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          establishment 33,47 , a suitable microsite is then expected to provide  Favignana and Capo Feto seedlings were anchored on bedrocks covered by
          shelter from the drag forces acting on the seedlings and/or to increase  macroalgal turf and Cystoseira spp. stands or laid down on sand. With the exception
                                                              of those collected on sand - that were not anchored- all seedling offered a resistance
          the seedling anchoring ability. It can be hypothesized that hard sub-
                                                              when collected as they were attached to the substrate. We conducted a specific
          strates have higher potential compared to soft ones to provide suit-  measurement of the seedling anchorage strength in October 2009 at Ustica, on
          able microsite for P. oceanica seedling establishment due to the  specimens settled at a depth of approximately 3 m on volcanic cobbles, no seedlings
          presence of adhesive root hairs. Hence, a new microsite driven bottle-  were recorded on other substrates in this occasion.
          neck in P. oceanica seedling survival linked to substrate features can
                                                              Morpho-anatomical and ultrastructural analyses. Morpho-anatomical and
          be forecasted (Fig. 5). To test this hypothesis a specific manipulative
                                                              ultrastructural analyses were performed on seedlings collected between June and July
          experiment contrasting seedling recruitment success on hard vs soft  at Ustica (1997), Favigana (2004) and Capo Feto (2004), where possible without
          substrates should be run.                           separating the seedlings from the substrate. Seedlings were transported to the
           Settling on rocky habitats rather than on sand might have negative  laboratory, photographed using a stereomicroscope, and fixed in a 5% buffered
          effects on seedlings survival due to predation by the main consumers  formalin/seawater solution. Seed size, number of roots, maximum root length, total
                                                              number of leaves produced from germination, maximum leaf length and width were
          of P. oceanica, namely the sea urchin Paracentrotus lividus (Lamarck,  recorded (n 5 12 at each location). Variation among locations was tested for each
                                               48
          1816) and the sparid Sarpa salpa (Linnaeus, 1758) . It has recently  variable using one-way ANOVA.
          been shown that P. oceanica patches growing on rocky matrix are  Subapical sections of adventitious roots were obtained from specimens collected at
          more vulnerable to herbivores than those growing on sandy  Ustica (1997) on bare cobbles and at Capo Feto on rocks covered by algae and on sand
                                                              (2004). Root sections were dehydrated in a tertiary butyl alcohol series and processed
               49
          patches . However, the canopy provided by seedling is smaller if  in paraffin. Next, the samples were mounted on SEM stubs, sputter-coated with gold,
          compared to that provided by P. oceanica patches or Cystoseira  and examined using a Leica 5420 SEM at a 15 KV operating voltage to analyse
          spp. forests, therefore sea urchins might not find suitable refuges  morpho-anatomical features of seedling roots and root hairs. Root-hair length and
                                                 49
          there, remaining exposed to higher risk of predation . Although S.  width and hair-tip morphology and width were recorded (n 5 12).
                                                               Structures observed under the stereomicroscope and SEM were compared with
          salpa bite marks can be found on P. oceanica seedling leaves no
                                                              those reported in the literature for seedlings of P. oceanica and for other aquatic
          evidence of grazing by this herbivore on P. oceanica seedlings was  phanerogams.
                                        25
          found in a predator exclusion experiment . Moreover, sites charac-  To obtain a first chemical characterization of the adhesive substance covering root
          terized by the presence of turf usually record a higher sedimentation  hairs, the whole mounts of seedling roots were stained with Periodic acid-Schiff (PAS)
                                  50
          rate than in Cystoseira spp. forest and represent an obstacle for P.  to search for the presence of polysaccharides and glycoproteins.
                       51
          lividus movement . It can be hypothesized that seedlings recruiting  Measurement of anchorage strength. The anchorage strength was measured on
          on turf may thus experience a microsite where sea urchins are less  seedlings settled on bare volcanic cobbles at Ustica Island in October 2009. Twelve
                            51
                 52
          abundant , move slowly and a desirable amount of sediment is  cobbles (greatest diameter: mean 16.50 6 0.60 SE cm), each with an attached seedling,
              50
          found . Specific manipulative experiments should be run to dis-  were haphazardly chosen and carefully moved from the seafloor into 50 l plastic
          entangle the relative importance of the nature of substrate (e.g. vege-  boxes on board the research vessel. The force needed to detach seedlings from the
                                                              substrate was immediately measured and used as a proxy for anchorage strength. A
          tated and not vegetated rocky bottoms, sand, etc.) in the presence or  hook-shaped plastic-coated iron wire 3 mm in diameter was carefully passed
          absence of herbivores.                              underneath the seed body. One end of the wire was connected to a digital spring scale
           The results of the present study have far-reaching ecological impli-  (Vetek, precision 5 g). Measurements (n 5 12) were taken by pulling the seedling
          cations as they provide new insight into the habitat preferences of P.  perpendicular to the substrate until detachment while an operator kept the cobble still
                                                              at the bottom of the box. The pull weight was converted to force (Newtons). Seedlings
          oceanica juveniles, the colonisation potential and distribution of this  were then transported to the laboratory and stored frozen for morphological analysis
          species and its role in successional series. P. oceanica, described in  (seed size, number of roots, maximum root length, total root length, total number of
          historical literature as a species mainly growing on sandy bot-  leaves produced from germination, maximum leaf length and width).
          toms 11,13 , is shown here to be able to colonise bare rocky substrates
          without the need for precursor assemblages, in contrast with tra-
                                                              1. den Hartog, C. The Sea-grasses of The World. (North-Holland, Amsterdam, 1970).
          ditional paradigms. Moreover adhesive root hairs appear to repres-  2. Les, D. H., Cleland, M. A. & Waycott, M. Phylogenetic studies in alismatidae, II:
          ent an adaptive advantage for early seedling establishment on hard  Evolution of marine angiosperms (seagrasses) and hydrophily. Syst. Bot. 22,
          substrates over the sandy ones.                       443–463 (1997).
           In seagrasses that produce large, fleshy fruits with high dispersal  3. Kuo, J. & den Hartog, C. Seagrass Morphology, Anatomy and Ultrastructure. In:
                                                                Seagrasses: Biology, Ecology and Conservation (eds. Larkum, A. W. D., Orth, R. J. &
          capabilities such as the species belonging to the genus Posidonia,  Duarte, C. M.) 51–87 (Springer, Dordrecth, 2006).
          sexual propagation represents the colonisation strategy that acts over  4. Short, F. T., & Coles, R. G. (eds.)Global seagrass research methods. (Elsevier,
          larger spatial scales (hundreds of kilometres, according to Kendrick  Amsterdam, 2001).
             53
          et al. ), and seedlings are expected to be responsible for the initial  5. Cooper, L. W. & McRoy, C. P. Anatomical adaptation to rocky substrates and surf
                                                                exposure by the seagrass genus Phyllospadix. Aq. Bot. 32, 365–381 (1988).
                               54
          establishment of the meadow . The strong anchorage displayed by P.
                                                              6. Tomlinson, P. B. Anatomy of the Monocotyledons. VII. Helobiae (Alismatidae).
          oceanica seedlings on hard substrates provided by adhesive root hairs  (Clarendon Press, Oxford, 1982).
          leads us to predict a more successful recruitment by sexual propa-  7. Barnabas, A. D. Anatomical, histochemical and ultrastructural features of the
          gules on hard bottoms respect to the soft ones, in accordance with the  seagrass Phyllospadix scouleri Hook. Aq. Bot. 49, 167–182 (1994).
          findings of several studies 24,26,27,28 . If this hypothesis would be con-  8. den Hartog, C. & Kuo, J. Taxonomy and Biogeography of Seagrasses. In:
                                                                Seagrasses: Biology, Ecology and Conservation (eds. Larkum, A. W. D., Orth, R. J.
          firmed, we could reasonably expect that the patterns of colonisation
                                                                & Duarte, C. M.) 1–23 (Springer, Dordrecth, 2006).
          by sexual propagules of this species have been strongly influenced by  9. Pasqualini, V., Pergent-Martni, C., Clabaut, P. & Pergent, G. Mapping of
          the availability and distribution of hard substrates at the regional and  Posidonia oceanica using aerial photographs and side-scan sonar: Application off
          basin scale. This, in turn, could shed light on current and historical  the islands of Corsica (France). Estuar. Coast. Shelf S. 47, 359–367 (1998).
          patterns of recolonisation, such as after the last Pleistocene ice age ,  10. Vassallo, P. et al. The value of the seagrass Posidonia oceanica: A natural capital
                                                          55
                                                                assessment. Mar. Poll. Bull. 75, 1, 157–167 (2013).
          when populations persisting in relict zones began to spread to suit-  11. Molinier, R. & Picard, J. Recherches sur les herbiers de Phane ´rogames marines du
          able areas after the subsequent sea level rise.       littoral me ´diterrane ´en français. Ann. Inst. oce ´anogr. 27, 3, 157–234 (1952).
                                                              12. Pe ´re `s, J. M. Major Benthic Assemblages. In: Marine Ecology. A Comprehensive
                                                                Integrated Treatise on Life in Oceans and Coastal Waters (ed. Kinne, O.) 821–995
          Methods                                               (Wiley-lnterscience, New York, 1982).
          Study area. Observations were made on P. oceanica seedlings found along the  13. Boudouresque, C. F. & Meinesz, A. De ´couverte de l’herbier de Posidonies. Cahier
          northwestern and western coasts of Sicily (Italy) at Favignana Island (37u559590N;  du Parc Naturel de Port-Cros 4, 1–79 (1982).
          12u199130E), Ustica Island (38u43900N; 13u119180E) and Capo Feto (37u399200N,  14. Pe ´re `s, J. M. & Picard, J. Nouveau Manuel de Bionomie Benthique de la Mer
          12u32970E). Seedlings were collected in July 1997 at Ustica and in June and July 2004  Me ´diterrane ´e. Rec. Trav. Stn. Mar. Endoume 47, 31, 1–137 (1964).
          at Favignana and Capo Feto in shallow waters (1–3 m). At Ustica seedlings were  15. Marba `, N. & Duarte, C. M. Rhizome elongation and seagrass clonal growth. Mar.
          anchored on large cobbles, on Cystoseira spp. stands or laid down on sand. At  Ecol.-Prog. Ser. 174, 269–280 (1998).
          SCIENTIFIC REPORTS | 5 : 8804 | DOI: 10.1038/srep08804                                               5
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