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Contribution of a Dense Population of the Brittle Star Acrocnida Brachiata (Montagu) to the Biogeochemical Fluxes of C 02 in a Temperate Coastal Ecosystem

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Contribution of a Dense Population of the Brittle Star Acrocnida Brachiata (Montagu) to the Biogeochemical Fluxes of C 02 in a Temperate Coastal Ecosystem Estuaries and Coasts (2009) 32:1103-1110 DOI 10.1007/s 12237-009-9216-2 Contribution of a Dense Population of the Brittle Star Acrocnida brachiata (Montagu) to the Biogeochemical Fluxes of C 02 in a Temperate Coastal Ecosystem Dominique Davoult • Jérôme Harlay • Franck Gentil Received: 3 March 2009/Revised: 5 August 2009/Accepted: 7 August 2009/Published online: 25 August 2009 (C> Coastal and Estuarine Research Federation 2009 Abstract The production of organic matter and calcium the atmosphere, emphasizing the important role of the carbonate by a dense population of the brittle star biomineralization (estimated here) and dissolution (endo- Acrocnida brachiata (Echinodermata) was calculated using skeletons of dead individuals) in the carbon budget of demographic structure, population density, and relations temperate coastal ecosystems. between the size (disk diameter) and the ash-free dry weight (AFDW) or the calcimass. During a 2-year survey in KeywordsCalcium carbonate • Secondary production • the Bay of Seine (Eastern English Channel, France), Respiration • C 02 fluxes • Echinoderm • Temperate organic production varied from 29 to 50 gAFDw m~2 year 1 and CaCC >3 production from 69 to 104 gcaC 0 3 m 2 year 1. Respiration was estimated between Introduction 1.7 and 2.0 molco 2 m 2 year 1. Using the molar ratio (\|/) of C 02 released: CaC 0 3 precipitated, this biogenic precipita­ Precipitation of biogenic calcium carbonate (CaCC^) is tion of calcium carbonate would result in an additional nearly exclusively restricted to marine environments. It has release between 0.5 and 0.7 molco 2 m year that been widely investigated in tropical ecosystems (Gattuso et represented 23% and 26% of total CO 2 fluxes (sum of al. 1996; Chisholm and Barnes 2005) and in the open ocean calcification and respiration). The results of the present (Balch et al. 1992, 2007; Holligan et al. 1993; Garcia-Soto study suggest that calcification in temperate shallow et al. 1995) but is still poorly documented for the temperate environments should be considered as a significant source coastal ecosystems. Chave (1967) reviewed the definition of CO 2 to seawater and thus a potential source of C02 to of the carbonate sediments from a geologist’s point of view and concluded that their distribution is not only restricted to shallow tropical waters where they characterize paleoenvir- D. Davoult (H ) • F. Gentil onmental conditions. Moreover, he pointed out that (first), UPMC Univ Paris 06, in temperate and cold-water shallow seas, some organisms UMR 7144 AD2M, Station Biologique de Roscoff, are able to produce large amounts of calcium carbonates in BP 74, the form of calcite, aragonite, or magnesium calcite at a 29680 Roscoff, France e-mail: [email protected] high rate and (second) the enrichment of the sediment with calcium carbonates is mainly due to the biological activity D. Davoult • F. Gentil of calcareous benthic communities. In the English Channel, CNRS, UMR 7144 AD2M, Station Biologique de Roscoff, the carbonate sediments are of two origins, Holocene and BP 74, 29680 Roscoff, France present (Reynaud et al. 1999). The description and the dating of the various carbonated fractions in the thanato- J. Flarlay coenosis are the keys to understanding the mechanisms that Laboratoire d’Océanographie Chimique et Géochimie des Eaux are responsible for the accumulation of CaC 0 3 in the (LOCGE), Université Libre de Bruxelles (ULB), Campus de la Plaine, CP208, Boulevard du Triomphe, sediments (Reynaud et al. 1999; Stride et al. 1999). Besides 1050 Brussels, Belgium the mid- to long-term accumulation of CaC 0 3 and hence of Ô Springer 1104 Estuaries and Coasts (2009) 32:1103-1110 Carbon into the seafloor, biogenic precipitation is also CaC03 gross productions, and C 02 fluxes during a 2-year responsible for the instantaneous consumption of carbonate survey in a temperate ecosystem. The originality of our alkalinity (Eq. 1). Due to thermodynamic equilibrium, this approach is to reconsider some data obtained on the brittle leads to the release of carbon dioxide (C02) in the star Acrocnida brachiata population in the Bay of Seine surrounding water (Ware et al. 1991). (Gentil and Zakardjian 1990) to demonstrate the usefulness of ancient surveys in reconstructing C02 fluxes in the contemporary context of ocean acidification (Caldeira and Ca2+ + 2HCC>3~---------> C aC 03 + C 0 2 + H20 ( 1 ) Wickett 2003). Those data were only partly published to For each mole of biogenic calcium carbonate precipitat­ describe the reproductive cycle of the species. ed, one mole of dissolved C 02 is released to the medium. Due to the strong buffering capacity of the dissolved carbonate system in seawater, the amount of C 02 released Material and Methods by calcification is lower than suggested by the stoichiom­ etry of Eq. 1. The released C 02 to precipitated carbonate The Brittle StarAcrocnida brachiata ratio (TO is close to 0.6 under standard pC02 conditions and will increase with increasing pC02 and decreasing The common brittle star A. brachiata (Montagu) (Ophiur­ temperature (Frankignoulle 1994). oidea: Echinodermata) is an infaunal suspension feeder The English Channel, especially its western part, is found in dense aggregations on sandy bottoms of Northern considered to be abnormally rich in recent carbonate Europe (Bourgoin and Guillou 1990). The arms and the deposits, principally of biogenic origin (Reynaud et al. dorsal and ventral surfaces of the disk are covered in 1999), which suggests an intense contemporary benthic calcified scales and form a calcareous endoskeleton. A. activity. Some estimates of biogenic production of calcium brachiata has a well-defined annual reproductive cycle carbonate by benthic species or communities (Smith 1972; without a sexual pause (Bourgoin and Guillou 1990; Gentil Beukema 1980, 1982; Potin et al. 1990; Migné et al. 1998; and Zakardjian 1990). The spawning period takes place in Chauvaud et al. 2003; Gollety et al. 2008) display values May-June and does not coincide with the annual temper­ ranging between 10 and 1,800 gcaC 0 3 m 2 year-1, i.e. up ature peak (Gentil and Zakardjian 1990). Reproductive to the same magnitude as the estimates for the average studies on the species indicate an abbreviated larval calcification of an entire coral reef (Gattuso et al. 1998). development (Muths et al. 2006), allowing young individ­ However, few studies have to date investigated the air-sea uals to settle in the spawning zone. Bourgoin et al. (1991) C02 fluxes associated to biomineralization. Coral reefs described the population dynamics of the species in the and pelagic systems (e.g., due to coccolithophorid Douamenez Bay and gave information about the distribu­ blooms) have shown an air-sea C02 disequilibrium tion of postlarvae, the adult density, and the growth rate. (Gattuso et al. 1996; Buitenhuis et al. 1996) due to C 0 2 Investigations realized through four surveys (1986, 1987, release by calcification. 1988, and 1991) revealed that A. brachiata always In addition, molhisk farming is particularly developed on appeared as the second or third most abundant species of numerous shores, particularly on French coasts (mainly the Abra alba—Pectinaria koreni muddy-fine sand commu­ Mytilus edulis and Crassostrea gigas cultivation), and it is nity of the Bay of Seine (Thiébaut et al. 1997 ). More recent assumed to generate both supplementary organic and surveys completed in 1996, 2001, and 2006 confirmed that CaC0 3 productions, then supplementary C02 fluxes due A. brachiata remained one of the dominant species of the both to respiration and CaC03 precipitation processes. community (unpublished data). Unfortunately, these recent Only few authors, to date, have investigated the potential surveys were carried out once during these years and did acidification of the surrounding seawater by macrobenthic not allow us to estimate the secondary production of the communities in temperate ecosystems (Migné et al. 1998; population. Chauvaud et al. 2003; Gollety et al. 2008). Given the diversity of species and biotopes concerned by these Sampling Procedure processes, it seems obvious that the role of temperate coastal benthic communities in the C02 fluxes appears Sampling was realized at 10-m depth, using ten samples of largely underestimated. Most studies such as ecosystem a 0.1-m2 Smith-Mclntyre grab, from May 1981 to Septem­ carbon fluxes modeling generally do not take into account ber 1983, at the station A (49° 27' 12" N; 0° 1' 30" E) in the calcification processes and their consequences. Bay of Seine (Eastern English Channel), a macrotidal The purpose of this study is to investigate the role of a estuary (Gentil et al. 1986). Samples were sieved on a 1- dense population in terms of biomass, calcimass (as the mm circular mesh and retained material was preserved in mass of calcium carbonate precipitated), organic and 10% neutral formalin. £ ) Springer Estuaries and Coasts (2009) 32:1103-1110 1105 Individual body size was measured as the diameter of the Table 1 Acrocnida brachiata', estimations of 4/, pCCE, and measured temperature for each period between samplings disk on the dorsal side, from the base of one arm to the opposite interradius (Guille 1964). Period p C 0 2 (ppm) Temperature (°C) Determination of Size to Biomass and Calcimass M ay-Jim 1981 0.682 327 12.5 Relationships Jun-Jul 1981 0.664 340 15.3 Jul-Sep 1981 0.674 380 16.5 The dry weight of brittle stars was measured after a 48 h Sep-Nov 1981 0.688 381 14.8 drying at 60°C, and the ash-free dry weight (calcinations N ov-Jan 1982 0.696 373 13.5 during 6 h at 520°C) was measured on 166 complete Jan-M ar 1982 0.720 371 10.5 individuals by subtracting the weight of ashes (i.e., the M ar-M ay 1982 0.716 342 9.5 calcimass) from the dry weight.
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