Regional scale estimation of carbon fluxes from long-term monitoring of intertidal exposed rocky shore communities

Journal of Marine Systems 149 (2015) 25–35

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Regional scale estimation of carbon fluxes from long-term monitoring of intertidal exposed rocky shore communities Morgana Tagliarolo a,⁎, Jacques Grall b, Laurent Chauvaud a, Jacques Clavier a a b

Laboratoire des Sciences de l'Environnement Marin, Institut Universitaire Européen de la Mer, rue Dumont d'Urville, 29280 Plouzané, France IUEM Observatory UMS 3113 CNRS, Institut Universitaire Européen de la Mer, rue Dumont d'Urville, 29280 Plouzané, France

a r t i c l e

i n f o

Article history: Received 28 November 2014 Received in revised form 10 April 2015 Accepted 12 April 2015 Available online 18 April 2015 Keywords: Carbon flux Rocky shore Metabolism Intertidal environment Long-term monitoring Temperature variations

a b s t r a c t The observed increase in the atmospheric concentration of carbon dioxide due to anthropogenic emissions is predicted to lead to significant changes in climate. Recent studies highlight the importance of identifying the role of marine coastal communities in carbon exchanges. Our objective was to couple macrozoobenthos abundance data from long-term monitoring with species metabolism rates to contribute to the estimation of CO2 fluxes from an intertidal exposed rocky shore community at a regional scale. The carbon fluxes due to respiration and calcification were calculated both during emersion and immersion, and the effect of temperature variation on carbon emissions was then predicted. Spatial and temporal natural variations of carbon fluxes were investigated and the contribution of exposed intertidal rocky shore communities to regional carbon emissions was calculated. The method was used to calculate the carbon budget allowed to account for the natural spatial variability of the community composition and carbon emissions. Mean annual calculated CO2 emission was 14.3 mol C m−2 yr−2, and the annual regional CO2 flux was estimated at 2978 t C yr−1. Simulations showed that the potential feedback of a rise in temperature of 1 °C would lead to an increase of 4–7% in carbon emissions for this type of community. The results give a first quantification of intertidal exposed rocky shore carbon emissions that could be considered in evaluating further the global CO2 budget. © 2015 Elsevier B.V. All rights reserved.

1. Introduction Coastal marine ecosystems are among the most ecologically and socioeconomically important ecosystems (Harley et al., 2006). Although the continental margins, considered here to extend from the coastline to a depth of 200 m, occupy only a little over 7% of the seafloor and less than 0.5% of the ocean volume, they play a major role in oceanic biogeochemical cycling (Chen and Borges, 2009). Unfortunately, the contribution of the coastal zone to carbon global cycles is not yet clarified because coastal ecosystems are characterized by strong temporal and spatial heterogeneities (Middelburg et al., 2005). The metabolism of rocky shore organisms has mostly been studied in the laboratory, with each species examined separately (Babarro et al., 2000; Bjelde and Todgham, 2013; Branch and Newell, 1978; Houlihan and Newton, 1978). Carbon fluxes of the intertidal hard-bottom communities have only been directly estimated for macroalgae dominated shores (Golléty et al., 2008b) and isolated rocky blocks through benthic chamber Abbreviations: IPCC, Intergovernmental Panel on Climate Change; MDS, non-metric multidimensional scaling; REBENT, REseau BENThique; SHOM, Service Hydrographique et Océanographique de la Marine; SST, sea surface temperature. ⁎ Corresponding author at: LEMAR (UMR CNRS 6539), Institut Universitaire Européen de la Mer, IUEM, rue Dumont d'Urville, F-29280 Plouzané, France. Tel.: +27 763889938; fax: +27 33 2 98 49 86 45. E-mail address: [email protected] (M. Tagliarolo).

http://dx.doi.org/10.1016/j.jmarsys.2015.04.004 0924-7963/© 2015 Elsevier B.V. All rights reserved.

techniques (Lejart, 2009). A recent indirect estimation of CO2 fluxes performed on the Brittany rocky shores communities emphasized the importance of calcified intertidal invertebrates for the carbon budgets (Hily et al., 2013). Although the importance of coastal areas to the global CO2 budget is irrefutable, our current knowledge of carbon fluxes is still lacking. One of the major obstacles in our understanding is the lack of a typology for the European coastal areas (Gazeau et al., 2004). Information on near-shore and intertidal areas is often missing because of the difficulty of applying traditional measurement techniques. Previous estimations of coastal carbon fluxes on global scales have considered only data measured on soft-bottom communities (Borges, 2011; Cai et al., 2003; Chen and Borges, 2009). Although benthic communities living in continental margins could either be a sink or a source for atmospheric carbon (Siefert and Plattner, 2004; Staehr et al., 2012), different studies indicate that this zone is generally a source of CO2 to the atmosphere (Smith and Hollibaugh, 1993; Smith and Mackenzie, 1987, 1987). Considering such uncertainty, the estimation of total carbon emissions related to these communities still requires further investigation. Increasing concentrations of CO2 and other greenhouse gases in the atmosphere are considered to have been a major cause of global mean surface air temperature rise during the twentieth century and are projected to accelerate the rate of climate change (Meeht and Stocker, 2007). Because temperature generally influences metabolism, carbon emissions can change depending on temperature variations. According

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M. Tagliarolo et al. / Journal of Marine Systems 149 (2015) 25–35

to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (IPCC-2013), the globally averaged combined land and ocean surface temperatures show a warming of 0.85 °C over the period 1880–2012 (Hartmann et al., 2013; Levitus et al., 2009). Such warming, however, has been neither steady nor the same in different locations. Thus, European seas have experienced a rapid increase in temperature of about 0.67–0.80 °C between 1982–2006 (Belkin, 2009). Measurements performed in the English Channel during the period 1986–2006 indicate that warming is not homogeneous either in this area and that the central part of the Channel and the western part of the French Brittany exhibit a lower warming rate (around 0.6 °C) compared to the northern part of the Channel (around 1.6 °C) (Saulquin and Gohin, 2010). Reliable predictions of climate change in the immediate future are difficult, especially at the regional scale where natural climate variations might amplify or mitigate anthropogenic warming (Lean and Rind, 2009). In long-term projections extending towards the end of this century and beyond, a large part of the uncertainty is associated with the trend of anthropogenic greenhouse gas emissions and the resulting external forcing of the climate system. The mean climate change for the period 2016–2035 estimated by the IPCC multi-model varies from 0.3 °C to 0.7 °C (medium confidence) (Kirtman et al., 2013), and mean temperature in Europe is predicted to increase more than the global average. Consequently, the greatest climate warming is expected to occur in northern Europe, especially in winter, while cooling would rather occur in southern Europe throughout the year as well as in central Europe in summer (Christensen et al., 2007). Coastal perennial monitoring programs are powerful tools for understanding the natural variability of benthic community structures and the relationship with environmental factors and their variations. The French monitoring network, REseau BENThique (REBENT), was launched by the Ministry of the Environment in 2003 following the 1999 Erika oil spill. REBENT aimed to acquire baseline knowledge on biodiversity and structure of several coastal benthic habitats through time. It aims at defining a reference state and provides monitoring of these habitats to detect changes at various scales over time and space (Ehrhold et al., 2006). This network has focused on 7 different habitats, four sedimentary habitats (sandy beaches, zostera beds, infralittoral fine sands, maerl beds) and three rocky habitats (fauna dominated rocky shore, algae dominated rocky shore, infralittoral rocky communities) (Derrien-Courtel et al., 2013; Hily et al., 2013). Here, we only focus on fauna dominated rocky communities, the most prominent and widely distributed communities living in the intertidal rocky shore in Brittany (EUNIS — A1.11 habitat “mussel and barnacle communities” see http://eunis.eea.europa.eu/habitats/5395). In such exposed and semiexposed habitats, the macrozoobenthos is very largely predominant, representing from 90 up to 100% of the benthic biomass, while algal cover is very limited or absent (Lewis, 1964). Compared to other coastal communities, the intertidal rocky shore is characterized by considerable biodiversity and various adaptations to aerial exposure (Davidson et al., 2004). CO2 release from the intertidal macrozoobenthic community is the result of both respiration and calcification processes (Frankignoulle et al., 1994). Quantification of carbon fluxes from intertidal rocky shore communities requires the consideration that immersion and emersion succession cause variation in different physico-chemical parameters (such as temperature, light, desiccation, salinity) and changes in community composition along the coast. The present study aimed to generate estimates of annual CO2 emissions from intertidal exposed rocky shore communities at a regional scale. For this, mean annual biomass of species, obtained from REBENT intertidal rocky shores data set, was coupled with specific respiration– temperature relationships and mean calcification rates. To examine the spatiotemporal variability of these estimates, calculation was performed at two shore levels in nine sites and for six years. The effect of different scenarios of annual mean temperature variation on mean CO2 emission was also tested for the two levels.

2. Material and methods 2.1. Sampling strategy Data on the abundance of the studied benthic species were provided by the REBENT network. REBENT has been monitoring rocky intertidal fauna at 9 sites (Fig. 1) with similar hydrodynamic conditions between 2004 and 2012. These sites are representative of exposed or moderately exposed shores where the algal cover is limited or nil. Abundance was monitored at two shore levels; here we use the term “high-shore” to refer to communities living in the upper eulittoral zone and “lowshore” for animals living in the lower part of the eulittoral zone. Since 2004, non-destructive methods have been used annually to estimate the macrozoobenthic community composition and abundance in each studied zone. Samples were collected at the beginning of spring in order to include winter mortalities and avoid late spring recruitments. Such a design was employed, to sample communities at their ‘baseline’ and thus avoid yearly variability. Ten quadrats of 0.1 m2 divided into 40 smaller quadrats of 25 cm2 are sampled once a year at the same position on the shore. On each 0.1 m2 quadrat, abundance of large macrofauna (more than 0.5 cm) is evaluated directly in situ. Photographs of five randomly selected 25 cm2 quadrats are taken on each 0.1 m2 quadrat, and photo analysis is performed using Quantum GIS software to assess barnacle and small gastropod abundances. In this study, we have used data from six years of monitoring (2004–2007 and 2009–2010) since data from 2008 were not available. Species abundance was averaged from seven quadrats of 0.1 m2 for large species and 21 quadrats of 25 cm2 (3 for each 0.1 m2 quadrat) for small animals to standardize the data. Some samples were not available because of technical problems or poor weather conditions. Carbon fluxes were estimated for five species groups that contained all the species found during the sampling period: barnacles (Semibalanus balanoides, Elminius modestus, Chthamalus stellatus, Chthamalus montagui), limpets (Patella vulgata, Patella depressa, Patella ulyssiponensis), mussels (Mytilus spp.), oyster (Crassostrea gigas), and gastropods (Gibbula pennanti, Gibbula umbilicalis, Littorina littorea, Littorina obtusata, Littorina saxatilis, Melarhaphe neritoides, Nucella lapillus, Osilinus lineatus). 2.2. Environmental parameters Immersion/emersion times as well as aerial and underwater temperatures were considered in order to extrapolate carbon fluxes on an annual scale. Water height was calculated every 15 min according to SHOM (Service Hydrographique et Océanographique de la Marine) tide tables. The high-shore was immersed for 640 h yr−1 while the low-shore was immersed for 4103 h yr−1. Average annual air and sea surface temperatures were calculated from data recorded in the vicinity of each sampling site by Météo-France and PREVIMER (IFREMER) (Table 1). 2.3. Biomass measurements During summer 2012 specimens of each group have been collected at low tide from rocky shores near Brest, France (48°21′5″N, 4°34′11″ W). For each species, average biomass for each level and season was calculated by multiplying the average individual biomass (g ash-free dry weight, AFDW) by the number of individuals. To obtain more accurate biomass estimates for larger animals, limpets and mussels were divided into two size classes (above 25 mm or below 25 mm in length) during photo analysis, and the average individual biomass was then estimated accordingly. To calculate average individual biomass of each species, five groups with 1 to 5 individuals of the same species were dried at 60 °C for 24 h and subsequently calcinated at 450 °C for 4 h in a muffle furnace. Average individual biomass was calculated from the regression between biomass and number of individuals.

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Fig. 1. REBENT sites for intertidal rocky shore community monitoring.

Non-metric multidimensional scaling (MDS) multivariate analysis was applied to species biomass results to reveal the spatial and temporal community variabilities. This analysis was performed using Primer 6.0 ® software, and the Bray–Curtis distance was applied in the original data. 2.4. Carbon fluxes Carbon fluxes were calculated considering underwater (μmol DIC g−1 h−1) respiration and calcification (μmol CaCO3 g−1 h−1) processes during immersion, and only respiration (μmol CO2 g−1 h−1) during emersion periods. Respiration was estimated for each site as a function of temperature and annual average biomass using the Arrhenius equation (Table 2). Data were provided by previous studies conducted within the same geographical area from direct measurements in the

Table 1 Annual average air (top value) and sea surface (bottom value) temperatures in °C from 2004 to 2010 (raw data from Météo-France and PREVIMER-IFREMER). See Fig. 1 for location of sites.

Saint-Briac Arcouest Callot Sainte-Marguerite Molène Bay of Brest Aber Island Doëlan Locmariaquer

2004

2005

2006

2007

2008

2009

2010

11.81 13.04 12.53 13.04 11.63 13.04 12.34 13.04 12.16 13.45 11.53 13.45 11.53 13.45 12.16 13.85 12.50 13.85

12.06 13.02 12.75 13.02 11.89 13.02 12.44 13.02 12.30 13.47 11.77 13.47 11.77 13.47 12.22 13.79 12.80 13.79

12.32 12.82 12.80 12.82 12.07 12.82 12.50 12.82 12.55 13.28 12.04 13.28 12.04 13.28 12.58 13.69 12.78 13.69

12.15 13.41 12.92 13.41 11.93 13.41 12.59 13.41 12.53 13.46 11.89 13.46 11.89 13.46 12.39 13.87 12.40 13.87

11.65 12.88 12.38 12.88 11.63 12.88 12.25 12.88 12.11 13.05 11.41 13.05 11.41 13.05 11.68 13.50 12.05 13.50

11.62 12.67 12.33 12.67 11.68 12.67 12.08 12.67 12.02 12.86 11.53 12.86 11.53 12.86 11.82 13.39 12.53 13.39

10.84 12.20 11.60 12.20 10.96 12.20 11.58 12.20 11.63 12.60 10.70 12.50 10.70 12.50 11.02 13.20 11.59 13.20

laboratory using closed chambers in immersion (dissolved inorganic carbon fluxes) and emersion (CO2 fluxes) (Table 2) (Clavier et al., 2009; Lejart et al., 2012; Tagliarolo et al., 2012, 2013a, 2013b). Because mussel underwater respiration is not significantly influenced by temperature (Tagliarolo et al., 2012), average fluxes were used in the calculations. Mussel carbon fluxes are known to differ between large and small individuals. Respiration and calcification parameters were then chosen for each year and site, as a function of the predominant mussel size, according to the results given in Tagliarolo et al. (2012). Because no accurate data were available for L. obtusata, parameters measured for G. pennanti, which has a similar size and distribution, were used (Tagliarolo et al., 2013a). Calcification contribution to carbon fluxes during immersion was calculated using average net annual fluxes available for the different species (Table 2). When calcification occurs in the aquatic environment, CO2 is released into the surrounding water. The deposition of one mole of calcium carbonate releases approximately 0.6 mol of CO2 into the seawater at 25 °C temperature and a salinity of 35 (Frankignoulle et al., 1995). To calculate the contribution of calcification to carbon fluxes, we then estimated the molar ratio of CO2 released by calcification to calcium carbonate precipitated, as a function of average sea water temperature (Frankignoulle et al., 1994). Salinity and CO2 content of the seawater were assumed to be stable. In order to include the contribution of biofilm community on the total carbon fluxes we used data from measurements performed on estuarine artificial rocky surfaces (Magalhães et al., 2003). Values originally expressed in oxygen were converted to carbon, assuming a photosynthetic and a respiratory quotient of 1 (Carvalho, 2014; Ní Longphuirt et al., 2007). This study recorded average net primary production fluxes of −12.2 mmol C m−2 h−1 (389 mg O2 m−2 h−1) and respiration fluxes of 1.6 mmol C m−2 h−1 (50 mg O2 m−2 h−1) for an average Chl a content of 80 ± 40 μg cm− 2 (Magalhães et al., 2003). Since the average Chl a concentrations measured on intertidal rock surface varied between 0 and 12 μg cm− 2 (Boaventura et al., 2002, 2003; Fariña et al., 2003; Murphy et al., 2005; Underwood, 1984), an average net primary production rate of − 0.9 mmol C m− 2 h− 1 and a respiration rate of 0.12 mmol C m−2 h−1 were considered for intertidal rocky shore biofilm.

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Table 2 Mean calcification and parameters of Arrhenius plots relating the logarithm of hourly underwater and aerial respiration rates per g AFDW to the inverse of absolute temperature. All the studied species were sampled in the Bay of Brest. Underwater respiration Organisms

Ln a

Ea/K

Barnacles Gibbula pennanti Gibbula umbilicalis Littorina littorea Littorina obtusata Littorina saxatilis Melarhaphe neritoides Mytilus spp. large (N3 cm) Mytilus spp. small (b3 cm) Nucella lapillus Osilinus lineatus Ostreidae spp. Patella spp.

29.6 7.86 55.28 15.07 47.52 12.89 43.28 11.71 55.28 15.07 27.61 7.13 11.47 2.37 Mean flux of 26.4 μmol DIC g−1 h−1 Mean flux of 35.9 μmol DIC g−1 h−1 41.22 11.08 28.16 7.3 56.44 15.53 34.41 9.26

Aerial respiration

Mean calcification

Ln a

Ea/K

μmol CaCO3 g−1 h−1

Reference

28.75 22.68 16.84 16.33 22.68 6.69 29.97 49.15 54.95 36.4 27.21 27.74 11.82

7.63 5.75 3.99 4.07 5.75 1.07 7.65 13.77 14.99 9.79 7.15 8.02 2.55

1.01 6.84 7.56 3.36 7.56 16.12 19.11 4.3 15.7 3.50 1.92 4.5 3.2

Clavier et al. (2009) Tagliarolo et al. (2013a) Tagliarolo et al. (2013a) Tagliarolo et al. (2013a) Tagliarolo et al. (2013a) Tagliarolo et al. (2013a) Tagliarolo et al. (2013a) Tagliarolo et al. (2012) Tagliarolo et al. (2012) Tagliarolo et al. (2013a) Tagliarolo et al. (2013a) Lejart et al. (2012) Tagliarolo et al. (2013b)

a, normalization constant; Ea, activation energy (Joules per mole); K, Boltzmann's constant (8.31 J K−1 mol−1); DIC, dissolved inorganic carbon.

The annual regional CO2 flux in the Brittany intertidal rocky shore communities was estimated by multiplying the habitat surface by the mean annual carbon emission. The surface of the intertidal rocky shore was estimated to 91 km2 and as the exposed areas correspond to 25% of the rocky shore the exposed rocky shore communities were expected to cover 22.7 km2 (Hily et al., 2013). To tentatively estimate the effect of temperature on average annual carbon fluxes, calculations for each sampling site were repeated for every year with increasing or decreasing mean annual temperature values of 0.5, 1, 1.5, or 2 °C, and results were averaged by shore level. An analysis of covariance (ANCOVA) was used to compare the slopes of the regression between temperature and carbon emissions. In order to compare air or SST temperatures between sites, years and mediums a one way ANOVA was applied since the data set was not big enough to allow a factorial ANOVA. To compare carbon fluxes between sites and years for each shore level, two-way ANOVAs were applied. Statistical analyses were performed with R environment (R Development Core Team, 2009). 3. Results 3.1. Environmental parameters The average annual air temperature in the Brittany coastal zone varied between 11.2 °C in 2010 and 12.3 °C in 2007 (Table 1). Minimal values were recorded near Brest and maximal values near the monitoring site of Arcouest. Average annual SST ranged between 12.2 °C in 2010 and 13.8 °C in 2007 (Table 1). Minimal values were recorded in the north of Brittany and maximal values in the south. Average annual temperature was significantly different between years (one-way ANOVA, F = 4.93, df = 6, p b 0.0005) as well as between air and water (oneway ANOVA, F = 179.14, df = 1, p b 0.0005) while it was not significant between sites (one-way ANOVA, F = 1.61, df = 8, p N 0.05). 3.2. Spatial and temporal variabilities of the communities The survey of macrozoobenthic communities allowed us to compare temporal natural variations among sites. The MDS plots showed a clear assemblage grouping both at high- (Fig. 2A) and low-shore (Fig. 2B), and the low stress value (b 0.1) indicated a good ordination with limited prospects of a misleading interpretation (Clarke, 1993). At the highshore, the Molène and Arcouest sites were broadly separated from the others, due to their lowest biomasses. Conversely, at the low-shore, only the Molène monitoring site was well separated from the others. The Doëlan and Aber Island low-shore communities showed high

temporal variability, in contrast to other sampling stations where inter-annual variability was minimal.

3.3. Carbon emissions estimations The data set of the total annual carbon fluxes is not complete (data from some sites were not available for all the years, see Appendices A and B), and thus some factor combinations are missing. Consequently, it proved impossible to estimate the interaction effect between the two factors years and sites. This incomplete design obliged the analysis of the single factors separately without considering the interactions. The annual carbon fluxes at the two shore levels were not significantly different across the six studied years (two-way ANOVA, F = 2.50, df = 5, p N 0.05 for the high shore and F = 0.75, df = 5, p N 0.5 for the low shore). Conversely, carbon fluxes varied significantly between sites (two-way ANOVA, F = 20.53, df = 8, p N 0.00005 for the high shore, F = 6.41, df = 8, p b 0.00005 for the low shore). The Tukey's HSD post doc table revealed that numerous statistical differences were present between the 9 sampling sites. The most important differences were for Doëlan site that significantly differed from all the other sites except from Aber Island on both high and low shore levels. Also Aber Island fluxes were significantly different from most sites especially at the high level except only from Doëlan and Locmariaquer (Fig. 3). High- and low-shore carbon fluxes were maximal at the Doëlan site (27.1 and 59.9 mol C m−2 yr−1, respectively) and minimal at Molène (0.7 and 0.9 mol C m−2 yr−1, respectively). The contribution of the five species groups to the total carbon fluxes differed among sites and between levels at the same site. While barnacle carbon fluxes were large at both shore levels, emissions due to gastropods were higher at high-shore and those due to mussels were higher at the low-shore level (Tables 3 and 4). Barnacles were present at all studied sites, and their contribution to total average fluxes was high (4.3 and 4.2 mol C m−2 yr−1, average between sites in high- and low-shore, respectively); conversely, mussels showed a patchy distribution with higher abundances, and thus fluxes, at the Doëlan and Aber Island sites (Tables 3 and 4, Appendices A and B). Limpets were widely distributed on all sites, but their contribution to total carbon fluxes was usually minimum when present. Mean carbon fluxes from high-shore (10.7 mol C m−2 yr−1) were mostly due to respiration during emersion (90% of total fluxes); respiration plus the calcification process during immersion was less important (8 and 2%, respectively). In low-shore, underwater respiration was predominant (58% of total fluxes), while aerial respiration represented 30% and calcification 12% of total carbon fluxes.

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A

B

Fig. 2. Non-metric multidimensional scaling by monitoring sites and sampling years. Analyses were performed on the biomasses of macrozoobenthic communities (A: high-shore; B: low-shore).

The mean annual carbon emission of the intertidal exposed rocky macrozoobenthic community calculated in this study was 14.3 mol C m− 2 yr− 1 and the average biofilm net primary production estimated from the literature considering a 12 h:12 h day/night cycle was −3.4 mol C m−2 yr−1. Thus, if we consider the exposed intertidal shore area, the emissions should be around 2978 t C yr−1. 3.4. Effect of temperature variation on carbon fluxes The average carbon emission calculated for the different studied years and monitoring sites was 10.7 mol C m− 2 yr− 1 at the highshore and 17.8 mol C m−2 yr−1 at the low-shore level. Simulation of temperature effect on carbon fluxes showed a linear increase for both levels (Fig. 4). The two levels exhibited similar responses to temperature changes, and regression slopes did not differ significantly (ANCOVA homogeneity of slopes, F = 0.4, df = 1, p N 0.5) with an increase of about 10 g C m−2 yr−1 for each 1 °C change in temperature.

4. Discussion 4.1. Spatial and temporal natural variations of carbon fluxes In this study, calcification and respiration related carbon fluxes were calculated for each species as a function of the average annual temperature of the air and the sea surface. The average total annual carbon emission was 213 g C m−2 yr−2 in low-shore and 129 g C m−2 yr−2 in high-shore. Despite this study using an indirect method to estimate the carbon emissions from macrozoobenthos data and laboratory experiments, results were in the same order of magnitude than previous studies performed in the field. Our results were similar to studies using benthic chamber methods in intertidal sandy and muddy substrates (14–188 g C m− 2 yr− 2) (Migné et al., 2009) but much lower than respiration measured on maerl beds (407 g C m− 2 yr−2) (Martin et al., 2007). Moreover, the average carbon production of 14.3 mol C m−2 yr−1 calculated for the macrozoobenthic community

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Fig. 3. Geographical variation of average annual carbon fluxes (mol C m−2 yr−1) in high-shore (light gray point) and low-shore (dark gray point).

was in the same order of magnitude as the fluxes estimated by Hily et al. (2013) on the same area (22.9 mol C m−2 yr−1). We believe our estimation is more accurate than the one calculated by Hily et al. (2013) since they used a general allometric equation relating biomass to respiration without distinction between species. Rocky shores support a wide variety of habitats (see website http:// eunis.eea.europa.eu/habitats.jsp) and are characterized by a high heterogeneity due to varying physical conditions (Kostylev et al., 2005). Estimation of coastal system fluxes depends on measures of different coastal community parameters (such as species composition, temperature, irradiance, and tidal regime) and on their respective surface area (Laruelle et al., 2010). Little is known about the contribution of intertidal exposed rocky shore communities to global carbon emission (Hily et al., 2013). For this reason, the present study has considered both the temporal and spatial variabilities of the macrozoobenthic community and temperature to give an evaluable estimation of carbon fluxes. Considering both average annual macrozoobenthic biomass and carbon fluxes showed that the spatial (inter-site) variability was more important than the inter-annual variations. The analysis of the carbon fluxes spatial variations showed that Doëlan and Aber Island exhibited clearly higher carbon fluxes than the other sites and the MDS analysis

performed on the biomass/species matrix revealed that those sites were also characterized by higher inter-annual community variability. Those statistically significant differences were probably caused by the highly variable mussel abundance on those two sites. Mussels respond strongly to short-term and long-term climatic patterns, varying recruitment and growth rates (Menge et al., 2008). Mussel-dominated communities seem more affected than other intertidal rocky shore communities (especially those dominated by barnacle only) by interannual variability. Both carbon fluxes and biomass are minimal in Molène station, where the community strongly differed from the community of the other sites (as shown on the MDS analysis) on both high- and lowshore. In Molène, macrozoobenthos biomass is very low, probably because of harsh environmental conditions (strong wind, waves and boulder movements) prevailing on this oceanic island. While the temporal community composition variations were too small to result in significant fluxes variations, geographical variability was highly significant in both shore levels. Indeed within exposed shores, local factors such as temperature, water currents, substrate type, and biological interactions may explain the variability among sites (Lewis, 1964). The different spatial dynamics in biomass and carbon emissions estimated for the two shore levels were principally due to different

Table 3 Estimated annual average carbon fluxes (mol C m−2 yr−1) calculated at high-shore level for each site and species group (respiration in emersion–respiration in submersion–calcification in submersion) and total values.

Saint-Briac Arcouest Callot Sainte-Marguerite Molène Bay of Brest Aber Island Doëlan Locmariaquer

Barnacle

Mussel

Limpet

Oyster

Gastropod

Total

3.7–0.3–0.0 0.5–0.0–0.0 2.6–0.2–0.0 4.2–0.4–0.0 0.2–0.0–0.0 4.7–0.5–0.0 7.7–0.7–0.1 5.2–0.5–0.0 5.6–0.5–0.0

0.1–0.1–0.0 / / / / / / / /

0.8–0.0–0.0 0.7–0.0–0.0 0.3–0.0–0.0 3.5–0.1–0.0 / / 2.4–0.1–0.0 0.5–0.0–0.0 /

/ / / / / / / / /

2.2–0.2–0.1 0.1–0.0–0.0 2.0–0.1–0.1 2.2–0.2–0.1 0.4–0.0–0.0 1.0–0.1–0.0 8.5–0.7–0.4 18.5–1.6–0.8 6.5–0.5–0.3

7.5 1.4 5.3 10.7 0.7 6.3 20.7 27.1 13.5

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Table 4 Estimated annual average carbon fluxes (mol C m−2 yr−1) calculated at low-shore for each site and species group (respiration in emersion–respiration in submersion–calcification in submersion), and total values.

Saint-Briac Arcouest Callot Sainte-Marguerite Molène Bay of Brest Aber Island Doëlan Locmariaquer

Barnacle

Mussel

Limpet

Oyster

Gastropod

Total

1.7–1.7–0.1 1.6–1.5–0.1 1.6–1.6–0.1 1.0–1.0–0.1 / 2.3–2.4–0.2 2.8–3.0–0.2 3.6–3.9–0.3 2.9–3.0–0.2

/ 0–0.1–0 / / / / 3.1–29.3–3.5 9.1–27.2–8.2 0.3–0.7–0.2

1.0–0.4–0.1 1.1–0.4–0.1 1.3–0.5–0.1 1.3–0.5–0.1 0.6–0.2–0.1 1.2–0.5–0.1 0.9–0.4–0.1 1.3–0.5–0.1 1.7–0.7–0.2

/ 0–0.4–0.2 / / / 0.1–0.9–0.3 / / 0.1–1.4–0.4

1.0–1.0–0.5 0.1–0.2–0 0.5–0.7–0.1 0.2–0.2–0.1 / 0.1–0.1–0 0.2–0.2–0.1 2.4–2.3–1.2 0.9–1.0–0.3

7.7 5.9 6.5 4.4 0.9 8.4 43.8 59.9 14.0

communities composition and immersion/emersion times. At the highshore level, populations of barnacles and of M. neritoides are predominant, and their contributions to total fluxes are 40 and 51%, respectively. At the low-shore level, mussels contribute 55% of the total fluxes, but they are present only on a few sites. Mussels are known to form extensive beds of juveniles on wave-exposed shores but the distributions are often patchy (Little et al., 2009). Conversely, limpets and other gastropods are largely distributed on both shore levels and were recorded at all studied sites. While high-shore is immersed for 26 days per year on average, lowshore is immersed much longer (average 171 days per year). The different contributions to high- and low-shore level fluxes in emersion and immersion are mainly due to their different air/water exposition times. Because we postulate that the calcification process is possible only underwater (Buschbaum and Saier, 2001; Pannella, 1976), carbon emission from calcification is higher at the low-shore than at the highshore level. At the low-shore level, the carbon originating from calcification corresponds to 12% of the total carbon emission. This estimation for the entire community is in accordance with the data for each individual species used in this study (11% for limpets, 25% for oyster, 3% for barnacles, between 7 and 14% for mussels, and between 13 to 23% for the other gastropods) (Clavier et al., 2009; Lejart et al., 2012; Tagliarolo et al., 2012, 2013a, 2013b). Previous studies performed in the same area however, provided substantially higher estimates of the contribution of the calcification process to total carbon emission (between 47 and 82%) (Golléty et al., 2008a; Hily et al., 2013). Those differences in estimation could mostly be due to the various calculation methods. In the study by Golléty et al. (2008a) the respiration was calculated using a general equation established for all the benthic organisms (i.e., not for each individual species such as in the present study) and the

calcification rates were approximated from calcimass values. The study of Hily et al. (2013) was based on estimations from the literature of CaCO3 production data measured in the California coastal waters. In comparison, our study used respiration and calcification data directly measured from the individual species inhabiting Brittany shores, thereby our results will be able to give a more accurate estimation of the carbon fluxes. Respiration, primary production, and calcification are the three principal components of coastal community metabolism. Our study evaluated the contribution of the major populations of fauna living on an exposed rocky shore; macroalgal respiration and production were not considered. Algae and microalgae were indeed not studied during the REBENT program involving the exposed rocky shore community because they are mostly absent from the monitored sites and thus should not significantly contribute to carbon fluxes. The contribution of bacteria to carbon fluxes however can also be important, and in situ measurements would be necessary to evaluate the entire ecosystem respiration and primary production contribution to carbon fluxes (Golléty and Crowe, 2013; Golléty et al., 2008b). The data used in this study to calculate the contribution of the primary producers were extrapolated from literature data on artificial rocky shores (Magalhães et al., 2003) since data on temperate exposed rocky shore are not available yet. Our estimations show that biofilm's net primary production can compensate only 31% of macrozoobenthic carbon emissions, but further studies are necessary in order to evaluate the possible contribution of bacteria, microphytobenthos and meiobenthos to the total carbon fluxes (Schwinghamer et al., 1986). Moreover, a better knowledge of macrozoobenthic species metabolism (such as for L. obtusta and G. pennanti) can also improve the accuracy of our estimations. Our extrapolation for regional carbon emissions suggests that the intertidal exposed rocky shore community is a heterotrophic community that could be a source of CO2 for the surrounding environment. 4.2. Effect of temperature variation on carbon fluxes

Fig. 4. Estimated average annual carbon fluxes for the different studied years and monitoring sites (mol C m−2 yr−1) for exposed rocky shore communities as a function of temperature variation. 0 corresponds to the average annual temperature calculated for the studied period.

Temperature is the single best predictor of respiration rates of a specific community (Raich and Schlesinger, 1992). During high tide, intertidal organisms are submerged, and their body temperature is in equilibrium with water. Conversely, during emersion, an organism's body temperature may differ from air temperature (Lima et al., 2011). In our study, we assumed that air and water temperatures approximate organism's body temperatures, which could be considered reasonable for small ectotherms living in shaded environments (Hertz et al., 1993). However, most rocky shores in Brittany may reach high temperatures due to sun exposure in summer. It has still to be confirmed whether this approximation could lead to an underestimation of the body temperature, since benthic animals living in sun-exposed shores can reach much higher temperatures than the individuals attached to a shaded surface (Seabra et al., 2011). Increased temperatures lead to higher respiration rates which could result in increased carbon fluxes from the community. The response of communities to changes in temperature involves biologically mediated metabolic processes.

32

M. Tagliarolo et al. / Journal of Marine Systems 149 (2015) 25–35

According to the IPCC estimations, global air and sea surface temperatures have risen in the past century, and warming trends are expected to accelerate in the current century (Hartmann et al., 2013). In our study, the impact of a variation of ± 2 °C was tested to evaluate the response of benthic community to temperature variations. The two mediolittoral levels showed similar responses with a variation of 10 g C m − 2 yr− 2 for each 1 °C shift in temperature. The potential feedback to an increase of 1 °C would lead to an increase of 4–7% in carbon emissions from the intertidal exposed rocky shore community. Further analysis of seasonal data is required, however, to define the temperature–metabolism relationship on a finer time scale than our annual analysis provides. Temperature changes would probably not be exactly the same in different seasons and might lead to different responses of metabolism rates (Christensen et al., 2007; Solomon et al., 2007). Climate change can enhance coastal community metabolism through changes in coastal physics, increases in terrestrial inputs, and shifts in carbonate chemistry by pH modification. Carbon fluxes estimated in this study may contribute to an understanding of metabolic carbon flux responses to climate warming. We did not consider however the possible influence of temperature variation on community composition and the effect of possible ocean acidification induced by the increase in atmospheric CO2 (Byrne, 2011; Harley et al., 2006). Many marine organisms live close to their thermal tolerance limits, and an increase in temperature could negatively affect the performance and survival of a large number of species living on temperate rocky shores (Somero, 2002). In the present study, we have shown that even if community composition varied among years (mostly changes in biomass of filter feeders), CO2 fluxes remained constant over the seven years. The intertidal hard-bottom communities have already been shown to compensate the loss or decline of species by others and maintain a relative stability in community abundance and metabolism (Valdivia et al., 2012). Thus, even if species composition may change because of climate change if we consider longer time data series, we estimate that the carbon emission calculated for a site should remain roughly the same. Despite the fact that carbon emissions seemed to be stable during the studied period, other factors such as food availability and composition can in the future influence the community composition and consequently the carbon emissions (Harley et al., 2006).

4.3. Conclusion The contribution of the intertidal exposed rocky shore to global carbon production, calculated from temperature and community abundances from 2004 to 2010, varies between 132 and 216 g C m−2 yr−2 for the high- and low-shore, respectively. Our results showed that the most important factor influencing the carbon emission was the community composition and biomass dictated by the position on the shore. Further studies will be necessary to evaluate the communities' variability along the vertical tidal gradient to evaluate the effect of long-term environmental changes in those communities. Intertidal rocky shore assemblages are generally accessible and relatively easy to monitor. They are thus considered good site candidates for studying the effects of climate changes on coastal areas (Cruz-Motta et al., 2010). In situ measurements of carbon fluxes are possible, but they are still complicated and expensive; for these reasons, they have been used only for short-term and small-scale assessments (Golléty et al., 2008b). The study of metabolic rates of individual species in the laboratory is more simple and consistent and this method allows for coupling of data with species abundances to monitor large areas and different sites. Because of the important spatial and temporal variabilities of intertidal communities, large-scale studies for global carbon estimations are required to encompass such variability; carbon fluxes estimated in our study could therefore be considered representative for the temperate barnacle-dominated rocky shore. Responses of the coastal ecosystems to climate change are almost unpredictable, but the influence of climate change on community metabolism is clearly compelling. The responses of intertidal exposed rocky shore invertebrates to temperature increases could intensify CO2 emission and consequently influence climate change processes.

Acknowledgments This study was supported by the ANR CHIVAS (Chimie des Valves de la Coquille Saint Jacques Européenne) (ANR-09-BLAN-0335-01) program. We thank the REBENT group for providing species abundances data (www.rebent.org). We thank the IUEM observatory for help with species identification.

Appendix A. Biomasses of a macrozoobenthic community living in the high shore (g AFDW m−2) calculated for each year and studied site

2004

2005

2006

Saint-Briac Arcouest Callot Sainte-Marguerite Bay of Brest Aber Island Doëlan Locmariaquer Saint-Briac Arcouest Callot Sainte-Marguerite Molène Aber Island Doëlan Locmariaquer Saint-Briac Arcouest Callot Sainte-Marguerite Molène

Barnacles

G. pennanti

G. umbilicalis

L. littorea

L. obtusata

68 10 48 76 94 132 92 88 58 7 48 61 3 86 65 71 59 6 47 75 3

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 1 0 0 0 0

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

L. saxatilis 0 0 0 0 0 0 0 1 0 0 1 0 0 0 0 0 0 0 0 0 0

Mussels

N. lapillus

O. lineatus

Oysters

Limpets

2 0 0 0 0 0 0 0 7 0 0 0 0 0 0 0 5 0 0 0 0

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 2 0 0 0

6 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 0 0 0 0

5 4 2 26 0 2 6 0 2 3 3 13 0 7 2 1 7 5 2 27 0

M. neritoides 12 0 0 8 4 52 74 23 0 0 0 7 3 72 77 12 13 0 4 6 0

M. Tagliarolo et al. / Journal of Marine Systems 149 (2015) 25–35

33

Appendix A (continued) (continued)

2007

2009

2010

Bay of Brest Aber Island Doëlan Locmariaquer Saint-Briac Arcouest Sainte-Marguerite Molène Bay of Brest Aber Island Doëlan Locmariaquer Saint-Briac Arcouest Callot Sainte-Marguerite Molène Bay of Brest Aber Island Doëlan Locmariaquer Saint-Briac Arcouest Callot Molène Bay of Brest Aber Island Doëlan Locmariaquer

Barnacles

G. pennanti

G. umbilicalis

L. littorea

L. obtusata

L. saxatilis

Mussels

N. lapillus

O. lineatus

Oysters

Limpets

M. neritoides

67 147 43 69 52 7 66 4 84 162 90 104 71 7 38 67 4 94 111 121 112 69 7 43 6 74 175 117 98

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 2

0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 1 0 0 0 1 0 0 13 0 0 0 0 0 0 0 0 11 0 0 0 0 0

0 1 0 0 6 0 0 0 0 1 0 0 3 0 0 0 0 0 1 0 0 0 0 0 0 0 1 0 0

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

0 1 0 0 0 0 0 0 0 1 0 0 0 1 1 0 0 2 0 0 2 0 1 0 0 0 0 0 0

0 0 0 0 2 0 0 0 0 0 0 0 4 0 0 0 0 0 0 0 0 2 0 0 0 0 0 0 0

0 10 1 0 6 5 22 0 0 12 2 1 7 5 1 30 0 0 65 5 0 7 7 3 0 0 4 3 0

4 42 40 43 5 0 21 2 0 43 76 28 10 0 15 14 4 13 47 200 51 30 0 13 1 4 22 130 40

Appendix B. Biomasses of a macrozoobenthic community living in the low shore (g AFDW m−2) calculated for each year and studied site

2004

2005

2006

2007

2009

Saint-Briac Arcouest Callot Sainte-Marguerite Bay of Brest Aber Island Doëlan Locmariaquer Saint-Briac Arcouest Callot Sainte-Marguerite Molène Aber Island Doëlan Locmariaquer Saint-Briac Arcouest Callot Sainte-Marguerite Molène Bay of Brest Aber Island Doëlan Locmariaquer Saint-Briac Arcouest Sainte-Marguerite Molène Bay of Brest Aber Island Doëlan Locmariaquer Saint-Briac Arcouest Callot

Barnacles

G. pennanti

G. umbilicalis

L. littorea

L. obtusata

L. saxatilis

Mussels

N. lapillus

O. lineatus

Oysters

Limpets

M. neritoides

33 54 60 52 95 124 109 77 41 46 32 27 0 73 91 84 60 46 45 29 0 38 60 46 54 36 26 23 0 44 100 113 115 44 30 48

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 3 0 0 0 0 0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 2 0 0 0 0 2 0 0 2 0 0 0 0 2 0 1 1 0 0 0 0 1 2 0 0 0 0 0

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 16 0 0 0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0

0 0 0 0 0 0 0 4 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 0 0 0

0 2 0 0 0 146 46 9 0 2 0 0 0 120 29 7 0 2 0 0 0 0 19 289 0 0 0 0 0 0 874 126 6 0 0 0

0 0 0 1 0 1 0 1 3 0 0 1 0 0 0 0 0 0 0 0 0 2 0 1 0 0 1 1 0 0 0 5 0 0 0 0

0 2 15 0 0 0 0 26 0 4 8 0 0 0 0 11 0 4 10 0 0 0 0 0 7 0 2 0 0 0 1 0 4 0 2 12

0 17 0 0 28 0 0 88 0 18 0 0 0 0 0 56 0 9 0 0 0 24 0 0 26 0 6 0 0 17 0 0 24 0 13 0

39 14 21 13 18 8 10 22 4 1 9 14 4 3 3 16 8 24 13 18 5 13 35 5 22 7 12 15 6 15 7 46 23 6 12 20

19 0 0 5 0 4 29 5 0 0 0 1 0 0 12 0 7 0 0 0 0 0 0 12 3 0 0 0 0 0 0 22 0 7 0 1

(continued on next page)

34

M. Tagliarolo et al. / Journal of Marine Systems 149 (2015) 25–35

Appendix B (continued) (continued)

2010

Sainte-Marguerite Molène Bay of Brest Aber Island Doëlan Locmariaquer Saint-Briac Arcouest Callot Molène Bay of Brest Aber Island Doëlan Locmariaquer

Barnacles

G. pennanti

G. umbilicalis

11 1 93 62 123 70 95 66 51 0 78 93 150 92

0 0 0 0 0 0 0 0 0 0 0 0 0 0

0 0 3 1 0 0 0 0 0 0 2 1 0 0

L. littorea 0 0 0 0 0 0 0 0 0 0 0 0 0 3

L. obtusata

L. saxatilis

Mussels

N. lapillus

O. lineatus

Oysters

Limpets

M. neritoides

0 0 0 0 0 0 0 0 0 0 0 0 0 0

0 0 0 0 0 2 0 0 0 0 0 0 2 3

0 0 0 429 229 1 0 0 0 0 0 22 389 6

0 0 0 4 1 0 0 0 0 0 0 0 0 0

1 0 1 0 0 0 0 3 14 0 0 0 0 0

0 0 28 0 0 4 0 11 0 0 21 0 0 6

15 10 9 7 17 26 9 12 17 12 22 8 13 12

2 0 0 1 32 4 23 0 0 0 0 0 22 0

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