted the importance of assessing the number of shoots grazed in a P. oceanica meadow to quantify grazing activity of sea urchins, which would be otherwise underestimated if research focus would be limited to leaf level. Acknowledgments This work was carried out with financial support from the MIUR (project STM nr. 20 Cluster Acquacoltura) and the EU (project EMPAFISH SSP ). The authors wish to thank Simone Simeone, Andrea Satta, G. Andrea de Lucia, Ettore Lutzu and Enrico Stara for field and logistic assistance. We also thank Giuseppe Di Carlo for improving the English text and an anonymous reviewer for his useful criticism on the manuscript. Bibliography ALCOVERRO T., DUARTE C.M., ROMERO J. (1995) - Annual growth dynamics of Posidonia oceanica: contribution of large-scale versus local factors to seasonality. - Mar. Ecol. Prog. Ser., 120: ALCOVERRO T., DUARTE C.M., ROMERO J. (1997) - The influence of herbivores on Posidonia oceanica epiphytes. - Aq. Bot., 56: BAROLI M., DE FALCO G., ANTONINI C., COPPA S., FACHERIS C. (2006) - Analisi della distribuzione e struttura della popolazione di Paracentrotus lividus finalizzata alla gestione della pesca del riccio di mare nell Area Marina Protetta Penisola del Sinis - Isola di Mal di Ventre (Sardegna occidentale). - Biol. Mar. Medit., 13 (1): BOUDOURESQUE C.F., VERLAQUE M. (2007) - Ecology of Paracentrotus lividus. - In: Lawrence J.M. (Ed.), Edible sea urchin: Biology and Ecology. Elsevier, Oxford UK: CANCEMI G., BAROLI M., DE FALCO G., AGOSTINI S, PIERGALLINI G., GUALA I. (2000) - Cartografia integrata delle praterie marine superficiali come indicatore dell impatto antropico sulla fascia costiera. - Biol. Mar. Medit., 7 (1): CANCEMI G., PASQUALINI V., PIERGALLINI G., BAROLI M., DE FALCO G., PERGENT-MARTINI C. (1997) - Indagine cartografica sulla prateria a Posidonia oceanica (L.) Delile di Capo San Marco (Golfo di Oristano), mediante elaborazione di immagini fotoaeree. Biol. Mar. Medit., 4 (1): CEBRIAN J., DUARTE C.M., MARBA N., ENRIQUEZ S., GALLEGOS M., OLESEN B. (1996) - Herbivory on Posidonia oceanica and variability in the Spanish Mediterranean. - Mar. Ecol. Prog. Ser., 130:

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