The role of pelagic-benthic coupling in structuring littoral benthic communities at Terra Nova Bay ( Ross Sea ) and in the Straits of Magellan *

In Antarctic and peri-Antarctic regions, benthic communities are persistent in time and show high biomass and large numbers of individuals, mainly consisting of suspension and deposit feeders. In fact, apart from recruitment, the major factor structuring these communities is the high flow of organic matter from the pelagic domain to the bottom, representing an important energy source for the benthic organisms. The aim of this paper is to review, compile and compare the data from earlier investigations in Terra Nova Bay (Ross Sea) and the Straits of Magellan, in order to come to a more general conclusion about the role of the pelagic-benthic coupling in structuring littoral benthic communities in southern coastal areas. Few measurements of flux rates and the biochemical composition of the sinking particles occurring in Antarctic and peri-Antarctic shallow waters are available, but a compilation of our own data and others allows a comparison of these two systems. The different environmental conditions between Antarctica and the Straits of Magellan lead to differences in the origin of the particulate organic matter and in its biochemical composition, and consequently in the coupling between pelagic and benthic domains. At Terra Nova Bay the summer particulate matter shows a high labile fraction of a good food value: its flux has been evaluated at about 0.67 g m-2d-1. Conversely, the Straits of Magellan show multi-structured ecosystems where the quality and quantity of the organic matter flux towards the bottom change according to the local geomorphology and current dynamics. Moreover, the three-dimensional assemblages of suspension-feeders, so common in Antarctic shallow waters, seem to be absent in the Magellan area. In particular sponges, gorgonarians and bryozoans play a secondary role inside the Straits of Magellan, where polychaetes (60%) and molluscs (9-10%) are dominant on soft bottoms, and where they reach high values in density and biomass. Bivalves seem to play an important role in both regions: for instance, at Terra Nova Bay, the scallop Adamussium colbecki processes about 14 % of the total carbon flux, with an assimilation efficiency of 36 %. This scallop seems to be able to adapt its reproductive period and its trophic behaviour to the changes in the quality and quantity of the pelagic events. The pulsing trend of the vertical flux, which in a few weeks can reach the total annual input, produces significant changes in the physiology (growth, reproduction, spawning) and trophic behaviour of many benthic species, such as sponges and polychaetes. The study of the pelagic-benthic coupling could be essential in the evaluation of the trophic capacity and the environmental response around sites of sea-farming, which are an ever-growing activity in the Magellan area.


INTRODUCTION
In high productive marine areas, the major biological factor structuring benthic communities, excluding recruitment, is the flow of organic matter from the pelagic domain to the bottom.It may represent the main energy source for the heterotrophic benthic organisms (Graf, 1992).This is particularly true in Antarctica (Grebmeier and Barry, 1991), as well as in the Arctic, where the primary production, higher in coastal waters (83-170 g C m -2 y -1 ) and over continental shelves than in oceanic waters (26 g C m -2 y -1 ; Wefer et al., 1988), occurs in a short summer time, with blooms of Phaeocystis (Palmisano et al., 1985;SooHoo et al., 1987) and/or diatoms (Krebs, 1983).
The influence of the organic matter in the water column on the benthos has been evidenced at McMurdo Sound: Dayton and Oliver (1977) observed strong quantitative and qualitative differences in the soft-bottom communities living in areas influenced by oligotrophic currents flowing from beneath the Ross Ice Shelf and those influenced by more eutrophic waters, flowing southward.
Several studies have been carried out on particle flux and sedimentation in Antarctica (Wefer et al., 1988;Peinert et al., 1989;Smetacek et al., 1990;Grebmeier and Barry, 1991;Knox, 1994).However, despite the great importance of the primary production as food supply in littoral and ice-covered waters, few measurements of the flux rate and the biochemical composition of the sinking particles are available from Antarctic and peri-Antarctic littoral areas.
In the shallow waters of Terra Nova Bay (Ross Sea), Fabiano et al. (1996;1997) found that the amount of total suspended matter (TSM) reaching the bottom during the summer (generally 30-40 days) can rise to 14 g m -2 d -1 , practically 97% of the total flux as, during all other months, it is about 10-100 times lower.This pulsing input supports numerous littoral benthic communities which are persistent in time, showing high biomass and large numbers of individuals.They are mainly constituted by deposit-and active and passive suspension feeders (sponges, bivalves, polychaetes, echinoderms), whose trophic strategies are strongly related to the flux occurring in the water column.
The aim of this paper is to compare the different environmental conditions occurring at a shallow water site in Antarctica (Terra Nova Bay, Ross Sea) and in the Straits of Magellan, paying particular attention to possible adaptations of suspension-feeders to face changes in the flux rates.Moreover, the Straits of Magellan, a peri-Antarctic area, show environmental conditions so different from those generally found along the Antarctic coasts, to be a significant place to study these phenomena under completely different hydrodynamic forces.

PELAGIC-BENTHIC COUPLING IN TERRA NOVA BAY
In Terra Nova Bay phytoplankton blooms occur during and immediately after the pack-ice melting (Fabiano et al., 1997).Significant differences can arise, linked to the annual sea-ice cover variation 114 R. CATTANEO-VIETTI et al.
Palabras clave: Antártica, Estrecho de Magallanes, acoplamiento pelágico-bentónico.and upper layer stratification, e.g., if the pack-ice melting starts early in the season, and a second bloom occurs at the beginning of February.During the summer, inshore primary production at Terra Nova Bay can be evaluated as an average value of about 2-3 mg C m -3 h -1 , but it is also important to take into account that, for a few days, the sympagic algae can reach the impressive primary production of about 500 mg C m -3 h -1 with biomass values ranging about 1-7 g Chl-a m -3 and making a heavy contribution to the final flux (Lazzara et al., 1995).
Another organic source comes from the benthic algae.Between 3 and 10 m depth, Iridaea cordata reaches a density of 4,336 plants m -2 in January, but the highest biomass value (about 3.5 kg m -2 WW), at the beginning of summer, suggests that it also grows, although at a low rate, during the Antarctic winter.Deeper, from 10 to 25 m, Phyllophora antarctica forms dense and expansive beds, reaching its highest density and biomass values (about 10,000 plants m -2 , 1.5 kg m -2 WW, respectively) at the end of January (Cormaci et al., 1996).
Moreover, all the bottoms, down to 150-200 m depth, show a patchy distribution of highly dense seasonal populations of benthic diatoms, revealed by greenish layers seen using a ROV.Their biomass ranges from 4 to 80 µg Chl-a g -1 , with an average value of around 10 µg Chl-a g -1 (A.Pusceddu, pers.comm.).
In January the intense flux of living diatoms, organic matter and fecal pellets can reach 0.69 g POC m -2 d -1 .The high values of TSM/POC sometimes recorded in the same period (Fabiano et al., 1997) depend on the large amount of inorganic matter due to eolic input, which varies greatly (3-300 g m -2 y -1 ) according to the distance from the rocky outcrop.
All these species play a key role in transferring energy from the water column to the benthos, a behaviour that allows them to reach high biomass values.For example, considering the average filter-ing rate of Adamussium colbecki, of about 1 l h -1 g -1 DW soft tissues, and the biodeposition rate, measured as faecal pellet production, of about 5-6 mg DW g -1 DW soft tissues d -1 (Chiantore et al., 1998), it is possible to estimate that the C org flux, through A. colbecki towards the bottom, is about 21 mg C m -2 d -1 .Locally this scallop may process about 14 % of total carbon flux from the water column to the sediments, with an assimilation efficiency of 36 % (Fig. 2).A large part of the flux is also utilized by bacterial communities, with densities (n g -1 ) varying between 8.7 * 10 5 and 1.56 * 10 8 with an average biomass of 8.3 µg C g -1 (A.Pusceddu, unpublished data; Fabiano et al., 1995).
The summer food supply increase may influence the life cycle of many benthic species: the comparison between the gonado-somatic indices in Adamussium colbecki populations in December and in January shows, in fact, that sexual maturity is reached late in summer, closely linked to the phytoplankton bloom (Chiantore et al., 1998).
The flux of organic matter, being quantitatively variable during the year, could represent a metabolic constraint for suspension feeders when the winter oligotrophic condition occurs (Matsuda et al., 1987).But suspension-feeding communities are persistent in time and they do not seem to show significant differences between summer and winter, when the maximum oligotrophy is reached.All this could be faced and overcome thanks to different adaptations with a change of the trophic behaviour during the year (Barnes and Clarke, 1994).
Suspension-feeding polychaetes could easily become deposit feeders, while the large bivalve Adamussium, using clapping activities, seems to be able to resuspend the sunken organic matter (Chiantore et al., 1998).In this species, it is also possible to note a change in its behaviour: the juveniles are bissally attached on the free adults and use the organic matter resuspended by the clapping of the adults (Ansell et al., 1998).Other forms of epibiosis, adopted by serpuloids, bryozoans, holothurians and ophiuroids, are frequent in well structured communities and could be considered an adaptation to find better feeding conditions above the seafloor (Arntz et al., 1994).
Another example of change in the trophic strategy to overcome the oligotrophic period and to face the severe fluctuations in food availability in the environment has been described in sponges.Many demosponges take up and store planktonic and benthic diatoms by phagocytic activity (Gaino et al., 1994).This new functional adaptation is confirmed by the high Chl-a and Chl-c values extracted from several sponges collected from Terra Nova Bay at 80-120 m depth (Cattaneo-Vietti et al., 2000).
Particularly rich and 3-dimensionally structured communities (Fig. 3) develop in areas characterized by the presence of sponge spicule mats (Dearborn, 1967;Koltun, 1968;Dayton et al., 1974;Barthel, 1992): the amount of Chl-a, biomass and species richness increase in comparison with spicule-free sediments.A possible explanation is the fact that sponge spicules, creating a 3-D substratum, favour diatom population development, probably supported by the capacity of the opale spicules to channel light as natural optical fibres (Cattaneo-Vietti et al., 1996).

PELAGIC-BENTHIC COUPLING IN THE STRAITS OF MAGELLAN
In contrast to the rather uniform environment at Terra Nova Bay, the Straits of Magellan, a 570 km long V-shaped channel between Southern Patagonia and Tierra del Fuego, show a complex geomorphology, turbulent tidal currents, different precipitation rates and fresh water inputs.No studies on the pelagic-benthic coupling in this area have been made, but available data regarding some water column parameters (TSM, Chl-a, POC, C:N) suggest that it may be considered as a multi-structured system with strong spatial differences in the composition and origin of the particulate organic matter.Thanks to the rich variety of sills and shelves, it is possible to distinguish at least three well defined sectors (Fig. 4): the Angosturas connect the Straits with the Atlantic and are characterized by a series of narrows and bays in which tidal amplitudes vary from 8 to 1.5 m and the shallow bottoms (30-50 m) are mainly constituted by gravel; Paso Ancho represents the wider part of the channel, characterized by mud and sandy mud bottoms and a maximum depth of 400 m; and the Pacific section, from Cabo Froward to the Pacific, shows depths down to 1100 m and is characterized by important glacio-fluvial runoff constituting coarse sediments.
These sectors have different hydrological and trophic characteristics.The Angosturas are dominated by resuspension processes due to the strong currents (4.5 m sec -1 ), consequently TSM is high (> 2mg l -1 ), TSM/POC high (16.36)and the quality of the organic matter is generally poor, as suggested by the high ratio between C and N (C:N > 7; Carrada et al., 1994).
In the third area, towards the Pacific Ocean, the particulate matter is characterized by large amounts of heterotrophic detritus (0.36 Chl-a µg l -1 ) of quite low energetic value (C:N = 6.07;Carrada et al., 1994).
Considering the different hydrodynamic conditions, the quantity and the biochemical composition of the organic particulate matter of the considered sectors, it is reasonable to suppose that important biological coupling processes may occur mainly in Paso Ancho.

CONCLUSIONS
In the shallow waters of Terra Nova Bay, the lack of physical disturbance (excluding occasional events such as anchor ice and scouring) favours the development of well-structured benthic communities which depend mainly on the pulse-like particulate organic matter flux.If the environmental conditions are favourable, it supports a strong development of suspension-feeding communities, dominated at different depths by sponges, bivalves, brachiopods, polychaetes and echinoderms.This vertical flux (Fig. 1), which in a few weeks can reach the total annual input, produces significant changes in the physiology (growth, reproduction, spawning) and in the trophic behaviour of many benthic species.Finally, seasonally restricted availability of food may force organisms to save energy by adopting low metabolic rates and slow growth, while many suspension-feeding species seem to be able to take advantage of smaller size particles or to shift to deposit-feeding behaviour with surprising facility.
Conversely, the Straits of Magellan (Fig. 4) are generally dominated by strong currents and the organic input controlled by turbulent diffusion which brings large amounts of detritus.Intense processes of inorganic matter resuspension, occurring mainly in the Angosturas and in the Pacific Channel, reduce the trophic value of the flux, and consequently the benthic communities are poor and less structured.The sessile taxa that are so dominant in Antarctic waters, such as sponges, gorgonarians, and bryozoans, are not so common inside the Straits of Magellan probably because the elevated inorganic component (TIM) can impede and even damage their filtering structures.Accordingly, the communities are dominated by deposit feeders, scavengers and omnivores, such as crustacean decapods.Anyway, bivalves, reaching high values of biomass and density, play an important role in the coupling processes in both areas.
Food input from the water column may sometimes be insufficient to cover the requirements of some communities which reach high values of biomass and density (Arntz et al., 1994) suggesting a lateral advection of suspended matter as an additional resource.At Terra Nova Bay and at Paso Ancho, large macroalgal communities can certainly support this secondary input, which is used by large deposit-feeding populations of crustaceans.
Finally, it is import to underline that studies on the pelagic-benthic coupling also have an applied significance and could be essential in the evaluation of the trophic capacity and the environmental response in the location of sea-farming sites, which is an ever-growing activity in the Magellan region.These activities will in fact play an important role in changing the pristine features of the Magellan environment, determining more or less heavy phenomena of dystrophy, through the input of high amounts of catabolites and particulate organic matter.

FIG. 2
FIG.2.-Scheme showing the pelagic-benthic coupling, measured as flux of POC, through the littoral scallop Adamussium colbecki at 40 m depth (Terra Nova Bay, Ross Sea).Summer primary production, measured total suspended matter (TSM), organic matter (POM) and organic carbon (POC) fluxes, TSM and POC concentration at 40 m depth and utilisation by Adamussium colbecki are reported.The POC assimilation of this scallop reaches about 4-5% of the summer primary production (fromChiantore et al., 1998, modified).
FIG. 3. -Scheme of the superficial texture of a spicule mat in a soft-bottom at Terra Nova Bay (Ross Sea), showing sponge spicules in the sediments.The amount of Chl-a inside the sediments rich in spicules does not change in the first 5 cm depth.
FIG. 4. -Scheme showing the different sectors into which the Straits of Magellan can be classified according to different trophic parameters (TSM = Total Suspended Matter; TIM = Total Inorganic Matter; POC = Particulate Organic Carbon; chl-a = chlorophyll-a; C/N = Particulate Organic Carbon/Particulate Organic Nitrogen ratio).The isolines indicate water masses of different contents of TSM (from Fontolan and Panella, 1991, modified).