Differential responses of benthic microbes and meiofauna to fish-farm disturbance in coastal sediments

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Abstract

Bacterial and meiofaunal abundance and biomass and their response to the disturbance induced by fish-farm biodeposition were investigated from March to October 1997 on a monthly basis at two stations of the Gaeta Gulf (Tyrrhenian Sea, Mediterranean Sea). The biopolymeric fraction of the organic matter was characterized by high concentrations which was similar at both fish-farming-impacted and control stations. Similarly, bacteria accounted for a small fraction of the biopolymeric organic carbon (<1%), while the contribution due to auto-fluorescent cell biomass (i.e. prokaryotic and eukaryotic cells displaying auto-fluorescence) to the total biopolymeric carbon was quantitatively negligible (<0.1%). Benthic bacteria appear to be sensitive to organic enrichment as their abundance increased significantly beneath the cage, whilst numbers of meiofauna was lower than in the control. Changes occurred also in terms of individual nematode biomass that increased as result of the biodeposition. A particularly useful tool appeared to be represented by the ratio of benthic auto-fluorescent cells to bacterial abundance, bacteria to meiofaunal biomass and auto-fluorescent cells to meiofauna biomass. All these parameters described well the impact due to biodeposition on the benthic environment as their ratios displayed significantly higher values in farm sediments, but recovered rapidly (15 days) to values observed in the control (i.e. undisturbed conditions) immediately after cage removal. Changes observed in the present study highlight that the increased organic loading determined a shift of the relative contribution of the different benthic components to the total biopolymeric carbon, so that in highly impacted systems total benthic biomass becomes increasingly dominated by microbial components.

Introduction

Trophic interactions between bacteria, protozoa and organic matter within the pelagic microbial loop have been widely investigated (Billen et al., 1990, Sherr and sherr, 1991, Gonzales and Suttle, 1993, Jurgens et al., 1994, Bidle and Azam, 1999), but little is known on the quantitative role of these components in benthic ecosystems (Kemp, 1988, Kemp, 1994, Bak and Nieuwland, 1989, Deming and Barros, 1993, Hondeveld et al., 1994, Danovaro, 1996). Benthic bacteria play a fundamental role in converting organic detritus into living biomass and, being largely consumed (up to 90% per day) by heterotrophic nanoflagellates (Danavaro et al., 1998, Danovaro, 2000), might be channelled to higher trophic levels (e.g. meiofauna), thus structuring the microbial loop in benthic ecosystems (Kemp, 1988, Bak and Nieuwland, 1989, Hondeveld et al., 1994). This, in turn, might have important implications for material and energy transfer efficiency through the benthic food webs.

The structure of benthic assemblages and the relative significance of the different benthic components are sensitive to changes in environmental conditions and trophic state (Danovaro, 2000), in particular in shallow marine sediments subjected to major nutrient inputs related to anthropogenic activity (Jensen et al., 1990, Hansen and Blackburn, 1992). The increased organic matter load due to the strong fish-farm biodeposition, generally results in highly eutrophic conditions determining a strong reduction of the oxygen penetration in the sediments with a consequent reduction of benthic infaunal density and diversity (Brown et al., 1987, Frid and Mercer, 1989, Weston, 1990, Holmer, 1991, Hansen and Blackburn, 1992, Mirto, 1998, Mirto et al., 1999, Mazzola et al., 1999). Among benthic components meiofauna proved to be a sensitive tool for detecting biodeposition impact (Duplisea and Hargreaves, 1996, Danovaro, 2000, Mazzola et al., 2000).

Previous studies demonstrated that the accumulation of large amounts of organic matter on the sediments induces long-term changes in the structure of the benthic assemblages, increasing the relative importance of the smaller components (i.e. bacteria) of the benthic food web (La Rosa, 1998, Danovaro et al., 1999). In other words, one of the main effects of organic enrichment on benthic communities is the increase of the bacteria to meiofauna biomass ratio with respect to unpolluted conditions (Albertelli et al., 1999).

In the present study, benthic microbial and meiofaunal biomass and dynamics were monitored during strong biodepositional conditions (due to intensive fish-farming) and after cage removal to test the sensitivity of the relative significance of the biomass of different benthic components to changing organic matter impact. We also present a new approach for detecting the impact of biodeposition over the benthic system based on the change of the relative importance of the benthic microbial versus metazoan biomass.

Section snippets

Study area and sampling

This study was conducted from March 1997 to October 1997 in the Gaeta Gulf (Tyrrhenian Sea, northwest Mediterranean Sea, latitude 41°21′ N; longitude 13°60′ E; Fig. 1). The area is characterized by limited seasonal changes in temperature and by the presence of two major rivers: the Garigliano and the Volturno, both in the southern part of the Gulf. Dominant currents flow in southeast–northwest direction following the cyclonic circulation of the Tyrrhenian Sea. The study area is sheltered and

Environmental parameters and sedimentary organic matter

Average values (±S.E.) relative to RPD depth, pore water and BPC content are reported in Table 1. During fish farming (i.e., from March to June), the RPD depth was significantly lower beneath the cage station that at the control (2.2±0.2 and 0.3±0.2 cm at the cage and control stations, respectively; Kruskal–Wallis test, P=0.02; Table 2). After fish-farm removal (i.e. from July on), RPD depth at the cage station increased (1.5±0.1 cm), thus showing values similar than at the control station

Discussion

The sediment beneath the cage, during fish-farming, was characterized by reduced oxygen penetration into the sediments as evident from the reduced depth of the RPD layer. Fish-farm sediments have been observed to be organic-enriched environments relative to adjacent areas outside of the region of direct impact of increased sediment accumulation [Hargrave et al., 1993, Mazzola et al., 1999, Fabiano et al., 1995, for comparison] but differences between cage and control were not detectable, in our

Acknowledgements

The authors are particularly indebted with the staff of the Medfish s.r.l. (Gaeta) for precious collaboration during sampling. Thank are due to Professor A. Manganaro (University of Messina) for support provided to S.M. during his PhD activity and to Professor T. Maugeri (University of Messina) for support provided to T.L.R. during her PhD activity. We thank also Dr. E. Favaloro and Dr. B. Savona (University of Palermo) for kind support during sampling and to Dr. A. Giampieri (University of

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