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Biochemical characteristics of settling particulate organic matter at two north-western Mediterranean sites: a seasonal comparison
Estuarine, Coastal and Shelf Science 58 (2003) 423–434
Biochemical characteristics of settling particulate organic matter at two north-western Mediterranean sites: a seasonal comparison Sergio Rossia,*, Antoine Gre´mareb, Josep-Marı´ a Gilia, Jean-Michel Amourouxb, Esther Jordanaa, Gilles Ve´tionb a Instituto Ciencias del Mar (CSIC), Paseo Marı´timo de la Barceloneta 37-49, Barcelona 08003, Spain Observatoire Oce´anologique de Banyuls, Laboratoire d’Oce´anolographie Biologique de Banyuls, UMR 7621, CNRS-UPMC, BP44 F66651 Banyuls Cedex, France
b
Received 12 December 2002; accepted 31 March 2003
Abstract Gross sedimentation rates (GSR) and the main biochemical characteristics of settling particulate matter were monitored at two NW Mediterranean sites (the Bay of Banyuls-sur-Mer, France, and the Medes Islands, Spain) throughout a year to assess possible differences in particulate organic matter (POM) availability to the benthic community. A similar seasonal pattern was observed at both sites with higher organic contents and lower GSR during the spring–summer than during the autumn–winter period. At both sites, there was a negative correlation between GSR and sediment trap organic contents, which is indicative of the importance of resuspension in driving GSR. Along the same line, GSR in Medes correlated positively with wave height. The principal component analysis based on GSR and biochemical characteristics of sediment trap material always segregated samples from the two studied sites mostly due to the occurrence of higher lipid and lower carbohydrate contents in Medes. These differences were indicative of the presence of more labile settling POM in the Medes Islands. They were more pronounced during the spring–summer than during the autumn–winter period. Such a pattern may reflect differences in the sensitivity of the two studied sites to resuspension. According to this interpretation, between-sites differences would be high when resuspension is low (i.e. during the spring–summer period when resuspension would mainly affect Banyuls) and become low when resuspension is high (autumn–winter period when resuspension would affect both sites). Ó 2003 Elsevier Ltd. All rights reserved. Keywords: gross sedimentation rates; seasonality; settling particulate organic matter; biochemical characteristics; spatial comparison; north-western Mediterranean
1. Introduction The sources of particulate organic matter (POM) in the coastal environment are heterogeneous and exhibit seasonal patterns both from a quantitative and a qualitative standpoint (Cripps & Clarke, 1998; Gre´mare et al., 1997; Navarro & Thompson, 1995; Tenore, 1988). Because an important component of their diet is derived from settling or sedimented POM, seasonal pulses of available organic matter influence the abundance, the * Corresponding author. E-mail address: [email protected] (S. Rossi). 0272-7714/03/$ - see front matter Ó 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S0272-7714(03)00108-2
biomass and the activity of bottom communities (Graf, Bengtsson, Schulz, & Theede, 1982; Graf, Shulz, Peinert, & Meyer-Reil, 1983). Due to seasonality in primary production, suspension, deposit and detritus feeders may thus show seasonal patterns in warm temperate, cold temperate and polar seas (Barnes & Clarke, 1995; Coma, Ribes, Gili, & Zabala, 1998; Ribes, Coma, & Gili, 1998; Riisgard, 1998). The relationship between pulses of settling POM and reproduction or growth has been already documented in several benthic species (Charles, Gre´mare, Amouroux, & Baudart, 1995; Gre´mare, 1994; Gre´mare et al., 1997; Marsh, Gre´mare, & Tenore, 1989). The activity of benthic
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organisms, as assessed through direct observations, ATP, heat or biomass production is also influenced by seasonal inputs of organic matter (Ducheˆne & Rosenberg, 2001; Graf et al., 1982, 1983; Jordana, Ducheˆne, Charles, Gre´mare & Amouroux, 2000; Meyer-Reil, 1983; Pfannkuche, 1993). One of the difficulties in relating POM characteristics and benthic fauna is the assessment of POM nutritional value. Bulk POM biochemical characteristics such as total organic matter, organic carbon and nitrogen in both sediments and settling POM have been used as a proxy of food availability for benthic primary consumers (Charles et al., 1995; Gre´mare, 1994; Levinton, Bianchi, & Stewart, 1984; Tenore, 1981; Valiela et al., 1984). This approach is limited because most of the settling and/or sedimented POM is refractory, and cannot be absorbed by benthic invertebrates (Plante & Jumars, 1992; Plante & Shriver, 1998). During the last 20 years both biological and biochemical assays have been developed to better assess true nutritional organic matter availability for benthic primary consumers (Dell’Anno, Fabiano, Mei, & Danovaro, 2000; Gre´mare et al., 1997, 2002, in press; Mayer, Schick, Sawyer, & Plante, 1995; Mayer, Schick, & Setchell, 1986; Medernach, Gre´mare, Amouroux, Colomines, & Ve´tion, 2001). It appears that some specific POM biochemical descriptors such as enzymatically hydrolysable amino acids (Mayer et al., 1995) and lipids better correlate with the abundance and the biomass of benthic fauna than bulk characteristics (Gre´mare et al., 2002, in press). These results are supported by the good correlation of those specific parameters with growth rates of selected invertebrates during laboratory experiments (Gre´mare et al., 1997). Seasonality in pelagic primary production is strong in the Mediterranean due to the winter–spring phytoplanktonic bloom (Estrada, 1996; Estrada, Vives, & Alcaraz, 1985). Seasonality affects the availability of POM to interface feeders (Gre´mare et al., 1997). The relationship between POM characteristics and benthic standing stocks has already been documented several times in this area (Danovaro, Tselepides, Otegui, & Della Croce, 2000; Gre´mare et al., 2002, in press). Even if the study of temporal and spatial changes in potential food items is a key step in understanding the dynamics of benthic communities, studies considering specific biochemical characteristics such as lipids are yet relatively scarce in the Mediterranean (Fichez, 1991; Gre´mare et al., 1997, 1998; Medernach et al., 2001; Posedel & Faganeli, 1991; Pusceddu, Sara`, Armeni, Fabiano, & Mazzola, 1999), and only very few of those studies have considered small scale spatial variations (Airoldi & Cinelli, 1996; Fichez, 1991; Pusceddu et al., 1999). The aim of this work was to compare both the absolute values and seasonal changes in gross sedimentation rates (GSR) and in the main biochemical
characteristics of settling POM at two sites located only 50 km apart but which exhibit differences in some key environmental features and differ in the abundance and the composition of their benthic fauna (Gili & Ros, 1985; Guille, 1971a,b). The working hypotheses were that: (1) both the GSR and the biochemical characteristics of settling POM may differ at the two sites, and (2) the magnitude of between-sites differences may vary seasonally. In order to test these hypotheses, GSR together with the main biochemical characteristics of sediment trap collected materials were monitored both in the Bay of Banyuls-sur-Mer (Banyuls) and in the Medes Islands (Medes) (NW Mediterranean). The main environmental parameters were also monitored to identify some of the factors potentially accounting for between-sites differences.
2. Materials and methods 2.1. Environmental parameters Wind maximum speed and direction were registered daily together with rain fall both in Medes (Servei Meteorolo´gic de l’Estartit) and in Banyuls (Station Me´te´o France du Cap Be´ar). Wave height was also recorded in Medes (Servei Meteorolo´gic de l’Estartit). In Banyuls, wave data consisted in the estimation of the state of the sea (a rough index that can be used as a proxy for wave height) by the Cap Be´ar Meteo France station. Water samples were collected at both sites to assess chlorophyll a (chl a) concentrations. Samples were collected at 24 m depth in Banyuls and at 20 m depth in Medes. They were collected weekly in Banyuls and 2–5 times a month in Medes. Samples (0.2 l) were filtered on Whatman GF/F filters and chl a was then assessed on triplicates after Parsons, Maita, and Lalli (1985).
2.2. Sediment traps Two sets of sediment traps were moored in Banyuls (42 2993099N, 3 0897099E, France), and in Medes (42 0295599N, 3 1393099E, Spain) (Fig. 1A, B). The traps were moored over 27 m deep sandy bottoms in Banyuls and over 30 m deep sandy-stone bottoms in Medes. The two sets of traps were identical. They consisted of two polyethylene pipes prolonged by a cone and a collector with an aspect ratio of 4.75. The mouths of the traps were located 3 m above the bottom. The traps were collected by SCUBA divers weekly in Banyuls, and every other week in Medes between July 1997 and August 1998. Deployment duration was always less than 10 days.
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Fig. 1. Map showing the location of the two studied sites. Arrows indicate study areas: (A) Banyuls-sur-Mer, (B) Medes Islands. The stars indicate sediment trap moorings.
2.3. Biochemical assays Immediately after collection, samples were centrifuged (4000 rpm, 15 min), briefly rinsed with distilled water, frozen (20 C) and freeze-dried. The collected material was then sieved on a 200 lm mesh, weighed (both fractions, <200 and >200 lm) and stored at 20 C. GSR were computed as the total amount of
POM collected within the traps per unit of time and surface area. All biochemical characteristics were measured on the <200 lm size fraction. Organic contents were assessed by measuring combustion weight loss (450 C for 5 h). Organic carbon and nitrogen were measured using a CHN LECO CC-100 elemental analyser, after acidification with 1 N HCl. Proteins were assayed after Lowry,
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Rosebrough, Farr, and Randall (1951) as modified by Rice (1982) to account for the absorption of phenolic compounds. Carbohydrates were assayed after Dubois, Gilles, Hamilton, Rebers, and Smith (1956). Lipids were assayed after Barnes and Blackstock (1973). All analyses were ran on triplicates.
data, two samples (i.e. M2 and M20) were excluded from this analysis.
3. Results 3.1. Environmental parameters
2.4. Statistical analysis Environmental parameters at both sites were compared using t-tests for paired samples. General trends in the characteristics of settling POM at both sites were first compared using a principal component analysis (PCA) based on GSR and all measured biochemical parameters. Between-sites differences were then further assessed for each single biochemical parameter. Because: (1) there were significant correlations between GSR and biochemical characteristics of sediment trap materials at both sites, and (2) the range of GSR differed among sites, covariance analyses were used to compare the slopes and intersections of the correlation models linking biochemical characteristics and GSR (log10 transformed data). These tests were performed to assess whether or not between-sites differences in biochemical characteristics were associated to differences in GSR patterns. To better assess within site seasonal changes, GSR and biochemical data were pooled into two groups (i.e. spring–summer period and autumn–winter period) as proposed by Gre´mare et al. (1997, 1998). The mean values of these seasonal samples were then compared using t-tests for independent samples. Since this was the first report of sediment trap data in Medes, a second PCA was ran to assess the relationship between sediment trap characteristics and environmental parameters in this area. This PCA was based on GSR and all the environmental parameters and biochemical characteristics measured at this site. Due to the lack of chl a
Wind speed (Fig. 2) was higher in Banyuls than in Medes during the studied year (t-test for paired samples, p < 0:001). Wind direction also differed between sites. Rainfall was of the same magnitude and tended to occur simultaneously at both sites (Fig. 3A). Waves tended to be higher in Banyuls than in Medes (data not shown). Chl a concentrations (Fig. 4) were higher in Medes than in Banyuls-sur Mer (t-test for paired samples, p ¼ 0:006). Between-sites differences were larger during winter and spring. At both sites, the highest chl a concentrations occurred during February. The period characterised by high chl a concentrations started earlier and lasted much longer in Medes than in Banyuls, however. December corresponded both to the onset of increase in chl a concentrations in Medes and to the highest flow of the Ter River (Fig. 3B). There were other slight betweensites differences in temporal changes in chl a concentrations: (1) the autumn bloom was only apparent in Banyuls (November), and (2) there were secondary peaks in Medes during August (Figs. 3B and 4). 3.2. Sediment trap characteristics At both sites, small grain sizes dominated the minerals in the trap. In Banyuls-sur-Mer, the average diameter of the collected material was typically between 10 and 20 lm, whereas it was close to 20 lm in Medes Islands (Gre´mare, personal observation). The GSR and the biochemical characteristics recorded during the
Fig. 2. Daily wind maximum speed (m s1) and direction in Banyuls-sur-Mer and Medes Islands.
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Fig. 3. (A) Rainfall record in Banyuls-sur-Mer (white dot-solid line) and Medes Islands (black dot-dashed line) meteorological stations. (B) Flow of the Ter River (Medes Islands only).
present study are listed in Table 1. Proteins, lipids and carbohydrates accounted for an average of 45 and 42% of total organic carbon in Banyuls and in Medes, respectively. In Banyuls, this proportion was as low as 17% immediately after a strong resuspension event (B10). This trend was less apparent in Medes. The projections of variables and sampling dates on the first plane of the PCA involving all the sediment trap characteristics measured at both sites are presented in Fig. 5A, B, respectively. The first and the second principal components accounted for 62.5 and 15.4% of total variance, respectively. The first component was mainly defined by the opposition between GSR and C/N ratios on one side and all the concentrations of the biochemical descriptors of settling POM on the other side. It can thus be considered as representative of the negative correlation between settling POM biochemical characteristics and GSR probably resulting from resus-
pension (Gre´mare et al., 1997; Medernach et al., 2001). The second component was more difficult to interpret. It opposed lipids and carbohydrates and in this sense could be considered as indicative of POM lability (Gre´mare et al., in press). However, the positive score of C/N ratio on this component remains problematic in this context. The projections of Medes and Banyuls sampling dates never mixed together. The Banyuls sampling dates were mostly separated by the first component of the PCA, whereas the Medes ones were separated by both components. Seasonality was especially apparent in Medes with a clear difference between the spring–summer sampling dates and the autumn– winter ones. These differences appear to be related to lower GSR and higher biochemical concentrations during spring and summer. For some of the sampling dates (i.e. M4, M19, M22, M23 and M24), the trend was especially pronounced for lipids and organic contents.
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3.3. Relationships between sediment trap characteristics and environmental parameters in the Medes Islands
Fig. 4. Temporal changes in chl a concentrations in Banyuls (white dot-solid line) and in Medes (black dot-dashed line).
This corresponded either to very low (M4 and M19) or to intermediate GSR (M22, M23, M24). Seasonality in Banyuls did also occur but less clearly than in Medes. This was due to a both higher variability during the spring–summer period and to the occurrence of extremely high GSR (B7, B8, B9, B10) during the autumn– winter period. Differences between Medes and Banyuls were associated to the second component of the PCA. They corresponded to higher carbohydrate and nitrogen, and lower lipid, organic contents and C/N ratios in Banyuls. Those differences tended to be high during the spring–summer period and low during the autumn– winter period except when GSR were maximal in Banyuls. The relationships linking GSR and organic contents at both sites are presented in Fig. 6. In both cases, there was a significant (p < 0:0001) negative correlation between these two parameters. However, this relationship was tighter in Banyuls (r2 ¼ 0:843, N ¼ 24) than in Medes (r2 ¼ 0:601, N ¼ 24). There were significant correlations between GSR and the other characteristics of settling POM as well (data not shown) and the results of the between sites comparison of those relationships are presented in Table 2. For all biochemical parameters but organic carbon, there were significant differences between the slopes and/or the interceptions of the corresponding regression models. Except for GSR and C/N ratio in Medes, all sediment trap characteristics showed significant seasonal differences with higher concentrations and lower GSR and C/N ratios during spring and summer than during autumn and winter (Table 3).
The projections of the variables and sampling dates on the first plane of the PCA based on all the measurements carried out in Medes are presented in Fig. 7A and B, respectively. The two first principal components accounted for 50.3 and 14.6% of the total variance, respectively. The projections of the variables clearly showed the opposition between the biochemical characteristics of settling POM on one side and C/N ratio and GSR along the first component of the PCA. The second component was mainly defined by the opposition between wind speed and the flow of the Ter River. GSR correlated better with wave height than with wind speed and chl a concentrations. GSR also seemed to be independent of river flow. The projections of sampling dates clearly allowed for the separation of a spring– summer (group I) and an autumn–winter period (group II), thereby confirming the results obtained with the first PCA. This projection also allowed for the identification of two subgroups within each of these periods. During spring and summer (i.e. subgroup IA and IB), this distinction was clearly associated with inter-annual variations, 1998 (except M19) being characterised by higher GSR and lipid contents than 1997. During autumn and winter, sampling dates within the subgroup IIB were all associated with higher GSR than those of subgroup IIA.
4. Discussion There have been only few studies simultaneously assessing both seasonal and spatial changes in the biochemical characteristics of settling POM in the littoral zone of the Mediterranean. Existing studies have dealt with specific environments such as caves (Airoldi & Cinelli, 1996) and semi-enclosed areas (Pusceddu et al., 1999). The present study thus constitutes the first report considering simultaneously both seasonal and spatial changes in the characteristics of settling POM in a Mediterranean open littoral area. 4.1. Between-sites differences Between-sites differences were associated to the second component of the first PCA and thus mostly resulted from differences in biochemical characteristics. Lipid contents were higher in Medes whereas carbohydrate contents were higher in Banyuls. Gre´mare et al. (in press) stated that carbohydrates are associated to a much more refractory fraction of settling POM than lipids. According to Pusceddu et al. (1999), the dominance of carbohydrates relative to proteins is indicative of oligotrophic environments where labile compounds are
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Table 1 Gross sedimentation rates and biochemical characteristics of sediment trap collected material in the Bay of Banyuls-sur-Mer and in the Medes Island Sampling intervals Banyuls-sur-Mer 15–21/7/1997 5–12/8/1998 19–26/8/1997 2–9/8/1997 16–23/9/1997 30/9–7/10/1997 7–15/10/1997 12–18/11/1997 25/11–2/12/1997 9/12/1997–6/ 1/1998 6–13/1/1998 22–27/1/1998 9–17/2/1998 17–15/2/1998 9–17/3/1998 25–31/3/1998 31/3–7/4/1998 28/4–6/5/1998 12–19/5/1998 19–26/5/1998 9–16/6/1998 30/6–7/7/1998 29/7–6/8/1998 18–25/8/1998 Medes Island 11–21/7/97 4–11/8/1997 18–27/8/1997 1–9/9/1997 16–24/9/1997 2–10/10/1997 10–16/10/1997 11–19/11/1997 7–12/12/1997 31/12/1997–9/ 1/1998 9–15/1/1998 23–30/1/1998 12–18/2/1998 19–27/2/1998 4–20/3/1998 26/3–1/4/1998 1–9/4/1998 29/4–10/5/1998 10–15/5/1998 22–29/5/1998 7–16/6/1998 28/6–6/7/1998 31/7–6/8/1998 18–27/8/1998
Code
GSR (gDW m2 day1)
OM OC N Proteins Carb. Lipids P-C-L OC % P-C-L (%) (%) (%) C/N (lg mgDW1) (lg mgDW1) (lg mgDW1) (lg mgDW1) OC/LECO OC
B1 B2 B3 B4 B5 B6 B7 B8 B9 B10
3.18 6.2 1.43 2.64 0.58 2.23 14.72 12.51 44.4 96.25
8.9 9.0 12.2 10.9 14.2 9.5 5.6 6.0 5.5 3.4
4.5 4.2 6.5 5.0 7.3 4.3 2.4 1.7 2.1 2.0
0.66 7 0.5 8 1.11 6 0.68 7 1.26 6 0.74 6 0.28 9 0.24 7 0.19 11 0.1 20
15.4 11.8 24.9 22.5 25.9 17.6 7.1 5.9 1.2 1.3
28.0 21.5 38.4 26.4 37.7 29.8 13.5 11.5 10.7 6.4
8.4 3.8 11.8 9.0 18.7 7.8 1.9 1.9 1.0 0.2
25 17 36 28 42 26 10 9 6 3
56 41 56 57 57 61 43 52 27 17
B11 B12 B13 B14 B15 B16 B17 B18 B19 B20 B21 B22 B23 B24
17.71 25.06 5.33 6.13 9.99 23.54 2.99 15.78 6.23 1.97 5.66 3.41 2.5 1.71
5.4 5.3 8.7 8.2 5.0 5.7 6.9 6.3 8.1 9.8 9.0 10.7 9.5 8.7
2.6 3.0 3.6 3.5 3.1 2.9 3.1 3.2 4.1 6.0 4.5 4.3 4.2 4.9
0.22 0.22 0.38 0.38 0.21 0.25 0.32 0.29 0.36 0.65 0.62 0.58 0.45 0.59
12 14 9 9 15 12 10 11 11 9 7 7 9 8
7.1 7.2 12.7 13.5 4.7 5.2 8.9 6.1 8.8 15.5 20.0 14.1 7.3 11.3
9.6 11.8 17.7 20.2 13.9 13.8 15.2 13.4 19.5 48.1 37.4 31.1 23.0 24.9
1.3 1.7 6.4 6.8 1.7 2.5 7.3 2.7 5.3 9.2 6.7 7.2 5.5 6.4
8 10 18 20 9 10 16 10 16 34 30 25 17 20
32 32 50 57 29 34 51 32 39 56 66 58 40 41
M1 M2 M3 M4 M5 M6 M7 M8 M9 M10
0.54 1.66 0.78 0.84 0.97 4.42 13.57 1.08 4.1 6.46
16.8 12.8 14.0 22.0 18.0 12.7 10.0 12.3 8.0 8.0
4.3 5.9 5.8 6.6 5.3 3.8 2.8 2.6 2.7 2.7
0.4 0.57 0.55 0.63 0.6 0.45 0.22 0.25 0.19 0.17
11 10 11 10 9 9 13 10 14 16
14.6 14.2 12.2 12.4 11.4 10.5 9.9 9.1 7.2 8.3
19.3 22.1 16.9 18.4 14.1 15.6 8.2 6.7 7.5 7.2
10.8 14.9 12.3 14.8 4.7 7.0 2.6 2.5 1.2 7.3
23 27 22 25 15 17 10 9 7 12
53 46 38 37 28 44 36 35 28 46
M11 M12 M13 M14 M15 M16 M17 M18 M19 M20 M21 M22 M23 M24
15.69 8.65 14.06 23.05 18.61 6.99 15.36 7.27 0.74 3.39 15.52 12.45 8.48 6.58
6.0 6.7 7.3 7.0 8.0 8.0 9.0 13.0 16.0 12.3 10.3 11.0 13.7 12.7
2.9 3.2 3.0 3.1 3.5 3.2 3.1 4.0 5.0 4.3 4.2 4.8 5.8 7.2
0.21 0.23 0.16 0.18 0.2 0.17 0.21 0.34 0.5 0.37 0.39 0.37 0.45 0.44
14 14 19 17 17 19 15 12 10 12 11 13 13 16
8.4 8.9 8.2 9.1 10.7 8.5 10.2 14.4 29.4 11.7 11.9 13.1 12.4 13.3
6.7 7.8 9.7 6.8 7.9 11.6 8.8 12.5 12.6 12.6 13.4 15.7 17.8 18.1
7.7 6.6 5.3 3.0 4.2 3.4 3.0 9.0 21.8 9.8 17.2 19.0 19.4 21.5
13 12 12 9 12 11 11 19 36 18 24 27 28 30
43 39 40 30 33 35 35 47 72 42 57 56 48 42
OM, organic matter; OC, organic carbon; N, nitrogen; C/N, C/N ratio; Proteins; carbohydrates, Carb.; and Lipids. P carbon ¼ mg protein mgDW1 0,49; C carbon ¼ mg carbohydrate mgDW1 0, 4; L carbon ¼ mg lipid mgDW1 0, 75; C transformations from Pusceddu, Dell’Anno, and Fabiano (2000); % of the P-C-L OC respect LECO OC ¼ ((P-C-L OC)/10)/LECO OC.
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Fig. 5. Projections of the variables (A) and sampling dates (B) on the first plane of the PCA based on all the measured characteristics of settling POM. GSR, gross sedimentation rates; OM, organic matter; OC, organic carbon; N, nitrogen; C : N, C/N ratio; PRO, proteins; CARB, carbohydrates. See Table 1 for sampling dates code. In Fig. 4B, the use of italics refers to spring–summer sampling dates, the use of plain text to autumn–winter sampling dates with no extreme GSR, and the use of bold character to autumn–winter sampling dates with extreme GSR.
quickly utilised. The mean values of this ratio were 2.4 and 1.1 in Banyuls and in Medes, respectively. Settling POM was thus more labile in Medes than in Banyuls. Although there was significant between-sites differences in chl a concentrations, this parameter does not appear to control between-sites differences in settling POM characteristics. Those differences indeed tended to be larger during summer when chl a concentrations were closer in Banyuls and in Medes. The comparison of wind and wave conditions at both sites suggests that resuspension is less important in Medes. This is consistent with the lack of high GSR during wintertime at that site. However, it must also be pointed that such events may also not have been sampled due to the non-
continuous deployment of the traps. Another factor which may contribute to between-sites differences in GSR is sediment granulometry. In Banyuls, sediment traps were moored over a sandy mud. In Medes, mud and sandy muds are rare near the study site where most of the bottoms is made of rocks and gravels (Gili & Ros, 1985), which are less sensitive to resuspension accounting for the fact that minerals of similar size were collected at both sites. Despite apparent differences in the intensity of resuspension, there was a significant negative relationship between GSR and the organic contents of sediment trap material at both sites. Such a relationship is indicative of the importance of sediment resuspension
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Table 3 Probability associated with the t-test used for comparing the mean value of GSR and sediment trap material biochemical characteristic during the spring–summer and the autumn–winter periods both in the Bay of Banyuls-sur-Mer and in the Medes Islands
GSR OM OC N C/N Carbo. Proteins Lipids
Fig. 6. Relationship linking gross sedimentation rates and the organic contents of settling POM in Banyuls (open dot-solid line) and in Medes (black dot-dashed line).
in driving GSR (Gre´mare et al., 1997, 1998; Medernach et al., 2001). The results of the second PCA showed that in Medes, GSR correlated better with wave height than with any other environmental parameters. Since in the NW Mediterranean resuspension is mostly caused by waves, this suggests that sediment resuspension is a key factor in controlling temporal changes in GSR in Medes as well. 4.2. Seasonality Seasonality was apparent at both sites with a spring– summer period characterised by low GSR and high organic contents of sediment trap material and an autumn–winter period characterised by highly variable (occasionally very high) GSR and low organic contents of sediment trap material, such as already reported by Gre´mare et al. (1997, 1998) for the Bay of
Banyuls-sur-Mer
Medes Islands
<0.05 <0.01 <0.01 <0.01 <0.001 <0.01 <0.05 <0.05
0.06 <0.001 <0.001 <0.001 0.09 <0.01 <0.01 <0.001
Banyuls-sur-Mer. The results of the first PCA suggest that seasonality in settling POM characteristics was clearer in Medes than in Banyuls despite the lack of extremely high GSR during wintertime. This was partly due to between-sites differences in the pattern of changes in settling POM characteristics during spring and summer. In Banyuls those changes are mainly cued by changes in GSR, which tend to be lower during summer than spring (Medernach, personal communication), whereas in Medes they appear to be related with pulses of POM with high lipids contents. Settling POM characteristics differed most between sites during the spring–summer period, which may seem surprising due to stronger between-sites differences in GSR during wintertime. One possible explanation is that Medes station becomes more affected by resuspension during wintertime accounting for smaller between-sites differences in settling POM characteristics at that time of the year, except when extremely high GSR take place in Banyuls. The winter–spring phytoplanktonic bloom constitutes another important factor in controlling seasonality of settling POM characteristics. This bloom occurred in February at both sites. In Banyuls, it occurred simultaneously with a transitory increase in the organic content of settling POM as already reported by Medernach et al. (2001). This confirms that the effects
Table 2 Main characteristics of the correlation models linking GSR and organic matter, organic carbon, nitrogen, C/N ratio, proteins, carbohydrates, and lipids
Organic matter Organic carbon Nitrogen C/N Proteins Carbohydrates Lipids
Intercept Medes Islands
Intercept Banyuls-sur-Mer
p
Slope Medes Islands
Slope Banyuls-sur-Mer
p
Sum of squares
d.f.
1.183 0.683 0.338 1.017 1.128 1.169 1.089
1.086 0.770 0.031 0.803 1.360 1.579 1.214
*** n.s. *** *** n.s. *** *
0.219 0.122 0.249 0.132 0.102 0.157 0.285
0.257 0.267 0.466 0.200 0.517 0.377 0.774
n.s. n.s. * n.s. *** * **
5.327 8.202 10.019 9.126 11.403 8.678 25.207
3 3 3 3 3 3 3
The results of the ANCOVAs comparing these relationships among sites are also provided. ðN ¼ 48Þ (n.s. ¼ non-significant; *p < 0:01; **p < 0:001; ***p < 0:0001; d.f. ¼ Degrees of freedom).
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Fig. 7. Projections of the variables (A) and sampling dates (B) on the first plane of the PCA based on all the environmental parameters and the characteristics of settling POM measured in Medes. GSR, gross sedimentation rates; OM, organic matter; OC, organic carbon; N, nitrogen; C : N, C/N ratio; PRO, proteins; CARB, carbohydrates; FLOW, Ter River flow; WIND, Wind speed; WAVES, wave height. See Table 1 for sampling dates code. In Fig. 4B, group I refers to the spring–summer and group II to the autumn–winter sampling dates.
of the main biological processes on settling POM remain limited relative to those of hydrodynamical processes cuing sediment resuspension. This is even more true in Medes where despite of much higher chl a concentration, the spring–winter bloom was not associated to any significant changes in settling POM biochemical characteristics. This pattern may be related with the occurrence of high GSR during February. It is very unlikely that those GSR were caused by sediment resuspension since wave height was relatively low at that time of the year. They are probably indicative of the existence of another source of refractory POM, which may be constituted by inputs from the Ter River (Rossi, unpublished data). In this sense, it should be stressed
that GSR are certainly not the only factor driving settling POM biochemical characteristics at both sites as also indicated by significant between-sites differences in correlation models linking GSR and sediment trap biochemical characteristics. In Medes, there was an increase in GSR and in some of the settling POM biochemical characteristics (including lipid content) during summer 1998. This pattern is interesting because: (1) in NW Mediterranean, this portion of summer is usually associated with very low GSR and pelagic primary productivity, and (2) increase in GSR due to resuspension and/or terrestrial inputs are usually associated with a decrease in the biochemical parameters associated with the labile component of
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settling POM (Gre´mare et al., 1997, 1998; Medernach et al., 2001). The current hypothesis is that, during summer, GSR in Medes are cued by the interaction between the Ter River flow and local hydrodynamics, and that lower GSR during July 1997 would result from the strong dominance of North-South currents during that particular month, whereas high GSR (in spite of the low Ter River flow) would result from the alternation of North-South and South-North currents during July 1998 (Pasqual, personal communication). Further monitoring of GSR and currents during summer months are clearly needed to further test this hypothesis.
Acknowledgements Meteorological data were supplied by Josep Pasqual of the Meteorological station of l’Estartit. Wind data treatment was provided by E Garcı´ a. Carbon/Nitrogen analysis of Medes benefited from the assistance of A Cugat and L Cerasi with the LECO Elemental Analyser of the Instituto de Ciencias del Mar. Support for this work was provided by an F.P.I. fellowship from ÔMinisterio de Educacio´n y CienciaÕ to SR, in the project DGICYT, PB94-0014-C02-01 and DGICYT 1999–2000, PB98-0496-C03-01. We also acknowledge support from the MAST-III-ELOISE METRO MED and the SOMLIT projects and from the LEA (Laboratorio Europeo Asociado) for marine research. References Airoldi, L., & Cinelli, F. (1996). Variability of fluxes of particulate material in a submarine cave with chemolithoautotrophic inputs of organic carbon. Marine Ecology Progress Series 139, 205–217. Barnes, H., & Blackstock, J. (1973). Estimation of lipids in marine animals tissues: detailed investigation of the sulphophosphovanillin method for ‘‘total’’ lipids. Journal of Experimental Marine Biology and Ecology 12, 103–118. Barnes, D. K. A., & Clarke, A. (1995). Seasonality of feeding activity in Antarctic suspension feeders. Polar Biology 15, 335–340. Charles, F., Gre´mare, A., Amouroux, J. M., & Baudart, J. (1995). A bioassay approach to temporal variation in the nutritional value of sediment trap material. Journal of Experimental Marine Biology and Ecology 19, 65–81. Coma, R., Ribes, M., Gili, J. M., & Zabala, M. (1998). An energetic approach to the study of life-history traits of two modular colonial benthic invertebrates. Marine Ecology Progress Series 162, 89–103. Cripps, G. C., & Clarke, A. (1998). Seasonal variation in the biochemical composition of particulate material collected by sediment traps at Signy Island, Antarctica. Polar Biology 20, 414–423. Danovaro, R., Tselepides, A., Otegui, A., & Della Croce, N. (2000). Dynamics of meiofaunal assemblages on the continental shelf and deep sea sediments of the Cretan Sea (NE Mediterranean): relationships with seasonal changes in food supply. Progress in Oceanography 46, 367–400. Dell’Anno, A., Fabiano, M., Mei, M. L., & Danovaro, R. (2000). Enzymatically hydrolysed protein and carbohydrate pools in deepsea sediments: estimates of the potentially bioavailable fraction and
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Mayer, M. M., Schick, L. L., & Setchell, F. W. (1986). Measurements of protein in nearshore marine sediments. Marine Ecology Progress Series 30, 159–165. Mayer, M. M., Schick, L. L., Sawyer, T., & Plante, C. J. (1995). Bioavailable amino acids in sediments: a biomimetic, kineticsbased approach. Limnology and Oceanography 40, 511–520. Medernach, L., Gre´mare, A., Amouroux, J. M., Colomines, J. C., & Ve´tion, G. (2001). Temporal changes in the amino acid contents of particulate organic matter sedimenting in the Bay of Banyuls (northwestern Mediterranean). Marine Ecology Progress Series 214, 55–65. Meyer-Reil, L. A. (1983). Benthic response to sedimentation events in the western Kiel Bight. II. Analysis of benthic bacterial populations. Marine Biology 77, 247–256. Navarro, J. M., & Thompson, R. J. (1995). Seasonal fluctuations in size spectra, biochemical composition and nutritive value of the seston available to suspension feeding bivalve in a subartic environment. Marine Ecology Progress Series 125, 95–106. Parsons, T. R., Maita, Y., & Lalli, C. M. (1985). Fluorometric determination of chlorophylls. A manual of chemical and biological methods for sea water analysis (pp. 201–203). Oxford: Pergamon Press. Pfannkuche, O. (1993). Benthic response to sedimentation of particulate organic matter at the BIOTRANS station, 47 N, 20 S. Deep-Sea Research II 40, 135–149. Plante, C. J., & Jumars, P. A. (1992). The microbial environment of marine deposit feeder guts characterized via microelectrodes. Microbial Ecology 23, 257–277. Plante, C. J., & Shriver, A. G. (1998). Differential lysis of sedimentary bacteria by Arenicola marina L. : examination of cell wall structure and exopolymeric capsules as correlates. Journal of Experimental Marine Biology and Ecology 229, 35–52.
Posedel, N., & Faganeli, J. (1991). Nature and sedimentation of suspended particulate matter during density stratification in shallow coastal waters (Gulf of Trieste, northern Adriatic). Marine Ecology Progress Series 77, 135–145. Pusceddu, A., Sara`, G., Armeni, M., Fabiano, M., & Mazzola, A. (1999). Seasonal and spatial changes in the sediment organic matter of a semi-enclosed marine system (W-Mediterranean Sea). Hydrobiologia 397, 59–70. Pusceddu, A., Dell’Anno, A., & Fabiano, M. (2000). Organic matter composition in coastal sediments at Terra Nova Bay (Ross Sea) during summer 1995. Polar Biology 23, 124–132. Ribes, M., Coma, R., & Gili, J. M. (1998). Seasonal variation of in situ feeding rates by the temperate ascidian Halocyntia papillosa. Marine Ecology Progress Series 175, 201–213. Rice, D. L. (1982). The detritus nitrogen problem: new observations and perspectives from organic geochemistry. Marine Ecology Progress Series 9, 153–162. Riisgard, H. U. (1998). Filter feeding and plankton dynamics in a Danish fjord: a review of the importance of flow, mixing and density-driven circulation. Journal of Environmental Management 53, 195–207. Tenore, K. R. (1981). Organic nitrogen and caloric content of detritus. I. Utilization be the depositi-feeding polychaete Capitella capitata. Estuarine, Coastal and Shelf Science 12, 39–47. Tenore, K. R. (1988). Nitrogen in benthic food chains. In T. H. Blackburn, & J. Sorensen (Eds.), Nitrogen cycling in coastal marine environment (pp. 191–206). New York: Wiley. Valiela, I., Wilson, J., Buchsbaum, R., Rietsma, C., Bryant, D., Foreman, K., & Teal, J. (1984). Importance of chemical composition of salt marsh litter on decay rates and feeding for detritivores. Bulletin of Marine Science 35, 261–269.
Biochemical characteristics of settling particulate organic matter at two north-western Mediterranean sites: a seasonal comparison Sergio Rossia,*, Antoine Gre´mareb, Josep-Marı´ a Gilia, Jean-Michel Amourouxb, Esther Jordanaa, Gilles Ve´tionb a Instituto Ciencias del Mar (CSIC), Paseo Marı´timo de la Barceloneta 37-49, Barcelona 08003, Spain Observatoire Oce´anologique de Banyuls, Laboratoire d’Oce´anolographie Biologique de Banyuls, UMR 7621, CNRS-UPMC, BP44 F66651 Banyuls Cedex, France
b
Received 12 December 2002; accepted 31 March 2003
Abstract Gross sedimentation rates (GSR) and the main biochemical characteristics of settling particulate matter were monitored at two NW Mediterranean sites (the Bay of Banyuls-sur-Mer, France, and the Medes Islands, Spain) throughout a year to assess possible differences in particulate organic matter (POM) availability to the benthic community. A similar seasonal pattern was observed at both sites with higher organic contents and lower GSR during the spring–summer than during the autumn–winter period. At both sites, there was a negative correlation between GSR and sediment trap organic contents, which is indicative of the importance of resuspension in driving GSR. Along the same line, GSR in Medes correlated positively with wave height. The principal component analysis based on GSR and biochemical characteristics of sediment trap material always segregated samples from the two studied sites mostly due to the occurrence of higher lipid and lower carbohydrate contents in Medes. These differences were indicative of the presence of more labile settling POM in the Medes Islands. They were more pronounced during the spring–summer than during the autumn–winter period. Such a pattern may reflect differences in the sensitivity of the two studied sites to resuspension. According to this interpretation, between-sites differences would be high when resuspension is low (i.e. during the spring–summer period when resuspension would mainly affect Banyuls) and become low when resuspension is high (autumn–winter period when resuspension would affect both sites). Ó 2003 Elsevier Ltd. All rights reserved. Keywords: gross sedimentation rates; seasonality; settling particulate organic matter; biochemical characteristics; spatial comparison; north-western Mediterranean
1. Introduction The sources of particulate organic matter (POM) in the coastal environment are heterogeneous and exhibit seasonal patterns both from a quantitative and a qualitative standpoint (Cripps & Clarke, 1998; Gre´mare et al., 1997; Navarro & Thompson, 1995; Tenore, 1988). Because an important component of their diet is derived from settling or sedimented POM, seasonal pulses of available organic matter influence the abundance, the * Corresponding author. E-mail address: [email protected] (S. Rossi). 0272-7714/03/$ - see front matter Ó 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S0272-7714(03)00108-2
biomass and the activity of bottom communities (Graf, Bengtsson, Schulz, & Theede, 1982; Graf, Shulz, Peinert, & Meyer-Reil, 1983). Due to seasonality in primary production, suspension, deposit and detritus feeders may thus show seasonal patterns in warm temperate, cold temperate and polar seas (Barnes & Clarke, 1995; Coma, Ribes, Gili, & Zabala, 1998; Ribes, Coma, & Gili, 1998; Riisgard, 1998). The relationship between pulses of settling POM and reproduction or growth has been already documented in several benthic species (Charles, Gre´mare, Amouroux, & Baudart, 1995; Gre´mare, 1994; Gre´mare et al., 1997; Marsh, Gre´mare, & Tenore, 1989). The activity of benthic
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organisms, as assessed through direct observations, ATP, heat or biomass production is also influenced by seasonal inputs of organic matter (Ducheˆne & Rosenberg, 2001; Graf et al., 1982, 1983; Jordana, Ducheˆne, Charles, Gre´mare & Amouroux, 2000; Meyer-Reil, 1983; Pfannkuche, 1993). One of the difficulties in relating POM characteristics and benthic fauna is the assessment of POM nutritional value. Bulk POM biochemical characteristics such as total organic matter, organic carbon and nitrogen in both sediments and settling POM have been used as a proxy of food availability for benthic primary consumers (Charles et al., 1995; Gre´mare, 1994; Levinton, Bianchi, & Stewart, 1984; Tenore, 1981; Valiela et al., 1984). This approach is limited because most of the settling and/or sedimented POM is refractory, and cannot be absorbed by benthic invertebrates (Plante & Jumars, 1992; Plante & Shriver, 1998). During the last 20 years both biological and biochemical assays have been developed to better assess true nutritional organic matter availability for benthic primary consumers (Dell’Anno, Fabiano, Mei, & Danovaro, 2000; Gre´mare et al., 1997, 2002, in press; Mayer, Schick, Sawyer, & Plante, 1995; Mayer, Schick, & Setchell, 1986; Medernach, Gre´mare, Amouroux, Colomines, & Ve´tion, 2001). It appears that some specific POM biochemical descriptors such as enzymatically hydrolysable amino acids (Mayer et al., 1995) and lipids better correlate with the abundance and the biomass of benthic fauna than bulk characteristics (Gre´mare et al., 2002, in press). These results are supported by the good correlation of those specific parameters with growth rates of selected invertebrates during laboratory experiments (Gre´mare et al., 1997). Seasonality in pelagic primary production is strong in the Mediterranean due to the winter–spring phytoplanktonic bloom (Estrada, 1996; Estrada, Vives, & Alcaraz, 1985). Seasonality affects the availability of POM to interface feeders (Gre´mare et al., 1997). The relationship between POM characteristics and benthic standing stocks has already been documented several times in this area (Danovaro, Tselepides, Otegui, & Della Croce, 2000; Gre´mare et al., 2002, in press). Even if the study of temporal and spatial changes in potential food items is a key step in understanding the dynamics of benthic communities, studies considering specific biochemical characteristics such as lipids are yet relatively scarce in the Mediterranean (Fichez, 1991; Gre´mare et al., 1997, 1998; Medernach et al., 2001; Posedel & Faganeli, 1991; Pusceddu, Sara`, Armeni, Fabiano, & Mazzola, 1999), and only very few of those studies have considered small scale spatial variations (Airoldi & Cinelli, 1996; Fichez, 1991; Pusceddu et al., 1999). The aim of this work was to compare both the absolute values and seasonal changes in gross sedimentation rates (GSR) and in the main biochemical
characteristics of settling POM at two sites located only 50 km apart but which exhibit differences in some key environmental features and differ in the abundance and the composition of their benthic fauna (Gili & Ros, 1985; Guille, 1971a,b). The working hypotheses were that: (1) both the GSR and the biochemical characteristics of settling POM may differ at the two sites, and (2) the magnitude of between-sites differences may vary seasonally. In order to test these hypotheses, GSR together with the main biochemical characteristics of sediment trap collected materials were monitored both in the Bay of Banyuls-sur-Mer (Banyuls) and in the Medes Islands (Medes) (NW Mediterranean). The main environmental parameters were also monitored to identify some of the factors potentially accounting for between-sites differences.
2. Materials and methods 2.1. Environmental parameters Wind maximum speed and direction were registered daily together with rain fall both in Medes (Servei Meteorolo´gic de l’Estartit) and in Banyuls (Station Me´te´o France du Cap Be´ar). Wave height was also recorded in Medes (Servei Meteorolo´gic de l’Estartit). In Banyuls, wave data consisted in the estimation of the state of the sea (a rough index that can be used as a proxy for wave height) by the Cap Be´ar Meteo France station. Water samples were collected at both sites to assess chlorophyll a (chl a) concentrations. Samples were collected at 24 m depth in Banyuls and at 20 m depth in Medes. They were collected weekly in Banyuls and 2–5 times a month in Medes. Samples (0.2 l) were filtered on Whatman GF/F filters and chl a was then assessed on triplicates after Parsons, Maita, and Lalli (1985).
2.2. Sediment traps Two sets of sediment traps were moored in Banyuls (42 2993099N, 3 0897099E, France), and in Medes (42 0295599N, 3 1393099E, Spain) (Fig. 1A, B). The traps were moored over 27 m deep sandy bottoms in Banyuls and over 30 m deep sandy-stone bottoms in Medes. The two sets of traps were identical. They consisted of two polyethylene pipes prolonged by a cone and a collector with an aspect ratio of 4.75. The mouths of the traps were located 3 m above the bottom. The traps were collected by SCUBA divers weekly in Banyuls, and every other week in Medes between July 1997 and August 1998. Deployment duration was always less than 10 days.
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Fig. 1. Map showing the location of the two studied sites. Arrows indicate study areas: (A) Banyuls-sur-Mer, (B) Medes Islands. The stars indicate sediment trap moorings.
2.3. Biochemical assays Immediately after collection, samples were centrifuged (4000 rpm, 15 min), briefly rinsed with distilled water, frozen (20 C) and freeze-dried. The collected material was then sieved on a 200 lm mesh, weighed (both fractions, <200 and >200 lm) and stored at 20 C. GSR were computed as the total amount of
POM collected within the traps per unit of time and surface area. All biochemical characteristics were measured on the <200 lm size fraction. Organic contents were assessed by measuring combustion weight loss (450 C for 5 h). Organic carbon and nitrogen were measured using a CHN LECO CC-100 elemental analyser, after acidification with 1 N HCl. Proteins were assayed after Lowry,
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Rosebrough, Farr, and Randall (1951) as modified by Rice (1982) to account for the absorption of phenolic compounds. Carbohydrates were assayed after Dubois, Gilles, Hamilton, Rebers, and Smith (1956). Lipids were assayed after Barnes and Blackstock (1973). All analyses were ran on triplicates.
data, two samples (i.e. M2 and M20) were excluded from this analysis.
3. Results 3.1. Environmental parameters
2.4. Statistical analysis Environmental parameters at both sites were compared using t-tests for paired samples. General trends in the characteristics of settling POM at both sites were first compared using a principal component analysis (PCA) based on GSR and all measured biochemical parameters. Between-sites differences were then further assessed for each single biochemical parameter. Because: (1) there were significant correlations between GSR and biochemical characteristics of sediment trap materials at both sites, and (2) the range of GSR differed among sites, covariance analyses were used to compare the slopes and intersections of the correlation models linking biochemical characteristics and GSR (log10 transformed data). These tests were performed to assess whether or not between-sites differences in biochemical characteristics were associated to differences in GSR patterns. To better assess within site seasonal changes, GSR and biochemical data were pooled into two groups (i.e. spring–summer period and autumn–winter period) as proposed by Gre´mare et al. (1997, 1998). The mean values of these seasonal samples were then compared using t-tests for independent samples. Since this was the first report of sediment trap data in Medes, a second PCA was ran to assess the relationship between sediment trap characteristics and environmental parameters in this area. This PCA was based on GSR and all the environmental parameters and biochemical characteristics measured at this site. Due to the lack of chl a
Wind speed (Fig. 2) was higher in Banyuls than in Medes during the studied year (t-test for paired samples, p < 0:001). Wind direction also differed between sites. Rainfall was of the same magnitude and tended to occur simultaneously at both sites (Fig. 3A). Waves tended to be higher in Banyuls than in Medes (data not shown). Chl a concentrations (Fig. 4) were higher in Medes than in Banyuls-sur Mer (t-test for paired samples, p ¼ 0:006). Between-sites differences were larger during winter and spring. At both sites, the highest chl a concentrations occurred during February. The period characterised by high chl a concentrations started earlier and lasted much longer in Medes than in Banyuls, however. December corresponded both to the onset of increase in chl a concentrations in Medes and to the highest flow of the Ter River (Fig. 3B). There were other slight betweensites differences in temporal changes in chl a concentrations: (1) the autumn bloom was only apparent in Banyuls (November), and (2) there were secondary peaks in Medes during August (Figs. 3B and 4). 3.2. Sediment trap characteristics At both sites, small grain sizes dominated the minerals in the trap. In Banyuls-sur-Mer, the average diameter of the collected material was typically between 10 and 20 lm, whereas it was close to 20 lm in Medes Islands (Gre´mare, personal observation). The GSR and the biochemical characteristics recorded during the
Fig. 2. Daily wind maximum speed (m s1) and direction in Banyuls-sur-Mer and Medes Islands.
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Fig. 3. (A) Rainfall record in Banyuls-sur-Mer (white dot-solid line) and Medes Islands (black dot-dashed line) meteorological stations. (B) Flow of the Ter River (Medes Islands only).
present study are listed in Table 1. Proteins, lipids and carbohydrates accounted for an average of 45 and 42% of total organic carbon in Banyuls and in Medes, respectively. In Banyuls, this proportion was as low as 17% immediately after a strong resuspension event (B10). This trend was less apparent in Medes. The projections of variables and sampling dates on the first plane of the PCA involving all the sediment trap characteristics measured at both sites are presented in Fig. 5A, B, respectively. The first and the second principal components accounted for 62.5 and 15.4% of total variance, respectively. The first component was mainly defined by the opposition between GSR and C/N ratios on one side and all the concentrations of the biochemical descriptors of settling POM on the other side. It can thus be considered as representative of the negative correlation between settling POM biochemical characteristics and GSR probably resulting from resus-
pension (Gre´mare et al., 1997; Medernach et al., 2001). The second component was more difficult to interpret. It opposed lipids and carbohydrates and in this sense could be considered as indicative of POM lability (Gre´mare et al., in press). However, the positive score of C/N ratio on this component remains problematic in this context. The projections of Medes and Banyuls sampling dates never mixed together. The Banyuls sampling dates were mostly separated by the first component of the PCA, whereas the Medes ones were separated by both components. Seasonality was especially apparent in Medes with a clear difference between the spring–summer sampling dates and the autumn– winter ones. These differences appear to be related to lower GSR and higher biochemical concentrations during spring and summer. For some of the sampling dates (i.e. M4, M19, M22, M23 and M24), the trend was especially pronounced for lipids and organic contents.
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3.3. Relationships between sediment trap characteristics and environmental parameters in the Medes Islands
Fig. 4. Temporal changes in chl a concentrations in Banyuls (white dot-solid line) and in Medes (black dot-dashed line).
This corresponded either to very low (M4 and M19) or to intermediate GSR (M22, M23, M24). Seasonality in Banyuls did also occur but less clearly than in Medes. This was due to a both higher variability during the spring–summer period and to the occurrence of extremely high GSR (B7, B8, B9, B10) during the autumn– winter period. Differences between Medes and Banyuls were associated to the second component of the PCA. They corresponded to higher carbohydrate and nitrogen, and lower lipid, organic contents and C/N ratios in Banyuls. Those differences tended to be high during the spring–summer period and low during the autumn– winter period except when GSR were maximal in Banyuls. The relationships linking GSR and organic contents at both sites are presented in Fig. 6. In both cases, there was a significant (p < 0:0001) negative correlation between these two parameters. However, this relationship was tighter in Banyuls (r2 ¼ 0:843, N ¼ 24) than in Medes (r2 ¼ 0:601, N ¼ 24). There were significant correlations between GSR and the other characteristics of settling POM as well (data not shown) and the results of the between sites comparison of those relationships are presented in Table 2. For all biochemical parameters but organic carbon, there were significant differences between the slopes and/or the interceptions of the corresponding regression models. Except for GSR and C/N ratio in Medes, all sediment trap characteristics showed significant seasonal differences with higher concentrations and lower GSR and C/N ratios during spring and summer than during autumn and winter (Table 3).
The projections of the variables and sampling dates on the first plane of the PCA based on all the measurements carried out in Medes are presented in Fig. 7A and B, respectively. The two first principal components accounted for 50.3 and 14.6% of the total variance, respectively. The projections of the variables clearly showed the opposition between the biochemical characteristics of settling POM on one side and C/N ratio and GSR along the first component of the PCA. The second component was mainly defined by the opposition between wind speed and the flow of the Ter River. GSR correlated better with wave height than with wind speed and chl a concentrations. GSR also seemed to be independent of river flow. The projections of sampling dates clearly allowed for the separation of a spring– summer (group I) and an autumn–winter period (group II), thereby confirming the results obtained with the first PCA. This projection also allowed for the identification of two subgroups within each of these periods. During spring and summer (i.e. subgroup IA and IB), this distinction was clearly associated with inter-annual variations, 1998 (except M19) being characterised by higher GSR and lipid contents than 1997. During autumn and winter, sampling dates within the subgroup IIB were all associated with higher GSR than those of subgroup IIA.
4. Discussion There have been only few studies simultaneously assessing both seasonal and spatial changes in the biochemical characteristics of settling POM in the littoral zone of the Mediterranean. Existing studies have dealt with specific environments such as caves (Airoldi & Cinelli, 1996) and semi-enclosed areas (Pusceddu et al., 1999). The present study thus constitutes the first report considering simultaneously both seasonal and spatial changes in the characteristics of settling POM in a Mediterranean open littoral area. 4.1. Between-sites differences Between-sites differences were associated to the second component of the first PCA and thus mostly resulted from differences in biochemical characteristics. Lipid contents were higher in Medes whereas carbohydrate contents were higher in Banyuls. Gre´mare et al. (in press) stated that carbohydrates are associated to a much more refractory fraction of settling POM than lipids. According to Pusceddu et al. (1999), the dominance of carbohydrates relative to proteins is indicative of oligotrophic environments where labile compounds are
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Table 1 Gross sedimentation rates and biochemical characteristics of sediment trap collected material in the Bay of Banyuls-sur-Mer and in the Medes Island Sampling intervals Banyuls-sur-Mer 15–21/7/1997 5–12/8/1998 19–26/8/1997 2–9/8/1997 16–23/9/1997 30/9–7/10/1997 7–15/10/1997 12–18/11/1997 25/11–2/12/1997 9/12/1997–6/ 1/1998 6–13/1/1998 22–27/1/1998 9–17/2/1998 17–15/2/1998 9–17/3/1998 25–31/3/1998 31/3–7/4/1998 28/4–6/5/1998 12–19/5/1998 19–26/5/1998 9–16/6/1998 30/6–7/7/1998 29/7–6/8/1998 18–25/8/1998 Medes Island 11–21/7/97 4–11/8/1997 18–27/8/1997 1–9/9/1997 16–24/9/1997 2–10/10/1997 10–16/10/1997 11–19/11/1997 7–12/12/1997 31/12/1997–9/ 1/1998 9–15/1/1998 23–30/1/1998 12–18/2/1998 19–27/2/1998 4–20/3/1998 26/3–1/4/1998 1–9/4/1998 29/4–10/5/1998 10–15/5/1998 22–29/5/1998 7–16/6/1998 28/6–6/7/1998 31/7–6/8/1998 18–27/8/1998
Code
GSR (gDW m2 day1)
OM OC N Proteins Carb. Lipids P-C-L OC % P-C-L (%) (%) (%) C/N (lg mgDW1) (lg mgDW1) (lg mgDW1) (lg mgDW1) OC/LECO OC
B1 B2 B3 B4 B5 B6 B7 B8 B9 B10
3.18 6.2 1.43 2.64 0.58 2.23 14.72 12.51 44.4 96.25
8.9 9.0 12.2 10.9 14.2 9.5 5.6 6.0 5.5 3.4
4.5 4.2 6.5 5.0 7.3 4.3 2.4 1.7 2.1 2.0
0.66 7 0.5 8 1.11 6 0.68 7 1.26 6 0.74 6 0.28 9 0.24 7 0.19 11 0.1 20
15.4 11.8 24.9 22.5 25.9 17.6 7.1 5.9 1.2 1.3
28.0 21.5 38.4 26.4 37.7 29.8 13.5 11.5 10.7 6.4
8.4 3.8 11.8 9.0 18.7 7.8 1.9 1.9 1.0 0.2
25 17 36 28 42 26 10 9 6 3
56 41 56 57 57 61 43 52 27 17
B11 B12 B13 B14 B15 B16 B17 B18 B19 B20 B21 B22 B23 B24
17.71 25.06 5.33 6.13 9.99 23.54 2.99 15.78 6.23 1.97 5.66 3.41 2.5 1.71
5.4 5.3 8.7 8.2 5.0 5.7 6.9 6.3 8.1 9.8 9.0 10.7 9.5 8.7
2.6 3.0 3.6 3.5 3.1 2.9 3.1 3.2 4.1 6.0 4.5 4.3 4.2 4.9
0.22 0.22 0.38 0.38 0.21 0.25 0.32 0.29 0.36 0.65 0.62 0.58 0.45 0.59
12 14 9 9 15 12 10 11 11 9 7 7 9 8
7.1 7.2 12.7 13.5 4.7 5.2 8.9 6.1 8.8 15.5 20.0 14.1 7.3 11.3
9.6 11.8 17.7 20.2 13.9 13.8 15.2 13.4 19.5 48.1 37.4 31.1 23.0 24.9
1.3 1.7 6.4 6.8 1.7 2.5 7.3 2.7 5.3 9.2 6.7 7.2 5.5 6.4
8 10 18 20 9 10 16 10 16 34 30 25 17 20
32 32 50 57 29 34 51 32 39 56 66 58 40 41
M1 M2 M3 M4 M5 M6 M7 M8 M9 M10
0.54 1.66 0.78 0.84 0.97 4.42 13.57 1.08 4.1 6.46
16.8 12.8 14.0 22.0 18.0 12.7 10.0 12.3 8.0 8.0
4.3 5.9 5.8 6.6 5.3 3.8 2.8 2.6 2.7 2.7
0.4 0.57 0.55 0.63 0.6 0.45 0.22 0.25 0.19 0.17
11 10 11 10 9 9 13 10 14 16
14.6 14.2 12.2 12.4 11.4 10.5 9.9 9.1 7.2 8.3
19.3 22.1 16.9 18.4 14.1 15.6 8.2 6.7 7.5 7.2
10.8 14.9 12.3 14.8 4.7 7.0 2.6 2.5 1.2 7.3
23 27 22 25 15 17 10 9 7 12
53 46 38 37 28 44 36 35 28 46
M11 M12 M13 M14 M15 M16 M17 M18 M19 M20 M21 M22 M23 M24
15.69 8.65 14.06 23.05 18.61 6.99 15.36 7.27 0.74 3.39 15.52 12.45 8.48 6.58
6.0 6.7 7.3 7.0 8.0 8.0 9.0 13.0 16.0 12.3 10.3 11.0 13.7 12.7
2.9 3.2 3.0 3.1 3.5 3.2 3.1 4.0 5.0 4.3 4.2 4.8 5.8 7.2
0.21 0.23 0.16 0.18 0.2 0.17 0.21 0.34 0.5 0.37 0.39 0.37 0.45 0.44
14 14 19 17 17 19 15 12 10 12 11 13 13 16
8.4 8.9 8.2 9.1 10.7 8.5 10.2 14.4 29.4 11.7 11.9 13.1 12.4 13.3
6.7 7.8 9.7 6.8 7.9 11.6 8.8 12.5 12.6 12.6 13.4 15.7 17.8 18.1
7.7 6.6 5.3 3.0 4.2 3.4 3.0 9.0 21.8 9.8 17.2 19.0 19.4 21.5
13 12 12 9 12 11 11 19 36 18 24 27 28 30
43 39 40 30 33 35 35 47 72 42 57 56 48 42
OM, organic matter; OC, organic carbon; N, nitrogen; C/N, C/N ratio; Proteins; carbohydrates, Carb.; and Lipids. P carbon ¼ mg protein mgDW1 0,49; C carbon ¼ mg carbohydrate mgDW1 0, 4; L carbon ¼ mg lipid mgDW1 0, 75; C transformations from Pusceddu, Dell’Anno, and Fabiano (2000); % of the P-C-L OC respect LECO OC ¼ ((P-C-L OC)/10)/LECO OC.
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Fig. 5. Projections of the variables (A) and sampling dates (B) on the first plane of the PCA based on all the measured characteristics of settling POM. GSR, gross sedimentation rates; OM, organic matter; OC, organic carbon; N, nitrogen; C : N, C/N ratio; PRO, proteins; CARB, carbohydrates. See Table 1 for sampling dates code. In Fig. 4B, the use of italics refers to spring–summer sampling dates, the use of plain text to autumn–winter sampling dates with no extreme GSR, and the use of bold character to autumn–winter sampling dates with extreme GSR.
quickly utilised. The mean values of this ratio were 2.4 and 1.1 in Banyuls and in Medes, respectively. Settling POM was thus more labile in Medes than in Banyuls. Although there was significant between-sites differences in chl a concentrations, this parameter does not appear to control between-sites differences in settling POM characteristics. Those differences indeed tended to be larger during summer when chl a concentrations were closer in Banyuls and in Medes. The comparison of wind and wave conditions at both sites suggests that resuspension is less important in Medes. This is consistent with the lack of high GSR during wintertime at that site. However, it must also be pointed that such events may also not have been sampled due to the non-
continuous deployment of the traps. Another factor which may contribute to between-sites differences in GSR is sediment granulometry. In Banyuls, sediment traps were moored over a sandy mud. In Medes, mud and sandy muds are rare near the study site where most of the bottoms is made of rocks and gravels (Gili & Ros, 1985), which are less sensitive to resuspension accounting for the fact that minerals of similar size were collected at both sites. Despite apparent differences in the intensity of resuspension, there was a significant negative relationship between GSR and the organic contents of sediment trap material at both sites. Such a relationship is indicative of the importance of sediment resuspension
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Table 3 Probability associated with the t-test used for comparing the mean value of GSR and sediment trap material biochemical characteristic during the spring–summer and the autumn–winter periods both in the Bay of Banyuls-sur-Mer and in the Medes Islands
GSR OM OC N C/N Carbo. Proteins Lipids
Fig. 6. Relationship linking gross sedimentation rates and the organic contents of settling POM in Banyuls (open dot-solid line) and in Medes (black dot-dashed line).
in driving GSR (Gre´mare et al., 1997, 1998; Medernach et al., 2001). The results of the second PCA showed that in Medes, GSR correlated better with wave height than with any other environmental parameters. Since in the NW Mediterranean resuspension is mostly caused by waves, this suggests that sediment resuspension is a key factor in controlling temporal changes in GSR in Medes as well. 4.2. Seasonality Seasonality was apparent at both sites with a spring– summer period characterised by low GSR and high organic contents of sediment trap material and an autumn–winter period characterised by highly variable (occasionally very high) GSR and low organic contents of sediment trap material, such as already reported by Gre´mare et al. (1997, 1998) for the Bay of
Banyuls-sur-Mer
Medes Islands
<0.05 <0.01 <0.01 <0.01 <0.001 <0.01 <0.05 <0.05
0.06 <0.001 <0.001 <0.001 0.09 <0.01 <0.01 <0.001
Banyuls-sur-Mer. The results of the first PCA suggest that seasonality in settling POM characteristics was clearer in Medes than in Banyuls despite the lack of extremely high GSR during wintertime. This was partly due to between-sites differences in the pattern of changes in settling POM characteristics during spring and summer. In Banyuls those changes are mainly cued by changes in GSR, which tend to be lower during summer than spring (Medernach, personal communication), whereas in Medes they appear to be related with pulses of POM with high lipids contents. Settling POM characteristics differed most between sites during the spring–summer period, which may seem surprising due to stronger between-sites differences in GSR during wintertime. One possible explanation is that Medes station becomes more affected by resuspension during wintertime accounting for smaller between-sites differences in settling POM characteristics at that time of the year, except when extremely high GSR take place in Banyuls. The winter–spring phytoplanktonic bloom constitutes another important factor in controlling seasonality of settling POM characteristics. This bloom occurred in February at both sites. In Banyuls, it occurred simultaneously with a transitory increase in the organic content of settling POM as already reported by Medernach et al. (2001). This confirms that the effects
Table 2 Main characteristics of the correlation models linking GSR and organic matter, organic carbon, nitrogen, C/N ratio, proteins, carbohydrates, and lipids
Organic matter Organic carbon Nitrogen C/N Proteins Carbohydrates Lipids
Intercept Medes Islands
Intercept Banyuls-sur-Mer
p
Slope Medes Islands
Slope Banyuls-sur-Mer
p
Sum of squares
d.f.
1.183 0.683 0.338 1.017 1.128 1.169 1.089
1.086 0.770 0.031 0.803 1.360 1.579 1.214
*** n.s. *** *** n.s. *** *
0.219 0.122 0.249 0.132 0.102 0.157 0.285
0.257 0.267 0.466 0.200 0.517 0.377 0.774
n.s. n.s. * n.s. *** * **
5.327 8.202 10.019 9.126 11.403 8.678 25.207
3 3 3 3 3 3 3
The results of the ANCOVAs comparing these relationships among sites are also provided. ðN ¼ 48Þ (n.s. ¼ non-significant; *p < 0:01; **p < 0:001; ***p < 0:0001; d.f. ¼ Degrees of freedom).
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Fig. 7. Projections of the variables (A) and sampling dates (B) on the first plane of the PCA based on all the environmental parameters and the characteristics of settling POM measured in Medes. GSR, gross sedimentation rates; OM, organic matter; OC, organic carbon; N, nitrogen; C : N, C/N ratio; PRO, proteins; CARB, carbohydrates; FLOW, Ter River flow; WIND, Wind speed; WAVES, wave height. See Table 1 for sampling dates code. In Fig. 4B, group I refers to the spring–summer and group II to the autumn–winter sampling dates.
of the main biological processes on settling POM remain limited relative to those of hydrodynamical processes cuing sediment resuspension. This is even more true in Medes where despite of much higher chl a concentration, the spring–winter bloom was not associated to any significant changes in settling POM biochemical characteristics. This pattern may be related with the occurrence of high GSR during February. It is very unlikely that those GSR were caused by sediment resuspension since wave height was relatively low at that time of the year. They are probably indicative of the existence of another source of refractory POM, which may be constituted by inputs from the Ter River (Rossi, unpublished data). In this sense, it should be stressed
that GSR are certainly not the only factor driving settling POM biochemical characteristics at both sites as also indicated by significant between-sites differences in correlation models linking GSR and sediment trap biochemical characteristics. In Medes, there was an increase in GSR and in some of the settling POM biochemical characteristics (including lipid content) during summer 1998. This pattern is interesting because: (1) in NW Mediterranean, this portion of summer is usually associated with very low GSR and pelagic primary productivity, and (2) increase in GSR due to resuspension and/or terrestrial inputs are usually associated with a decrease in the biochemical parameters associated with the labile component of
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settling POM (Gre´mare et al., 1997, 1998; Medernach et al., 2001). The current hypothesis is that, during summer, GSR in Medes are cued by the interaction between the Ter River flow and local hydrodynamics, and that lower GSR during July 1997 would result from the strong dominance of North-South currents during that particular month, whereas high GSR (in spite of the low Ter River flow) would result from the alternation of North-South and South-North currents during July 1998 (Pasqual, personal communication). Further monitoring of GSR and currents during summer months are clearly needed to further test this hypothesis.
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