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Authors requiring further information regarding Elsevier’s archiving and manuscript policies are encouraged to visit: http://www.elsevier.com/authorsrights Author's personal copy Marine Environmental Research 87-88 (2013) 85e95 Contents lists available at SciVerse ScienceDirect Marine Environmental Research journal homepage: www.elsevier.com/locate/marenvrev Dynamics of wood fall colonization in relation to sulfide concentration in a mangrove swamp Mélina C.Z. Laurent a, Nadine Le Bris b,c, Françoise Gaill d, Olivier Gros a,e,* a UMR-CNRS-IRD-MNHN-UPMC 7138, Systématique-Adaptation-Evolution, Equipe « Biologie de la mangrove », Université des Antilles et de la Guyane, UFR des Sciences Exactes et Naturelles, Département de Biologie, BP 592, 97159 Pointe-à-Pitre Cedex, Guadeloupe, France b Université Pierre et Marie Curie-Paris 6, CNRS-UPMC UMR 8222, LECOB, Benthic Ecogeochemistry Laboratory, Laboratoire Arago, Rue du Fontaulé, 66650 Banyuls-sur-Mer, France c Ifremer, DEEP, 29280 Plouzané, France d CNRS, Institut Ecologie et Environnement (INEE), Rue Michel-Ange, 75016 Paris, France e C3MAG, Université des Antilles et de la Guyane, UFR des Sciences Exactes et Naturelles, BP 592, 97159 Pointe-à-Pitre Cedex, Guadeloupe, France article info abstract Article history: Wood debris are an important component of mangrove marine environments. Current knowledge of the Received 26 May 2012 ecological role of wood falls is limited by the absence of information on metazoan colonization processes Received in revised form over time. The aim of this study was to provide insights to their temporal dynamics of wood eukaryotic 23 March 2013 colonization from a shallow water experiment in a mangrove swamp. Combined in situ chemical Accepted 27 March 2013 monitoring and biological surveys revealed that the succession of colonizers in the mangrove swamp relates with the rapid evolution of sulfide concentration on the wood surface. Sulfide-tolerant species are Keywords: among the first colonizers and dominate over several weeks when the sulfide content is at its maximum, Biodiversity fi Colonization followed by less tolerant opportunistic species when sul de decreases. This study supports the idea that Sulfide woody debris can sustain chemosynthetic symbioses over short time-scale in tropical shallow waters. Mangrove Ó 2013 Elsevier Ltd. All rights reserved. Chemosynthetic communities Symbiosis In situ measurement Chemical sensors 1. Introduction (ii) experimentally immersed wood substrates (Turner, 1977; Maddocks and Steineck, 1987; Lorion et al., 2009; Bernardino Distributed at various depths on the seafloor, sunken woods et al., 2010; Gaudron et al., 2010; Bienhold et al., 2013) have retained scientist interest for long time. Since they were first (iii) analyses of fossil sunken wood communities (Kiel and reported from more than 1500 m depth during the Challenger Goedert, 2006) expedition in the 19th century, so-called ‘sunken wood’ colonizer assemblages have been described from a variety of sources These studies particularly emphasized the abundance and di- including: versity of wood associated fauna in tropical areas where vegetable debris are naturally abundant on the seafloor. (i) natural sunken wood collected from dredge materials (Wolff, According to Turner (1977), wood ingesters and microbe grazers 1979; Pailleret et al., 2007; Samadi et al., 2007; Nishimoto would constitute the basis of the food web completed by detri- et al., 2009) tivores, with predators and scavengers feeding on these groups. Recent isotopic studies confirmed wood as a carbon source for both direct and indirect users (Nishimoto et al., 2009). Focusing on the surrounding sediment, first experimental studies of macrofaunal * Corresponding author. UMR-CNRS-IRD-MNHN-UPMC 7138, Systématique- succession have confirmed the relatively slow decomposition of Adaptation-Evolution, Equipe « Biologie de la mangrove », Université des Antilles et wood compared to other vegetable remains and the mediating role de la Guyane, UFR des Sciences Exactes et Naturelles, Département de Biologie, BP of wood borers in the utilization of woody material in the deep sea 592, 97159 Pointe-à-Pitre Cedex, Guadeloupe, France. E-mail address: [email protected] (O. Gros). (Bernardino et al., 2010; Bienhold et al., 2013). Fossil wood-fall 0141-1136/$ e see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.marenvres.2013.03.007 Author's personal copy 86 M.C.Z. Laurent et al. / Marine Environmental Research 87-88 (2013) 85e95 communities could have displayed the same structure as modern timescales of days to weeks? 2 e Do these groups relate to sulfide wood falls, although different wood ingesters might have lead to concentration on wood surface? Answers to these questions pro- different temporal patterns in the colonization and degradation of vide insights to the role of wood fall in tropical mangrove wood (Kiel and Goedert, 2006; Kiel et al., 2008). ecosystem, where they are naturally abundant. These substrates More unexpected was the observation that sunken woods in the remain an overlooked component of the mangrove ecology, despite deep-sea share numerous colonizers with so-called chemosyn- vegetable debris are recognized as a primary source of energy for thetic habitats. The reliance of wood invertebrate species to the ecosystem (e.g. leaves, roots) (Nagelkerken et al., 2008). The chemosynthetic lineages was first hypothesized by Distel et al. results also offer additional cues to the general mechanisms driving (2000). The observation of bacterial ectosymbionts on the gills of sunken wood community dynamics in marine environments, a deep-sea wood mussels (Gros and Gaill, 2007; Gros et al., 2007), providing interesting comparative information to address differ- that were later confirmed to be sulfide-oxidizers (Duperron et al., ences or common features with deep-sea wood falls. 2008) provided further evidence to this idea. Wood falls host a Two types of wood substrates were experimentally immersed number of higher taxonomic levels known from hydrothermal and monitored over 3 months: Rhizophora mangle (Rhizophorae), vents and cold seeps (Kiel and Goedert, 2006; Samadi et al., 2007; the local mangrove tree, and, for comparison, Cocos nucifera (Are- Kiel et al., 2008; Bernardino et al., 2010; Gaudron et al., 2010). caceae), which is a major component of natural sunken wood col- Sulfide can be produced from wood in the marine environment lections from tropical areas (Wolff, 1979)(Fig. S1). Temporal from synergetic microbial activities involving cellulolytic bacteria changes in the sulfide concentration on the wood surface and in the and sulfate reducing bacteria (SRB) with or without the mediation abundance and diversity of main eukaryotic groups were both of wood borers, at shallow to great depth (Fors et al., 2008; Palacios monitored. The biogeochemical mechanisms sustaining sulfide et al., 2006, 2009; Bienhold et al., 2013). Owing to the difficulty of production during wood degradation in those particular conditions accessing deep-sea environments, previous studies have provided lie outside the scope of the present paper. The settlement dynamics only snapshots in the succession of species on wood, preventing to of different faunal groups were analyzed in the light of the sulfide address the relationship between wood habitat conditions and concentration recorded on the wood surface over the experiment colonization dynamics. In particular, the temporal variation of duration. The reliance on sulfide as an energy source was further sulfide, a major factor in metazoan colonization, is still poorly considered by exploring the occurrence of chemoautotrophic constrained, although a recent aquarium study simulating deep-sea symbioses among the colonizers. Similarly to the succession model conditions have revealed a relatively rapid temporal dynamics proposed for whale and wood falls by previous authors, a model is (Yücel et al., 2013). proposed to explain the temporal colonization pattern on wood Even if diversity is likely to be represented by different groups, falls in the mangrove swamp, and its consistency with the obser- mangrove swamps offer an opportunity to further investigate the vations performed at greater depth is further discussed. relationships between sulfide enrichment and colonizers diversity, and their temporal dynamics, on degrading wood in tropical en- 2. Methods vironments. In a mangrove swamp, sulfide enrichment was confirmed on natural sunken wood surface (Laurent et al., 2009; 2.1. Experimental strategy and colonizer surveys Muller et al., 2010), combined with the occurrence of a strict chemoautotrophic symbiosis between a ciliate Zoothamnium Parcels composed of a metallic structure covered by a plastic niveum and sulfide-oxidizing bacterial ectosymbionts (Rinke et al., mesh (1 Â 0.5 Â 0.5 m) were filled either with freshly cut fractions 2006). The dynamics of such sulfide emission is however poorly of branches (10 pieces about 30