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The Impact of Small Benthic Passive Suspension Feeders in Shallow Marine Ecosystems: the Hydroids As an Example

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The Impact of Small Benthic Passive Suspension Feeders in Shallow Marine Ecosystems: the Hydroids As an Example Commemorative volume for the 80th birthday of Willem Vervoort in 1997 The impact of small benthic passive suspension feeders in shallow marine ecosystems: the hydroids as an example Gili, J.-M., V. Alvà, R. Coma, C Orejas, F. Pagès, M. Ribes, M. Zabala, W. Arntz, J. Bouillon, F. Boero & R.G. Hughes Gili, J.-M., V. Alvà, R. Coma, C Orejas, F. Pagès, M. Ribes, M. Zabala, W. Arntz, J. Bouillon, F. Boero & R.G Hughes. The impact of small benthic passive suspension feeders in shallow marine ecosys• tems: the hydroids as an example. Zool. Verh. Leiden 323, 31.xii.1998:99-105, tabs 1-2.— ISSN 0024-1652/ISBN 90-73239-68-0. J.-M. Gili, V. Alvà, R. Coma, C. Orejas, F. Pages & M. Ribes, Institut de Ciències del Mar (CSIC), Plaça del Mar, 08039 Barcelona, Spain. M. Zabala, Departament d'Ecologia, Universität de Barcelona, Avda. Diagonal 645, 08028 Barcelona, Spain. W. Arntz, Alfred-Wegener-Institut für Polar- und Meeresforschung, Columbusstrasse, 27658 Bremer• haven, Germany. J. Bouillon, Laboratoire de Biologie Marine, Faculté des Sciences, Université Libre de Bruxelles, Av. F.D. Roosevelt, Bruxelles, Belgium. F. Boero, Dipartimento di Biologia, Università di Lecce, 73100 Lecce, Italy. R.G. Hughes, School of Biological Sciences, Queen Mary and Westfield College, University of Lon• don, London El 4NS, United Kingdom. Key words: benthic passive suspension feeders; shallow marine ecosystems; hydroids. Benthic suspension feeders are abundant in littoral and shallow sub-littoral ecosystems, where they feed on the plankton and on organic matter suspended in the water column. Recent studies indicate that active suspension feeders with powerful water filtration mechanisms (e.g., bivalve molluscs) may exert an important influence on the abundance and production of phytoplankton, and probably zoo- plankton as well. Passive suspension feeders, such as hydrozoans, have received less attention, and their effect on shallow planktonic communities is poorly understood. This paper presents evidence that hydrozoans, which make only a minor contribution to benthic community biomass, capture large amounts of zooplankton and seston, and that they may play an important role in transferring energy from pelagic to benthic ecosystems over a wide range of latitudes. Recently, assessments of the individual components of food webs within or between different marine ecosystems have been attempted (Margalef, 1978; Paine, 1988; Goldwasser & Roughgarden, 1993). In particular, attention has focused energy transfer between the pelagic and benthic ecosystems (Bonsdorff & Blomqvist 1993). In the open ocean energy transfer flows vertically, gradually descending through the water column, with considerable reduction of surface production by the time it reach• es the bottom (Smetacek, 1984). In contrast, in shallow waters benthic organisms have more immediate access to planktonic production, because of the proximity of the photic layer, and because of tidal or wind vertical mixing. Benthic suspension feeders in shallow marine ecosystems are responsible for a large proportion of the energy flow from the plankton to the benthos (Parsons et al., 1979). For example, benthic organisms that are active suspension feeders, such as bivalves, have been shown to have a major impact on the planktonic ecosystems in which they feed (Jorgensen, 1990). They capture large amounts of phytoplankton and may regulate primary pro• duction directly, and regulate secondary production indirectly (Dame et al., 1980; 100 Gili et al. Benthic suspension feeders in shallow marine ecosystems. Zool. Verh. Leiden 323 (1998) Officer et al., 1982; Cohen et al., 1984). Models of energy flow have ignored passive suspension feeders such as hydrozoans and gorgonians because their impact has been assumed to be minor, on account of their negligible contribution to the biomass of benthic communities (Boero, 1984; Gili & Ros, 1985). It is clear from their diets that some passive suspension feeders, which capture small particles, zooplankters and organic matter, may also play a significant role in pelagic-benthic coupling (Sebens, 1987). Recent data on benthic hydrozoans in a number of different areas around the world have yielded capture rates for hydrozoans of over 105 prey items m"2 day"1 (Coma et al., 1995). This high level of feeding fuels the high rates of growth and reproduction shown by modular hydrozoans (Hale, 1973; Coma et al., 1996). This paper reviews the recent literature and presents the case that passive suspension feeders, even the most inconspicuous organisms such as hydrozoans, need to be taken into account when assessing energy flow into shallow benthic assemblages. In our recent studies of the feeding of benthic hydroids samples were taken regu­ larly, every 2 to 4 h over 24h periods. On each occasion a minimum of 50 hydranths were dissected and all the items present in the gastric cavity were identified and mea­ sured. Prey biomass was estimated and the mass-specific ingestion rate was calculat­ ed, as the percentage ratio between prey biomass ingested daily and hydranth bio­ mass. The dry weight of hydranths was measured by drying several replicates of 100- 200 hydranths to constant weight at 70° C. Daily capture rates (mean prey number hydranth"1 day"1) were calculated for each species on the basis of the number of items per hydranth sampled and prey digestion times (Gili et al., 1996a). Digestion times were studied in situ using incubation chambers or were estimated from other studies. Capture rates, mean number of prey items m"2 day'1, were estimated on the basis of the natural density of the species considered. To determine the composition and rela­ tive abundance of potential prey items, concurrent plankton samples were taken from around the hydrozoans (Coma et al., 1995). Table 1 presents the results for all the species. The diet of most species was varied, consisting largely of algal cells (e.g. Nemalecium lighti) and zooplankton (e.g. Eudendri­ um racemosum or Tubularia larynx). In some species particulate organic matter (POM) also contributed a significant portion of the diet (e.g. Campanularia everta = Orthopyxis crenata). Benthic organisms (e.g. nematodes or small bivalves) were found only occa­ sionally. The diet of Silicularia rosea was almost exclusively benthic diatoms, captured when the bottom sediment was disturbed and resuspended. The results confirm that benthic hydroids can feed on a great variety of prey. Apart from zooplankton they can feed on Bacteria, Protozoa, phytoplankton, detritus, and even on metabolites of algal origin or dissolved organic matter (see Bouillon, 1956-57; 1995). The maximum size of the prey ingested varied between species. Hydrozoans that fed on zooplankton, e.g., E. racemosum and T. larynx, were able to capture large prey items because the mouth of the hydranths is able to expand. The mean size of E. race­ mosum hydranths was 600 μιη (table 1), but this hydrozoan was able to capture crus­ taceans of up to 1000 μ m in size. The prey size in hydrozoans that fed on algal cells (e.g. S. rosea and N. lighti) did not exceed 50 μιη. The numbers of prey items per hydranth of Obelia geniculata, T. larynx and E. race­ mosum were proportional to the density of potential prey in the habitat, and conse­ quently the capture rates were highest when zooplankton abundance in the water Table 1. Different trophic features analysed for six species of hydroid following the same experimental methodology: for each species two diel cycles, collect­ ρ ed every 2 or 4 h, and a minimum of 1200 polyps per species, were examined (polyp size: diameter of expanded tentacle crown). Et Si­ Silicularia rosea Nemalecium lighti Campanularia everta Eudendrium racemosum Tubularia larynx Obelia geniculata σα 3 Meyen, 1834 (Hargitt, 1924) Clarke, 1876 (Cavolini, 1785) Ellis & Solander, 1786 (Linnaeus, 1758) §- η S Geographic area King George I. Panama Catalonia Catalonia Scotland Arauco Gulf •3 (South Shetland Is) (Caribbean Sea) (NW Mediterranean) (NW Mediterranean) (NE Atlantic) (SE Pacific) § Polyp size (mm) 0.4 0.3 0.25 0.6 1­1.2 0.3 cr» Habitat Tide pools Sublittoral Sublittoral Sublittoral Sublittoral Sublittoral Growth form reptant reptant reptant erect erect reptant/erect δ' Life cycle no medusa no medusa with medusoid form no medusa with well with well developed medusa developed medusa Ci­ Dominant prey Diatoms (95) Diatoms (32) POM (88) Copepod eggs (28) Copepod eggs (28) Faecal pellets (48) S s- (mean % of the diet) Eggs (2) POM (21) Copepod eggs (7) Copepod adults (22) Copepod adults (22) Copepod eggs (29) s- Invertebrate Invertebrate Cladocera (21) Diatoms (17) CD larvae (20) larvae(10) î Mean prey size 38.6 ± 0.32 50 54.8 350 710 47.7 3 (in μπι) and range (9.7­436.5) (5­325) (6­110) (40­1050) (520­930) (20­420) Observed mean prey 61.2 ±6.7 3.5 4.4 2.5 3.4 9.3 su number hydranth"1 * (818) (14) (8) (9) (26) (40) Estimated mean prey 225.8 35.7 18.6 5.4 36.0 ** 124.2 ** n> number hydranth"1 day"1 26.1 ** 8 «53 Estimated mean prey 4.4 χ 106 3.97 χ 105 4.3 χ 105 1.2 xlO5 4.5 χ 105 3.2 χ 106 3 number m"2 day"1 mg C removed m"2 day"1 66 6 6.4 12 225 48 Prey biomass hydranth"1 0.18 2.4 0.3 0.4 8.5 28.1 I day"1 (in μg) $ Diel mass­specific 12.6 136 19 39.1 89.9 113.2 3­ E* ingestion rate (in %) α 3 * Maximum prey number observed. 8 **Prey capture during reproductive period 00 H­k ο 102 Gili et al. Benthic suspension feeders in shallow marine ecosystems. Zool. Verh. Leiden 323 (1998) column was highest. The highest diel capture rates were recorded in O. geniculata, which inhabits the most productive waters of all the species studied.
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