Estuarine, Coastal and Shelf Science 58S (2003) 55–61

Temporal and spatial variability of sedimentary organic matter in sandy beaches on the northwest coast of the Iberian Peninsula M. Incera*, S.P. Cividanes, M. Lastra, J. Lo´pez Departamento de Ecoloxı´a e Bioloxı´a Animal, Universidade de Vigo, 36200 Vigo, Spain Received 23 October 2001; accepted 31 July 2002

Abstract Temporal and spatial changes in sedimentary organic matter have been studied in several localities of the northwest coast of Spain. Biochemical composition of the sedimentary organic matter was studied in August and September 1997 in 10 beaches subjected to a different exposure degree to the wave action. Temporal variations in main biochemical classes were investigated in two of them (the more exposed and the more sheltered) over a 1-year period from January 1997 to January 1998 every 3 months. Sediment samples for the analysis of lipids, proteins and carbohydrates were collected at three tidal levels: high, medium and low, when the tide was on the ebb. Biochemical compounds concentrations were significantly higher in the sheltered beaches than in the exposed ones. The low hydrodynamic conditions of the sheltered beaches favour a high accumulation of sedimentary organic matter. There were significant differences among seasons and tidal levels. The biopolymeric carbon (BPC, i.e. the sum of lipid, protein and carbohydrate carbon) was dominated by proteins, followed by lipids and carbohydrates, pointing out the no limitation for heterotrophic metabolism in intertidal sediments. The exposure degree to the wave action was calculated by means of the beach slope. The relation between this parameter and the biochemical compounds showed that localities with low slopes (i.e. sheltered beaches) were related to high concentrations of lipids, proteins and carbohydrates and vice versa. The three biochemical classes showed different trends with time and changes were more pronounced in the sheltered beach than in the exposed one. These results could be explained by the influence of allochthonous inputs in the sheltered beach, which were not observed in the exposed one. Ó 2003 Elsevier Ltd. All rights reserved. Keywords: sedimentary organic matter; lipids; proteins; carbohydrates; intertidal sediments; exposure degree

1. Introduction Spatial and temporal changes of sedimentary organic matter in marine environments affect spatial distribution, metabolism and dynamics of all benthic organisms, from bacteria to macrofauna (Buchanan & Longbottom, 1970; Duineveld et al., 1997; Graf, Shulz, Peinert, & Meyer-Reil, 1983, Grant & Hargrave, 1987). Moreover, it is suggested that there are generalizable patterns of faunal community structure as a response to spatial or temporal changes in organic loading (Pearson & Rosenberg, 1978). As benthic deposit-feeders achieve

* Corresponding author. E-mail address: [email protected] (M. Incera). 0272-7714/03/$ - see front matter Ó 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S0272-7714(03)00040-4

their food requirement by ingesting sedimentary organic matter, quantity and composition of sedimentary organic matter are of primary importance in determining food availability (Buchanan & Longbottom, 1970; Graf, 1989). The gross measure of total organic matter content in the sediment, furnishes only scant information on its availability to consumers (Bianchi & Levinton, 1984; Newell & Field, 1983). In recent years much attention has been paid to the nutritional value of sedimentary organic matter, assessed by its biochemical composition (Fabiano, Danovaro, & Fraschetti, 1995). Total organic matter (as determined by combustion) is generally an over estimation of food available for consumers, mainly because various inorganic compounds may be oxidised at about 500
C (Bretschko & Leichtfried, 1987). The determination of carbohydrate, lipid and protein

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M. Incera et al. / Estuarine, Coastal and Shelf Science 58S (2003) 55–61

concentrations could be suitable to estimate the fraction potentially available to sediment ingesting organisms (Fichez, 1991) because these biochemical classes are assumed to be easier to digest and assimilate (Danovaro, Fabiano, & Della Croce, 1993; Dell’Anno, Fabiano, Mei, & Danovaro, 2000; Fabiano et al., 1995; Fichez, 1991). In recent years this approach has been widely used (Cividanes, Incera, & Lo´pez, 2002; Fabiano & Danovaro, 1994; Fabiano et al., 1995). It is generally admitted that biological richness, abundance and biomass differ between sheltered and exposed intertidal sediments. Thus, sheltered environments have a high abundance and fauna diversity being important nursery areas for a large number of fish and invertebrate species (Adam, 1990). By contrast, in exposed beaches the biological richness decreases. This has been explained by the different physical characteristics of these opposite environments (McLachlan, 1983). It is suggested that the major hydrodynamic stress of exposed localities limits their biological richness (McLachlan, De Ruyck, & Hacking, 1996). However, there is a conspicuous lack of information concerning the sediment biochemical composition in intertidal sediments. Since most studies of faunal structure do not include detailed sediment biochemical composition anal-

yses, the influence of these parameters on the distribution of sandy beach populations is still poorly understood. In this paper, the composition of sedimentary organic matter is studied over a range of intertidal sediments under different degrees of tidal exposure (from sheltered to exposed). Moreover, the extremes of this range, i.e. the more sheltered and the more exposed beaches, were studied during 1-year period. The aims of this study were to investigate: (1) the biochemical composition variability of the sedimentary organic matter in 10 beaches subjected to a different degree of tidal exposure; (2) the temporal changes in quantity of sedimentary organic matter composition in the more sheltered and the more exposed beaches; and (3) the relationship between the exposure to wave action and the three biochemical classes (proteins, lipids and carbohydrates) concentrations.

2. Materials and methods 2.1. Study site Sediment sampling was carried out at 10 localities placed on the northwest coast of the Iberian Peninsula (Fig. 1). These localities are influenced by a macrotidal

Fig. 1. Location of the 10 beaches studied on the northwest coast of the Iberian Peninsula. (a) Relative position on the Iberian Peninsula. (b) Intertidal slope of each studied beach.

M. Incera et al. / Estuarine, Coastal and Shelf Science 58S (2003) 55–61

regime with a medium tidal range of 3 m. According to their geographical situation on the rı´ as system (i.e. typical inlets of the northwest coast of Spain), the localities were under a different degree of tidal exposure. Five of them, namely Cesantes, Lourido, Bamio, Barran˜a and Testal, are located in the inner part of the rı´ as and were characterised by low wave exposure, shallow reduced sediment layers and the presence of macrofaunal burrows. According to McLachlan (1980), this group was named Ôsheltered beachesÕ. The others, namely Ame´rica, Espin˜eirido, Carnota, Llas and Pen˜arronda, are placed in the outer part of the rı´ as and characterised by moderate to heavy wave action, deep reduced sediment layers and usually no macrofaunal burrows. According to McLachlan, this group was called Ôexposed beachesÕ. Autochthonous inputs are the major source of organic matter in the exposed group whereas the sheltered group is also affected by large amounts of allochthonous organic matter (land derived material and debris). 2.2. Sediment sampling Sediment sampling was carried out in August and September 1997 at the 10 beaches described previously (Fig. 1). Moreover, temporal variations in main biochemical compounds were investigated in two of them (one exposed, Espin˜eirido, and one sheltered, Barran˜a) over a 1-year period from January 1997 to January 1998 every 3 months. Sediment samples were collected in three replicates by hand coring (15.5 cm inner diameter core) from sediment surface down to 25 cm depth at three tidal levels (high, medium and low levels), when the tide was on the ebb. Each sediment sample was mixed and subsamples were taken for the analysis of lipids, proteins and carbohydrates. All subsamples were frozen at 30
C until further processing.

carbohydrates (CHO) were analysed from the supernatant according to Dubois, Gilles, Hamilton, and Rebers (1956) and expressed as glucose equivalents. Total proteins (PRT) were determined using the method of Lowry and Rosenbrough (1951) as modified by Markwell, Haas, Bieber, and Tolbert (1978). Protein concentrations are given as bovine serum albumin (BSA) equivalents. Total lipids (LIP) were extracted from dried sediment samples by direct elution with a 2 : 1 (v/v) chloroform and methanol solution according to Bligh and Dyer (1959). Lipid analysis was carried out according to Marsh and Weinstein (1966) applied to sediments and expressed as tripalmitine equivalents. About 0.5–2.5 g of sediment was used for each analyses and data were normalised to sediment dry weight. Sediment samples combusted at 500
C for 6 h and processed as described previously were utilised as blanks for all biochemical analyses. Carbohydrate, protein and lipid concentrations were converted to carbon equivalents assuming a conversion factor of 0.45, 0.50 and 0.70, respectively (Fabiano et al., 1995; Fichez, Dennis, & Fontaine, 1993). The sum of lipid, protein and carbohydrate carbon was reported as the biopolymeric carbon fraction (BPC sensu Fabiano & Danovaro, 1994; Fabiano et al., 1995; Fichez, 1991; Mayer, 1989), assumed as a reliable estimate of the labile fraction of total organic matter, i.e. the fraction which was readily available to benthic consumers. 2.5. Data analysis Temporal and spatial fluctuations in biochemical parameters were assessed by a two-way ANOVA with time (months) and space (tidal levels) as factors (Sokal & Rohlf, 1995). SPSS release 10.0 was used for these statistical analyses (Nie, Hull, Jenkins, Steinbrenner, & Bent, 1975).

2.3. Beach profile

3. Results

Beach profile was measured at low tidal level according to Emery’s method (Emery, 1961) with a LEICA NA820 theodolite, from the dry zone to the lower limit of the saturation zone (Salvat, 1964). The beach face was measured by the ratio between the intertidal width and the height of the high tidal level.

3.1. Temporal changes in the biochemical composition of sedimentary organic matter

2.4. Biochemical composition of the sedimentary organic matter All the biochemical analyses were carried out on samples that had been oven-dried at 60
C until constant weight and finely powdered with a pestle (Pulverisette 2, FRITSCH). After a previous extraction from the dried sediment with 5% trichloroacetic acid (TCA), total

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Temporal variations of carbohydrates, proteins, lipids and BPC are shown in Fig. 2. Biochemical compounds concentrations were significantly higher in the sheltered area (N ¼ 90, P < 0:001), of the order of 70, 8 and 10 times higher for carbohydrates, proteins and lipids, respectively. The two-way ANOVA analyses revealed that all biochemical compounds and BPC displayed significant differences with seasons and tidal levels (N ¼ 45, P < 0:001 for each, Table 1) in both beaches. Maxima concentrations of biochemical compounds were found at the medium tidal level of the sheltered beach and at

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M. Incera et al. / Estuarine, Coastal and Shelf Science 58S (2003) 55–61 Table 1 Summary of two-way ANOVA results of protein (PRT), carbohydrate (CHO), lipid (LIP) and carbon of the biopolymeric fraction (BPC) data for the two beaches of the temporal study (Barran˜a and Espin˜eirido, N ¼ 45 each) Barran˜a

Espin˜eirido

Source of variation

F ratio

P

F ratio

P

PRT

Month Tidal level Month  tidal level

25.3 230.3 13.5

*** *** ***

21.3 202.3 7.8

*** *** ***

CHO

Month Tidal level Month  tidal level

58.3 364.5 16.6

*** *** ***

17.3 70.1 4.2

*** *** ***

LIP

Month Tidal level Month  tidal level

8.6 74.7 4.1

*** *** ***

77.0 88.9 20.0

*** *** ***

BPC

Month Tidal level Month  tidal level

5.1 209.3 3.7

*** *** ***

17.0 193.7 8.5

*** *** ***

Significance levels: ***P < 0:001, ns: P > 0:05.

respectively) and carbohydrates (14% in Barran˜a and 1.9% in Espin˜eirido). 3.2. Spatial changes in the biochemical composition of sedimentary organic matter

Fig. 2. Temporal variations in the concentrations of carbohydrates (CHO), proteins (PRT), lipids (LIP) and biopolymeric carbon (BPC) in Barran˜a and Espin˜eirido. Mean values  standard deviations are indicated.

the low tidal level of the exposed one. Carbohydrate, protein and lipid concentrations in Barran˜a showed different temporal patterns with maximum values of 589 lg g1 sed dw (sediment dry weight) (October 1997), 3218 lg g1 (January 1997) and 1108 lg g1 (October 1997), respectively. Maxima recorded in the exposed beach were 6.54 lg g1 (July 1997), 234 lg g1 (January 1998) and 55 lg g1 (October 1997) for the same compounds. The BPC showed a similar trend to protein pattern, because of it high contribution, with maxima of 2219 lg g1 (January 1997) in Barran˜a and 152 lg g1 (July 1997) in Espin˜eirido. Proteins were the dominant class among labile compounds in both areas (60.5% on annual average in Barran˜a and 70.5% in Espin˜eirido), followed by lipids (25.5 and 27.6% in sheltered and exposed beaches,

Carbohydrate, lipid and protein concentrations were significantly related (P < 0:05) with the intertidal slope at the three tidal levels, except for protein concentrations at low and high tidal levels (Fig. 3). The three biochemical classes concentrations increased exponentially from steep beaches to the flat ones at the three tidal levels. The concentration variability among tidal levels increased along the gradient steep to flat intertidal sediments (Fig. 3). High, medium and low tidal levels were more similar in biochemical compounds concentrations in the steeper beaches than in the sheltered ones. Sedimentary carbohydrates ranged between 3.32 lg g1 sed dw in Espin˜eirido high tidal level and 1038 lg g1 in Cesantes low tidal level. Proteins varied between 48.93 lg g1 in Carnota high tidal level and 2208.22 lg g1 in Cesantes low tidal level. Lipids ranged from 5.28 lg g1 in Espin˜eirido high tidal level to 445 lg g1 in Cesantes low tidal level (Table 2).

4. Discussion 4.1. Common patterns of the temporal and spatial studies Biochemical compound concentrations of sedimentary organic matter showed clear differences between sheltered and exposed beaches. Such differences were

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Fig. 3. Relation between the intertidal slope (expressed as 1/slope) and protein, lipid and carbohydrates concentrations in the three tidal levels studied. Means values are reported for each locality. Proteins high tidal level: P > 0:05; proteins medium tidal level: y ¼ 108:76 e0:027X , r2 ¼ 0:58, P < 0:05; proteins low tidal level: P > 0:05. Lipids high tidal level: y ¼ 8:71 e0:015X , r2 ¼ 0:37, P < 0:05; lipids medium tidal level: y ¼ 22:60 e0:022X , r2 ¼ 0:63, P < 0:05; lipids low tidal level: y ¼ 33:38 e0:02X , r2 ¼ 0:52, P < 0:05. Carbohydrates high tidal level: y ¼ 3:31 e0:03X , r2 ¼ 0:82, P < 0:001; carbohydrates medium tidal level: y ¼ 9:62 e0:04X , r2 ¼ 0:69, P < 0:01; carbohydrates low tidal level: y ¼ 24:70 e0:03X , r2 ¼ 0:56, P < 0:05.

Table 2 Carbohydrates, lipids and proteins concentrations (lg g1 sediment dry weight) at the 10 beaches studied during summer 1997 Carbohydrates

Lipids

Beaches

Mean

SE

Mean

SE

Proteins Mean

SE

Llas Espin˜eirido Testal Ame´rica Carnota Pen˜arronda Bamio Lourido Cesantes Barran˜a

51.15 4.49 20.05 64.77 109.10 70.85 109.32 191.20 537.19 315.20

23.63 1.03 7.83 32.92 68.40 43.79 40.81 97.04 267.84 140.17

53.43 18.17 58.51 90.11 45.45 35.39 45.25 190.37 236.20 486.33

14.70 8.91 14.30 2.98 17.06 12.61 19.48 67.73 98.10 177.18

259.99 102.92 93.83 486.19 315.87 402.16 758.80 316.91 1114.96 736.43

21.88 43.07 19.47 116.82 133.48 123.11 396.87 107.98 570.71 303.74

Data are mean values of the three tidal levels studied (high, medium and low). Standard errors are indicated.

probably related to the morphodynamic and physicochemical characteristics of each group of beaches that determined the presence of a higher or lower amount of organic matter. The low hydrodynamism of the sheltered beaches favoured the accumulation of sedimentary organic matter due to the scarce renewal of interstitial water. In addition, the low energy of the surge permitted the formation of fine and stable sediments that allowed the settlement of a large amount of fauna (Nordstrom, 1992). By contrast, the strong hydrodynamism of the exposed beaches permitted the deposition of coarser sediments through which water run easily, preventing the accumulation of organic matter. Moreover, the hydrodynamic stress of wave environment limited biological richness, as found by McLachlan et al. (1996) in Australian sandy beaches.

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4.2. Temporal changes in the biochemical composition of sedimentary organic matter In both beaches, the different temporal patterns of the various components suggested a distinct composition and/or origin of the organic matter inputs during the different sampling periods. In the sheltered beach (Barran˜a), temporal variations of carbohydrates and lipids showed completely opposite trends to those of proteins (Fig. 2). Moreover, the particularly high protein values recorded in January 1997 could be attributed to allochthonous inputs, in coincidence with the results obtained by Danovaro (1996) in sediments of Prelo Bay (Ligurian Sea). On the contrary, in the exposed beach (Espin˜eirido), seasonal trends in proteins, carbohydrates and lipids were completely different from those in Barran˜a. These results could suggest that while the exposed area might present a ÔnaturalÕ seasonal variation in biochemical composition of the sedimentary organic matter, the temporal changes in the sheltered locality could be masked by episodic allochthonous inputs. The temporal variation of BPC in both beaches was largely influenced by high protein concentrations, pointing out the no limitation for heterotrophic metabolism in intertidal sediments (Fabiano et al., 1995). These results were in contrast with those found by Pusceddu, Sara`, Armeni, Fabiano, and Mazzola (1999) in an oligotrophic area (Marsala lagoon) where carbohydrates were the dominant class. Higher BPC values in January and April 1997 in Barran˜a and January 1998 in Espin˜eirido indicated that sedimentary organic matter in these months was more readily available to benthic consumers. 4.3. Spatial changes in the biochemical composition of sedimentary organic matter The intertidal slope of a beach is one of the parameters used to estimate the degree of hydrodynamic force experienced on an intertidal sandy beach (McLachlan, 1980). This factor usually increases with decreasing exposure. In this study, over the entire intertidal sediment gradient (from sheltered to exposed intertidal localities), protein, lipid and carbohydrate concentrations were significantly correlated with the intertidal slope at the three tidal levels (Fig. 3), except for protein concentrations at low and high tidal levels. Thus, protein, lipid and carbohydrate concentrations decreased with increasing intertidal slope. McLachlan (1990) investigated the ÔglobalÕ trends in biological features of 23 beaches in relation to physical changes. Beach slope gave a good correlation with diversity and abundance. His study showed that species diversity increased linearly and total abundance exponentially from steep to flat beaches. Another study

conducted by Dexter (1992) in 284 beaches showed that the number of species, H9, density and species richness increased with reducing exposure to wave action. It is generally admitted that sandy shores show an increase in diversity of species (Little, 2000), abundance and biomass as exposure decreases (McLachlan, 1990). It is suggested that the decrease in fauna along the gradient of exposure degree is caused by an increasingly harsh swash climate and/or coarser sand leading towards the more exposure extreme (McLachlan et al., 1996). From the present study it can be concluded that protein, carbohydrate and lipid concentrations increased from steep to flat localities, in coincidence with the abundance of organisms. Thus, it is suggested that the control of the beach fauna is complex and determined not only by the physical environment but also by the overall characteristics of the beach where probably the biochemical composition of the organic matter has an important role.

Acknowledgements This research was supported by the Xunta de Galicia (XUGA 30105A98) and the Universidade de Vigo (64102C859). The authors would like to thank ÔEquipo de BentosÕ for their useful help during sampling. Thanks are also due to two anonymous referees for suggestions and improvements of the manuscript.

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