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Spatial Oxygen Heterogeneity in a Hediste Diversicolor Irrigated Burrow Laura Pischedda, Philippe Cuny, Josã© Luis Esteves, Jean-Christophe Poggiale, Franck Gilbert

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Spatial Oxygen Heterogeneity in a Hediste Diversicolor Irrigated Burrow Laura Pischedda, Philippe Cuny, Josã© Luis Esteves, Jean-Christophe Poggiale, Franck Gilbert Spatial oxygen heterogeneity in a Hediste diversicolor irrigated burrow Laura Pischedda, Philippe Cuny, Josã© Luis Esteves, Jean-Christophe Poggiale, Franck Gilbert To cite this version: Laura Pischedda, Philippe Cuny, Josã© Luis Esteves, Jean-Christophe Poggiale, Franck Gilbert. Spa- tial oxygen heterogeneity in a Hediste diversicolor irrigated burrow. Hydrobiologia, Springer, 2012, vol. 680, pp.109-124. 10.1007/s10750-011-0907-x. hal-00780258 HAL Id: hal-00780258 https://hal.archives-ouvertes.fr/hal-00780258 Submitted on 23 Jan 2013 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Open Archive Toulouse Archive Ouverte (OATAO) OATAO is an open access repository that collects the work of Toulouse researchers and makes it freely available over the web where possible. This is an author-deposited version published in: http://oatao.univ-toulouse.fr/ Eprints ID: 6080 To link to this article: DOI: 10.1007/s10750-011-0907-x URL: http://dx.doi.org/10.1007/s10750-011-0907-x To cite this version: Pischedda, Laura and Cuny, Philippe and Esteves, José Luis and Poggiale, Jean-Christophe and Gilbert, Franck Spatial oxygen heterogeneity in a Hediste diversicolor irrigated burrow. (2012) Hydrobiologia, vol. 680 (n° 1). pp. 109-124. ISSN 0018-8158 Any correspondence concerning this service should be sent to the repository administrator: [email protected] DOI 10.1007/s10750-011-0907-x Spatial oxygen heterogeneity in a Hediste diversicolor irrigated burrow Laura Pischedda • Philippe Cuny • Jose´ Luis Esteves • Jean-Christophe Poggiale • Franck Gilbert Abstract The heterogeneity of oxygen distribution in lumen and wall (up to 2 mm) reflecting the balance a Hediste diversicolor burrow environment was inves- between worm ventilation activity and oxygen con- tigated in a laboratory experiment using a 6-mm thick sumption. The magnitude of the three surrounding tank equipped with oxygen planar optodes. The two- micro-horizons (oxic, oscillating and anoxic) induced dimensional oxygen distribution in a complete burrow by the intermittent worm ventilation was spatially and was monitored every 2 min for 4 h. Oxygen concentra- temporally variable within the structure. Oxygen vari- tions fluctuated over a scale of minutes in the burrow ations appeared to be controlled by distance from the sediment–water interface and the direction of water circulation. Moreover, there was an apparent ‘buffer effect’, induced by the proximity to the overlying water, which reduced the variations of lumen and wall oxygen L. Pischedda Á P. Cuny Á J.-C. Poggiale Laboratoire de Microbiologie, Ge´ochimie et Ecologie in the upper part of the structure. These results highlight Marines (UMR CNRS 6117), Centre d’Oce´anologie de the heterogeneous distribution and dynamics of oxygen Marseille, Universite´ de la Me´diterrane´e, Campus de associated with H. diversicolor burrows and ventilation Luminy, Case 901, 13288 Marseille Cedex 9, France activity. They also highlight the necessity of integrating e-mail: [email protected] this complexity into the current burrow-base models in J.-C. Poggiale order to estimate the ecological importance of burrow- e-mail: [email protected] ing species in coastal ecosystems. J. L. Esteves Centro Nacional Patago´nico, Unidad de Investigacio´n de Keywords Bioturbation Á Bio-irrigation Á Oxygen Oceanografı´a y Meteorologı´a, Laboratorio de heterogeneity Á Hediste diversicolor burrow Á Oceanografı´a Quı´mica y Contaminacio´n de Aguas, CONICET, Bv. Brown 2825, U9120ACF Puerto Madryn, Marine sediments Argentina e-mail: [email protected] Introduction F. Gilbert (&) EcoLab, Laboratoire d’Ecologie Fonctionnelle et Environnement, UPS, INP, Universite´ de Toulouse, Macrobenthic fauna profoundly alter the distribution 118 route de Narbonne, 31062 Toulouse Cedex 9, France of sediment particles, solutes and microbial commu- e-mail: [email protected] nities, especially in coastal marine ecosystems where F. Gilbert benthic organisms are densely distributed (e.g. Franc¸- EcoLab,CNRS, 31055 Toulouse, France ois et al., 2002; Meile & Van Cappellen, 2003; Papaspyrou et al., 2006; Gilbert et al., 2007). Through Due to the lack of data about solute distribution, these sediment reworking and irrigation, a process referred bio-irrigation models do not include the macro- and to as bioturbation (sensu Richter, 1952), the macro- micro-scale heterogeneity of solute distribution within fauna directly affect the decomposition, remineralisa- the burrow and in its immediate vicinity. The introduc- tion and preservation of organic matter in sediments tion of planar optodes into benthic ecology now makes it (Aller, 1994; Reise, 2002). In particular, the gallery- possible to determine the 2D distribution and dynamics diffusor organisms burrow into otherwise anoxic of oxygen, ammonium, pCO2 or pH in sediments (e.g. sediments and actively ventilate them for respiration Glud et al., 1996; Hulth et al., 2002; Stromberg & Hulth, or feeding purposes (e.g. Anderson & Meadows, 1978; 2003; Zhu et al., 2006). With regard to oxygen, so far Osovitz & Julian, 2002). The sediment–water inter- only a few studies have been undertaken using planar face is increased by their burrowing activity, and in optodes to monitor oxygen distribution and dynamics in addition worm ventilation activity greatly enhances macrofaunal burrows. For instance, Timmermann et al. solute exchanges between the sediments and the (2006), Polerecky et al. (2006) and Behrens et al. (2007) overlying water (Fenchel, 1996; Aller, 2001; reported a highly dynamic pattern of oxygen distribution Pischedda et al., 2008). in laboratory experiments with the polychaete Arenicola Macrofaunal burrows have been extensively stud- marina, the sand eel Ammodytes tobianus and the ied in terms of sediment reworking (e.g. Duport et al., Chironomid larvae Chironomus plumosus, respectively. 2006), morphology (e.g. Davey, 1994), irrigation rate In shallow water environments, Wenzho¨fer & Glud, (e.g. Kristensen, 2000), solute distribution and fluxes (2004) reported patchiness and variability of the benthic (e.g. Kristensen & Hansen, 1999), redox oscillations oxygen distribution on a diel scale, primarily induced by (e.g. Sun et al., 2002), mineralisation rate (e.g. Aller, the distinct diel pattern in Hediste diversicolor activity 1994) and associated microbial communities (e.g. and photosynthesis. More precisely, they showed that Papaspyrou et al., 2006). However, the distribution the volume of oxic sediments around burrow structures and dynamics of solutes within a macrofaunal burrow was influenced by these changing environmental con- structure have proven difficult to determine. Conse- ditions, and that oxygen uptake through the burrow quently, methods such as determinations of global walls just after sunset accounted for most of the total exchanges between the entrance and the exit of the oxygen uptake. In those studies, however, the oxygen burrow, or local concentration measurements using distribution and dynamics were only quantified in microelectrode(s) at the burrow openings or localised particular or localised areas of the burrows, and this within or in the vicinity of the burrow structure (e.g. in did not make it possible to define the oxygen heteroge- the burrow wall) have been developed, often in neity in a complete bio-irrigated burrow. association with simultaneous active ventilation Hediste diversicolor (OF Mu¨ller, 1776) is a polychaete recording (e.g. Kristensen, 1989; Forster & Graf, worm widely distributed in estuarine and lagoonal 1995). Based on these data, efforts have been made to habitats from North Africa to North Europe (Mettam, model the solute distribution in actively ventilated 1979; Gillet, 1993) at a density of 500–5,000 individuals burrow environments. Currently, there are two main per square metre (Vedel & Riisgard, 1993). This species types of bio-irrigation models: the diffusive tube- shows high physiological tolerance of extreme variations irrigation model (Aller, 1980), which was further in environmental factors, and can grow and reproduce in improved by authors such as Boudreau & Marinelli different sediment types and also in stressed environ- (1994), Furukawa (2001) and Koretsky et al. (2002), ments (e.g. Bartels-Hardege & Zeeck, 1990; Miron & and the advective pocket-injection model (Meysman Kristensen, 1993; Scaps, 2002). It lives in a semi- et al., 2006). One significant difference between these permanent U- or Y-shaped mucus-lined burrow extend- models is that the former is relevant to muddy ing 6–12 cm into muddy or sandy–muddy sediments. sediments where bio-irrigation is intrinsically driven The worm actively ventilates its burrow structure (Kris- by diffusion across the burrow wall, whereas the latter tensen, 1981; Davey, 1994) with regular alternations of describes sandy sediments where active ventilation by active ventilation periods of *10 min followed by rest worms induces the advective transport of water in the periods of *5 min (Kristensen, 2001). surrounding
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