Food web structure and trophodynamics of deep-sea plankton from the Bari Canyon and adjacent slope (Southern Adriatic, central Mediterranean Sea)
Introduction
Although in the last decades the biology and ecology of deep-sea organisms received an increasing attention, the information on some components of deep-sea fauna is still very scarce. This is particularly true for deep pelagic fauna (i.e., meso- and bathypelagic organisms) and especially deep-sea zooplankton (Burd et al., 2002, Koppelmann et al., 2003, Tamelander et al., 2008), which are more difficult to collect compared to other components such as the deep-sea benthos (O’Dor et al., 2009). Deep-sea zooplankton represent a key component of deep-sea ecosystems, linking Particulate Organic Matter (POM) to higher trophic levels through both vertical migrations from the photic zone, i.e. the so-called swimmer flux (Miquel et al., 1994), and being prey of several megafaunal species, including demersal and benthopelagic organisms (Fowler and Knauer, 1986). Recently, some studies in the Mediterranean Sea analysed the species composition of deep-sea zooplankton (Cartes et al., 2010, Cartes et al., 2013, Fanelli et al., 2009, Danovaro et al., 2017), but very few investigations analysed its trophic structure or changes in their trophodynamics (Koppelmann et al., 2003, Koppelmann et al., 2009, Fanelli et al., 2009, Fanelli et al., 2011b). Depicting the food-web structure is fundamental to understand the exchange of matter among organisms within an ecosystem, including the energy flow from basal resources to top predators (Krumins et al., 2013). In this sense, classical studies encompassed the use of stomach contents analysis (SCA), which is still a powerful tool to depict food web structure or trophic relationships in aquatic organisms, but has the limitation of offering a snapshot of the diet of a species in a specific time. It also requires strong taxonomic skills and is heavily time-consuming (Fanelli and Cartes, 2010). Further, SCA is hard to perform for macrofauna such as the deep-sea zooplankton, due to their small size. In the last decades, stable isotope analyses (here after SIA) of nitrogen and carbon (δ13C and δ15N) have been widely used in food-web studies to analyze community structure and ecosystem function (Post, 2002), to understand source links and processes of marine and estuarine food webs (Cabana and Rasmussen, 1996), and to provide time-integrated data about feeding relationships and energy flow (Peterson and Fry, 1987). SIA is based on the predictable and quantifiable way that tissue nitrogen (δ15N) and carbon (δ13C) isotopes change along the food web (Hobson and Clark, 1992). δ15N increases about 3‰ per trophic level (Post, 2002) and δ13C changes according to the area prey items inhabit. More specifically, carbon isotope ratios of organisms in a marine trophic system are influenced by the primary producers at the base of the food web, which are affected in turn by different factors (i.e. phytoplankton size growth rate, amount and types of primary productivity etc.). These contribute to geographic patterns of δ13C values in marine environments, including higher δ13C values in benthic versus pelagic habitats and in nearshore versus off-shore food webs (France, 1995). SIAs provide a continuous measure of trophic position that integrates the assimilation of energy or mass flow through all the different trophic pathways leading to an organism. In this way, complex interactions are simultaneously captured, including trophic omnivory, and energy or mass flows are tracked through ecological communities (Peterson and Fry, 1987, Cabana and Rasmussen, 1996). SIA is also very effective for macrofaunal species: if the analyses can be performed at species level, the results mirror the high trophic complexity of lower trophic level species that can include in the same family carnivorous, deposit-feeders, filter feeders or herbivorous species.
In this study we analysed, by means of SIA of carbon and nitrogen, deep-sea macrozooplanktonic species collected by automatic sediment traps in the Bari Canyon and the adjacent slope of the Southern Adriatic (central Mediterranean Sea). Submarine canyons play a fundamental role in organic matter distribution in oligotrophic deep-sea environments and therefore in the contribution of food sources to deep zooplankton. Mediterranean canyons are responsible for inorganic/organic material accumulation (e.g., Alvarez et al., 1996, Granata et al., 1999) strongly stimulating biological production. Further, shelf-slope water exchanges occurring in canyons have a significant impact on the dispersion and recruitment processes of fish larvae (Sabates and Masó, 1992, Cowen et al., 1993), with greater abundances found on the canyon rims than in the shelf area (i.e. the case of Palamós canyon: Alvarez et al., 1996) and high densities of migratory micronekton observed over submarine canyons of the NW Mediterranean (Macquart-Moulin and Patriti, 1996).
The area of the Bari Canyon is characterized by North Adriatic Dense Water (NAdDW) cascading events, which play a relevant role in biogeochemical cycles (Shapiro et al., 2003) as in other areas of the Mediterranean, such as the Gulf of Lions (north-western Mediterranean) and the Aegean Sea (eastern Mediterranean). The Mediterranean is an oligotrophic system, with increasing oligotrophy eastwards, with low surface primary production and in turn low organic matter sinking to deep waters. As in the Adriatic Sea Dense Shelf Water (DSW) cascading sustains transport of particles and organic matter from shallow areas to the deep sea (Turchetto et al., 2007, Tesi et al., 2008, Cantoni et al., 2016, Langone et al., 2016, Taviani et al., 2016). Thus new food inputs from cascading events have a strong influence on deep-water communities by altering food availability and especially the origin of food sources for deep-sea food webs.
Here, we used SIA of carbon and nitrogen to depict the food-web structure of deep-sea macrozooplanktonic species collected by automatic sediment traps in the Bari Canyon and the adjacent slope of the Southern Adriatic. Specifically, we aimed to: (1) depict the food web structure of deep-sea macrozooplanktonic communities of south Adriatic and analyse seasonal changes in the isotopic signatures, (2) identify which environmental variables best explain the observed patterns, particularly if the NAdDW cascading has a role in such trends, and (3) define the main food sources for deep-sea zooplankton species.
Section snippets
Study area
The Adriatic Sea is a shallow semi-enclosed basin (ca. 200 × 800 km) situated in the northern central portion of the Mediterranean Sea (Cattaneo et al., 2003). The basin is commonly divided into three sub-basins: the northern Adriatic, a broad shelf characterized by a low longitudinal gradient (∼0.02°) with depths shallower than 100 m (north of Ancona), the middle Adriatic with a relatively steep shelf (∼0.5°) where the water depth reaches 260 m in the Middle Adriatic Pit, and the Southern
Results
Overall, 27 taxa were identified and analyzed (Table 1): copepods, hyperiids and euphausiids were the most represented groups. The δ15N mean values of deep-sea zooplanktonic taxa ranged between 1.32‰ (Clio sp.) and 9.25‰ (Clione sp.), measured at stations EE and BB, respectively. The range of δ13C mean values was between –22.00‰ (Ostracoda sp.) and −14.76‰ (Clio sp.) both at EE.
Discussion
This study elucidates the food web structure of deep-sea zooplankton species collected in sediment traps in southern Adriatic Sea, and presents, to our knowledge, the first isotopic data on some species of the deep-sea swimming fauna of the Mediterranean, i.e. Heterorabdus sp., Haplostylus sp., Clio sp. and Clione sp. among others. The study included 27 taxonomic groups, encompassing copepods, hyperiids, euphausiids, decapods, pelagic mollusks, chaetognats and mesopelagic fishes, describing
Conclusions
Meso- and macrozooplankton organisms play a key role in biological processes in all marine ecosystems, linking phytoplankton/micro-zooplankton to the higher trophic levels. Through their vertical migrations, zooplankton organisms may transfer the organic matter from the euphotic, productive layer to the dark deep ocean (Siokou-Frangou et al., 2010, Williamson et al., 2011). In this context, the present study represents an important contribution to the knowledge of the ecology of deep-sea
Acknowledgements
This study was carried out within the framework of the projects HERMIONE (Grant agreement No. 226354) and COCONET (Grant agreement No. 287844) of the European Commission, and the Flagship project RITMARE SP5_WP3_AZ1 (the Italian Research for the Sea). EF was also supported by IDEM (Implementation of the MSFD to the Deep Mediterranean Sea; contract EU No 11.0661/2017/750680/SUB/EN V.C2.). We wish to acknowledge the cruise participants who helped us with the mooring servicing, in particular the
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These authors equally contributed to this work.