The effects of season and wrack subsidy on the community functioning of exposed sandy beaches

Estuarine, Coastal and Shelf Science 95 (2011) 165e177

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The effects of season and wrack subsidy on the community functioning of exposed sandy beaches Sílvia C. Gonçalvesa, b, *, João C. Marquesb a

School of Tourism and Maritime Technology, Marine Resources Research Group - GIRM, Polytechnic Institute of Leiria, Campus 4, Santuário Na. Sra. dos Remédios, 2520-641 Peniche, Portugal b IMAR - Marine and Environmental Research Centre, Department of Life Sciences, Faculty of Sciences and Technology, University of Coimbra, Largo Marquês de Pombal, 3004-517 Coimbra, Portugal

a r t i c l e i n f o

a b s t r a c t

Article history: Received 12 January 2011 Accepted 21 August 2011 Available online 14 September 2011

Seasonality is an important component of the climate, known to influence several biological events that can be reflected in community structure and organization. However, sandy beach macrofaunal community ecological studies are frequently based on snapshot sampling events, neglecting this important dimension and its effects. In the present study, the effects of seasons and wrack subsidies on macrofaunal communitie’s function of two similar exposed sandy beaches of Portugal was monitored for approximately 18 months by sampling all the beach area, from the shoreline to the base of the dunes. The study assessed the beach physical environment, community density and composition, trophic structure, secondary production of key species and the potential relationships between biological data and environmental parameters. Seasonality, particularly temperature variations, and the interaction between seasons and the beach zones (supralittoral vs. intertidal areas) had a strong influence on the communities, promoting a differential utilization of the beach by several species. Seasons also shaped the density of trophic groups, with consequences in community composition and function. Differences between beaches were observed on wrack subsidy, community composition and relative contribution of the dominant species, but the trophic structure was stable and dominated by scavengers. Talitrus saltator was the most productive key species, and the contribution of the resident key species regarding secondary productions and standing stocks was different between beaches. Wrack quantity and deposition frequency on the beach had a positive influence on several faunal descriptors such as density and number of species of various functional groups. The present study also highlights the clear dependence of macrofauna of exposed sandy beaches on the wrack subsidies brought ashore by the tides, illustrating their role on community organization regarding several wrack-associated species and not only scavengers. Ó 2011 Elsevier Ltd. All rights reserved.

Keywords: macrofaunal communities function seasonality wrack subsidy exposed sandy beaches secondary production Regional terms: Atlantic sandy beaches western coast of Portugal Cabedelo and Quiaios

1. Introduction Despite their terrestrial appearance, sandy beaches are dynamic and complex transitional systems that interface between the sea and land, where food chains normally begin and end in the sea. Large resident primary producers, such as macroalgae and seagrasses, are usually absent and benthic microflora and surf-zone phytoplankton (when present) often represent small primary

* Corresponding author. School of Tourism and Maritime Technology, Marine Resources Research Group - GIRM, Polytechnic Institute of Leiria, Campus 4, Santuário Na. Sra. dos Remédios, 2520-641 Peniche, Portugal. E-mail addresses: [email protected] (S.C. Gonçalves), [email protected] (J. C. Marques). 0272-7714/$ e see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2011.08.036

production values (McLachlan and Brown, 2006). On exposed sandy beaches, allochthonous inputs of organic matter with marine origin and stranded by tides subsidise the beach food webs (Dugan et al., 2003), and function as the primary food resource for the local macrofaunal community. These allochthonous inputs might include several types of stranded macrophytes, which are usually the most abundant and frequent component of beach wrack, but also carrion, phytoplankton and other types of particulate organic matter (Colombini and Chelazzi, 2003; McLachlan and Brown, 2006). Macrofaunal communities of sandy beaches play an important ecological role in sandy shore function, because they occupy a key position in the centre of food chains (McLachlan and Brown, 2006). Several species of scavengers, such as crustaceans and insects, are

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known to feed upon beach wrack, having an important impact on organic detritus processing (see for instance Lastra et al., 2008). In turn, macrofaunal organisms serve as prey for other macrofaunal elements and for top predators such as fishes and shorebirds (e.g. Hubbard and Dugan, 2003). In recent years, sandy beach ecologists have focused their attention on the dual-side interactions between beach wrack and macrofaunal organisms and improved the understanding about sandy beach energetics and the function of macrofauna. The temporal and spatial use of stranded wrack by macrofauna and the importance of these animals in beach wrack consumption and processing have been considerably enhanced with studies (e.g. Colombini et al., 2000; Lastra et al., 2008). There have also been advances on the effects of beach wrack on macrofaunal communities, especially upon community structure descriptors (e.g. Dugan et al., 2003; Jaramillo et al., 2006; Gonçalves et al., 2009). However, the trophic structure of these communities and the effects of seasons on community function are still poorly understood and further research is needed. Several parameters of the beach environment, such as food supply in the form of wrack subsidies, temperature and the occurrence of storms, oscillate throughout the year and may have considerable effects, for instance on the community trophic structure. Also, there is a clear lack of knowledge with regard to macrofaunal secondary production and standing stock estimates. These estimations, although timeconsuming and difficult to obtain, are of great importance, as they elucidate and quantify the role of macrofaunal organisms in the energy balance of beach ecosystems. Studies on the macrofaunal communities of sandy beaches are frequently based on snapshot sampling events (e.g. McLachlan, 1990; Defeo et al., 1992; Rodil et al., 2006). Nevertheless, Defeo and Rueda (2002) strongly criticised this approach because it could lead, for instance, to biases on the temporal and spatial abundance patterns observed for each species. Similarly, a fortnightly sampling program, with a proper spatial replication across the beach area, appears to be extremely important if, for instance, the influence of seasons on community structure and function are to be assessed. However, these kind of sampling programmes are very rare in sandy beach studies. A recent study using a temporally and spatially replicated sampling program (Gonçalves et al., 2009) illustrated that seasons had a strong influence on beach communities, namely on the densities and on the horizontal distribution of the dominant species. Also, the influence of seasons on beach zones (intertidal vs. supralittoral) caused significant effects on several important faunal components. However, the influence of seasons upon community function descriptors was not analysed. This study compared the community structure at two similar exposed sandy beaches with some degree of environmental variation, namely important differences in wrack subsidies. These differences led to distinct community structures and differences in community composition. Also, distinct relative contributions regarding the abundant species were observed, although the talitrids Talitrus saltator (Montagu, 1808) and Talorchestia brito Stebbing, 1891 and the tylid Tylos europaeus Arcangeli, 1938 were key species at both communities (see Gonçalves et al., 2009 for more details). All these differences may be reflected for instance in distinct trophic structures and in distinct secondary production and standing stock estimates. The main objective of the present work was to investigate the effects of seasons and wrack subsidies on the macrofaunal community function of exposed sandy beaches. To achieve this goal, the following hypotheses were tested: (i) do seasons influence the trophic structure of macrofaunal communities? (ii) are there interactions between seasons and beach zones capable of influencing community organization? (iii) do wrack subsidies influence

the density and the species richness of the trophic (functional) groups? Additionally, the trophic relevance of talitrids and tylids to the community’s energy balance was also investigated. 2. Materials and methods 2.1. Study sites Two sandy beaches e Cabedelo and Quiaios e on the Western coast of Portugal (Fig. 1) were studied because of their relatively undisturbed nature and because of clear differences in the inputs of drift wrack. The Cabedelo sandy beach (40
070 3200 N 8
5104900 W) is located 1 km South of the Mondego estuary mouth, while Quiaios beach (40
120 210 ’ N 8
530 480 ’ W) is located further to the North, approximately 8 km north from Cabo Mondego. However, in recent years Cabedelo has probably been subjected to comparatively higher human pressure. This beach is closer to the important tourist centre town of Figueira da Foz which has recently supported several recreational activities (e.g. surf championships). The two beaches present relatively similar conditions of exposure to wave action. According to the McLachlan’s (1980) rating scheme, Cabedelo is classified as an exposed beach (exposure rate: 15) and Quiaios as very exposed (exposure rate: 16). Tides on the western Portuguese coast are semidiurnal and mesotidal, with a tidal range between 2 and 3.5 m. Portugal presents a warm temperate AtlanticMediterranean climate, with a distinct wet but mild winter and a dry and also mild summer, especially in the regions at North of the Montejunto-Estrela Mountain System. During storms, the beach at Cabedelo may be almost completely submerged, causing depositions of large amounts of drift wrack, mainly composed of macroalgae from rocky shores located north of the beach, and possibly also from the Mondego estuarine system. The input of drift wrack at Quiaios is clearly more limited, since there are no rocky shores or other potential sources of debris nearby. The exposed nature of both beaches implied that no vegetation was found on their supralittoral areas. However, Quiaios beach exhibits a more developed dune system, although the foredune height is similar between both beaches. Additional information on the characteristics of these two sandy beaches is provided in Table 1.

Fig. 1. Location of the sandy beaches used as study sites: Cabedelo and Quiaios (western coast of Portugal). Cabedelo: 40
070 3200 N 8
5104900 W; Quiaios: 40
120 2100 N 8
530 4800 W.

S.C. Gonçalves, J.C. Marques / Estuarine, Coastal and Shelf Science 95 (2011) 165e177 Table 1 Basic characteristics observed in the two sandy beaches used as study sites. For quantitative characteristics averages  standard deviations for the period of study are given. Characteristic

Cabedelo

Quiaios

Width of the beach (m) Average slope (%) Extension of the intertidal area (m) Foredune height (m) Sediment granulometry (mm)

60 2.0 Neap tides: 30 Spring tides: 45 2.5e3 Medium sand (0.250e0.500) 3.24 (1.22) 2.53 (1.44) 4.11 (1.88) 0.15 (0.05) 0.13 (0.03) 0.15 (0.04)

100 1.8 Neap tides: 50 Spring tides: 75 2.5e3 Coarse sand (0.500e1.0) 2.64 (0.95) 2.08 (1.30) 3.07 (0.88) 0.19 (0.35) 0.19 (0.35) 0.21 (0.38)

Sediment moisture (%) Supralittoral Intertidal Organic matter content (%) Supralittoral Intertidal

2.2. Sampling procedures The macrofaunal communities were sampled fortnightly, during low neap-tides, from January 1999 to June 2000 at Quiaios (18 months), and from March 1999 to June 2000 (16 months) at Cabedelo. Samples were taken on the supralittoral and intertidal zones. Sampling levels were defined at regular intervals along two transects extending from the low tide water mark to the base of the dunes. Ten equidistant sampling levels were considered along each transect. The mean high water neap tide mark, left by the previous tide, was always used as a reference point to define, in each occasion, the supralittoral and the intertidal zones, preventing seasonal variations of beaches width throughout the year. Along each transect, five sampling levels were considered in the supralittoral zone of the beaches, and other five at the intertidal one, adjusting the intervals between levels as necessary through the year. For each level and at each transect, a minimum of 2 replicates was collected. This sampling procedure was able to account for differences regarding the spatial distribution of the macrofauna along the year. Sampling was performed using a 0.25 m2 quadrat and removing the first 20 cm of the sand surface layer, with a small scoop. The sand was sieved through a 1 mm mesh and the animals collected were subsequently separated in the laboratory and preserved in 70% alcohol, after fixation in 4% formalin. Sediment grain size composition was determined from seasonal samples to check for significant differences, and classified according to the Wentworth scale described in McLachlan and Brown (2006). A set of physico-chemical parameters were measured over the study period to account for possible relationships between macrofaunal communities and their environment. Wrack quantity (potential food measured in g.m2), organic matter in the sediment (AFDW), and sediment moisture content were determined according to the procedures described in Marques et al. (2003). Meteorological data were obtained from the nearest meteorological stations (Coimbra for temperature and precipitation, and Figueira da Foz harbour for other parameters): precipitation, temperature, visibility, cloudiness, wave height, wave period, and wind velocity. 2.3. Data analysis All the marine, semi-terrestrial, and terrestrial animals collected were considered in the study. Density (individuals.m2) was calculated for each site using a proportionally weighted average approach regarding each level of the beach, and analysed through all sampling dates and for each season. The density and species composition of the supralittoral and intertidal zones were compared and species exhibiting a frequency of occurrence higher

167

than 10% during the whole sampling period were considered as residents. Diversity trends and trophic structure were analysed in order to understand community function including species richness and ShannoneWiener’s H’ was used as a measure of heterogeneity. As for the trophic structure, organisms were classified into the following functional groups, as a function of their feeding habits, according to the general approach described in McLachlan and Brown (2006): Scavengers (which also included vegetal detritivores), Herbivores, Predators, Filter/Suspension Feeders and Omnivores. Deposit feeders were not included since these are normally confined to relatively sheltered shores and both studied beaches were exposed. The contribution of the species presenting more than one feeding type was assumed to be evenly distributed amongst the different functional groups to which they could belong. Finally, when the organisms identification to the species level was not possible, their feeding type was inferred from related species (congeners or, when not possible, taxa belonging to the same family). Secondary production and standing stocks estimates were also carried out but only for talitrids and tylids, which were considered community key species in a previous study (Gonçalves et al., 2009). Growth (P) and elimination (E) production, as well as P=B and E=B ratios, were estimated based upon cohort recognition, following a method derived by Allen (1971) and fully described in Marques et al. (2003). This method was applied only to the populations of Talitrus saltator and Talorchestia brito, at Cabedelo and Quiaios beach respectively, where these species were particularly abundant. Tylos europaeus presented a very complex population structure (see Gonçalves et al., 2005), and a size-frequency method had to be used to estimate secondary production, instead of a cohort recognition based one. Such a method, which was modified by Benke (1979) and is fully described in Gonçalves et al. (2005), has the limitation of not allowing the estimation of elimination production. Moreover, estimations had to be done by pooling data from the Quiaios and Cabedelo populations. Before performing any kind of statistical analysis of community data, all faunal and environmental variables were previously checked for normality (normality tests: Anderson-Darling, RyanJoiner and KolmogoroveSmirnov), using the MINITAB 12.2 software package, and transformed whenever necessary (log transformation for wrack quantity). To test the effects of season and beach on community function descriptors, physico-chemical parameters measured at the beaches (wrack quantity, organic matter in the sediment, and sediment moisture content) and the faunal components were tested for differences using Two-Way ANOVA’s. These variables were also tested with Two-Way Nested ANOVA. In this case, in addition to the factor season, beach zones nested on beaches were also tested as a factor. In both cases, the significant effects detected were then subjected to post-hoc tests: (i) Tukey HSD and LSD tests to analyse the individual effects of the factors; (ii) Bonferroni tests to analyse the significant interactions between the factors (pairwise comparisons). To test for the influence of season and wrack subsidies, multiple regression models and multivariate methods were developed for each community. Total density, functional groups density, species richness within each functional group and key species densities were correlated with environmental factors using multiple regressions. Models were fitted with data following the Stepwise Regression method and Curve Estimations, with the display of ANOVA results, were used to determine the curve model with a better fit. All the procedures were performed using the SPSS 18.0 software package. Potential relationships between the density of resident functional groups and environmental parameters were tested using multivariate techniques performed with the statistical software  package CANOCO 4.0 for Windows (ter Braak and Smilauer, 1998).

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Table 2 ANOVA and post-hoc tests results for environmental and faunal responses considering the effects of beaches (Cadedelo and Quiaios), seasons (Spring, Summer, Autumn and Winter), and beach zones (Supralittoral and Intertidal, nested on beaches) as factors. Only the variables that presented significant results are represented (p < 0.05). df e degrees of freedom; MS e Mean Square. ANOVA Source of variation

df

Environmental parameters: Sediment moisture content (%) Seasons Zones nested in Beaches Wrack quantity (g.m2) Zones nested in Beaches Faunal components: Resident scavengers density (ind.m2) Seasons  Zones nested in Beaches Resident herbivores density (ind.m2) Beaches Zones nested in Beaches Resident predators density (ind.m2) Seasons  Beaches Seasons  Zones nested in Beaches Number of species Seasons  Zones nested in Beaches Number of resident scavenger species Seasons  Beaches Number of resident herbivore species Seasons  Beaches Number of resident predator species Seasons  Beaches

MS

F-statistic

p-value

3 3

5.900 8.451

4.037 8.724

0.013 0.000

3

215.546

7.386

0.001

9

6123.749

4.714

0.000

1 3

282.324 397.339

6.923 4.859

0.012 0.007

3 9

0.481 0.631

7.633 5.280

0.000 0.001

9

32.833

5.324

0.000

3

13.533

4.054

0.013

3

5.143

4.278

0.010

3

1.890

4.386

0.009

Post-hoc tests Dependent variable and factors tested Environmental parameters: Sediment moisture content (%) Effect of seasons Effect of beach zones Homogeneous subsets

Detritus quantity (g.m2) Effect of beach zones

Test

p-value

Tukey HSD LSD

Comparison: autumn and summer Comparison: autumn and summer

0.032 0.006

Tukey HSD

Subs. 1: Qsupra ¼ Csupra Subs. 2: Csupra ¼ Qinter Subs. 3: Qinter ¼ Cinter

0.554 0.400 0.583

Tukey HSD

Comparison: Comparison: Comparison: Comparison: Comparison: Comparison:

0.000 0.000 0.013 0.000 0.000 0.003

LSD

Faunal components: Resident scavengers density (ind.m2) Interaction: seasons  beach zones

Condition

Bonferroni

Csupra and Cinter csupra and qinter csupra and qsupra Csupra and Cinter Csupra and Qinter Csupra and Qsupra

Summer Comparison: Cinter and Csupra Comparison: Cinter and Qsupra

0.002 0.000

2

Resident herbivores density (ind.m Effect of beach zones Homogeneous subsets

) Tukey HSD

Subs. 1: Csupra ¼ Cinter ¼ Qsupra Subs. 2: Qinter

Resident predators density (ind.m2) Interaction: seasons  beaches

Bonferroni

Interaction: seasons  beach zones

Bonferroni

Autumn Comparison: Cabedelo and Quiaios Autumn Comparison: Cinter and Csupra Comparison: Cinter and Qsupra

Number of species Interaction: seasons  beach zones

Bonferroni

Autumn Comparison: Comparison: Winter Comparison: Comparison: Comparison: Comparison: Spring Comparison: Comparison:

0.639 1.000

0.000 0.000 0.000

Qinter and Csupra Qinter and Qsupra

0.003 0.012

Cinter and Qsupra Cinter and Csupra Qinter and Csupra Qinter and Qsupra

0.000 0.012 0.018 0.000

Csupra and Qinter Csupra and Cinter

0.000 0.000

S.C. Gonçalves, J.C. Marques / Estuarine, Coastal and Shelf Science 95 (2011) 165e177

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Table 2 (continued ) Post-hoc tests Dependent variable and factors tested

Test

Condition

p-value

Number of resident scavenger species Interaction: seasons  beaches

Bonferroni

Spring Comparison: Cabedelo and Quiaios

0.010

Winter Comparison: Cabedelo and Quiaios

0.003

Winter Comparison: Cabedelo and Quiaios

0.006

Number of resident herbivore species Interaction: seasons  beaches Number of resident predator species Interaction: seasons  beaches

Bonferroni

Bonferroni

In the analysis, there was no down-weighting of rare species, and biological data were square-root transformed. Environmental parameters tested as explanatory variables were previously checked for multi-colinearity. Biological data matrixes were firstly submitted to Detrended Correspondence Analysis (DCA), with detrending by segments, in order to measure the gradient lengths. This first procedure allowed a decision whether a linear species response-based or a unimodal species response-based ordination method should be used. In all cases, the gradient length of the first axis obtained was less than 3.0, and an analysis based on linear species response was used: the constrained ordination method Redundancy Analyses (RDA). The forward selection procedure was applied with a Monte Carlo Permutation Test (999 permutations) to determine which environmental variables were significant (p < 0.05), explaining the largest amount of variation in each biological data set. The significance of the reduced RDA models finally obtained was also assessed using Monte Carlo Permutation Tests (p < 0.05 after 999 permutations). 3. Results 3.1. The physical environment and the macrofaunal communities Quiaios beach is considerably wider than Cabedelo and has a smaller average slope (Table 1). There were no significant seasonal variations in sediment grain size composition (p > 0.05). According to the Wentworth scale, Cabedelo had medium sand grains, while in Quiaios the sediment was coarse (Table 1). In autumn and summer, the water contents of the sand were significantly distinct and, regarding beach zones, 3 homogeneous subsets were identified (Table 2). Cabedelo beach had a much higher and a more regular input of wrack subsidies (4.5 times on average) than Quiaios (Fig. 3C). Wrack subsidies varied significantly between beach zones - for instance the supralittoral at Cabedelo received much higher quantities than other beach zones (Table 2) e while the sand organic content did not show significant differences. On both beaches, the communities were dominated by arthropods, namely crustaceans (the most abundant group) and insects. ANOVA showed that there were no significant differences between the diversity indices of the beaches (p > 0.05). Only a small number of the species were resident e 16 species at Cabedelo and 14 species at Quiaios. This included crustaceans (mainly talitrid amphipods and isopods), coleopterans (mainly tenebrionids and scarabids, in addition to different kinds of larvae) and dipteran larvae. These groups represented the bulk of both communities: in average 98.6%  4.13 of the community density at Cabedelo, and 98.3%  4.20 at Quiaios. The talitrids Talitrus saltator and Talorchestia brito, and the isopod Tylos europaeus were the most abundant species in both beaches (Fig. 2B and C). T. saltator was the dominant species at Cabedelo but at Quiaios, T. europaeus and T. brito were the most abundant. The two beaches exhibited some differences in species

composition. The mysid Gastrosaccus sanctus (Van Beneden, 1861) and the coleopterans Callicnemis latreillei Castelnau, 1832, Aegiala arenaria Fabricius, 1787 and Saprinus sp. occurred only at Cabedelo, while the residents Gonioctena olivacea Forster, 1771 (coleopteran), and Cochlicella barbara (Linnaeus, 1758) (mollusc), were never observed at Cabedelo. Community total densities were similar in both beaches (p > 0.05), with minima being recorded in January (winter) and maxima in July (summer) (Fig. 2a), reflecting the dominant species patterns of variation (Fig. 2). Taking only the resident species into account, densities between beaches were also similar (p > 0.05). 3.2. Trophic structure and the effects of beach zones and seasonality on community organization In both communities, scavengers were the dominant functional group and the trophic structure was in general stable (Fig. 3a and b). Supralittoral crustaceans, coleopterans and diptera larvae constituted the main resident scavenger species. Herbivores were always second in importance, except in November 1999 at Cabedelo, when filter feeders exceeded them in abundance. Talorchestia brito, a few insects (especially coleopterans), and the mollusc C. barbara were the main resident herbivores, and the only resident filter feeders were the crustaceans G. sanctus and Pontocrates arenarius (Bate, 1858). Resident predators were mainly represented by coleopterans, and also by a few species of crustaceans. However, differences were observed between the two beaches regarding the relative importance of functional groups: (i) herbivores were significantly more important in the community at Quiaios (18.5% in comparison to 6.6% at Cabedelo); (ii) filter feeders were more abundant at Cabedelo. Omnivores were a residual group in both cases, representing less than 0.05%. The species richness in the intertidal zone of the beaches was almost the double that found in the supralittoral, although only a small proportion were resident (Table 3). Additionally, the supralittoral resident fauna was more diverse than the intertidal. Seasonality and beach zones had a significant effect on the number of species present in the communities (Table 2). Distinct means were observed in autumn at the intertidal of Quiaios (lowest values observed), and in spring at the supralittoral of Cabedelo (highest values observed). Beach zones were also different during winter, with a higher species richness in the supralittoral. Crustaceans, such as Armadillidium album, Pontocrates arenarius and Gastrosaccus sanctus, and insects, such as Callicnemis latreillei and Aegiala arenaria, were only seasonally present in the beaches. The number of species was higher in spring and attained the lowest values during summer (Fig. 4b). ShannoneWiener H’ values also reached the lowest values during summer in both beaches, but the highest values were attained during autumn at Cabedelo and spring at Quiaios (Fig. 4a). However, H’ values did not present significant differences when the Two-Way ANOVA was performed (p > 0.05).

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Total density (ind.m -2)

a

Cabedelo

600

Quiaios

500 400 300 200 100 0 J99 F

M

A

M

J

J

A

S

O

N

D J00 F

M

A

M

J

b

Density (ind.m -2)

300

Talitrus saltator

Talorchestia brito

Tylos europaeus

200

100

0 J99

F

M

c

A

M

J

J

A

S

Talitrus saltator

500

O

N

D J00

F

M

A

Talorchestia brito

M

J

Tylos europaeus

Density (ind.m -2)

400

300

200

100

0 J99

F

Winter

M

A

M

Spring

J

J

A

S

Summer

O

N

Autumn

D

J00

F

Winter

M

A

M

J

Spring

Fig. 2. Variation of community density in the western coast of Portugal. (a) Variation of total density in each community during the study period; (b) Variation of population density in the dominant species at Cabedelo during the study period; (c) Variation of population density in the dominant species at Quiaios during the study period.

S.C. Gonçalves, J.C. Marques / Estuarine, Coastal and Shelf Science 95 (2011) 165e177

a

Scavengers

Herbivores

Predators

Filter feeders

171

Omnivores

100

Density (%)

80

60

40

20

0 J99

F

b

M

A

M

Scavengers

J

J

A

S

Herbivores

O

N

Predators

D

J00

F

M

Filter feeders

A

M

J

Omnivores

100

Density (%)

80

60

40

20

0 J99

F

M

A

M

J

J

A

S

O

N

D

J00

F

M

A

M

J

c Cabedelo

Quiaios

Temperature (ºC)

25

Precipitation (mm)

20 30

15 20 10

10 5

0

Other environmental parameters

Wrack subsidies (g.m-2)

40

0 J99

F

Winter

M

A

M

Spring

J

J

A

Summer

S

O

N

Autumn

D

J00

F

Winter

M

A

M

J

Spring

Fig. 3. Relative contribution of the functional groups in two sandy beach communities at the western coast of Portugal and relevant environmental parameters during the study period. (a) e Cabedelo community; (b) e Quiaios community; (c) e Variation of the most relevant environmental parameters.

At both beaches, the density of scavengers showed a seasonal pattern of variation (Fig. 4c), with the highest values in late spring and on summer months, and the lowest during the colder months. Scavenger densities were relatively similar between both beach communities, but an extremely high peak was attained at Quiaios in July (483 ind.m2 cf. 83 ind.m2 at Cabedelo), due to a very high abundance of Tylos europaeus (Fig. 2c). Two-Way Nested ANOVA

showed that season and beach zones influenced the density of resident scavengers and that in summer the densities were significantly higher at the intertidal zone of Cabedelo in comparison with the supralittoral levels of both beaches (Tables 2 and 3). Herbivores densities differed significantly between beaches and between beach zones (Table 2). Higher abundances were attained at Quiaios, especially at the intertidal (Fig. 4d and Table 3). The

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Table 3 Trophic structure of the resident communities at the beach zones and functional relevance of Talitrids and Tylids e comparative analysis. Seasonal values are given only for the trophic groups significantly influenced by seasons. Average data  standard deviations are given where appropriate; n.r. e not resident.

Scavengers Spring Summer Autumn Winter Herbivores Predators Spring Summer Autumn Winter Filter feeders Omnivores Total number of species Mean number of species Number of resident species Diversity, H’ Minimum density Maximum density

Cabedelo

Quiaios

Average density (ind.m2)

Average density (ind.m2)

Supralittoral

Intertidal

Supralittoral

Intertidal

75.5 (57.1) 66.3 (44.3) 41.1 (52.7) 96.8 (80.8) 90.9 (59.0) 3.2 (5.6) 0.05 (0.1) 0.0 (0.0) 0.0 (0.0) 0.2 (0.2) 0.08 (0.09) n.r. n.r. 44 7.6 (4.2) 13 1.24 (0.49) Spring (May) Summer (September)

84.4 (93.5) 117.6 (108.1) 149.0 (69.5) 21.7 (19.3) 8.5 (6.0) 5.9 (5.6) 0.5 (0.8) 0.3 (0.4) 0.08 (0.15) 1.3 (1.2) 0.04 (0.09) 2.7 (9.9) n.r. 90 6.5 (12.7) 6 1.17 (0.58) Winter (December) Spring (May)

39.0 (46.2) 27.2 (27.6) 7.9 (6.1) 53.7 (38.2) 62.5 (66.5) 1.5 (2.3) 0.05 (0.1) 0.03 (0.07) 0.0 (0.0) 0.0 (0.0) 0.1 (0.2) n.r. n.r. 40 6.0 (4.4) 12 0.87 (0.53) Summer (July) Winter (February)

54.2 (85.5) 54.9 (23.4) 154.2 (176.4) 21. (19.5) 13.3 (12.1) 12.8 (10.8) n.r. e e e e n.r. n.r. 77 5.3 (7.9) 3 0.96 (0.55) Winter (January) Summer (July)

Secondary production and standing stock estimates of the key species P g.m2.yr1

E g.m2.yr1

B g.m2

P/B

E/B

Average contribution to the community

0.74 e

1.40 e

0.13 e

5.70 e

10.80 e

69.5% 6.2%

Talitrus saltator Cabedelo Quiaios Talorchestia brito Cabedelo Quiaios Tylos europaeus Cabedelo þ Quiaios Cabedelo Quiaios

e 0.19

e 0.35

e 0.03

e 5.90

e 10.90

7.7% 24.5%

0.08 e e

e e e

0.05 e e

1.58 e e

e e e

e 15.2% 66.0%

Cabedelo Quiaios

0.75 0.24

e e

0.14 0.06

e e

e e

92.4% 96.7%

density of the resident predators was significantly influenced by the interaction between seasons and beaches, as well as by the interaction of seasons and beach zones (Table 2). In autumn, densities on the Cabedelo beach were clearly higher and the intertidal zone exhibited higher densities compared to the supralittoral areas of both beaches (Tables 2 and 3). The interaction between season and beach had a significant effect on the species richness of resident scavengers, herbivores and predators (Table 2). In spring the number of resident scavenger species was higher at Cabedelo, while during winter the number of resident herbivore and predator species was higher at Quiaios (Fig. 4e and f).

3.3. Secondary production and standing stocks of key species populations Talitrus saltator was the most productive population, presenting at Cabedelo the highest standing stock of both beaches (Table 3). Throughout the study, Talorchestia brito was the most important secondary producer at Quiaios, exhibiting nevertheless a standing stock similar to Tylos europaeus. Talitrids showed much higher population turnovers than the tylids. Resident key species populations at Cabedelo beach presented approximately 3 times more production and twice the standing stock compared to Quiaios (Table 3).

3.4. Influence of the environmental variables on community function descriptors Stepwise regression techniques showed that temperature and wrack quantity were the most influential environmental variables on the faunal communities (Table 4). Similar regression models were obtained for the species richness of resident scavengers and herbivores and wrack quantity at both beaches. However, filter feeders presented a different relationship with temperature, despite quadratic models being adjusted for both beaches. At Cabedelo, the number of filter feeder species decreased with increasing temperature, while the opposite was observed at Quiaios. At Cabedelo, total faunal density and scavenger density (in the beach or in a specific beach zone) were positively correlated to both wrack quantity and temperature. Similar relations were not observed at Quiaios, except for the density of scavengers and wrack quantity in the supralittoral (Table 4).The species richness of resident scavengers at Cabedelo was also correlated with temperature and visibility. At Quiaios, positive correlations were obtained for the density of resident herbivores and temperature, and the number of omnivore species and the organic matter content of the sand (Table 4). Stepwise regressions also showed that (i) the densities of talitrids and tylids (DTs; DTb; DTe) were positively correlated with temperature (T); (ii) the density of Talitrus saltator was positively

S.C. Gonçalves, J.C. Marques / Estuarine, Coastal and Shelf Science 95 (2011) 165e177

a

173

b Shannon-Wiener's index

3,0

Quiaios

80

Cabedelo

Number of species

2,0 1,5 1,0 0,5

Cabedelo

60 50 40 30 20 10 0

0,0 J99

A

J

O

J00

J99

A

c

A

J

O

J00

A

d Scavengers Cabedelo

500

Scavengers Quiaios

50

Density (ind.m -2)

300 200

30 20

0

0 J99 F M A M 12 Number of resident species

Herbivores Quiaios

10

100

e

Herbivores Cabedelo

40

400 Density (ind.m-2)

Quiaios

70

2,5

J

J A

S O N D J00 F M A

Scavengers Cabedelo

M J

J99 F M A M

f

Scavengers Quiaios

12

10

10

8

8

6

6

4

4

2

2

J

J

A

S O N D J00 F M A

Herbivores Cabedelo

M J

Herbivores Quiaios

0

0 J99 F M A Winter

M Spring

J

J

A

S O

Summer

N D J00 F M A

Autumn

Winter

M

Spring

J

J99 F M A M J Winter

Spring

J A

S O N D J00 F M A M J

Summer

Autumn

Winter

Spring

Fig. 4. Diversity trends and density of selected functional groups in two sandy beach communities at the western coast of Portugal. (a) Variation of Shannon-Wienner’s index in each community; (b) Variation of the number of species in each community; (c and d) Variation of the number of resident scavenger and herbivore species, respectively, at both communities; (e and f) Variation of the total density of the resident scavenger and herbivore species, respectively, in both communities.

correlated with the wrack quantity (Wra) at Cabedelo; (iii) the density of Talitrus europaeus was positively correlated with the wrack quantity at the supralittoral of Quiaios, according to the following regression models: (1) Ln DTs ¼ 0.847 (Ln T) 1.517 (r2 ¼ 0.66; p ¼ 0.000) at Cabedelo; Ln DTb ¼ 0.056 (Ln T) 1.750 (r2 ¼ 0.56; p ¼ 0.000) at Quiaios; Ln DTe ¼ 0.031 (Ln T) 2.133 (r2 ¼ 0.66; p ¼ 0.000) at Cabedelo; (2) Ln DTs ¼ 73.071 (0.963) Wra (r2 ¼ 0.51; p ¼ 0.004) at Cabedelo; (3) DTe ¼ 0.495Wra2 þ 12.607Wra þ 1.972 (r2 ¼ 0.50; p ¼ 0.014) at Quiaios. Forward selection procedures applied to Redundancy Analysis showed that temperature and wrack quantity influenced significantly the variance in the resident functional groups, but differences between the beaches were observed (Fig. 5). At Cabedelo, temperature was significantly selected (p ¼ 0.001) as the only explanatory variable and therefore only the first axis is constrained to this variable. The first two axes account for 81% of the cumulative variance in the faunal data, and the final RDA model obtained was significant (p ¼ 0.002, F-ratio: 14.03, after 999 permutations). Filter feeders presented a negative relation with temperature, increasing from left to right along the first axis. However, the second axis

showed a higher influence on faunal data than temperature (Fig. 5a). In the ordination diagram all the trophic groups, except filter feeders, appear related with the second axis, scavengers presenting the highest fit. A second trial using all the remainder environmental variables and excluding temperature did not reveal any significant results (p > 0.05). Temperature (p ¼ 0.03) and wrack quantity (p ¼ 0.02) were significantly selected as explanatory variables for the functional groups at Quiaios, but the first two axes of the final RDA account only for 26% of the cumulative variance in the trophic data (p ¼ 0.004, F-ratio: 5.59 - test of significance of all canonical axes, after 999 permutations). Herbivores were positively related with temperature and are clustered opposite to wrack quantity (Fig. 5b). Scavengers were negatively related with the first ordination axis, increasing from right to left. The wrack quantity was related with the second ordination axis and explained only 2% of the model variance. 4. Discussion The talitrids Talitrus saltator and Talorchestia brito and the tylid Tylos europaeus had distinct contributions to the community structure of the two beaches. According to Gonçalves et al. (2009),

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Table 4 Regression models obtained between the biological data and environmental parameters using stepwise regression techniques. In all potential regressions the variables are log transformed. Biological response Cabedelo (C) and Quiaios (Q) Number of filter feeder species in the community (NSpFilt_Com) Number of resident scavenger species (NSpScv) Number of resident herbivore species (NSpHerb) Number of resident scavenger species at the supralittoral (NSpScv_Sup) Cabedelo Total density (TDen) Density of resident filter feeders (Den Filt) Density of resident scavengers (Den Scv) Number of resident scavenger species (NSpScv) Number of resident scavenger species (NSpScv) Density of resident scavengers at the intertidal (Den Scv_Int) Quiaios Density of resident herbivores (Den Herb) Number of omnivore species in the community (NSp Omn_Com) Density of resident scavengers at the supralittoral (DenScv_Sup) Number of resident herbivore species at the supralittoral(NSpHerb_Sup)

Environmental predictor

Regression model (quadratic, potential, linear or cubic)

r2

p

Temperature (T)

Wrack quantity at the supralittoral (WraSup)

C: NSpFilt_Com ¼ 0.005T2  0.223T þ 2.914 Q: NSpFilt_Com ¼ 0.007T2  0.158T þ 0.877 C: NSpScv ¼ 4.115 Wra0.176 Q: NSpScv ¼ 0.032 Wra2 þ 0.575 Wra þ 3.462 C: NSpHerb ¼ 1.286 Wra0.201 Q: NSpHerb ¼ 0.011 Wra2 þ 0.614 Wra þ 1.008 C: NSpScv_Sup ¼ 0.002 WraSup2 þ 0.184WraSup þ 3.440 Q: NSpScv_Sup ¼ 0.555 WraSup2 þ 14.045 WraSup þ 2.898

0.54 0.58 0.65 0.62 0.54 0.67 0.51 0.52

0.009 0.002 0.000 0.000 0.002 0.000 0.024 0.008

Wrack quantity (Wra) Temperature (T) Cloudiness (Cloud)

TDen ¼ 342 þ 99.3 Ln (1 þ Wra) TDen ¼ 2.701T1.264 Den Filt ¼ 1.141 Cloud2 e10.964 Cloud þ 24.912

0.89 0.62 0.60

0.000 0.000 0.003

Temperature (T)

Den Scv ¼ 1.724T1.392

0.66

0.000

Temperature (T)

NSpScv ¼ 0.065T2 þ 1.857T  6.167

0.62

0.002

Visibility (Vis)

NSpScv ¼ 3.644Vis2 e 41.237 Vis þ 120.917

0.70

0.000

Wrack quantity (Wra) Wrack quantity (Wra)

3

2

Wrack quantity at the intertidal (WraInt)

DenScv_Int ¼ 1.517 WraInt  10.218 WraInt þ 38.95 WraInt þ 51.317

0.57

0.014

Temperature (T)

Den Herb ¼ 0.137T1.462

0.52

0.001

Organic matter content (OM) Wrack quantity at the supralittoral (WraSup) Wrack quantity at the supralittoral (WraSup)

NSp Omn_Com ¼ 0.243OM2 0.087OM þ 0.036

0.70

0.000

DenScv_Sup ¼ 0.137 WraSup þ 3.045 WraSup  4.138 WraSup þ 16.922

0.58

0.007

NSpHerb_Sup ¼ 0.024 WraSup2 þ 0.580 WraSup þ 0.247

0.59

0.002

3

combined differences in habitat preferences and feeding habits of each species, and the local conditions observed at the beaches, explain these results. However, there is a considerable niche overlap between T. europaeus and T. saltator, especially at Cabedelo, and competition for food and space must also be considered. Some of the differences in species composition might be explained by distinct local environmental conditions. Our results show that species richness of scavengers increases with wrack quantity, possibly explaining the exclusive occurrence of the scavenger coleopterans Callicnemis latreillei, Aegiala arenaria and Saprinus sp. at Cabedelo. However, a direct relationship with species density was not proven for these animals (p > 0.05). Also, the presence of the benthoplanktonic mysid Gastrosaccus sanctus at Cabedelo (lower intertidal area), is most probably caused by the presence of an adequate surf-zone area, essential for this species, and absent at Quiaios. The presence of Cochlicella barbara and Gonioctena olivacea at Quiaios, is most probably related to a higher environmental stability and a higher development of the supralittoral zone and of the adjacent dune system, leading to colonization by terrestrial forms. These habitats are favoured by Cochlicella barbara and might be temporarily used by Gonioctena olivacea while dispersing between patchy habitats of their host plants since, according to Biedermann (2005), there seem to be no critical barriers to the dispersal of this beetle. According to McLachlan and Brown (2006), supralittoral scavengers may dominate the trophic structure of impoverished communities in sandy beaches with harsh physical conditions. Therefore, a strong and stable dominance of scavengers over the other trophic groups was expected. All the most abundant species e Talitrus saltator, Talorchestiabrito and Tylos europaeus e have scavenger feeding habits, although T. brito is preferentially a herbivore, feeding on the interstitial flora of the sediment (Lagardère, 1966). If

2

one considers only the resident species of each community, 75% and 79% of the fauna (at Cabedelo and Quiaios respectively) depend on the debris transported to the beach, although some of them also present other feeding habits, predominantly herbivory. The importance of scavengers in processing wrack subsidies on sandy beaches is widely recognised (e.g. Inglis, 1989; Colombini et al., 2000; Lastra et al., 2008). Through their activity these animals fragment the debris, accelerate decomposition by spreading bacteria and enhance the availability of the material to decomposition with their burrowing activities (as reviewed in Colombini and Chelazzi, 2003). Using trophic groups to characterise the role of macrofauna in marine communities may be advantageous as it allows the incorporation of community structure estimates and allows the assessment of community functioning (Gaston et al., 1995). Considering the methodology used in the present work, trophic groups represent functions of the communities, hence the value of functional groups. In this sense, the functional role of scavengers in sandy beach ecosystems can be better termed as energy accelerators. However, besides functioning as food, wrack also has another important role for scavengers and other wrack-associated species of other trophic groups: provision of habitat e refuge, favourable microclimatic conditions and availability of prey (see for instance Jaramillo et al., 2006; Ince et al., 2007; Colombini et al., 2009). On sandy beaches, herbivores possibly rely on the interstitial flora, as well as on the vegetation forms that colonize embryo and primary dunes, as food resources. In both cases, Quiaios offers better ecological conditions for the development of this type of flora. This beach is wider, presents extended intertidal and supralittoral zones, has a coarse grain size that probably favours the development of interstitial primary producers, and has a more developed and stable dune system. Talorchestia brito was the most

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175

Fig. 5. RDA ordination diagrams of macrofaunal communities data and environmental parameters at Cabedelo and Quiaios sandy beaches (western coast of Portugal). (a) e RDA ordination diagram of the resident functional groups and environmental parameters at Cabedelo beach; (b) e RDA ordination diagram of the resident functional groups and environmental parameters at Quiaios beach.

abundant herbivore in the communities but this species can also feed on wrack as an alternative food resource. Like other tylids, Tylos europaeus is known to feed on stranded wrack (Kensley, 1974) and so it was considered as being an exclusive scavenger in the present study. In fact, the density of T. europaeus was positively correlated with the wrack quantity in the supralittoral of Quiaios. Nevertheless, if the hypothesis advanced by Gonçalves et al. (2009) concerning the use of living plants as an alternative food resource by this tylid is accepted, the importance of herbivores at Quiaios may be much higher (approximately 6 times more important) at Quiaios than at Cabedelo, and almost equivalent to the relative importance of scavengers. Further studies on the feeding diet of T. europaeus along the western coast of Portugal would be valuable to clarify this hypothesis. This could be complemented with an analysis of the feeding habits of T. brito, in order to provide a better understanding of the functional role of these two key species on a beach ecosystem energy balance. Seasons and beach zones had important effects on the community composition and function. Several residents were only seasonally present on the beaches. Terrestrial insects such as Callicnemis latreillei and Aegiala arenaria disappeared from the beach during summer and winter, possibly as a way to avoid extreme environmental conditions (viz. extreme temperatures and severe storms). Some marine crustaceans (e.g. Gastrosaccus sanctus) did not use the beach during winter, possibly avoiding severe dragging by winter storms and keeping the animals in a safe environment. Nevertheless, the beach zone e intertidal versus supralittoral e was also very important, interacting with seasons to promote differences on the number of species and on the spatial distribution of the macrofauna in the beach, namely with regard to abundant species like Talitrus saltator and Tylos europaeus (see also Gonçalves et al., 2009 for more details). Environmental conditions on beach zones exhibit clear seasonal variations, namely on sand temperature and water content. Such changes promote differences on the use of the beach zones, namely by the resident fauna, as a function of the seasonal habitat suitability. This allows macrofauna to avoid important problems such as desiccative and thermic stress or even dragging by waves during a sudden inundation caused by winter storms.

The ANOVA results indicate season had a consistent effect on the density of scavengers and predators, interacting with distinct factors for each group, but only beach and beach zone had an effect on herbivores. The prevalence of these effects on the density of herbivores is believed to result from the strong contribution of Talorchestia brito to this functional group and of its habitat preferences (intertidal zone). However, at Quiaios, temperature was proven to have: (i) a positive influence on herbivores by multivariate methods and (ii) a positive correlation with the density of T. brito, reinforcing the multivariate results previously obtained by Gonçalves et al. (2009). Differences regarding beaches vertical extension combined with seasonal oscillations in wrack subsidy frequency are reflected on the species richness of scavengers, herbivores and predators. Also species richness of scavengers and herbivores was positively correlated with wrack quantity. Therefore, our results demonstrate that seasons play a very important role on the organization of sandy beach communities, driving changes on environmental conditions of beach zones. This leads to distinct macrofaunal strategic adaptive responses to the dynamics and variability of beach environments, constraining community function and composition. Talitrus saltator was by far the most important secondary producer, at Cabedelo beach, exhibiting growth production values comparable to those estimated for a Tunisian population by Marques et al. (2003), using the same methodology. The talitrid Talorchestia brito had a similar P=B ratio to T. saltator, although the secondary production and the standing stock were approximately 4 times smaller. Since the two species have similar reproductive outputs (Marques et al., 2003; Gonçalves et al., 2003), such disparity appears to be primarily associated with the difference in their average population densities (4 times smaller for T. brito). The two species have different trophic needs and feeding habits, the two beaches offer distinct food resources and, at Cabedelo, there was a positive correlation between the density of T. saltator and wrack quantity. The highest population turnover exhibited by talitrids as compared to tylids are not unusual. The two talitrid species are characterized by rapid life histories with fast growing rates, short

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longevity and semiannual and bivoltine life cycles (Marques et al., 2003; Gonçalves et al., 2003). This contrasts with the typical bioecology of tylids. Tylos europaeus presents a slower life-history, with slower growing rates, longer longevity and a univoltine life cycle (Gonçalves et al., 2005). Naturally, this is reflected in the species population turnover and secondary production, and consequently in its smaller contribution to the communities annual energy flow. The standing stocks of Talorchestia brito and T. europaeus at Quiaios were nevertheless very similar, as a function of the comparatively higher population density of T. europaeus, which was the dominant species on this beach. Due to its location, a regular and abundant supply of wrack, mainly of marine origin, was observed at Cabedelo during the study period. This constituted the primary and most important food resource to the macrofauna, namely for Talitrus saltator, the most important consumer. At Quiaios, the scenario was very different because there are no relevant sources of marine debris nearby. The inputs were limited and scarce and the community structure was dominated by Tylos europaeus, also a scavenger. Despite local differences, the macrofaunal community performs an important role on the processing of the allochthonous debris and on the energy flow of the food webs of sandy beach ecosystems. According to Lastra et al. (2008), talitrid populations can have a significant impact on the processing and fate of stranded macrophytes, while the quantity and composition of this material can limit populations of beach consumers. Our results also point in this direction (e.g. low densities of T. saltator observed at Quiaios versus high densities observed at Cabedelo), and we believe that the influence of wrack quantity and composition might be extended to other scavenger species and even to other functional groups, namely herbivores and predators (see the following discussion). At present and because of its location, Cabedelo beach may be affected by regular and more intense human disturbances, especially those related with recreational activities. This includes for instance human and possibly mechanical trampling (off-road vehicles) and beach grooming. These type of activities may increase macrofaunal natural mortality rates, as demonstrated in previous studies (e.g. Llewellyn and Shackley, 1996; Weslawski et al., 2000; Veloso et al., 2006). Community descriptors were positively, and sometimes strongly, dependent on wrack quantity, namely the species richness of scavengers and herbivores (both beaches) and community density at Cabedelo. Therefore, we believe that if human disturbances, for instance beach grooming with heavy machinery on a regular basis, continues to increase on sandy beaches worldwide, macrofaunal communities may be seriously disturbed. This will be reflected in ecosystem processes, structure and function, jeopardizing the beach natural ecological condition. With regard to our study, the Cabedelo community is at a much higher risk because, besides being subjected to stronger human disturbances, the beach is smaller than Quiaios, representing a narrow stretch of coast. Management options such as the interspreading of groomed and naturally ungroomed areas, as suggested by Dugan et al. (2003), would not be possible at Cabedelo, neither the establishment of undisturbed areas that could function as recolonization patches for the impacted areas of the beach. Therefore, a serious decline of the macrofauna is expected. Although herbivores are generally not wrack consumers, this functional group depends on the debris cast ashore for the provision of shelter and habitat (e.g. Colombini and Chelazzi, 2003; Ince et al., 2007). This explains why the species richness of this group was positively influenced by wrack quantity at both beaches. The number of omnivore species in the community of Quiaios was positively influenced by the organic matter content in the sand, suggesting that this group may also depend directly from this food resource in terms of diet. On an exposed Italian beach, Colombini

et al. (2009) found that the seston of the water column may be the main source of organic matter for sandy beaches with low macroalgae inputs, and seems to be retained by the sand acting as a possible particle filter. These findings may as well be true for Quiaios and help to enrich the number of omnivorous species present on the beach in periods during an accumulation of organic matter in the sand. Multiple regressions and multivariate techniques were consistent regarding the influence of temperature on the studied communities, again reinforcing the relevance of seasons on shaping the community function in sandy beaches (e.g. density of scavengers, herbivores and key species, as well as community density at Cabedelo). The reversed relationship observed between the number of filter feeder species at Cabedelo and Quiaios is explained by the differences in the species composition of this functional group. For instance, Gonçalves et al. (2009) using multivariate techniques showed that, at Cabedelo, Gastrosaccus sanctus, the most important filter feeder in this community, responded negatively to temperature. This relationship is also reinforced by the present results of the RDA analysis, since filter feeders were the only functional group related with temperature at this beach. At Cabedelo, a hypothetical environmental variable or a combination of several variables, to which scavengers presented the best fit, had an influence higher than temperature on the functional groups. The combined effect of wrack quantity and wrack freshness might be a plausible explanation for these results. Several authors have demonstrated that wrack-associated macrofauna colonize the debris in a succession according to their metabolic and trophic needs (reviewed by Colombini and Chelazzi, 2003). Scavengers such as amphipods and isopods are recognised as early invaders, and herbivorous and carnivorous coleopterans are late invaders, colonizing the debris while it dries out. Since wrack quantity was not selected at Cabedelo as a significant explanatory variable and since it was quantified only in the dry weight form, we believe that freshness and ageing of the debris might be an important explanatory variable and should be measured in the future. However, beach morphodynamic indices are presently recognised as important physical predictors of macrofaunal responses (e.g. Schlacher et al., 2008) and might as well be the missing variable(s).

5. Conclusions This study demonstrates that season, both as an isolated factor and when combined with beach zones, has a clear influence on the trophic structure of macrofaunal communities, promoting changes on beach environments that induce distinct responses with regard to species richness throughout the year, density and the composition of functional groups. The differences observed on the frequency and availability of wrack subsidies between the two sandy beaches had important effects on the organization and function of the communities, which were clearly dominated by scavengers. Abundant and regular supplies increase the number of wrack-associated species, namely scavengers and herbivores, through the provision not only of food but also of an adequate habitat for several species. Wrack subsidies also increase the density of scavengers on specific beach zones and the density of the most important secondary producer studied in these communities, Talitrus saltator. Talitrids and tylids represented the bulk of the secondary production and of the energy flow in these macrofaunal communities. In general, the clear dependence of macrofauna in exposed sandy beaches upon the wrack subsidies brought ashore by tides, highlighted in this study, reinforces the need to adopt worldwide coastal management options that allow the establishment of several undisturbed areas, in order to reduce the negative

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impacts of human disturbances on these sensitive ecosystems, namely in widely touristic exploited areas. Acknowledgements The present study was partially supported by funds provided be the research Projects WADI (INCO2003 e MPC2 e 015226) and RECONNECT (PTDC/MAR/64627/2006). The research complies with the current laws in the country where it was conducted. The authors are indebted with all the colleagues at IMAR-CMA who assisted in the field and laboratory work. References Allen, K.R., 1971. Relation between production and biomass. Journal of the Fisheries Research Board of Canada 28, 1573e1581. Benke, A.C., 1979. A modification of the hynes method for estimating secondary production with particular significance for multivoltine populations. Limnology and Oceanography 24, 168e171. Biedermann, R., 2005. Incidence and population dynamics of the leaf beetle Gonioctena olivacea in dynamic habitats. Ecography 28, 673e681. Colombini, I., Aloia, A., Fallaci, M., Pezzoli, G., Chelazzi, L., 2000. Temporal and spatial use of stranded wrack by the macrofauna of a tropical sandy beach. Marine Biology 136, 531e541. Colombini, I., Chelazzi, L., 2003. Influence of marine allochthonous input on sandy beach communities. Oceanography and Marine Biology: an Annual Review 41, 115e159. Colombini, I., Mateo, M.A., Serrano, O., Fallaci, M., Gagnarli, E., Serrano, L., Chelazzi, L., 2009. On the role of Posidonia oceanica wrack for macroinvertebrates of a Tyrrhenian sandy shore. Acta Oecologica 35, 32e44. Defeo, O., Jaramillo, E., Lyonnet, A., 1992. Community structure and intertidal zonation of the macrofauna on the Atlantic coast of Uruguay. Journal of Coastal Research 8, 830e839. Defeo, O., Rueda, M., 2002. Spatial structure, sampling design and abundance estimates in sandy beach macroinfauna: some warnings and new perspectives. Marine Biology 140, 1215e1225. Dugan, J.E., Hubbard, D.M., McCrary, M.D., Pierson, M.O., 2003. The response of macrofauna communities and shorebirds to macrophyte wrack subsidies on exposed sandy beaches of southern California. Estuarine, Coastal and Shelf Science 58S (Supplement A), 25e40. Gaston, G.R., Brown, S.S., Rakocinski, C.F., Heard, R.W., Summers, J.K., 1995. Trophic Structure of Macrobenthic Communities in Northern Gulf of Mexico Estuaries, Gulf Research Reports 9: pp. 111e116. Gonçalves, S.C., Marques, J.C., Pardal, M.A., Bouslama, M.F., El Gtari, M., CharfiCheikhrouha, F., 2003. Comparison of Talorchestia brito (amphipoda, talitridae) biology, dynamics, and secondary production in Atlantic (Portugal) and Mediterranean (Tunisia) populations. Estuarine, Coastal and Shelf Science 58, 901e916. Gonçalves, S.C., Pardal, M.A., Cardoso, P.G., Ferreira, S.M., Marques, J.C., 2005. Biology, population dynamics and secondary production of Tylos europaeus (Isopoda, Tylidae) on the western coast of Portugal. Marine Biology 147, 631e641.

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Gonçalves, S.C., Anastácio, P.M., Pardal, M.A., Cardoso, P.G., Ferreira, S.M., Marques, J.C., 2009. Sandy beach macrofaunal communities on the western coast of Portugal e is there a steady structure under similar exposed conditions? Estuarine, Coastal and Shelf Science 81, 555e568. Hubbard, D.M., Dugan, J.E., 2003. Shorebird use of an exposed sandy beach in southern California. Estuarine, Coastal and Shelf Science 58S (Supplement A), 41e54. Ince, R., Hyndes, G.A., Lavery, P.S., Vanderklift, M.A., 2007. Marine macrophytes directly enhance abundances of sandy beach fauna through provision of food and habitat. Estuarine, Coastal and Shelf Science 74, 77e86. Inglis, G., 1989. The colonisation and degradation of stranded Macrocystis pyrifera (L.) C. Ag. by the macrofauna of a New Zealand sandy beach. Journal of Experimental Marine Biology and Ecology 125, 203e217. Jaramillo, E., de la Huz, R., Duarte, C., Contreras, H., 2006. Algal wrack deposits and macroinfaunal arthropods on sandy beaches of the Chilean coast. Revista Chilena de Historia Natural 79 (3), 337e351. Kensley, B., 1974. Aspects of the biology and ecology of the genus Tylos Latreille. Annals of the South African Museum 65 (11), 401e471. Lagardère, J.P., 1966. Recherches sur la biologie et l’écologie de la macrofaune des substrats meubles de la côte des Landes et de la côte Basque. Bulletin du Centre d’Etudes et de Recherches Scientifiques Biarritz 6, 143e209. Lastra, M., Page, H.M., Dugan, J.E., Hubbard, D.M., Rodil, I.F., 2008. Processing of allochthonous macrophyte subsidies by sandy beach consumers: estimates of feeding rates and impacts on food resources. Marine Biology 154, 163e174. Llewellyn, P.J., Shackley, S.E., 1996. The effects of mechanical beach cleaning on invertebrate populations. British Wildlife 7 (3), 147e155. Marques, J.C., Gonçalves, S.C., Pardal, M.A., Chelazzi, L., Colombini, I., Fallaci, M., Bouslama, M.F., El Gtari, M., Charfi-Cheikhrouha, F., Scapini, F., 2003. Comparison of Talitrus saltator (Amphipoda, Talitridae) biology, dynamics, and secondary production in Atlantic (Portugal) and Mediterranean (Italy and Tunisia) populations. Estuarine, Coastal and Shelf Science 58S (Supplement A), 127e148. McLachlan, A., 1980. The definition of sandy beaches in relation to exposure: a simple rating system. South African Journal of Science 76, 137e138. McLachlan, A., 1990. Dissipative beaches and macrofauna communities on exposed intertidal sands. Journal of Coastal Research 6, 57e71. McLachlan, A., Brown, A.C., 2006. The Ecology of Sandy Shores, second ed. Elsevier, California, 373 pp. Rodil, I.F., Lastra, M., Sánchez-Mata, A.G., 2006. Community structure and intertidal zonation of the macroinfauna in intermediate sandy beaches in temperate latitudes: north coast of Spain. Estuarine, Coastal and Shelf Science 67, 267e279. Schlacher, T.A., Schoeman, D.S., Dugan, J., Lastra, M., Jones, A., Scapini, F., McLachlan, A., 2008. Sandy beach ecosystems: key features, sampling issues, management challenges and climate change impacts. Marine Ecology 29 (suppl. 1), 70e90.  ter Braak, C.J.F., Smilauer, P., 1998. CANOCO Reference Manual and User’s Guide to Canoco for Windows: Software for Canonical Community Ordination (Version 4). Microcomputer Power, Ithaca, NY, USA, 351 pp. Veloso, V.G., Silva, E.S., Caetano, C.H.S., Cardoso, R.S., 2006. Comparison between the macroinfauna of urbanized and protected beaches in Rio de Janeiro State, Brazil. Biological Conservation 127, 510e515. Weslawski, J.M., Stanek, A., Siewert, A., Beer, N., 2000. The sandhopper (Talitrus saltator, Montagu 1808) on the Polish Baltic coast. Is it a victim of increased tourism? Oceanological Studies XXIX (1), 77e87.