The benthic macrofauna in the Zostera marina seagrass bed and bare sand ... juvenile specimens (Mattila et al., 1999; Adams et al., 2004; Ribeiro et al., 2006).
Benthic ecology, diversity and community structure of Zostera marina seagrass beds and adjacent sand habitats of Arcachon Bay lagoon in the Southwest of France Anthony Nzioka, Lingdi Tan, Doan Que and Dhiman Gain
Abstract The benthic macrofauna in the Zostera marina seagrass bed and bare sand bottom in Arcachon Bay, France is studied during the field trip. In total 5 sites were sampled, each including both seagrass bed and bare sand, with geographical position varying from the mouth of the lagoon to the inner bay. Species accumulation curve indicates that seagrass bed possesses a higher biodiversity and biomass compared to those of the bare sand bottom. Hierarchical Cluster Analysis identified two groups within all the sample points, corresponding to seagrass and bare sand, and each was further divided into three groups with respect to geographical position. Principal Component Analysis showed that the presence of seagrass is the major factor influencing the benthic macrofauna while the geographical position is the minor factor. Several adaptations of species to different habitats are discussed in this study. Keywords: benthic macrofauna, seagrass, Arcachon Bay
1. Introduction Seagrass habitats have long been described as an important nursery habitat for different benthic species (Tolan et al., 1997; Blanchet et al., 2004) mainly thanks to their higher biological structural complexity (Ribeiro et al., 2006). This complex structure plays many essential roles in constructing and maintaining a habitat. First, they can enhance the survival ability of organisms by reducing predation risk (Joseph et al., 2006), providing protection, shelter, food and refuge for juvenile specimens (Mattila et al., 1999; Adams et al., 2004; Ribeiro et al., 2006). For example, seagrass beds have also been described as crucial sources of nutrients that maintain a high degree of secondary productivity in the coastal areas where they are found (Dolbeth et al., 2003; Alfaro, 2006). Additionally, by the mean of epiphytes attached to seagrass leaves, sea grass species can make important contributions to the total primary production and increase prey abundance as well as spatial complexity (Bologna and Heck, 1999). In fact, it is beneficial for fish and other epifauna to stay in the intertidal area as long as possible because marshes function as foraging grounds (Cattrijsse et al., 1994). The different combination of intertidal habitats can offer diverse benefits to species. For example, heterogeneous seagrass beds provide more favorable foraging areas for some species, which can forage over the unvegetated areas, while they also remain in close proximity to their protective vegetated habitat (Orth et al., 1984). Successful propagation of these species is a match between environmental variations, such as seasonal changes inwater level (Rozas and Reed, 1993) or vegetated habitat (Rozas and Minello, 1998) and the ecological conditions for larval survival and recruitment, such as predator impact, food availability or currents (Sprung, 2001).
Biological communities in the coastal lagoon have always been of great interest (e.g. Sprung, 1994, 2001; Malaquias and Sprung, 2005; Ribeiro et al., 2006), among which the benthic macrofauna in the Archachon Bay has been well studied. Blanchet et al. (2004) who studied macrozoobenthic communities in Zostera notii bed and subtidal zones (including Zostera marina bed and bare sand area), suggested that sediment properties and distance to the ocean (overlying water mass) play as major structuring factors while the water depth is a minor factor (Blanchet et al., 2004, 2005). The presence of seagrass itself has an impact on zoobenthic community, although it is difficult to conclude whether seagrass extension can increase the ecosystem quality (Tu Do et al., 2011). Benthic communities in Arcachon Bay have been undergoing continuous changes, which are thought to be subjected to physical perturbation (Lavesque et al., 2009) and seagrass bed’s decline (Martin et al., 2010). According to the observation made in 2008, about 45.7 km2 of the tidal flat is covered by Zostera noltii, while Zostera marina occupies 1.0 km2 (Martin, P. et al., 2010). Furthermore, 42% of the high marsh surface is occupied by the invasive Spartina anglica (Cottet et al., 2007). Thus, long-term observation of the benthic macrofauna in Arcachon Bay and its structure should be taken into consideration. The study thus aims to understand the role played by seagrass in structuring benthic communities by assess the diversity of macrofauna in the Arcachon lagoon. 2. Materials and Methods 2.1 Study area The study was carried out in the Arcachon lagoon, a 180 km2 mesotidal shallow lagoon located on the French Atlantic coast (44º40´ N, 1º10´ W; Figure 1). This lagoon is connected to the Atlantic Ocean by a channel (2-3 km wide and 12 km length) that enables significant water exchanges, estimated at 384 x106 m3 for spring tide cycles (Plus et al., 2006). The amplitude of the semi-diurnal tide ranges from 1.1 to 4.9 m, with the large tidal mudflats (115 km2) being drained by the shallow tidal creeks in the inner lagoon (156 km2) during low tide. During high tide, surface water temperature and salinity fluctuations of 1 – 30ºC and 22 – 32 respectively, occur annually. The lagoons’ main portion of the intertidal zone consists of muddy sediments (grain size: 15-40 µm) and permeable sandy sediments (grain size: ~250 µm) in the upper portions, which can outcrop in the bed of the largest channels. The back of the lagoon is affected by moderate river inputs and underground freshwater discharges (1,044 x106 m3 yr-1; Auby and Labourg, 1996; Rimmelin et al., 1998), with a major proportion coming from the Leyre River (> 80%), the remaining is provided by the secondary channels and streams (Rimmelin et al., 1998). At low tide, these freshwater inputs constitute small-scale estuaries with a salinity gradient from 0 to 15-27, depending on the season (Deborde et al., 2008a). The study sites were selected in areas of Zostera marina occurrence. These were Belisaire at the mouth of the lagoon and closer to the open ocean, the west and east parts of the Channel Island in the inner part of the lagoon, and in between the mouth of the lagoon and Channel Island near the channel Courbey.
Figure 1: Sampling points of Arcachon Bay lagoon: (1) Belisaire, (2) Courbey East, (3) Channel island West, (4) Channel Island East and (5) Courbey North East. 2.2 Sample collection Zostera marina seagrass beds were sampled using a 1 cm mesh size net to avoid destruction of the bed while bare sand area employed the use of a 1 m wide beam trawl of the same mesh size. Replicate trawling was done at a constant speed of 1 m.s-1 and a distance of 50 m for each habitat and collected macrofauna were characterized and identified to the lowest taxonomic level possible using various identification keys. Biomass information was also collected for each taxonomic group. 2.3 Data analysis An assumption was made that sampling effort for both habitats was the same. Multivariate approach to statistical analysis was performed using a combination of Primer 6 (Clarke and Gorley, 2006), Statistica 8.0, Paleontological Statistics (PAST) v2.13 and R-statistics softwares. Log-transformation was applied to macrofaunal abundance data, non-metric Multidimensional Scaling (MDS) plots used for ordination of the data and one-way Analysis of Variance (ANOVA) was used to statistically test differences in abundance, biomass and diversity between habitats. SIMPER was used to test for statistical differences between species in all the habitats. Whenever normality or homogeneity of variance failed, the data was log-transformed. Post hoc Tukey’s test was used to distinguish pairwise differences between habitats whenever significant differences were observed. A Bray-Curtis similarity index was used to perform hierarchical cluster analysis (HCA) and create clustering dendograms and Principal Component Analysis (PCA) used to visualize the data.
3. Results A total of 20 samples were taken in both seagrass beds and bare areas, accounting for a total of 1589 individuals belonging to 68 species from 14 classes. Within the Zostera marina beds, 1423 individuals accounting for 58 taxa were encountered compared to 166 individuals accounting for 21 taxa in bare ground areas. Total species, species richness, evenness, diversity, abundance and biomass were significantly different by habitat (p < 0.05). The greatest density of macrofauna for the total sampled area (500 m2) was found in seagrass habitats with 1423 individuals compared to bare sand habitat having 166 individuals for the same sampling effort. The relative abundance for seagrass habitats was 142.3 ± 16.3 Ind. 50 m-2 and bare sand habitats were 16.6 ± 4.3 Ind. 50 m-2 (Figure 3). Mean biomass followed the same pattern with highest values in seagrass (320.0 ± 77.4 g 50 m-2) and lowest in sand (102.9 ± 41.3 g 50 m-2; Figure 3).
Figure 3: Relative abundance (individuals per 50 m2) and biomass ± SE observed in both Zostera marina and bare sand habitats of Arcachon Bay, France.
Figure 4: Total count (individuals per 50 m2) and species richness observed in Zostera marina and bare sand habitats of Arcachon Bay, France.
Species richness, mean macrofaunal density and biomass were significantly different by habitat (p < 0.05) implying that at least one habitat (seagrass) has species richness, density and biomass that is statistically different from the other (bare sand). The sample distribution in the collectors curve shows that the curve is still rising with increasing sampling effort for both seagrass and bare sand habitats (Figure 5). Comparing the two habitats shows that seagrass habitats have a higher species counts than bare sand habitats.
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The distribution of samples in the MDS plot (Figure 6) is scattered but with no overlap. Community assemblages in the seagrass and bare sand are dispersed. On comparing the two habitats types, significant differences in community structure were observed (ANOSIM: R = 1, at 0.4% sample statistic significance level) with significant differences between all possible combinations of studied habitats. The SIMPER statistical test showed that there were significant differences between species in all habitats. Macrofaunal species from seagrass habitats had a group similarity average of 60.69% compared to 55.87% from bare sand habitat. However, the group average dissimilarity of seagrass and bare sand was 88.27%. Hierarchical Cluster Analysis (HCA) based on Bray-Curtis dissimilarity index further reveals similarities and differences between habitats and sites based on group average sorting. Macrofaunal assemblages were separated into 3 groups of sites in each habitat (seagrass and bare sand; Figure 7). In Z. marina beds, these groups were Belisaire (HG1A, HG1B), Courbey East (HG2A, HG2B) and Courbey North East (HG5A, HG5B) forming a second group while Channel Island West (HG3A, HG3B) and Channel Island East (HG4A, HG4B) formed the third group (Figure 6). Bare ground had Belisaire (BG1A, BG1B) as one group, Channel Island East (BG4A, BG4B) as the second group while, Courbey East (BG2A, BG2B), Channel Island West (BG3A, BG3B) and Courbey North East (BG5A, BG5B) formed the third group (Figure 7).
On the PCA, 53.5% of variations can be explained in the first (33.3%) and second (22.2%) axis (Figure 8). The first factoral axis is related to the habitat while the second factorial axis is related to geographical position of the sites.
Figure 6: Non-metric MDS plots of community assemblages for each site and habitat (stress value: 0.11) of Arcachon Bay, France HCA - complete linkage
HCA - group average
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Figure 7: Hierarchical Cluster Analysis (HCA) using the Bray-‐Curtis dissimilarity index (redline = 0.65).
Figure 8: Principal Component Analysis of seagrass and bare habitats on the first (geographical position) and second (habitat) principal components.
4. Discussion In general, it is clear that there are significant differences in community structure between the two habitats, Z. marina bed and bare sand. The data also expresses the spatial similarity and dissimilarity among the communities in the different sampling points. Within each “nature” group, station 1 is dissimilar from other stations (distance to the ocean or overlying water mass). Station 2, 5 and Station 3, 4 can roughly be grouped together (again consistent with their geographical positions, may be due to distance to the ocean), except for one sample of Station 3. Replicates are usually grouped together, again except for one sample of Station 3. These biological indexes present a noticeable higher value in seagass communities while the bare-sand ones express lower. For example, the macrofauna diversity in sea grass bed is almost ten times higher than that in bare sand habitats with 1423 individuals and 166 individuals, respectively. In both the relative abundance and mean biomass, it can be seen that sea grass communities show by far superior to bare sand ones. It has been reported that in another temperate coastal, Ria Formosa (Portugal), seagrass bed has the highest diversity, abundance and biomass among all types of habitats including sandy bottom (Almeida et al., 2008). In Arcachon Bay, it has also been reported that another seagrass species, Zostera noltii, has had an effect of increasing most of the characteristics (abundance and biomass) of macrofauna community (Tu Do, V. et al, 2011). There are several possible explanations for the high different community structure in sea grass in comparison with bare sand, but the most reasonable one is the well adaptation of species for their habitat so that they become a representative species for the kind of environment. As seen in the observation space (Figure 8a), the principle factors affecting species distribution are related to
habitat (component 2, seagrass vs sand) and geographical position (component 1, separating Sites 3, 4 and 1, 2, 5 for seagrass). For example, Mactra glauca is only found in bare sand habitat, consistent with its sandburrowing behavior (Born, 1778) while Diogenes pugilator prefers the poor fine sands of the inner shelf (Serrano et al., 2006), well explained by the observed negative correlation to the component 2 (figure 8). In sea grass, Macropodia rostrata and their relative, Pisa armata, are found frequently. They are well adapted to the environment by wearing a lot of algae on their shell to hide better in the seagrass bed. Gobius niger use seabed as feeding and breeding ground (Froese, et al ,2013), they are found both on sandy or muddy bottoms and among seagrasses and seaweeds, but in this study, they are positively correlated to the presence of seagrass. Hippolyte inermis are also highly representative for the seagrass environment. It was reported that their reproductive periods were synchronic with the seasonal growth of the seagrass (Zupo, 1994), which indicates that they are adapted to this habitat. With regards to the effect of water masses on the community structure (component 2), Diogenes pugilator and Ophiura ophiura show the tendency to appear more in the inner bay where deeper medium and fine sediments with intermediate levels of organic content present (Serrano et al., 2006). 5. Conclusion: In this study, the presence of seagrass appears to be the most important factor affecting the benthic macrofauna in Arcachon Bay, with geographical position (determining the overlying water mass) being a minor factor. Thanks to its structuring effect, biogeochemical processes and ecological function, seagrass bed supports a higher biodiversity and biomass than the bare sand, and is home to some unique species such as Hippolyte inermis. However, there are also species only found on the bare sand, such as Mactra glauca. A difference of macrofauna community related to the physicochemical gradient from the open ocean to the inner bay is also observed. Acknowledgement We gratefully acknowledge the captain and all the personnel of RV Planula for their assistance during the trip. We want to express our gratitude to our Professors, Dr. Montaudouin and Dr. Blanchet for their cordial guidance and support during the whole study. Finally we want to express our sincere gratitude to the staff of the Arcachon Marine Station.
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