MARINE ECOLOGY PROGRESS SERIES Vol. 297: 61–70, 2005 Published August 1 Mar Ecol Prog Ser Processing of 13C-labelled phytoplankton in a fine-grained sandy-shelf sediment (North Sea): relative importance of different macrofauna species Anja Kamp1, 2,*, Ursula Witte1, 3 1Max Planck Institute for Marine Microbiology, Celsiusstr. 1, 28359 Bremen, Germany 2Present address: Institute for Microbiology, University of Hannover, Schneiderberg 50, 30167 Hannover, Germany 3Present address: Oceanlab, University of Aberdeen, Newburgh, Aberdeen AB41 6AA, UK ABSTRACT: On-board and in situ experiments with 13C-labelled diatoms were carried out to inves- tigate the processing of algal carbon by the macrofauna community of a fine sandy-shelf site in the southern German Bight (North Sea). The time series (12, 30, 32 and 132 h incubations) was supple- mented by additional laboratory experiments on the role of the dominant macrofauna organism, the bivalve Fabulina fabula (Bivalvia: Tellinidae), for particulate organic matter subduction to deeper sediment layers. The specific uptake of algal 13C by macrofauna organisms was visible after 12 h and constantly increased during the incubation periods. F. fabula, a facultative (surface) deposit- and suspension-feeder, Lanice conchilega (Polychaeta: Terebellidae), a suspension-feeder and the (sur- face) deposit-feeder Echinocardium cordatum (Echinodermata: Spatangidae) were responsible for the majority of macrofaunal carbon processing. Predatory macrofauna organisms like Nephtys spp. (Polychaeta: Nephtyidae) also quickly became labelled. The rapid subduction of fresh organic matter by F. fabula down to ca. 4 to 7 cm sediment depth could be demonstrated, and it is suggested that entrainment by macrofauna in this fine-grained sand is much more efficient than advective transport. KEY WORDS: Carbon processing · Macrofauna · Sandy sediments · 13C labelling · Stable isotopes · North Sea · German Bight Resale or republication not permitted without written consent of the publisher INTRODUCTION eable sediments (Huettel & Rusch 2000), and to enhance the remineralisation and nutrient release in Shelf areas such as the North Sea cover approxi- comparison to non-permeable sediments (Ehrenhauss mately 7.5% of the total ocean area (Wollast 2003) and et al. 2004b). 70% of the shelf is covered by sandy deposits (Emery In addition, the activities of macrofauna can signifi- 1968). This comparably small area has a very high bio- cantly affect the transport of solutes and particulates logical productivity, which amounts to 30% of the total across the sediment–water interface (Graf & Rosen- oceanic primary production (Jørgensen 1996). Despite berg 1997). For example, bioirrigation by tube-build- this, sandy-shelf sediments contain a low amount of ing worms is responsible for rapid water pumping; organic matter (Shum & Sundby 1996) and low bacter- bioturbation is well known to enhance the particle ial standing stocks (Llobet-Brossa et al. 1998). The low transport within the sediment (Forster & Graf 1995, organic carbon content may be a result of high turn- Ziebis et al. 1996). The macrofauna community of the over rates, rather than low activity; the high perme- North Sea shelf consists mainly of bivalves, poly- ability of most sands is thought to allow advective per- chaetes, crustaceans and echinoderms (Salzwedel et colation of the upper sediment layers. Advection, al. 1985). The infaunal suspension and (surface) deposit- however, has been shown to result in an effective feeders in particular, such as the bivalve Fabulina fab- exchange of pore water (Huettel et al. 2003), to rapidly ula and the polychaete Lanice conchilega, both com- transport particulate organic matter (POM) into perm- mon at our study site, may have immediate access to a *Email: [email protected] © Inter-Research 2005 · www.int-res.com 62 Mar Ecol Prog Ser 297: 61–70, 2005 fresh organic carbon source and may be responsible the composition, abundance and biomass of the macro- for fast transport of this POM into deeper sediment fauna community as well as the processing of added, layers by bioirrigation, bioturbation or defecation. This labelled diatom carbon by the different macrofauna matter is thus available for other benthic organisms, taxa. We report on the potential of Fabulina fabula, the living in deeper sediment layers. Carnivorous macro- dominant macrofauna organism, for POM subduction, fauna organisms are expected to have a delayed and discuss the relative importance of bioturbation and access to a fresh carbon source but can nevertheless advective transport. contribute to sediment mixing by bioturbation due to hunting activities. In recent years, pulse-chase experiments with iso- MATERIALS AND METHODS topically labelled substrates have been established as a useful tool for following and quantifying the process- Area of investigation. The study site was situated in ing and remineralisation of fresh organic carbon in a the southern German Bight (North Sea), seaward variety of marine sedimentary habitats (e.g. Levin et al. of the East Frisian island Spiekeroog (53° 51’ N, 1997, Middelburg 2000, Aberle & Witte 2003, Witte et 007° 44’ E) (Fig. 1). The water depth in this area was al. 2003a). However, information on the benthic pro- 19 m with a tidal range about 2 m. Salinity was 31 to 32 cessing of fresh POM in sandy-shelf environments is and the mean water temperature was 9°C in April and still scarce. We therefore carried out a series of on- 13°C in June. The sediment type is fine sand with a board and in situ pulse-chase experiments in North grain size of 163 ± 20 µm and a permeability of 3.0 ± Sea sandy sediments and followed the entrainment, 1.7 × 10–12 m2 (Janssen et al. 2005). processing and degradation of algal carbon by the The experiments and sampling took place during benthic community. Within the project, not only the Expeditions HE 145 in April 2001 (on-board and labo- macrofauna but also bacterial carbon processing was ratory experiments) and HE 148 in June 2001 (in situ studied (Bühring et al. 2004) as well as the entrainment experiments) of the RV ‘Heincke’. and degradation of diatoms into the sediment (Ehren- Cultivation of labelled phytoplankton. Ditylum bright- hauss et al. 2004a,b). wellii (Bacillariophyceae: Biddulphiales) was cultured This contribution focuses on the importance of with F/2 medium (Guillard & Ryther 1962) in sterile macrofauna for carbon transport processes in a fine- artificial seawater (Grasshoff et al. 1999) with a salinity grained, sandy North Sea sediment. We investigated of 33. The diatoms were labelled with 13C by replacing 13 25% of the NaHCO3 in the formula by NaH CO3 (99%; Cambridge Isotope Laboratories). The algae were incubated for 10 d at 25°C under a light:dark cycle of 16:8 h and a light intensity of 34.9 µmol pho- tons m–2 s–1. The algal carbon produced consisted of 15 at.% 13C (on-board experiments) and 9 at.% 13C (in situ experiments). For the laboratory experiments we used Chlorella sp. (Chlorophyceae: Chlorococcales). The algal carbon of Chlorella sp. consisted of >60 at.% 13C. Sampling and determination of macrofauna for nat- ural abundance and biomass. For the determination of the natural abundance and biomass of macrofauna, sediment samples were collected with a van Veen grab (surface area 0.1 m2). Each haul (9 during the cruise in April and 10 in June) was separately sieved (1.0 mm- mesh aperture), and the sieve contents were preserved in 4% formaldehyde buffered with sodium tetraborate until taxonomic identification under a stereomicro- scope. The wet weight (g WW m–2) for each taxonomic group was determined in the laboratory in Bremen. Sampling of macrofauna for natural isotope signa- tures. The macrofauna samples for the measurements of the natural isotope signatures (δ13C) were also taken Fig. 1. Area of investigation in the southern German Bight with a van Veen grab, but after sorting the individuals (North Sea) were immediately frozen at –20°C, as fixation with Kamp & Witte: Macrofaunal carbon processing 63 of 60°C. Before determination of the δ13C signatures, the dry weights (DW) of each individual was deter- mined (g DW ind.–1). Often the organisms had to be homogenised, and a subsample (approximately 0.5 to 1.5 mg) was transferred into tin cups for measurement. Organisms were pooled when their individual dry weight was <0.5 mg. Laboratory experiments. The experimental chambers used for the laboratory experiments were similar to those used for the in situ and on-board experiments. Sediment and Fabulina fabula organisms were sampled with a van Veen grab. The sediment was sieved to remove macro- fauna organisms and stored at 4°C. F. fabula were kept in an aquarium at in situ temperature (9°C). Prior to the experiments, the chambers were filled with the sediment (18 cm). The surface water from the area of investigation was sampled with a water sam- pler. Fabulina fabula were put into the sediment cores in abundances of 0 and 14 individuals per core (2 repli- Fig. 2. Experimental chambers within their frame cates each) and allowed to settle in the sediment for 1 wk. The experiments were initiated by injecting the formaldehyde would change the natural isotope signa- chambers with labelled Chlorella sp. (equivalent to tures (Kaehler & Pakhomov 2001). Measurements of 1gC m–2), and ran for 132 h. After incubation, the sed- δ13C were made with an isotope ratio mass spectro- iment of the chambers was sliced at 0.5 cm intervals for meter (IRMS) (see subsection ‘Measurements’). the first 1 cm and at 1 cm intervals to a depth of 10 cm, On-board and in situ experiments. The experiments followed by a 10 to 12.5 cm and then a 12.5 to 18 cm were conducted in cylindrical acrylic chambers (31 cm layer. F. fabula were picked out, and a carefully homo- high, 19 cm diameter) with a horizontally rotating disk.