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Evaluation of Sediment Particle Size Selection During Feeding by The 1 2 3 1 Evaluation of sediment particle size selection during feeding by the holothurian 4 5 6 2 Parastichopus regalis (Cuvier, 1817) 7 8 3 9 10 4 Montserrat Ramón*, Gonzalo Simarro*, Eve Galimany, Jordi Lleonart 11 12 5 Marine Sciences Institute (ICM-CSIC) 13 14 6 Passeig Marítim de la Barceloneta 37-49, 08003, Barcelona (Spain) 15 16 7 17 18 8 19 20 9 M. Ramón (Corresponding Author) e-mail: [email protected] 21 22 10 G. Simarro e-mail: [email protected] 23 24 25 11 E. Galimany e-mail: [email protected] 26 27 12 J. Lleonart e-mail: [email protected] 28 29 13 (*) The authors contributed equally to this work. 30 31 14 32 33 15 Abstract 34 35 16 Parastichopus regalis is an epibenthic holothurian common in the 36 37 17 Mediterranean Sea and the NE Atlantic, which feeds on the upper layer of the sediment 38 39 18 playing a significant role on soft-bottom dynamics. Whether or not P. regalis is able to 40 41 42 19 select the sediment ingested by size is the question of this study. For this purpose, a 43 44 20 comparison between grain size distributions of the seabed sediments and the digestive 45 46 21 contents of sea cucumbers were carried out. We performed the comparisons among 47 48 22 sediment distributions through the median diameter D 50 and the granulometric 49 50 23 dispersion D 84 /D 16 . The results showed that the size of the sediment within the 51 52 24 holothurians was significantly smaller and more uniform than the ones in the seabed. 53 54 25 Evidence showed that P. regalis select sediment by particle size during feeding, 55 56 57 58 59 60 61 62 26 choosing the smaller particles. This finding reports novel information on the feeding 63 64 65 27 behaviour of this species, a fishery resource of local interest and importance in the 66 67 28 Western Mediterranean region. 68 69 29 70 71 30 Key words: Holothurian; feeding; grain size selection; Mediterranean Sea 72 73 31 74 75 32 1. Introduction 76 77 33 Holothuroidea is a conspicuous and diverse group of invertebrates in the worlds 78 79 34 oceans. Aspidochirotid holothurians provide important ecosystem services enhancing 80 81 35 nutrient cycling and sediment dynamics through their feeding activities and bioturbation 82 83 84 36 (Uthicke, 1999) . Most species live on the sea bottom surface, where they ingest the 85 86 37 upper layer of sediment from which they assimilate a fraction of its organic matter 87 88 38 content. The capture of food is made with the tentacles, provided with contractile and 89 90 39 adhesive elements on its surface. During feeding, the tentacles extend over the 91 92 40 substratum, collect the particles, and contract and fold into the mouth to release the food 93 94 41 (Roberts et al., 2000). 95 96 42 Bottom sediment characteristics, hydrodynamics, and depth are crucial factors 97 98 43 affecting habitat preference of sea cucumbers (Sloan and Von Bodungen, 1980; Slater 99 100 101 44 and Jeffs, 2010; Dissanayake and Stefansson, 2012). Sediment characteristics have a 102 103 45 direct influence in feeding particle selection, which may be based on sediment grain size 104 105 46 or organic-rich content, depending on species and habitats (Roberts, 1979). For 106 107 47 example, no evidences of selectivity by size were found in Parastichopus parvimensis 108 109 48 (Yingst, 1976), Holothuria mexicana, H. arenicola (Hammond, 1982), Leptosynapta 110 111 49 tenuis (Powell, 1977), H. atra (Massin and Doumen, 1986), and Isostichopus 112 113 50 badionotus (Sloan and Von Bodungen, 1980; Hammond, 1982). Coarser grain sizes 114 115 116 117 118 119 120 121 51 tend to be excluded by H. atra , Bohadschia marmorata , and H. leucospilota (Massin 122 123 124 52 and Doumen, 1986; Dar, 2004). In addition, the burrower sea cucumber Molpadia 125 126 53 oolitica preferred smaller grain sizes (Rhoads and Young, 1971). On the contrary, 127 128 54 selection for larger grain sizes have been found in Stichopus tremulus (Hauksson, 1979) 129 130 55 and Holothuria scabra (Baskar, 1994). Grain size selection varies between species and 131 132 56 has been proposed as an important resource to establish niche separation between co- 133 134 57 existing deposit feeders (Massin and Doumen, 1986; Mezali and Soualili, 2013). For 135 136 58 instance, analyses of the digestive contents of the holothurian species H. tubulosa , H. 137 138 59 poli and H. stellate revealed that these ingested coarse and fine sediment, whereas H. 139 140 60 forskali and H. sanctori selected fine and very fine sediment (Mezali and Soualili, 141 142 143 61 2013). The size of the particles ingested influences the time needed for the holothurian 144 145 62 gut to efficiently extract the organic matter (Hudson et al., 2004), with implications in 146 147 63 the amount of sediment reworked by the holothurians and, by extension, in the 148 149 64 evaluation of their role in the ecosystems. 150 151 65 The importance of sea cucumbers in reworking muddy and sandy bottoms has 152 153 66 long been emphasized. Much of the work carried out worldwide on holothurian feeding 154 155 67 has been focused on shallow water species, mainly on tropical reefs, for its easy 156 157 68 accessibility and the high diversity of species (Yingst, 1976; Hauksson, 1979; Navarro 158 159 160 69 et al., 2013) . Knowledge on the feeding of deep-sea holothurians has increased recently 161 162 70 given the improvement of deep-sea exploration methods, highlighting the abundance of 163 164 71 sea cucumbers in such ecosystems (Wigham et al., 2003; Hudson et al., 2005; Navarro 165 166 72 et al., 2013). Nevertheless , information on holothurian species inhabiting the continental 167 168 73 shelf below 50 m depth is scarce. The sea cucumber Parastichopus regalis (Cuvier, 169 170 74 1817) belongs to the family Stichopodidae and is abundant in the Mediterranean Sea 171 172 75 and the NE Atlantic, between 50 and 300 m depth (Ramón et al., 2010). Its five 173 174 175 176 177 178 179 180 76 longitudinal muscle bands are commercialized for human consumption in Catalonia 181 182 183 77 (NW Mediterranean), where it is captured using bottom trawls (Ramón et al., 2010). 184 185 78 Despite its ecological and economic importance, there is little information on its basic 186 187 79 ecology. Understanding habitat use of P. regalis by studying feeding selectivity is a 188 189 80 necessary step towards the knowledge of its ecological role in the Mediterranean 190 191 81 continental shelf. 192 193 82 The aim of this study is to find out whether the sea cucumber P. regalis is able 194 195 83 to select the sediment ingested by size and, if so, to elucidate if selection is affected by 196 197 84 particle size availability. For this purpose, we compared the grain size distribution of the 198 199 85 ambient sediments to that of the gut sediments in situ. The statistical treatment of the 200 201 202 86 sediment grain distributions takes into account the particularity of the data set (each data 203 204 87 is a distribution of the sizes of the sediment). 205 206 88 207 208 89 2. Materials and Methods 209 210 90 2.1. Sampling 211 212 91 Specimens of Parastichopus regalis were collected on board a commercial 213 214 92 trawler from Arenys de Mar (41.5768°N, 2.5593ºE, NW Mediterranean) using a bottom 215 216 93 otter trawl operating around 100 m depth. They were transported to the laboratory in 217 218 219 94 coolers with sea water. On arrival, the sea cucumbers had ejected their internal organs, 220 221 95 making it impossible to perform feeding experiments in tanks therefore forcing a new 222 223 96 experimental approach, an in situ study. Then, sediments were collected on the 224 225 97 fishing ground, at the same time as sea cucumbers, using a stainless steel cylinder 226 227 98 coupled to the fishing gear (Del Rio et al., 2012) . This methodology has been 228 229 99 demonstrated to collect superficial sediment, which is where the sea cucumbers feed on 230 231 100 (Rufino et al., 2018) . Once on board, holothurians were dissected, the gut extracted and 232 233 234 235 236 237 238 239 101 placed individually in plastic bags to be transported to the Institute of Marine Sciences 240 241 242 102 (ICM-CSIC) in coolers with ice. A sample of 50g of sediment from each haul was kept 243 244 103 on board and stored in the fridge after returning to the laboratory. 245 246 104 Five daily surveys were performed in 2013 in the fishing ground of Arenys de 247 248 105 Mar. A total of eleven hauls were carried out at depths between 82 and 129 m. In 249 250 106 addition, a sediment sample from a trawl belonging to the oceanographic cruise 251 252 107 MEDITS_ES_CAL_13 on the Ebro river shelf (40.2983ºN, 01.2682ºE, NW 253 254 108 Mediterranean ) was added in order to analyze a different area. A total of 121 specimens 255 256 109 were analyzed (Table 1). 257 258 110 259 260 261 111 2.2. Sediment analysis 262 263 112 Sediment samples analyzed included 12 samples of seabed (one for each case in 264 265 113 table 1) and 121 of holothurians gut content, which allowed to perform a total of 133 266 267 114 analyses. Sediment was treated for size particle analysis, i.
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