Patterns of Spatial Variability of Mobile Macro-Invertebrate Assemblages Within a Posidonia Oceanica Meadow R

Journal of Natural History, 2015 Vol. 49, Nos. 41–42, 2559–2581, http://dx.doi.org/10.1080/00222933.2015.1021872

Patterns of spatial variability of mobile macro-invertebrate assemblages within a Posidonia oceanica meadow R. Bedini*, M. Bedini, L. Bonechi and L. Piazzi

Istituto di Biologia ed Ecologia Marina, Piombino, Italy

(Received 22 April 2013; accepted 22 January 2015; first published online 10 April 2015)

The study evaluated patterns of spatial variability of mobile macro-invertebrate assemblages associated with Posidonia oceanica leaves within a meadow at three different depths and three different coastal wave-exposures. A total of 171 taxa was found, among them two Nemertea, 65 Mollusca, 91 Arthropoda, eight Annelida and five Echinodermata. The total number of taxa per sample was higher in intermediate and deep stands than in shallow ones, while no significant differences among coastal wave-exposures were observed. Multivariate analyses detected significant differences in the structure of assemblages in relation to depth and coastal wave-exposure. Mollusca were more abundant in shallow stands, while Crustacea and Echinodermata increased in intermediate and deep stands. Moreover, patterns of spatial variability changed with depth: shallow and intermediate assemblages showed high small-scale (tens of metres apart) variability, while deep assemblages showed high variability at intermediate scale (hundreds of metres apart). Keywords: depth; mobile macro-invertebrates; orientation; Posidonia oceanica; spatial variability

Introduction Natural systems may vary in space and time, following patterns of organismal distribution (Menge and Olson 1990; Schneider 1994). Moreover, the variability of natural assemblages is scale dependent (Underwood and Chapman 1996; Benedetti- Cecchi 2001; Terlizzi et al. 2007), making it crucial for ecologists to identify the main scales of variability and the processes generating these patterns (Levin 1992). Downloaded by [University of Cambridge] at 05:12 08 April 2016 Knowledge of spatial patterns of assemblages may allow discrimination between natural variability and human-induced effects in environmental monitoring surveys and impact evaluation studies (Hewitt et al. 2001; Bishop et al. 2002; Fraschetti et al. 2005) and sampling design pertinent to ecological questions (Underwood 1993; Benedetti-Cecchi et al. 2003). Seagrasses and their associated assemblages represent one of the main coastal ecosystems and they are the object of a lot of studies because of their ecological relevance in coastal waters and their role as bioindicators (Kirkman 1996;Kuo et al. 1996). Seagrass meadows host complex macro-invertebrate assemblages both sessile, as epiphytes of leaves and rhizomes, and mobile (Mazzella et al. 1992). Mobile macro-invertebrate assemblages associated with seagrasses are particularly

*Corresponding author. Email: [email protected]

abundant and diverse thanks to the habitat complexity of meadows, and their role as refuges from predators and as a food supply (Heck and Orth 1980). In fact, the structure of seagrasses can create many microhabitats characterised by different environmental conditions, allowing the coexistence of species with different ecological requirements (Stoner 1980;Orthetal.1984). Moreover, plants and their epiphytes represent an important food source for both grazers and detritivorous organisms (Van Montfrans et al. 1984;KlumppandVanderValk1984; Edgar 1999;Duffyetal.2003). Although widely studied (Mattila et al. 1999; Atrill et al. 2000; Bostrom et al. 2006), patterns of spatial variability of macro- invertebrate assemblages of seagrass meadows and factors influencing these patterns are not completely known. In the Mediterranean Sea, Posidonia oceanica (L.) Delile represents the most important seagrass in terms of meadow extent and their role in coastal systems (Mazzella et al. 1992). The structure of macro-invertebrate assemblages associated with P. oceanica has been widely studied (Russo et al. 1991; Scipione et al. 1996; Bedini et al. 1997; Zakhama-Sraieb et al. 2011; Albano and Sabelli 2012; Urra et al. 2013) and spatial variability of assemblages has been evaluated at a large scale (among meadows and habitats) and in relation to depth gradients (Russo et al. 1984; Scipione and Fresi 1984; Mazzella et al. 1989; Gambi et al. 1992, 1995; Borg and Schembri 2000; Borg et al. 2010; Bedini et al. 2011; Belgacem et al. 2011, 2013). However, little is known about spatial patterns of variability within meadows, and about mechanisms determining these patterns. The present study aimed to evaluate patterns of spatial variability of mobile macro-invertebrate assemblages associated with the leaves within a Posidonia oceanica meadow, in relation to depth and coastal wave-exposure. For this purpose, a hierarchical sampling design was used to study a P. oceanica meadow at multiple spatial scales in relation to three different depths and three different coastal wave- exposures.

Material and methods The study was carried out around the Island of Pianosa, in the Tuscan Archipelago National Park (northwestern Mediterranean Sea), in July 2010 (Figure 1). The sampling period was chosen because it corresponds to the maximum vegetative development of Posidonia oceanica. The island has very

Downloaded by [University of Cambridge] at 05:12 08 April 2016 low anthropogenic pressure and all activities are forbidden for about 2 km from the shore. The seafloor slopes gently, allowing the development, between 5 and 40 m depth, of a Posidonia oceanica meadow about 16 km2 wide (Cinelli et al. 1995). The meadow is installed on matte (structures constituted of several layers of dead rhizomes and trapped sediment); rocky and sand bottoms are present above and below the meadow all around the island. The ecological quality of the site allows the elimination of variation due to anthropogenic disturbance; also, the structure of the meadow may be considered similar within a given depth range. Three depth ranges were sampled: 8–10 m (shallow = S), 18–20 m (intermediate = I) and 30–35 m (deep = D). Three sides of the island corresponding to different coastal wave-exposures (east = e, south = s, west = w) were considered, and four areas 100s of m distant from each other were sampled Journal of Natural History 2561

Downloaded by [University of Cambridge] at 05:12 08 April 2016 Figure 1. Map of Pianosa Island. Stars indicate the study areas.

at each depth and side. Western and southwestern winds are dominant in the area, making the western side the most exposed to water movements (Region of Tuscany 1993). At each area, 10 replicate measures of density were made using a 40 × 40 cm quadrat and 10 shoots were collected to assess the meadow canopy (Pergent et al. 1995). A hand-towed net (40 × 20 cm, 0.4-mm mesh size) was used to sample mobile organisms living in the leaf stratum. Two samples tens of metres distant from each other were collected at each area. Each sample consisted of a series of 60 strokes over the seagrass canopy (Russo et al. 1985; Buia et al. 2003). 2562 R. Bedini et al.

In the laboratory, taxa were identified and the abundance was expressed as number of individuals per sample. Species composition and abundance, were analysed by permutational analysis of variance (PRIMER 6 + PERMANOVA, Anderson 2001). A three-way model was used with depth (S vs I vs D) and side (e vs s vs w) as fixed and crossed factors, area (four levels) as random factor nested in the interaction depth × side. Species- abundance data were log(x + 1) transformed before calculation of Bray–Curtis index of dissimilarity. A two-dimensional non-metric multidimensional scaling (nMDS), based on centroids for replicated areas, was used for a graphical repre- sentation of the data. Pseudo-variance components in species composition and abundance were calculated for each spatial scale at each depth. The SIMPER (similarity percentages) routine was performed on untransformed data to establish which taxa contributed most to the dissimilarity. Shoot density, leaf length, the number of taxa, the abundance of organisms per sample and the abundance of the main phyla were analysed by analyses of variance (ANOVA), with the same factors and levels used for multivariate analyses. Cochran’s C-test was utilised before each analysis to check for homogeneity of variance, and data were transformed when necessary. The Student–Newman–Keuls (SNK) test was used for a posteriori multiple comparison of means (Underwood 1997).

Results Meadow structure Shoot density ranged from 665.3 ± 33.5 to 181.4 ± 21.1, decreasing from shallow to deep stands (Figure 2b), while values of mean leaf length were higher in intermediate stands (Figure 2b). ANOVA and SNK test detected significant differences among depths (even if non-homogeneity of data has to be considered for shoot density) but not among coast sides (Table 1).

Macro-invertebrate assemblages A total of 171 taxa was determined, among them two Nemertea, 65 Mollusca, 91 Arthropoda, eight Annelida, and five Echinodermata (Table 2). The total number of taxa per sample was higher in intermediate and deep

Downloaded by [University of Cambridge] at 05:12 08 April 2016 stands than in shallow ones, while no significant differences among sides were observed (Table 3; Figure 3a). Differences among depths and sides were not significant for the mean number of organisms per sample (Table 3)evenifthe abundance of the main taxa changed along the depth gradient: Mollusca were more abundant in shallow stands, while Crustacea and Echinodermata increased in intermediate and deep stands (Table 3; Figure 3b). Crustacea also differed between east and west sides (Table 3). PERMANOVA showed significant differences related to both depth and side for species composition and abundance of macro-invertebrate assemblages (Table 4). Pair-wise tests showed that depths were significantly different to each other. Differences were also significant between the east and west sides (Table 4). The nMDS showed that shallow stands were well separated from intermediate and deep ones, and, within the shallow stands, the west side was separated from the others (Figure 4). Journal of Natural History 2563

Figure 2. (a) Shoot density and (b) mean leaf length of Posidonia oceanica meadow of Pianosa Island (mean ± standard error, SE; n = 120).

Table 1. Results of analysis of variance (ANOVA) on the shoot density and the mean leaf Downloaded by [University of Cambridge] at 05:12 08 April 2016 length per shoot of the Posidonia oceanica meadow of Pianosa Island.

Source df Shoot density Leaf length

MS F P MS F P

Depth = D 2 97419 158.4 0.001 14171 150.4 0.001 Side = S 2 660 10.7 0.369 188 2.0 0.155 D × S 4 617 10.0 0.421 141 1.5 0.231 Area (D × S) 27 614 10.6 0.001 94 2.5 0.001 Residual 324 57 37 Total 359 C = 0.139 (P < 0.01) C = 0.062 (not significant) SNK test Depth D < I < S Depth D < S < I

Notes: S = shallow, I = intermediate, D = deep, SNK = Student–Newman–Keuls test. MS = mean squares. F = F-ratio. Significant effects are indicated in bold. Downloaded by [University of Cambridge] at 05:12 08 April 2016

Table 2. List of taxa. The mean number of individuals per sample is reported for each taxa. S = shallow, I = intermediate, D = deep; e = east, 2564 s = south, w = west.

TAXA S-e S-s S-w I-e I-s I-w D-e D-s D-w Bedini R.

NEMERTEA Anopla Cerebratulus fuscus (McIntosh, 1874) 0.0 0.0 0.0 0.0 0.1 0.0 0.0 0.0 0.0 al. et Enopla Tetrastemma melanocephalum (Johnston, 1837) 0.0 0.0 0.0 0.1 0.0 0.0 0.0 0.0 0.0 MOLLUSCA Polyplacophora Callochiton septemvalvis (Montagu, 1803) 0.0 0.1 0.0 0.0 0.0 0.0 0.0 0.0 0.0 Gastropoda Alvania cancellata (da Costa, 1778) juv. 0.0 0.0 0.0 0.0 0.0 0.0 0.1 0.0 0.0 Alvania discors (Allan, 1818) 4.0 0.3 0.1 0.0 0.0 0.0 0.0 0.0 0.0 Alvania lineata Risso, 1826 7.4 1.8 6.0 0.8 0.3 0.9 2.4 3.6 0.3 Alvania mamillata Risso, 1826 0.0 0.0 0.1 0.0 0.0 0.1 0.5 0.0 0.0 Aplysia parvula Mørch, 1863 0.0 0.0 0.0 1.6 0.3 1.0 2.0 0.6 1.8 Barleeia unifasciata (Montagu, 1803) 0.0 0.0 0.0 0.0 0.0 0.0 1.6 0.0 0.0 Bittium latreillii (Payraudeau, 1826) 168.5 133.9 128.9 83.8 11.0 33.6 43.5 65.1 44.0 Bittium reticulatum (da Costa, 1778) 0.0 0.0 4.5 9.5 1.6 4.1 4.5 5.5 3.8 Bolma rugosa (Linnaeus, 1767) juv. 0.0 0.0 0.0 0.0 0.0 0.0 0.3 0.5 0.0 Calliostoma conulus (Linnaeus, 1758) 0.0 0.0 0.0 0.0 0.1 0.3 0.0 0.6 0.0 Calliostoma laugieri (Payraudeau, 1826) 0.0 0.0 0.1 0.0 0.0 0.0 0.1 0.6 0.0 Calliostoma zizyphinum (Linnaeus, 1758) 0.0 0.0 0.0 0.1 0.0 0.1 0.0 0.1 0.0 Cerithiopsis minima (Brusina, 1865) 0.0 0.0 0.0 0.3 0.0 0.0 0.0 0.0 0.1 Cerithiopsis tubercolaris (Montagu, 1803) 0.0 0.0 0.0 0.0 0.0 0.0 0.1 0.0 0.3 Cerithium vulgatum Bruguière, 1792 0.0 0.0 0.0 0.0 0.0 0.1 0.0 0.0 0.6 Chauvetia mamillata (Risso, 1826) 9.4 15.6 20.3 0.6 0.5 0.0 1.3 1.5 0.4 Coralliophila meyendorffii (Calcara, 1845) 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.1 0.0 Epitonium clathrus (Linnaeus, 1758) juv. 0.0 0.0 0.0 0.0 0.0 0.0 0.1 0.0 0.0

(Continued) Downloaded by [University of Cambridge] at 05:12 08 April 2016

Table 2. (Continued). Felimare fontandraui (Pruvot-Fol, 1951) 0.0 0.0 0.0 0.0 0.1 0.1 0.0 0.0 0.0 Felimare tricolor (Cantraine, 1835) 0.0 0.0 0.0 0.1 0.0 0.0 0.0 0.0 0.0 Fusinus parvulus (Monterosato, 1884) 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.1 0.4 Gibberula miliaria (Linnaeus, 1758) 0.0 0.0 0.0 0.0 0.0 0.0 0.1 0.0 0.0 Gibbula varia (Linnaeus, 1758) 0.0 0.0 0.0 0.0 0.0 0.1 0.0 0.0 0.0 Granulina marginata (Bivona, 1832) 0.0 0.0 0.0 0.0 0.0 0.1 1.0 0.1 0.3 Haedropleura septangularis (Montagu, 1803) 0.0 0.0 0.0 0.1 0.0 0.0 0.0 0.0 0.0 Hancockia uncinata (Hesse, 1872) 0.1 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 Homalopoma sanguineum (Linnaeus, 1758) 0.0 0.0 0.0 0.3 0.8 0.3 0.3 9.8 1.6 Jujubinus exasperatus (Pennant, 1777) 1.6 1.9 3.5 1.3 0.8 1.5 1.8 10.8 7.0 Jujubinus striatus (Linnaeus, 1758) 0.1 0.0 0.0 0.1 0.5 0.8 0.5 3.0 3.1 Mangelia vauquelini (Payraudeau, 1826) 0.0 0.1 0.0 0.0 0.0 0.0 0.0 0.0 0.0 Marshallora adversa (Montagu, 1803) 0.0 0.0 0.1 0.1 0.1 0.1 0.3 0.1 0.1 Mitrella minor (Scacchi, 1836) 0.0 0.0 0.0 0.0 0.1 0.0 0.0 0.0 0.0 Monophorus perversus (Linnaeus, 1758) 0.1 0.0 0.0 0.0 01 0.0 0.0 0.0 0.0 Murexsul aradasii (Monterosato in Poirier, 1883) 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.1 0.0 Muricopsis cristatus (Brocchi, 1814) 0.0 0.0 0.0 0.0 0.0 0.3 0.1 0.0 0.0 Ocinebrina aciculata (Lamarck, 1822) 2.1 0.9 0.8 3.1 2.8 1.4 4.8 11.6 1.8 ora fNtrlHistory Natural of Journal Ocinebrina edwardsii (Payraudeau, 1826) 0.0 0.0 0.0 0.0 0.3 0.9 0.4 1.1 1.8 Petalifera petalifera (Rang, 1828) 0.0 0.0 0.0 0.0 0.0 0.3 0.0 0.0 0.0 Phyllaplysia lafonti (Fischer, P., 1870) 0.0 0.0 0.0 0.0 0.1 0.0 0.0 0.0 0.0 Pollia dorbignyi (Payraudeau, 1826) juv. 0.0 0.0 0.0 1.3 0.8 0.3 0.9 2.5 1.4 Pusillina inconspicua (Alder, 1844) 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.1 0.0 Pusillina marginata (Michaud, 1832) 0.0 0.0 0.0 0.0 0.0 0.0 0.3 0.0 0.0 Pusillina philippi (Aradas & Maggiore, 1844) 0.0 0.3 0.0 1.8 1.3 0.8 0.4 1.4 0.5 Pusillina radiata (Philippi, 1836) 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.1 0.0 Raphitoma linearis (Montagu, 1803) 0.0 0.0 0.0 0.0 0.0 0.1 0.0 0.1 0.5 Rissoa auriscalpium (Linnaeus 1758) 28.1 9.6 6.4 7.8 2.1 0.9 0.0 0.0 0.0 Rissoa guerinii Récluz, 1843 0.0 0.1 0.0 0.0 0.0 0.0 0.0 0.0 0.0 2565 (Continued) Downloaded by [University of Cambridge] at 05:12 08 April 2016 2566

Table 2. (Continued). .Bedini R. TAXA S-e S-s S-w I-e I-s I-w D-e D-s D-w

Rissoa monodonta Philippi, 1836 0.0 0.0 0.0 0.4 0.0 0.0 0.0 0.0 0.0

Rissoa variabilis (Von Mühlfeldt, 1824) 6.5 9.1 0.5 6.0 2.4 3.0 1.8 2.0 0.8 al. et Rissoa ventricosa Desmarest, 1814 0.6 1.4 0.0 0.8 0.4 0.0 0.3 0.4 0.1 Rissoa violacea Desmarest, 1814 0.0 0.0 0.0 0.8 0.0 0.1 0.1 0.0 0.0 Rissoella inflata (Monterosato, 1880) 5.9 6.0 2.3 12.4 4.1 8.5 6.0 10.5 9.5 Rissoina bruguieri (Payraudeau, 1826) 0.0 0.0 0.0 0.0 0.1 0.5 0.0 0.0 0.0 Smaragdia viridis (Linnaeus 1758) 0.1 0.1 0.0 1.9 1.0 0.4 0.0 0.3 0.1 Tricolia pullus pullus (Linnaeus 1758) 0.1 0.5 0.1 1.1 0.5 1.0 0.4 1.9 0.5 Tricolia speciosa (Megerle von Mühlfeld, 1824) 0.5 0.0 0.8 0.1 0.4 1.1 0.1 0.1 1.5 Tricolia tenuis (Michaud, 1829) 0.5 0.0 0.1 0.0 0.0 0.0 0.1 0.0 0.4 Tritonia striata Haefelfinger, 1963 0.0 0.0 0.0 0.3 0.0 0.1 0.1 0.0 0.0 Trivia multilirata (G. B. Sowerby II, 1870) 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.1 0.0 Vexillum (Pusia) ebenus (Lamarck, 1811) 0.0 0.0 0.1 0.0 0.0 0.0 0.1 0.0 0.0 Vexillum tricolor (Gmelin, 1791) 0.0 0.1 0.1 0.0 0.0 0.1 0.8 0.0 0.3 Zonaria pyrum Gmelin, (1791) 0.0 0.0 0.1 0.0 0.0 0.0 0.0 0.0 0.0 ANNELIDA Polychaeta Dorvillea rubrovittata (Grube, 1855) 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.1 0.0 Eunice vittata (Delle Chiaje, 1828) 0.0 0.0 0.0 0.0 0.1 0.0 0.0 0.0 0.0 Glycera tesselata Grube, 1840 0.0 0.0 0.0 0.0 0.0 0.0 0.1 0.0 0.0 Lysidice ninetta Audouin & Milne Edwards, 1833 0.0 0.0 0.0 0.0 0.0 0.0 0.1 0.0 0.0 Platynereis coccinea (Delle Chiaje, 1822) 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.1 0.0 Platynereis dumerilii (Audouin & Milne Edwards, 1833) 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.1 Syllis gracilis Grube, 1840 0.0 0.0 0.0 0.0 0.0 0.0 0.1 0.0 0.0 Syllis variegata Grube, 1860 0.0 0.0 0.3 0.0 0.0 0.0 0.0 0.0 0.0

(Continued) Downloaded by [University of Cambridge] at 05:12 08 April 2016

Table 2. (Continued). ARTHROPODA Crustacea OSTRACODA Cypridina mediterranea Claus 0.0 0.0 0.0 0.4 0.0 0.0 0.0 0.0 0.0 MAXILLOPODA Copilia mediterranea (Claus, 1863) 0.0 0.0 0.0 0.0 0.0 0.4 0.0 0.4 1.8 Porcellidium viride (Philippi, 1840) 0.0 0.0 0.0 0.0 0.0 0.0 0.1 0.0 0.0 MALACOSTRACA Decapoda Alpheus dentipes Guérin, 1832 0.1 0.0 0.0 0.0 0.1 0.0 0.0 0.0 0.0 Alpheus macrocheles (Hailstone, 1835) 0.0 0.0 0.0 0.0 0.1 0.0 0.0 0.0 0.0 Anapagurus laevis (Bell, 1845) 0.0 0.0 0.0 0.1 0.0 0.0 0.0 0.0 0.0 Athanas nitescens (Leach, 1813 [in Leach, 1813–1814]) 0.3 0.3 0.3 0.0 0.8 0.0 0.3 0.1 0.4 Calcinus tubularis (Linnaeus, 1767) 0.0 0.6 0.0 0.0 0.0 0.0 0.0 0.0 0.0 Cestopagurus timidus (Roux, 1830) 0.0 23.8 1.9 31.4 12.0 12.1 26.8 22.6 12.5 Clibanarius erythropus (Latreille, 1818) 0.0 0.5 0.0 0.0 0.0 0.4 0.1 0.3 0.3 Eualus cranchii (Leach, 1817 [in Leach, 1815–1875]) 0.0 0.0 0.0 0.0 0.0 0.1 0.0 0.0 0.0

Galathea squamifera Leach, 1814 0.0 0.0 0.0 0.0 0.0 0.1 0.0 0.0 0.0 History Natural of Journal Hippolyte holthuisi Zariquiey-Alvarez, 1953 2.8 1.9 0.0 1.4 0.5 0.1 1.5 0.3 0.0 Hippolyte inermis Leach, 1815 8.6 16.5 9.3 52.1 32.0 38.5 19.9 24.8 27.0 Hippolyte leptocerus (Heller, 1863) 0.1 0.0 0.0 0.4 1.4 0.3 1.5 1.9 0.5 Hippolyte leptometrae Ledoyer, 1969 0.5 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 Hippolyte prideauxiana Leach, 1817 [in Leach, 1815–1875] 0.0 0.1 0.0 0.0 0.0 0.0 0.4 0.0 0.0 Hippolyte varians Leach, 1814 [in Leach, 1813–1814] 0.1 1.0 0.9 0.0 0.0 0.3 0.0 0.0 0.0 Liocarcinus bolivari (Zariquiey-Alvarez, 1948) 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.1 0.0 Liocarcinus pusillus (Leach, 1816) 0.0 0.0 0.0 0.0 0.0 0.0 0.1 0.0 0.0 Pagurus alatus Fabricius, 1775 0.0 0.0 0.0 0.0 0.0 0.0 0.3 0.0 0.0 Pagurus anachoretus Risso, 1827 0.0 5.3 0.0 8.8 3.0 1.0 1.4 0.9 0.4

Palaemon xiphias Risso, 1816 0.0 0.0 0.1 0.0 1.1 0.0 0.9 1.6 0.6 2567

(Continued) Downloaded by [University of Cambridge] at 05:12 08 April 2016 2568 Table 2. (Continued).

TAXA S-e S-s S-w I-e I-s I-w D-e D-s D-w Bedini R.

Pilumnus hirtellus (Linnaeus, 1761) 0.0 0.0 0.0 0.1 0.0 0.0 0.0 0.0 0.0 Pandalina brevirostris (Rathke, 1843) 0.0 0.0 0.0 0.0 0.3 0.0 0.0 0.0 0.0

Pisa nodipes (Leach, 1815) juv. 0.0 0.1 0.0 0.0 0.0 0.0 0.0 0.0 0.0 al. et Mysidacea Siriella clausi G. O. Sars, 1877 0.0 0.1 0.0 10.4 4.3 2.3 13.5 0.0 0.0 Tanaidacea Apseudopsis latreillii (Milne-Edwards, 1828) 0.0 0.0 0.0 0.1 0.1 0.0 0.6 0.5 0.0 Leptochelia savignyi (Kroyer, 1842) 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.1 Isopoda Anilocra physodes (Linnaeus 1758) 0.0 0.0 0.1 0.0 0.0 0.0 0.0 0.0 0.0 Astacilla dilatata Sars, 1882 0.0 0.0 0.0 0.0 0.3 0.0 0.0 0.1 0.0 Cymodoce truncata Leach, 1814 0.0 0.0 0.0 0.1 0.0 0.0 0.0 0.0 0.0 Dynamene bidentata (Adams, 1800) 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.1 0.0 Eurydice pulchra Leach, 1815 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.1 0.0 Eurydice truncata (Norman, 1868) 0.0 0.0 0.0 0.0 0.1 0.0 0.0 0.0 0.0 Gnathia maxillaris (Montagu, 1804) 0.1 0.0 0.0 0.1 0.6 0.5 0.0 0.5 0.0 Idotea balthica (Pallas, 1772) 0.0 0.1 0.0 0.0 0.0 0.0 0.0 0.0 0.0 Idotea emarginata (Fabricius, 1793) 0.0 0.0 0.0 0.0 0.3 0.0 0.0 0.0 0.0 Idotea granulosa Rathke, 1843 0.0 0.0 0.0 1.3 0.8 1.1 0.6 0.1 0.5 Rocinela dumerilii (Lucas, 1849) 0.0 0.1 0.0 0.0 0.0 0.0 0.1 0.0 0.0 Sphaeroma serratum (Fabricius, 1787) 0.0 0.0 0.0 0.1 0.0 0.0 0.0 0.0 0.0 Stenosoma albertoi (Castellano & Junoy, 2005) 0.0 0.1 0.0 0.0 0.0 0.0 0.0 0.0 0.0 Stenosoma capito (Rathke, 1837) 0.0 0.1 0.0 0.0 0.0 0.0 0.0 0.0 0.0 Stenosoma lancifer Miers, 1881 0.0 0.0 0.0 0.3 0.0 0.0 0.3 0.0 0.0 Synischia hectica (Pallas, 1772) 0.0 0.3 0.0 0.0 0.1 0.0 0.1 0.0 0.0

(Continued) Downloaded by [University of Cambridge] at 05:12 08 April 2016

Table 2. (Continued). Amphipoda Ampelisca rubella A. Costa, 1864 0.0 0.0 0.0 0.0 0.0 0.1 0.0 0.0 0.0 Ampithoe helleri Karaman, 1975 0.0 0.0 0.3 0.1 0.0 0.1 0.0 0.0 0.3 Animoceradocus semiserratus (Bate, 1862) 0.0 0.0 0.1 0.0 0.0 0.1 0.0 0.0 0.0 Aora gracilis (Bate, 1857) 0.0 0.0 0.0 0.0 0.3 0.1 0.0 0.0 0.1 Aora spinicornis Afonso, 1976 0.0 0.0 0.0 0.0 0.4 0.1 0.0 0.0 0.5 Apherusa chiereghinii Giordani – Soika, 1849 0.0 0.0 0.4 0.1 0.4 0.1 0.3 0.1 1.1 Caprella acanthifera Leach, 1814 0.0 0.0 0.8 0.6 0.5 0.5 0.0 0.1 0.3 Caprella equilibra Say, 1818 0.0 0.0 0.1 0.0 0.1 0.5 0.0 0.1 0.3 Caprella mitis Mayer, 1890 0.0 0.0 0.0 0.1 0.0 0.4 0.0 0.0 0.0 Corophium sp. 0.0 0.0 0.0 0.1 0.4 2.1 1.8 0.0 0.0 Cymadusa crassicornis (Costa, 1853) 0.0 0.0 0.0 0.1 0.0 0.0 0.0 0.1 0.0 Dexamine spiniventris (Costa, 1853) 0.0 0.0 0.1 0.1 0.1 0.6 0.1 0.0 0.0 Dexamine spinosa (Montagu, 1813) 0.0 0.0 0.4 0.3 0.3 0.1 0.0 0.0 0.0 Eusiroides dellavallei Chevreux, 1899 0.0 0.0 0.0 0.1 0.0 0.0 0.0 0.0 0.0 Guernea (Guernea) coalita (Norman, 1868) 0.0 0.0 0.0 0.0 0.3 0.0 0.0 0.0 0.1 Hyale camptonyx (Heller, 1866) 0.0 0.0 0.0 0.1 0.0 0.0 0.0 0.0 0.0 Hyale schmidti (Heller, 1866) 0.0 0.0 0.0 0.3 0.0 0.1 0.1 0.3 0.0 ora fNtrlHistory Natural of Journal Iphimedia minuta G. O. Sars, 1882 0.0 0.0 0.0 0.0 0.1 1.4 0.0 0.0 0.0 Leptocheirus guttatus (Grube, 1864) 0.0 0.0 0.0 0.0 0.1 0.0 0.0 0.0 0.3 Leucothoe procera Bate, 1857 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.1 Leucothoe serraticarpa Della Valle, 1893 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.1 Leucothoe spinicarpa (Abildgaard, 1789) 0.0 0.0 0.0 0.1 0.0 0.0 0.0 0.0 0.0 Liljeborgia dellavallei Stebbing, 1906 0.0 0.0 0.1 0.0 0.0 0.0 0.0 0.0 0.0 Lysianassa costae (Milne – Edwards, 1830) 0.0 0.0 0.4 0.0 0.4 0.3 0.0 0.0 0.0 Lysianassina longicornis (Lucas, 1849) 0.0 0.0 0.0 0.0 0.1 0.1 0.0 0.0 0.0 Maera inaequipes (Costa, 1857) 0.0 0.1 0.3 0.0 0.0 0.0 0.0 0.0 0.0 Medicorophium rotundirostre (Stephensen, 1915) Microdeutopus obtusatus Myers, 1973 0.0 0.1 0.0 0.0 0.0 0.1 0.0 0.0 0.0 2569 (Continued) Downloaded by [University of Cambridge] at 05:12 08 April 2016 2570 Table 2. (Continued).

TAXA S-e S-s S-w I-e I-s I-w D-e D-s D-w Bedini R.

Microdeutopus stationis Della Valle, 1893 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.5 Nannonyx propinquus Chevreux, 1911 0.0 0.0 0.0 0.1 0.0 0.0 0.0 0.0 0.0

Pardia punctata (Costa, 1851) 0.0 0.0 0.0 0.0 0.0 0.1 0.0 0.0 0.1 al. et Parvipalpus linea Mayer, 1890 0.0 0.0 0.0 0.0 0.0 0.4 0.0 0.0 0.3 Parvipalpus major Carausu, 1941 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 Peltocoxa gibbosa (Schiecke, 1977) 0.0 0.0 0.1 0.0 0.0 0.0 0.0 0.0 0.0 Perrierella audouiniana (Bate, 1857) 0.0 0.0 0.0 0.3 0.0 0.0 0.0 0.0 0.0 Photis longipes (Della Valle, 1893) 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.1 Phtisica marina Slabber, 1769 0.0 0.0 1.0 3.9 11.6 4.5 6.0 17.4 2.6 Pseudoprotella phasma Montagu, 1804 0.0 0.1 0.1 0.5 0.3 0.0 0.3 0.5 0.1 Siphonoecetes (Centraloecetes) dellavallei Stebbing, 1899 0.0 0.0 0.0 0.0 0.5 0.0 0.0 0.0 0.0 Stenothoe sp. 0.0 0.0 0.0 0.0 0.1 0.0 0.0 0.0 0.0 Tmetonyx similis (Sars, 1891) 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.1 Tritaeta gibbosa (Bate, 1862) 0.0 0.0 0.0 0.0 0.0 0.1 0.0 0.0 0.0 Tryphosa nana (Krøyer, 1846) 0.0 0.0 0.0 0.0 0.4 0.0 0.0 0.0 0.0 Pycnogonida Callipallene emaciata (Dohrn, 1881) 0.0 0.0 0.0 0.0 0.0 0.0 0.3 0.0 0.0 Nimphon gracile Leach, 1814 0.0 0.0 0.0 0.1 0.0 0.0 0.0 0.0 0.0 Arachnida Pontarachna punctulum Philippi, 1840 0.0 0.0 0.0 1.0 0.5 1.0 1.0 0.5 1.0 ECHINODERMATA Ophiuroidea Amphipholis squamata (Delle Chiaje, 1828) juv. 0.0 0.0 0.0 0.0 0.5 0.0 0.0 0.0 0.0 Amphiura chiajei Forbes, 1843 juv. 0.0 0.1 0.0 0.1 0.0 0.0 0.0 0.0 0.0 Ophiotrix fragilis (Abildgaard, in O.F. Müller, 1789) 0.0 0.0 0.0 0.3 0.0 0.1 0.0 0.0 0.0 Asteroidea Asterina gibbosa Pennant, (1777) 0.4 0.1 0.4 14.9 3.8 2.6 7.1 19.1 14.4 Asterina pancerii (Gasco, 1870) 0.0 0.3 0.0 0.4 0.0 0.1 0.0 0.1 0.3 Journal of Natural History 2571

Table 3. Results of analysis of variance (ANOVA) on the number of species, the number of individuals per sample and the abundance of the main taxa of macro-invertebrate assemblages.

Source df MS F P MS F P

Number of species Number of individuals Depth = D 2 571.8 16.01 0.001 47.0 0.66 0.535 Side = S 2 2.3 0.07 0.935 222.3 3.15 0.059 D × S 4 12.0 0.34 0.851 145.8 20.72 0.104 Area (D × S) 27 35.7 3.84 0.001 70.3 3.23 0.001 Residual 36 9.3 21.7 Total 71 Cochran’s C test not significant Cochran’s C test not significant SNK test Depth S < I = D Mollusca Crustacea Depth = D 2 5407.9 34.63 0.025 15559.0 15.82 0.001 Side = S 2 4603.6 29.48 0.053 3024.3 30.76 0.030 D × S 4 1991.1 12.75 0.273 2093.2 21.29 0.068 Area (D × S) 27 1561.3 23.46 0.003 983.1 27.16 0.001 Residual 36 665.4 Total 71 Cochran’s C test not significant Cochran’s C test not significant SNK test Depth S > I = D SNK test Depth S < I = D Side w < e, e = s, w = s Echinodermata Polychaeta Depth = D 2 24559.0 14.76 0.001 34.7 0.24 0.805 Side = S 2 1552.0 0.93 0.429 81.2 0.56 0.659 D × S 4 2976.9 17.89 0.113 183.9 12.83 0.290 Area (D × S) 27 1663.9 24.35 0.001 143.3 14.85 0.164 Residual 36 683.1 96.4 Total 71 Cochran’s C test not significant Cochran’s C test not significant SNK test Depth S < I < D

Notes: S = shallow, I = intermediate, D = deep. e = east, s = south, w = west. SNK = Student– Newman–Keuls test. MS = mean squares. F = F-ratio. Significant effects are indicated in bold.

Pseudo-variance components increased from large (sides, kilometres apart) to Downloaded by [University of Cambridge] at 05:12 08 April 2016 small spatial scales (samples, tens of metres apart) at shallow and intermediate depths (Figure 5a and b), while deep stands had a higher variance at intermediate scale (areas, hundreds of metres apart, Figure 5c). The SIMPER test showed the taxa that mostly contributed to differences between depths were the Mollusca Bittium latreillii, Chauvetia mamillata and Rissoa auriscalpium which were more abundant in shallower assemblages; and the Crustacea Hippolyte inermis, Cestopagurus timidus and Phtisica marina,the Mollusca Jujubinus exasperatus and Ocinebrina aciculata and the Echinodermata Asterina gibbosa which increased their abundance with depth (Table 5). Differences between the west and east sides of the island were mostly related to a higher abundance of Bittium latreillii, Cestopagurus timidus and Rissoa auriscalpium ontheeastside(Table 5). 2572 R. Bedini et al.

Figure 3. (a) Mean species number and (b) number of individuals per sample of mobile macro- invertebrate assemblages of Posidonia oceanica meadow (mean ± standard error, SE; n = 24).

Downloaded by [University of Cambridge] at 05:12 08 April 2016 Discussion Results show that the structure of macro-invertebrate assemblages within the studied meadow varied in relation to depth and coastal wave-exposure. Moreover, patterns of spatial variability changed with depth. The structure of macro-invertebrate assemblages of Pianosa Island was similar to that described for other P. oceanica meadows, with a dominance of Mollusca and Crustacea (Russo et al. 1984, 1991; Scipione and Fresi 1984; Mazzella et al. 1989, 1992;Gambietal.1992; Scipione et al. 1996; Borg and Schembri 2000;Bedinietal.2011; Belgacem et al. 2011, 2013; Zakhama-Sraieb et al. 2011; Urra et al. 2013). However, differences in patterns of diversity and abundance may be highlighted between the pristine Pianosa assemblages and those described in meadows of the same geographic area but subjected to a higher human pressure (Bedini et al. 1997, 2011). The total number of taxa was higher Journal of Natural History 2573

Table 4. Results of permutational analysis of variance (PERMANOVA) on species composition and abundance of macro- invertebrate assemblages.

Source df MS Pseudo-F P (perm)

Depth = D 2 15755 8.83 0.001 Side = S 2 4086 2.29 0.010 D × S 4 1903 1.06 0.344 Area (D × S) 27 1783 2.47 0.001 Residual 36 722 Total 71 PAIRWISE TEST Depth P (perm) Side P (perm) S, I 0.001 e, s 0.087 S, D 0.001 e, w 0.005 I, D 0.001 s, w 0.054

Notes: S = shallow, I = intermediate, D = deep; e = east, s = south, w = west. Significant effects are indicated in bold. Downloaded by [University of Cambridge] at 05:12 08 April 2016

Figure 4. Non-metric multidimensional scaling (nMDS) ordination on macro-invertebrate assemblages of Pianosa Island. S = shallow, I = intermediate, D = deep; e = east, s = south, w = west.

at Pianosa than in the other meadows of the continental coasts of Tuscany, where three meadows were sampled at three depths with a sampling effort (98 samples) higher than that of the present study (171 taxa at Pianosa Islands vs 136 taxa at 2574 R. Bedini et al. Downloaded by [University of Cambridge] at 05:12 08 April 2016

Figure 5. Percentage pseudo-variance components of mobile macro-invertebrate assemblages of Posidonia oceanica meadow at (a) shallow, (b) intermediate and (c) deep stands.

three other localities of Tuscany, Bedini et al. 1997, 2011). The mean number of individuals and the mean number of species per sample were also higher at Pianosa (193.8 and 18.2, respectively) than in the other Tuscan meadows Journal of Natural History 2575

Table 5. Results of SIMPER (similarity percentages) test showing taxa that mostly contributed to differences among depths and East and West sides of Pianosa Island.

TAXA Av.Abund Av.Abund Contrib%

Shallow Intermediate Diss: 68.6 Bittium latreillii 115.29 79.33 34.31 Hippolyte inermis 11.46 40.88 13.06 Cestopagurus timidus 8.54 18.5 8.21 Chauvetia mamillata 15.08 0.38 6.07 Rissoa auriscalpium 14.71 3.58 5.13 Phtisica marina 0.33 6.67 2.98 Rissoa violacea 4.71 8.33 2.56 Asterina gibbosa 0.29 7.08 2.34 Alvania lineata 5.04 0.63 2.27 Pagurus anachoretus 1.75 4.25 2.23 Siriella clausi 0.04 5.63 2.14 Shallow Deep Diss: 72.9 Bittium latreillii 115.29 42.79 35.7 Cestopagurus timidus 8.54 20.63 8.46 Hippolyte inermis 11.46 23.88 6.79 Chauvetia mamillata 15.08 1.04 5.98 Rissoa auriscalpium 14.71 0 5.58 Asterina gibbosa 0.29 13.54 5.14 Phtisica marina 0.33 8.67 3.53 Rissoa violacea 4.71 8.67 2.73 Alvania lineata 5.04 2.08 2.41 Jujubinus exasperatus 2.33 6.5 2.04 Intermediate Deep Diss: 62.7 Bittium latreillii 79.33 42.79 27.75 Hippolyte inermis 40.88 23.88 12.23 Cestopagurus timidus 18.5 20.63 7.78 Asterina gibbosa 7.08 13.54 5.81 Siriella clausi 5.63 4.5 3.36 Jujubinus exasperatus 1.17 6.5 2.48 Ocinebrina aciculata 2.42 6.04 2.33 East West Diss: 67.8 Bittium latreillii 127.04 40.38 36.29 Downloaded by [University of Cambridge] at 05:12 08 April 2016 Hippolyte inermis 26.88 24.92 10.65 Cestopagurus timidus 19.38 8.83 7.26 Rissoa auriscalpium 11.96 2.42 5.2 Chauvetia mamillata 3.75 6.88 4.07 Asterina gibbosa 7.46 5.79 3.71 Rissoa violacea 8.08 6.75 2.74 2.71 # # Siriella clausi 7.96 0.75 # 2576 R. Bedini et al.

(34.1 and 14.8). The structure of the assemblages was strongly influenced by depth. Depth gradients in the structure of mobile epifauna of seagrasses are widely reported, especially for P. oceanica that can spread along a wide bathymetrical range (Gambi et al. 1992; Borg and Schembri 2000; Belgacem et al. 2011, 2013), even if this pattern does not seem to be consistent throughout the year (Bedini et al. 2011). Depth-related patterns of spatial variability have been interpreted as a consequence of the trophic distribution of invertebrates (Mazzella et al. 1992). In agreement with this model, the SIMPER test showed that herbivorous organisms (Bittium latreillii, Rissoa auriscalpium and Alvania lineata) were normally linked to shallower stands, where algal epiphytes are more abundant (Nesti et al. 2009), while carnivores–detritivores (Cestopagurus timidus, Hippolyte inermis, Phtisica marina, Asterina gibbosa, Siriella clausii) were mostly distributed in the deep parts of the meadow. However, depth-related patterns were also found within each trophic group, as shown by the higher abundance of Jujubinus exasperatus and other herbivores in the deeper stands. This finding highlights that other factors, such as hydrodynamism, temperature and dissolved oxygen (Russo et al. 1984; Scipione and Fresi 1984; Belgacem et al. 2013), may be important in determining changes in the structure of macro-invertebrate assemblages along a depth gradient. Changes in meadow density between shallow and deep stands may also influence mobile macro-invertebrates, both directly, modifying the habitat complexity, and indirectly, causing changes in epiphyte assemblages and in the effectiveness of protection from predators (Heck and Orth 1980;Orth et al. 1984;Gambietal.1998; Attrill et al. 2000; Bostrom et al. 2006; Belgacem et al. 2013). An interesting finding of the study is the differences in patterns of spatial variability among depths. Pseudo-variance components showed an increasing trend from larger to smaller spatial scales in shallow and intermediate assemblages, following a pattern widely reported for benthic assemblages, including seagrass epiphytes (Piazzi et al. 2004; Balata et al. 2007). A high small-scale variability characterises seagrass systems, as a consequence of a patch distribution of organisms related to biotic interactions or habitat heterogeneity (Vanderklift and Lavery 2000; Lavery and Vanderklift 2002). In contrast, the studied deep assemblages showed high variability at an intermediate scale, among areas hundreds of metres apart. Similar changes in spatial variability between shallow and deep meadows have been observed for epiphytic assem-

Downloaded by [University of Cambridge] at 05:12 08 April 2016 blages (Nesti et al. 2009). Differences in meadow structure may determine changes in the associated faunal assemblages at spatial scales similar to that observed in the present study (Parker et al. 2001). However, the studied meadow had a quite uniform structure at the same depths, excluding a similar model. High variability of mobile macro-invertebrate assemblages at small scales in shallow P. oceanica stands has already been described, and is considered related to the more stressful characteristics of a shallow environment as compared to deeper ones (Gambi et al. 1992). Recruitment may also have an important role, as the dispersion of larvae is influenced by water movements and stratification (Witman and Dayton 2001). The decreasing flow velocity with depth in tempe- rate seas (Denny and Wethey 2001) may reduce the connectivity between sites below the thermocline, concurring to increase the variability at this spatial scale (Witman and Dayton 2001). Journal of Natural History 2577

Sand bottom and rocky reefs were present below the deep edge of the meadow, and they could influence P. oceanica faunal assemblages. In fact, both modifications in the structure of assemblages near the deep limit of the meadow and changes in patterns of spatial variability could be related to a possible enrichment by organisms typical of the surrounding habitats (Mazzella et al. 1989; Urra et al. 2013). Some species typical of mobile bottoms (the Crustacea Leucothoe serraticarpa, Eurydice pulchra and Pagurus alatus) and rocky reefs (the Crustacea Leucothoe procera, Dynamene bidentata, the Mollusca Coralliophila meyendorffii and the Polychaeta Syllis gracilis) were found in the deep part of the meadow. The Mollusca Bolma rugosa, typical of bottoms characterised by detritus, was found only in juvenile forms, suggesting a nursery role of meadows for this organism. Moreover, proximity of rocky reefs may influence the intensity of predation and the recruitment of invertebrates, determining important changes in the structure of assemblages (Tuya et al. 2010; Urra et al. 2013). The role of surrounding habitats for P. oceanica invertebrate assemblages was not an aim of this study but may represent a goal for further investigations. Differences in seagrass-associated fauna between edges and the internal part of seagrass meadows has been already described and considered relative to larval settlement patterns, post-settlement processes and accumulation of organisms that are seeking refuge from predation (Virnstein and Curran 1986; Bologna and Heck 2002). These ‘edge effects’ could have a key role in determining the structure of meadow-associated assemblages, and represent an important aspect to be considered in interpreting patterns of variability in studies aiming to distinguish, at a small scale, between natural changes in ecological conditions and those induced by human pressure. Differences in assemblages related to coastal wave-exposure are not easily interpreted. Water movement represents one of the main factors structuring species composition of coastal benthic assemblages. In the study area, the west side is the most exposed to waves. Both wave intensity and the direction of dominant currents can determine changes in the structure of invertebrate assemblages through disturbance, larval dispersion or food supply (Commito et al. 1995; Harriague and Albertelli 2007: Van Colen et al. 2010). Water movements probably determine the main environmental differences among sides of the island, but other abiotic factors, such as light intensity or sedimentation rates, may be related to coastal wave- exposure.

Downloaded by [University of Cambridge] at 05:12 08 April 2016 The study was limited only to one period of the year; thus, it did not take into account seasonal changes of faunal distribution along the bathymetrical range (Gambi et al. 1992;Bedinietal.2011). Despite this limit, the results highlighted important patterns of variability within a P. oceanica meadow, suggesting that different causes, such as shoot density, epiphyte load and distance to other habitats, can determine small-scale changes in the structure of invertebrate assemblages. Results obtained in a very pristine meadow, such as that of the present study, may represent a useful tool to compare macro-invertebrate assemblages associated with meadows subjected to different ecological conditions. In this context, patterns of variability highlighted by the present study may give useful information to be considered in planning sampling designs suitable for separating natural variability within meadows from effects of ecological alterations. 2578 R. Bedini et al.

Acknowledgements We wish to thank the Italian National Research Council (CNR) which supported the study, and T. Krapp-Schickel for the taxonomic determination of Amphipoda.

Disclosure statement No potential conflict of interest was reported by the author(s).

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