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Ecology of twelve species of Thyasiridae (Mollusca: Bivalvia)
Marine Pollution Bulletin 62 (2011) 786–791
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Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Ecology of twelve species of Thyasiridae (Mollusca: Bivalvia) Keuning Rozemarijn a, Schander Christoffer a,b,c,⇑, Kongsrud Jon Anders d, Willassen Endre d a
University of Bergen, Department of Biology, 5020 Bergen, Norway Centre of GeoBiology, University of Bergen, 5020 Bergen, Norway c Uni Environment, 5020 Bergen, Norway d Bergen Museum, Natural History Collections, University of Bergen, 5020 Bergen, Norway b
a r t i c l e Keywords: Atlantic Ocean Sediment Oxygen Multivariate analysis Thyasira
i n f o
a b s t r a c t Benthic samples from coastal locations off Southwestern Norway were examined and the specimens of Thyasiridae were identified to species. A multivariate analysis based on 13 parameters was carried out and the environmental preferences of all thyasirid species present were determined. The potential of the Thyasiridae as indicators of organic enrichment was investigated by using direct canonical correspondence analyses to identify correlations between selected environmental parameters and the collected biological data. The presence of Thyasira sarsi together with a low biodiversity is a good indicator of organic enrichment. High thyasirid species diversity seems to indicate good environmental conditions, and single thyasirid species that lack symbiotic bacteria might also be useful as indicators of good environmental conditions. Ó 2011 Elsevier Ltd. All rights reserved.
1. Introduction The Thyasiridae is a family of bivalves with a fossil record going back to the Cretaceous period (McAlester, 1966). The family consists of 11 genera and around 90 described recent species with a worldwide distribution, living from shallow coastal waters to abyssal depths (Payne and Allen, 1991; Taylor et al., 2007). Thyasiridae occupy a variety of habitats with different sediment types, including cold seeps (Levin, 2005) and hydrothermal vents (Southward et al., 2001). They are often associated with organic enrichment (Dando et al., 2004) and some species can be found in high numbers beneath oil platforms where the sediment is polluted with oily drill cuttings (Oliver and Killeen, 2002). Several species live in symbiosis with sulphide oxidising bacteria (Dando and Spiro, 1993) and have gills that are modified to house bacteria. Some species possess a hyperextensible foot that can stretch up to 30 times the length of the shell (Dufour and Felbeck, 2003). With their extensive burrowing behaviour the Thyasiridae contribute to oxygenating the sediments in addition to ‘mining’ for sulphides (Dando et al., 1994; Dufour and Felbeck, 2003). This behaviour means that they are able to effectively exploit reducing and polluted sediments, and modify the sediments in such a way that the environment becomes more attractive to sulphide-intolerant benthos. Due to this behaviour some thyasirids are candidates for
environmental engineering in the literature (e.g. Dando et al., 2004). When sediment sulphide becomes depleted, the bacteria in the gills starve and the thyasirids disappear (Dando and Spiro, 1993). Thyasirids may therefore be suitable indicators of environmental pollution, and their ecology could aid in detecting environmental changes. Thyasirids collected from sediment samples taken at different locations in coastal waters off W. Norway (Table 1) were examined and identified. Environmental data were analysed in order to investigate the ecological preferences of the species, including their potential as indicators of organic enrichment. 2. Material and methods Material from environmental studies carried out by the Section for Applied Environmental Research, University in Bergen (‘SAM-marin’) was used for this study. Sediment samples were already analysed and environmental parameters reported (Botnen et al., 2000, 2002; Heggøy et al., 2004a,b, 2005a,b,c, 2007; Hjohlman et al., 2000; Johannessen et al., 1991; Johansen et al., 2000, 2001a,b, 2002a,b, 2003a,b,c, 2004a,b, 2006; Vassenden and Johannessen, 2002, 2005; Vassenden et al., 2005a,b, 2006). The material represents Hordaland and a small area in Møre og Romsdal. 2.1. Sampling procedure and environmental parameters
⇑ Corresponding author. Present address: 101 Life Sciences Building, Department of Biological Sciences, Auburn University, Auburn, AL 36849, USA. Tel.: +1 334 884 1636. E-mail address: [email protected] (C. Schander). 0025-326X/$ - see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.marpolbul.2011.01.004
2.1.1. Sediment Sediment samples were collected using a 0.1 m2 van Veen grab with the exception of two stations sampled in 1990 (St18 and St23)
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R. Keuning et al. / Marine Pollution Bulletin 62 (2011) 786–791 Table 1 Ranges of the environmental parameters for each species found in this study. Species
No. of specimens
Depth (m)
Salinity (‰)
Oxygen content (ml/l)
Organic content (% wl)
Grain size (% clay + silt)
Thyasira sarsi Thyasira flexuosa Thyasira polygona Thyasira granulosa Thyasira equalis Thyasira obsoleta Axinulus croulinensis Thyasira succisa Axinulus eumyarius Mendicula ferruginosa Adontorhina similis Thyasira gouldi
3148 5497 12 22 1337 156 72 2 343 734 115 3
24–545 9–130 41–83 535–585 27–675 40–675 40–224 225–330 330–675 40–675 71–585 29
23.73–35.00 23.73–35.00 33.52–34.36 34.91–35.13 30.78–35.53 32.26–35.53 32.26–35.06 35.01–35.05 34.74–35.53 32.26–35.53 33.12–35.26 23.73
1.31–7.78 0.44–7.78 5.20–6.64 3.38–4.88 2.47–7.78 3.13–6.06 3.76–6.58 5.71–5.77 3.38–5.77 3.38–6.58 3.13–5.94 6.48
1.6–33.3 0.6–32.1 1.8–4.7 6.4–14.4 2.7–33.3 2.7–27.3 2.7–10.6 4.5–10.8 6.4–14.9 1.6–14.9 3.2–27.3 7
10–100 1–100 10–96 89–99 13–99 46.4–99 20–98 69.5–82 63–99 14–99 35–99 58
and one in 2001 (Mje1), where a 0.2 m2 van Veen grab was used. A minimum of 5 replicates per station is recommended in the literature to correctly represent the sampled environment (Thomas, 1998), and this was therefore used as a criterion for selecting most of the stations. A few stations were sampled with only 3 replicates but were included in this study as they represent unique areas.
Stockholm) and Per Johannessen (Uni Environment) assisted with the identification of difficult specimens. Light Microscopy and Scanning Electron Microscopy were used as tools to provide the most correct identification and to document the material. 2.3. Statistics
2.1.2. Benthos The samples were washed through two sieves with 5 mm and 1 mm grids (Hovgaard, 1973). The samples were preserved in 4% buffered formalin and transported to the lab. At the lab the samples were washed and re-sieved to remove formalin and sediment remains. Animals were sorted under a dissecting microscope and placed in small containers with ethanol or formalin. The molluscs obtained from the samples were stored in ethanol. After identification the animals were transferred to the Natural History Collections of Bergen Museum. 2.1.3. Grain size and organic content Sediment was suspended in water and sieved through a 0.063 mm filter. Particles larger than 0.063 mm were dried, dry sieved, and grouped. For particles smaller than 0.063 mm the pipette analysis was used (Buchanan, 1984). The percentage of sediment that could be assigned to the different groups (Clay, Silt, Sand, and Cobble) was then calculated. The organic content was defined using a standard weight loss on ignition method (Anonymous, 1980). 2.1.4. Hydrogen sulphide Hydrogen sulphide (H2S) content in the sediment was measured qualitatively and registered as; 0 – no noticeable H2S odour, 1 – noticeable H2S odour, and 2 – strong H2S odour. 2.1.5. Hydrographical measurements Temperature and conductivity/salinity were measured using a CTD. The density of the seawater was calculated (rt = kg/m3 – 1000). The oxygen content was measured using Winkler’s method, and oxygen saturation was calculated. 2.1.6. Diversity The diversity index (Shannon – H0 ) was calculated (Shannon and Weaver, 1949) on basis of all animals found in the sediment samples. This index is assumed to represent the faunal diversity for each of the sampled stations. 2.2. Identification of the Thyasiridae Oliver and Killeen (2002) and Payne and Allen (1991) were used as identification keys. P. Graham Oliver (National Museum of Wales), Anders Warén (Swedish Museum of Natural History,
All raw data were entered into Microsoft Excel 2002. The total number of specimens per species per station was divided with the number of sample replicates per station. The mean value is the species density in an area of 0.1 m2 at a station. Canoco for Windows version 4.5 (Ter Braak and Smilauer, 2002) was used for direct gradient analyses with unimodal modelling (CCA-Canonical Correspondence Analyses) to identify any correlations between environmental parameters and biological data collected (Jongman et al., 1995). The species data (number of specimens per unit area) were not transformed, and rare species were included in the model, but down-weighted. A forward selection of the environmental parameters was used to identify those which significantly influenced the species distributions (unrestricted Monte Carlo permutation test). In total 13 parameters were initially included in the model: Depth, silt, cobble, clay, clay + silt, sand, Salinity, Organic content, Hydrogen sulphide content, Diversity, Oxygen content, Oxygen saturation, and Seawater density. 3. Results Ranges of environmental parameters for each species found in this study are presented in Table 1. The depth of the 81 examined stations ranged from 9 m to 675 m. Oxygen content ranged from 0.44 ml/l to 7.78 ml/l, salinity from 23.73% to 35.53%, organic content from 0.6% to 33.3% weight loss on ignition (% wl), and grain size from 1% to 100% Clay and Silt. 3.1. Statistics The variables Silt, Cobble, Sand, Clay, Oxygen saturation and Seawater density were either not significant or redundant and were eliminated from the model. The variables Silt and Clay were still included in the plots for illustrative purposes as they are commonly used in environmental studies. The following parameters significantly influenced the distribution of Thyasiridae and are here considered important: depth (p = 0.0020), organic content (organic) (p = 0.0020), species diversity (div) (p = 0.0060) and the amount of hydrogen sulphide (H2S) (p = 0.0240). Oxygen (ox) (p = 0.2460), grain size (clay + silt) (p = 0.4560) and salinity (salt) (p > 0.5) did not significantly alter thyasirid distribution after forward selection of the parameters and are considered less important.
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The variance in thyasirid distribution explained by all variables was 1.13 of which depth explained 0.67. This indicates that depth accounts for more than half of all species occurrences (ca. 59%) and is the most important parameter. The variance explained by the second parameter, organic content, is 0.22 (ca. 20%) and combined with depth explains 0.89 of 1.13 variance. This indicates that depth and organic content together explain ca. 79% of all species occurrences. Subsequent significant parameters for species occurrence in decreasing order from 5% are diversity and hydrogen sulphide content. The independent value of these environmental parameters on thyasirids can be tested with bi-plot correlations (Fig. 1) (Ter Braak, 1990). The correlation is positive when the angle is sharp (<90°), there is no correlation when the arrows are perpendicular to each other, and the correlation is negative when the angle is wide (>90°) (Ter Braak, 1990). Organic content and H2S are the most positively correlated, Organic content and depth are only slightly negatively correlated, diversity and organic content/H2S are negatively correlated, and H2S and depth are negatively correlated. The results indicate that oxygen, grain size and salinity are not important to thyasirids. 3.1.1. Thyasira sarsi (Philippi, 1845) Thyasira sarsi has wide geographical distribution and was in this study found at 39 of the 81 examined stations, including the stations in Møre og Romsdal. The depth distribution ranges from 24 m to 545 m, although the observation at 545 m is uncertain as the identity of the shell found at this depth could not be positively confirmed (P.G. Oliver, pers. comm.). According to Oliver and Killeen (2002) T. sarsi occurs in shallow waters rather than in deep
waters with a depth range of 50 m to 150 m in Scandinavia. The deepest certain observation of T. sarsi in this study is at 316 m. In other studies T. sarsi has been found at a depth ranging from 17 m to 340 m (Dufour, 2005). Statistical results indicate that the occurence of T. sarsi is, as expected, related to the organic content of the sediment. T. sarsi is often found in relatively shallow waters with a poor faunal composition and tolerates low salinity (Table 1). The species generally is quite adaptable and thrives in sediments where other benthos struggle, for example in the presence of poisonous compounds as hydrogen sulphide (H2S) with accompanying low oxygen content (Table 1). These thyasirids rely heavily on nutrition from their chemo-autotrophic symbiotic bacteria (Dando and Spiro, 1993; Dando et al., 2004; Dufour, 2005). 3.1.2. Thyasira flexuosa (Montagu, 1803) Thyasira flexuosa was found at 49 of the 81 examined stations, including a station in Møre og Romsdal at depths ranging from 9 m to 130 m and is the most numerous species found in this study (Table 1). According to K.W. Ockelmann (unpublished notes) T. flexuosa thrives at depths from 0 m to 20 m in Norway. Oliver and Killeen (2002) report the species at depths ranging from 32 m to 161 m in the North Sea oil and gas installations. In other studies T. flexuosa has been found at a depth ranging from 6 m to 3000 m (Dufour, 2005). The species occurs in large populations at some stations and has a wide geographical distribution. In this study T. flexuosa was often found in sediments with low biodiversity and a rather low organic content. The species seems to tolerate some hydrogen sulphide and can occur in sediments almost depleted of oxygen (Table 1), but thrives better in sediments with higher oxygen content. The species also tolerates low salinity (Table 1) which is supported by K. Ockelmann in his unpublished notes. 3.1.3. Thyasira polygona (Jeffreys, 1864) Only 12 specimens of Thyasira polygona were found at 4 locations in Hordaland at a depth range of 41 m to 83 m. In the North Sea oil fields the species was found in deeper waters at a depth ranging from 90 m to 115 m (Oliver and Killeen, 2002). An amphi-Atlantic distribution is suggested in Killeen and Oliver (2002), but more research is needed to confirm this. Statistical results indicate that T. polygona thrives in more shallow waters and prefers sediments with a low organic content and high biodiversity. It does not seem to tolerate hydrogen sulphide and seems to prefer well oxygenated sediments (Table 1). Although the species lives in symbiosis with sulphide oxidising bacteria (Taylor et al., 2007), it does not seem to require the presence of large quantities of sulphides in the sediment, and thrives in less polluted environments.
Fig. 1. Biplot showing the environmental variables that are influencing the occurrences of the Thyasiridae in Hordaland significantly (unbroken vector lines): depth (p = 0.002), organic content (Organic) (p = 0.002), species diversity (Div) (p = 0.006), amount of hydrogen sulphide (H2S) (p = 0.024). Dashed vector lines represent variables that were found insignificant when the previous variables had been accounted for in forward selection: Oxygen (Ox) (p = 0.246), substrate grain size (clay + silt) (p = 0.456) and salinity (salt) (p > 0.5). The species are A. croulinensis (A. crou), A. eumyarius (A. eumy), A. similis (A. simi), M. ferruginosa (M. ferr), T. equalis (T. equa), T. flexuosa (T. flex), T. gouldi (T. goul), T. granulosa (T. gran), T. obsoleta (T. obso), T. polygona (T. poly), T. sarsi (T. sars), T. succisa (T. succ).
3.1.4. Thyasira granulosa (Monterosato, 1874) Thyasira granulosa was found at 4 locations in Hordaland. It occurs at depths ranging from 535 m to 585 m in this study, which is well within the range of 100 m to 1300 m given for Norwegian waters in Oliver and Killeen (2002). Off the west coast of Shetland the species is recorded at a depth of 1800 m, but in samples taken at this depth T. granulosa can easily be confused with the bathyal species T. subcircularis (Oliver and Killeen, 2002). Ockelmann states in his notes that in Norway T. granulosa is only recorded off the west coast between Bergen (Hordaland) and Lofoten (Nordland). In this study the species was found in samples from the Hardanger fjord, which is located slightly south of Bergen, and a more southerly distribution cannot be excluded. T. granulosa seems to thrive in deeper waters and is intolerant to H2S (Fig. 1), preferring an environment with a high biodiversity
R. Keuning et al. / Marine Pollution Bulletin 62 (2011) 786–791
and low organic content. Symbiotic bacteria are present in the gills, but T. granulosa might not be dependent on them for nutrition. 3.1.5. Thyasira equalis (Verrill and Bush, 1898) Thyasira equalis was found at 45 of the 81 stations and has a wide geographical distribution. In this study it is the third most numerous species and occurs at depths ranging from 27 m to 675 m. In other studies T. equalis has been recorded at a depth ranging from 10 m to 4734 m (Dufour, 2005). However, Oliver and Killeen (2002) express some uncertainty about the identity of shells with morphology similar to T. equalis retrieved from deeper waters (below 400 m). In this study T. equalis seems to thrive in deeper waters, preferring sediments with low organic content and little or no H2S, as well as a higher biodiversity, although we found it under a wide variety of conditions in Hordaland (Fig. 1). This indicates that T. equalis thrives in a less polluted environment. Table 1). This species is probably able to both suspension feed and obtain nutrition from chemo-autotrophic bacteria in the gills. 3.1.6. Thyasira obsoleta (Verrill and Bush, 1898) Thyasira obsoleta was found at 23 of the 81 stations at depths ranging from 40 m to 675 m. Oliver and Killeen (2002) report a depth range of 43 m to 1159 m for material from Norway and the Faroes while Payne and Allen (1991) give an overall depth range of 24 m to 2900 m. K.W. Ockelmann states in his unpublished notes that T. obsoleta is most common below 200 m and the findings in this study support this. The species seems to prefer well oxygenated, fine sediments (Table 1) with low organic content and does not tolerate H2S. In addition the species thrives in an environment with a high biodiversity (Fig. 1). This indicated that T. obsoleta prefers a less polluted environment. This species is a suspension feeder and symbiotic bacteria are absent in the gills (Dufour, 2005). 3.1.7. Axinulus croulinensis (Jeffreys, 1847) Axinulus croulinensis was found at 10 of the 81 stations and at depths ranging from 40 m to 224 m. Oliver and Killeen (2002) state that it is very common near some North Sea oil installations at 85 m to 220 m, although a much wider depth preference of 40 m to 3861 m is reported in Payne and Allen (1991) who also state that this is a common species in their samples. In Hordaland A. croulinensis has a more limited shallow distribution in well-oxygenated waters with low organic content and little or no H2S (Fig. 1). It prefers an environment with a high biodiversity (Fig. 1). Symbiotic bacteria are present in the gills of A. croulinensis, but to a lesser extent than in other species (Dufour, 2005) and the survival does not seem to be dependent on sulphides in the sediment. 3.1.8. Thyasira succisa (Jeffreys, 1876) Only two specimens of Thyasira succisa were found at two of the 81 stations, at depths of 225 m and 330 m. In the North Sea oil fields the species was recorded at depths ranging from 145 m to 220 m and not further south than 60°550 N (Oliver and Killeen, 2002). The most southerly location recorded in our study is at 59°480 N, although T. succisa has been found at locations as far south as the Mediterranean, at depths ranging from 73 m to 2813 m (Payne and Allen, 1991). The preferred habitat is fine and well oxygenated sediments (Table 1) although the basis for conclusion is only two specimens and might not be representative for the species. It is not known whether T. succisa possesses symbiotic bacteria in the gills. Payne and Allen (1991) state that the abfrontal tissue in the gills is poorly developed and Dufour (2005) suggests that the gills are not modified to house symbiotic bacteria which may therefore be absent in T. succisa.
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3.1.9. Axinulus eumyarius (Sars, 1870) Axinulus eumyarius was found at ten of the 81 stations, at depths ranging from 330 m to 675 m. The species seems to have a limited distribution in Hordaland, but large numbers were found at some stations. It is uncommon in the North Sea oil fields (recorded from one location off the coast of Norway) and the species has not been recorded elsewhere on the British Shelf (Oliver and Killeen, 2002). A depth range of 50 m to 1350 m is noted by K.W. Ockelmann in Norwegian waters (Oliver and Killeen, 2002), and Payne and Allen (1991) state that the species can occur from 42 m to 2663 m depth. A. eumyarius thrives in deeper waters and an environment with a high biodiversity (Fig. 1), preferring fine and well oxygenated sediments (Table 1) with low organic content, and it does not tolerate H2S. The species is a suspension feeder and symbiotic bacteria in the gills are absent (Dufour, 2005). 3.1.10. Mendicula ferruginosa (Forbes, 1844) Mendicula ferruginosa was found at 29 of the 81 examined stations, from 40 m to 675 m. The species is quite common and has a wide geographical, possibly cosmopolitan, range (Payne and Allen, 1991 Oliver and Killeen, 2002) It occurs at depths ranging from 200 m to 1850 m in the North Atlantic (Oliver and Killeen, 2002) but a more extensive depth range of 40 m to 4825 m is stated in Dufour (2005). M. ferruginosa seems to thrive in deeper waters and an environment with a high biodiversity (Fig. 1). The species seems to prefer well oxygenated sediments (Table 1) with low organic content and does not tolerate H2S. The species is a suspension feeder and lacks symbiotic bacteria in the gills (Dufour, 2005). 3.1.11. Adontorhina similis Barry and McCormack, 2007 Adontorhina similis was found at 18 of the 81 stations and has a limited distribution from 71 m to 585 m. Previous records of depth distribution include from 85 m to 161 m in the North Sea (Oliver and Killeen, 2002) or a more general range of 30 m to >2000 m as noted by K.W. Ockelmann (Oliver and Killeen, 2002). A. similis seems to thrive in deeper waters and in an environment with a high biodiversity (Fig. 1). The species seems to prefer well oxygenated sediments with low organic content and does not tolerate H2S (Fig. 1). According to Dufour (2005) A. similis (identified as Mendicula pygmaea) has no symbiotic sulphide oxidising bacteria. 3.1.12. Thyasira gouldi (Philippi, 1845) Thyasira gouldi were found in a single sample taken in the province of Møre and Romsdal. Although T. gouldi is regarded to be a circum boreal/arctic species, it is present at several locations around the British Isles (Oliver and Killeen, 2002). The species has previously also been recorded off the coast of Hordaland (K.W. Ockelmann, unpublished notes) and its absence in our samples is not explained. 4. Discussion The statistical analysis chosen to apply to the dataset collected in this study was the direct gradient analyses with unimodal modelling (CCA-Canonical Correspondence Analyses). This analysis recognises species distribution patterns related to environmental parameters best in regard to the collected dataset. Other methods for selecting environmental indicators, as for example the method presented by Pearson et al. (1983) demand a different dataset. The stations included in our study were not randomly selected, but are incorporated in environmental survey studies related to pollution and disturbance. Stations included in this study are around discharge points or investigations of polluted or disturbed
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areas mostly in shallower waters, and the reference stations with good environmental conditions are situated in deeper waters. H2S is only qualitatively measured. This has influenced the correlations of environmental factors on thyasirid distribution. High organic content usually results in anoxic conditions in the sediment, triggering the formation of hydrogen sulphide, and reduce the local biodiversity (Clark, 2003). Organic content and depth are only slightly negatively correlated. Temperature is thought not to influence the occurrence of Thyasiridae in Hordaland as the geographical area is limited and a latitudinal gradient is not present. A rather surprising result of this study was that in other studies T. flexuosa was seen exploiting sulphides in the sediments (Dando et al., 1994, 2004), but in this study T. flexuosa could not be related to organic enrichment even though species numbers were sufficient to create valid significant results. Although the species often occurs together with Thyasira sarsi and has symbiotic bacteria in the gills, it does not seem to be depending on organic enrichment for survival. Indeed the species are able to share environmental conditions as shallow waters, low salinity and a low biodiversity (Table 1), but organic enrichment and H2S content are not shared preferences (Fig. 1). In this study T. flexuosa seems to thrive in an environment with coarser sediments that are better oxygenated, which could indicate that the species simply prefers an environment with stronger currents. Further research is necessary to better define the ecological preferences of T. flexuosa. Thyasira sarsi, is the only thyasirid species which seems to thrive in an environment where the organic content is high, hydrogen sulphide is present, and the biodiversity is low. Several studies have shown that this species relies heavily on nutrition from symbiotic bacteria (Spiro et al., 1986; Dando et al., 1994, 2004), The distribution of thyasirids in this study is not determined by grain size, despite this being an important determinant of habitat for bivalves in general (Bertness et al., 2001). Depth seems to be much more important for the occurrence of these species, although depth is often correlated with fine sediments in fjords (Erlandsson, 2008). Species diversity of Thyasiridae might be a useful indicator of environmental conditions. Also single thyasirid species that seem to be quite common in environments with good conditions and lack symbiotic bacteria, as for example Mendicula ferruginosa, could be used as indicators. Thyasira sarsi was found to be a useful indicator of organic enrichment. A typical habitat for T. sarsi would be in shallow waters, organically enriched sediments, often containing H2S, with a low biodiversity. Low biodiversity together with the presence of T. sarsi may be a very good indicator of organic enrichment. Large densities of T. sarsi indicate the presence of large amounts of sulphides in the sediments, which indicates a high organic content. However, the occurrence of T. sarsi is, as with most opportunistic species, not always related to the organic content in the sediment, and such symbiotic species can also be found in sediments with low organic content and low or undetectable sulphide levels (Dufour, 2005 – see also Table 1), but not in large densities. In addition T. sarsi is a secondary coloniser after the opportunistic polychaetes and requires oxygen for its existence (Pearson and Rosenberg, 1978). T. sarsi population densities can therefore fluctuate much in sediments that can become depleted of oxygen (Dando and Spiro, 1993). As soon as oxygen is reintroduced large populations quickly become established with sulphide being oxidised at a high rate, and as the sediments become depleted for sulphides heterotrophic benthic species can colonise the area (Dando et al., 2004). After that T. sarsi populations decline not only due to the lack of sulphides, but also due to bioturbation by later colonisers that disrupts their tunnel systems and makes it more difficult to mine for sulphides (Dando et al., 2004).
In conclusion, the presence of T. sarsi usually indicates organic enrichment, but it is recommended to examine the characteristics of the whole benthic community (biodiversity) in order to confirm organic enrichment and pollution. The presence of Thyasira sarsi together with low biodiversity is a good indicator of organic enrichment. High thyasirid species diversity might be indicative of good environmental conditions. Further research should be conducted to better define the ecological preferences of thyasirid species, as some might be indicators of good environmental conditions, and the capability of Thyasira sarsi as an environmental engineer should be readily exploited. Acknowledgements We extend our gratitude towards Graham Oliver, Anders Warén, and Per Johannessen for help with identification. Karin Pittman is thanked for valuable comments on the manuscript. The work was funded by a student grant from the department of biology, University of Bergen, Norway (Marine Biodiversity research group). References Anonymous, 1980. Norwegian Standard NS 4764. Water analysis. Total residue and total fixed residue in water, sludge and sediment. Norsk Standardiseringsforbund. Barry, P.J., McCormack, G.P., 2007. Two new species of Adontorhina Berry, 1947 (Bivalvia: Thyasiridae) from the Porcupine Bank, off the west coast of Ireland. Zootaxa 1526, 37–49. Bertness, M.D., Gaines, S.D., Hay, M., 2001. Marine Community Ecology. Sinauer Associates Inc. Botnen, H., Heggøy, E., Vassenden, G., Johansen, P.-O., Johannessen, P.J., 2002. ‘‘Byfjordsundersøkelsen’’ overvåking av fjordene rundt Bergen – miljøundersøkelse i 2001. IFM Rapport 5, 1–158. Botnen, H.B., Vassenden, G., Hjohlman, S., Johansen, P.-O., Johannessen, P.J., 2000. ‘‘Byfjordundersøkelsen’’ overvåking fjordene rundt Bergen – miljøundersøkelse i 2000. IFM Rapport 13, 1–155. Buchanan, J.B., 1984. Sediment analysis. In: Holme, N.A., McIntyre, A.D. (Eds.), Methods for the Study of Marine Benthos. Blackwell Scientific Publications, Oxford, pp. 41–65. Clark, R.B., 2003. Marine Pollution, fifth ed. Oxford University Press. Dando, P.R., Ridgway, S.A., Spiro, B., 1994. Sulphide ‘mining’ by lucinid bivalve molluscs: demonstrated by stable sulphur isotope measurements and experimental models. Mar. Ecol. Prog. Ser. 107, 169–175. Dando, P.R., Southward, A.J., Southward, E.C., 2004. Rates of sediment sulphide oxidation by the bivlave mollusc Thyasira sarsi. Mar. Ecol. Prog. Ser. 208, 181– 187. Dando, P.R., Spiro, B., 1993. Varying nutritional dependence of the thyasirid bivalves Thyasira sarsi and T. equalis on chemo-autotrophic symbiontic bacteria, demonstrated by isotope ratios of tissue carbon and shell carbonate. Mar. Ecol. Prog. Ser. 92, 151–158. Dufour, S.C., 2005. Gill Anatomy and the Evolution of Symbiosis in the Bivalve Family Thyasiridae. Biol. Bull. 208, 200–212. Dufour, S.C., Felbeck, H., 2003. Sulphide mining by the superextensile foot of symbiotic thyasirid bivalves. Nature 426, 65–67. Erlandsson, C.P., 2008. Vertical transport of particulate organic matter regulated by fjord topography. J. Geophys. Res. 113, 1–13. Heggøy, E., Botnen, H., Vassenden, G., Johannessen, P., 2004a. Marinbiologisk miljøundersøkelser i Lundevågen-Humlevik, Tysnesvik-Gjerdsvik, SøreidvikBeltestadvågen og Gripnesvågen, Tysnes kommune 2004. IFM Rapport 5, 1–60. Heggøy, E., Vassenden, G., Botnen, H., Johannessen, P., 2004b. Inbiologisk miljøundersøkelse ved fusa Fiskeanlegg AS i Sævareidfjorden, Fusa kommune i 2004. IFM Rapport 7, 1–36. Heggøy, E., Johansen, P.-O., Halvorsen, G.A., Vassenden, G., Botnen, H., Johannessen, P., 2005a. Miljøundersøking i Lindås Kommune i 2004. Vestbio 3, 1–105. Heggøy, E., Johansen, P.-O., Vassenden, G., Botnen, H., Johannessen, P., 2005b. ‘‘Byfjordundersøkelsen’’ – overvåking av Fjordene Rundt Bergen i 2004. Vestbio 6, 1–194. Heggøy, E., Vassenden, G., Johannessen, P.J., 2005c. Marinbiologisk miljøundersøkelse av resipienter i Os kommune i 2005. Vestbio 8, 1–61. Heggøy, E., Vassenden, G., Johannessen, P.J., 2007. Marinbiologisk miljøundersøkelse av resipienter i Os kommune i 2006. Vestbio 1, 1–110. Hjohlman, S., Botnen, H., Johannessen, P.J., 2000. Resipientundersøkelse i Eggesbøstraumen, Herøy kommune, i 2000. IFM Rapport 12, 1–73. Hovgaard, P., 1973. A new system of sieves for benthic samples. Sarsia 53, 15–18. Johannessen, P.J., Risheim, I., Botnen, H.B., 1991. ‘‘Byfjordsundersøkelsen’’ overvåking av fjordene rundt Bergen 1990. IFM Rapport 11, 1–108. Johansen, P.-O., Hjohlman, S., Botnen, H.B., Johannessen, P.J., 2000. Overvåking av Statoil’s raffineri på Mongstad i 2000. IFM Rapport 9, 1–108. Johansen, P.-O., Vassenden, G., Botnen, H., Johannessen, P.J., 2001a. Undersøkelser av miljøforholdene ved Mjelstad restdeponi på Osterøy i 2001. IFM Rapport 18, 1–56.
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Contents lists available at ScienceDirect
Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Ecology of twelve species of Thyasiridae (Mollusca: Bivalvia) Keuning Rozemarijn a, Schander Christoffer a,b,c,⇑, Kongsrud Jon Anders d, Willassen Endre d a
University of Bergen, Department of Biology, 5020 Bergen, Norway Centre of GeoBiology, University of Bergen, 5020 Bergen, Norway c Uni Environment, 5020 Bergen, Norway d Bergen Museum, Natural History Collections, University of Bergen, 5020 Bergen, Norway b
a r t i c l e Keywords: Atlantic Ocean Sediment Oxygen Multivariate analysis Thyasira
i n f o
a b s t r a c t Benthic samples from coastal locations off Southwestern Norway were examined and the specimens of Thyasiridae were identified to species. A multivariate analysis based on 13 parameters was carried out and the environmental preferences of all thyasirid species present were determined. The potential of the Thyasiridae as indicators of organic enrichment was investigated by using direct canonical correspondence analyses to identify correlations between selected environmental parameters and the collected biological data. The presence of Thyasira sarsi together with a low biodiversity is a good indicator of organic enrichment. High thyasirid species diversity seems to indicate good environmental conditions, and single thyasirid species that lack symbiotic bacteria might also be useful as indicators of good environmental conditions. Ó 2011 Elsevier Ltd. All rights reserved.
1. Introduction The Thyasiridae is a family of bivalves with a fossil record going back to the Cretaceous period (McAlester, 1966). The family consists of 11 genera and around 90 described recent species with a worldwide distribution, living from shallow coastal waters to abyssal depths (Payne and Allen, 1991; Taylor et al., 2007). Thyasiridae occupy a variety of habitats with different sediment types, including cold seeps (Levin, 2005) and hydrothermal vents (Southward et al., 2001). They are often associated with organic enrichment (Dando et al., 2004) and some species can be found in high numbers beneath oil platforms where the sediment is polluted with oily drill cuttings (Oliver and Killeen, 2002). Several species live in symbiosis with sulphide oxidising bacteria (Dando and Spiro, 1993) and have gills that are modified to house bacteria. Some species possess a hyperextensible foot that can stretch up to 30 times the length of the shell (Dufour and Felbeck, 2003). With their extensive burrowing behaviour the Thyasiridae contribute to oxygenating the sediments in addition to ‘mining’ for sulphides (Dando et al., 1994; Dufour and Felbeck, 2003). This behaviour means that they are able to effectively exploit reducing and polluted sediments, and modify the sediments in such a way that the environment becomes more attractive to sulphide-intolerant benthos. Due to this behaviour some thyasirids are candidates for
environmental engineering in the literature (e.g. Dando et al., 2004). When sediment sulphide becomes depleted, the bacteria in the gills starve and the thyasirids disappear (Dando and Spiro, 1993). Thyasirids may therefore be suitable indicators of environmental pollution, and their ecology could aid in detecting environmental changes. Thyasirids collected from sediment samples taken at different locations in coastal waters off W. Norway (Table 1) were examined and identified. Environmental data were analysed in order to investigate the ecological preferences of the species, including their potential as indicators of organic enrichment. 2. Material and methods Material from environmental studies carried out by the Section for Applied Environmental Research, University in Bergen (‘SAM-marin’) was used for this study. Sediment samples were already analysed and environmental parameters reported (Botnen et al., 2000, 2002; Heggøy et al., 2004a,b, 2005a,b,c, 2007; Hjohlman et al., 2000; Johannessen et al., 1991; Johansen et al., 2000, 2001a,b, 2002a,b, 2003a,b,c, 2004a,b, 2006; Vassenden and Johannessen, 2002, 2005; Vassenden et al., 2005a,b, 2006). The material represents Hordaland and a small area in Møre og Romsdal. 2.1. Sampling procedure and environmental parameters
⇑ Corresponding author. Present address: 101 Life Sciences Building, Department of Biological Sciences, Auburn University, Auburn, AL 36849, USA. Tel.: +1 334 884 1636. E-mail address: [email protected] (C. Schander). 0025-326X/$ - see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.marpolbul.2011.01.004
2.1.1. Sediment Sediment samples were collected using a 0.1 m2 van Veen grab with the exception of two stations sampled in 1990 (St18 and St23)
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R. Keuning et al. / Marine Pollution Bulletin 62 (2011) 786–791 Table 1 Ranges of the environmental parameters for each species found in this study. Species
No. of specimens
Depth (m)
Salinity (‰)
Oxygen content (ml/l)
Organic content (% wl)
Grain size (% clay + silt)
Thyasira sarsi Thyasira flexuosa Thyasira polygona Thyasira granulosa Thyasira equalis Thyasira obsoleta Axinulus croulinensis Thyasira succisa Axinulus eumyarius Mendicula ferruginosa Adontorhina similis Thyasira gouldi
3148 5497 12 22 1337 156 72 2 343 734 115 3
24–545 9–130 41–83 535–585 27–675 40–675 40–224 225–330 330–675 40–675 71–585 29
23.73–35.00 23.73–35.00 33.52–34.36 34.91–35.13 30.78–35.53 32.26–35.53 32.26–35.06 35.01–35.05 34.74–35.53 32.26–35.53 33.12–35.26 23.73
1.31–7.78 0.44–7.78 5.20–6.64 3.38–4.88 2.47–7.78 3.13–6.06 3.76–6.58 5.71–5.77 3.38–5.77 3.38–6.58 3.13–5.94 6.48
1.6–33.3 0.6–32.1 1.8–4.7 6.4–14.4 2.7–33.3 2.7–27.3 2.7–10.6 4.5–10.8 6.4–14.9 1.6–14.9 3.2–27.3 7
10–100 1–100 10–96 89–99 13–99 46.4–99 20–98 69.5–82 63–99 14–99 35–99 58
and one in 2001 (Mje1), where a 0.2 m2 van Veen grab was used. A minimum of 5 replicates per station is recommended in the literature to correctly represent the sampled environment (Thomas, 1998), and this was therefore used as a criterion for selecting most of the stations. A few stations were sampled with only 3 replicates but were included in this study as they represent unique areas.
Stockholm) and Per Johannessen (Uni Environment) assisted with the identification of difficult specimens. Light Microscopy and Scanning Electron Microscopy were used as tools to provide the most correct identification and to document the material. 2.3. Statistics
2.1.2. Benthos The samples were washed through two sieves with 5 mm and 1 mm grids (Hovgaard, 1973). The samples were preserved in 4% buffered formalin and transported to the lab. At the lab the samples were washed and re-sieved to remove formalin and sediment remains. Animals were sorted under a dissecting microscope and placed in small containers with ethanol or formalin. The molluscs obtained from the samples were stored in ethanol. After identification the animals were transferred to the Natural History Collections of Bergen Museum. 2.1.3. Grain size and organic content Sediment was suspended in water and sieved through a 0.063 mm filter. Particles larger than 0.063 mm were dried, dry sieved, and grouped. For particles smaller than 0.063 mm the pipette analysis was used (Buchanan, 1984). The percentage of sediment that could be assigned to the different groups (Clay, Silt, Sand, and Cobble) was then calculated. The organic content was defined using a standard weight loss on ignition method (Anonymous, 1980). 2.1.4. Hydrogen sulphide Hydrogen sulphide (H2S) content in the sediment was measured qualitatively and registered as; 0 – no noticeable H2S odour, 1 – noticeable H2S odour, and 2 – strong H2S odour. 2.1.5. Hydrographical measurements Temperature and conductivity/salinity were measured using a CTD. The density of the seawater was calculated (rt = kg/m3 – 1000). The oxygen content was measured using Winkler’s method, and oxygen saturation was calculated. 2.1.6. Diversity The diversity index (Shannon – H0 ) was calculated (Shannon and Weaver, 1949) on basis of all animals found in the sediment samples. This index is assumed to represent the faunal diversity for each of the sampled stations. 2.2. Identification of the Thyasiridae Oliver and Killeen (2002) and Payne and Allen (1991) were used as identification keys. P. Graham Oliver (National Museum of Wales), Anders Warén (Swedish Museum of Natural History,
All raw data were entered into Microsoft Excel 2002. The total number of specimens per species per station was divided with the number of sample replicates per station. The mean value is the species density in an area of 0.1 m2 at a station. Canoco for Windows version 4.5 (Ter Braak and Smilauer, 2002) was used for direct gradient analyses with unimodal modelling (CCA-Canonical Correspondence Analyses) to identify any correlations between environmental parameters and biological data collected (Jongman et al., 1995). The species data (number of specimens per unit area) were not transformed, and rare species were included in the model, but down-weighted. A forward selection of the environmental parameters was used to identify those which significantly influenced the species distributions (unrestricted Monte Carlo permutation test). In total 13 parameters were initially included in the model: Depth, silt, cobble, clay, clay + silt, sand, Salinity, Organic content, Hydrogen sulphide content, Diversity, Oxygen content, Oxygen saturation, and Seawater density. 3. Results Ranges of environmental parameters for each species found in this study are presented in Table 1. The depth of the 81 examined stations ranged from 9 m to 675 m. Oxygen content ranged from 0.44 ml/l to 7.78 ml/l, salinity from 23.73% to 35.53%, organic content from 0.6% to 33.3% weight loss on ignition (% wl), and grain size from 1% to 100% Clay and Silt. 3.1. Statistics The variables Silt, Cobble, Sand, Clay, Oxygen saturation and Seawater density were either not significant or redundant and were eliminated from the model. The variables Silt and Clay were still included in the plots for illustrative purposes as they are commonly used in environmental studies. The following parameters significantly influenced the distribution of Thyasiridae and are here considered important: depth (p = 0.0020), organic content (organic) (p = 0.0020), species diversity (div) (p = 0.0060) and the amount of hydrogen sulphide (H2S) (p = 0.0240). Oxygen (ox) (p = 0.2460), grain size (clay + silt) (p = 0.4560) and salinity (salt) (p > 0.5) did not significantly alter thyasirid distribution after forward selection of the parameters and are considered less important.
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The variance in thyasirid distribution explained by all variables was 1.13 of which depth explained 0.67. This indicates that depth accounts for more than half of all species occurrences (ca. 59%) and is the most important parameter. The variance explained by the second parameter, organic content, is 0.22 (ca. 20%) and combined with depth explains 0.89 of 1.13 variance. This indicates that depth and organic content together explain ca. 79% of all species occurrences. Subsequent significant parameters for species occurrence in decreasing order from 5% are diversity and hydrogen sulphide content. The independent value of these environmental parameters on thyasirids can be tested with bi-plot correlations (Fig. 1) (Ter Braak, 1990). The correlation is positive when the angle is sharp (<90°), there is no correlation when the arrows are perpendicular to each other, and the correlation is negative when the angle is wide (>90°) (Ter Braak, 1990). Organic content and H2S are the most positively correlated, Organic content and depth are only slightly negatively correlated, diversity and organic content/H2S are negatively correlated, and H2S and depth are negatively correlated. The results indicate that oxygen, grain size and salinity are not important to thyasirids. 3.1.1. Thyasira sarsi (Philippi, 1845) Thyasira sarsi has wide geographical distribution and was in this study found at 39 of the 81 examined stations, including the stations in Møre og Romsdal. The depth distribution ranges from 24 m to 545 m, although the observation at 545 m is uncertain as the identity of the shell found at this depth could not be positively confirmed (P.G. Oliver, pers. comm.). According to Oliver and Killeen (2002) T. sarsi occurs in shallow waters rather than in deep
waters with a depth range of 50 m to 150 m in Scandinavia. The deepest certain observation of T. sarsi in this study is at 316 m. In other studies T. sarsi has been found at a depth ranging from 17 m to 340 m (Dufour, 2005). Statistical results indicate that the occurence of T. sarsi is, as expected, related to the organic content of the sediment. T. sarsi is often found in relatively shallow waters with a poor faunal composition and tolerates low salinity (Table 1). The species generally is quite adaptable and thrives in sediments where other benthos struggle, for example in the presence of poisonous compounds as hydrogen sulphide (H2S) with accompanying low oxygen content (Table 1). These thyasirids rely heavily on nutrition from their chemo-autotrophic symbiotic bacteria (Dando and Spiro, 1993; Dando et al., 2004; Dufour, 2005). 3.1.2. Thyasira flexuosa (Montagu, 1803) Thyasira flexuosa was found at 49 of the 81 examined stations, including a station in Møre og Romsdal at depths ranging from 9 m to 130 m and is the most numerous species found in this study (Table 1). According to K.W. Ockelmann (unpublished notes) T. flexuosa thrives at depths from 0 m to 20 m in Norway. Oliver and Killeen (2002) report the species at depths ranging from 32 m to 161 m in the North Sea oil and gas installations. In other studies T. flexuosa has been found at a depth ranging from 6 m to 3000 m (Dufour, 2005). The species occurs in large populations at some stations and has a wide geographical distribution. In this study T. flexuosa was often found in sediments with low biodiversity and a rather low organic content. The species seems to tolerate some hydrogen sulphide and can occur in sediments almost depleted of oxygen (Table 1), but thrives better in sediments with higher oxygen content. The species also tolerates low salinity (Table 1) which is supported by K. Ockelmann in his unpublished notes. 3.1.3. Thyasira polygona (Jeffreys, 1864) Only 12 specimens of Thyasira polygona were found at 4 locations in Hordaland at a depth range of 41 m to 83 m. In the North Sea oil fields the species was found in deeper waters at a depth ranging from 90 m to 115 m (Oliver and Killeen, 2002). An amphi-Atlantic distribution is suggested in Killeen and Oliver (2002), but more research is needed to confirm this. Statistical results indicate that T. polygona thrives in more shallow waters and prefers sediments with a low organic content and high biodiversity. It does not seem to tolerate hydrogen sulphide and seems to prefer well oxygenated sediments (Table 1). Although the species lives in symbiosis with sulphide oxidising bacteria (Taylor et al., 2007), it does not seem to require the presence of large quantities of sulphides in the sediment, and thrives in less polluted environments.
Fig. 1. Biplot showing the environmental variables that are influencing the occurrences of the Thyasiridae in Hordaland significantly (unbroken vector lines): depth (p = 0.002), organic content (Organic) (p = 0.002), species diversity (Div) (p = 0.006), amount of hydrogen sulphide (H2S) (p = 0.024). Dashed vector lines represent variables that were found insignificant when the previous variables had been accounted for in forward selection: Oxygen (Ox) (p = 0.246), substrate grain size (clay + silt) (p = 0.456) and salinity (salt) (p > 0.5). The species are A. croulinensis (A. crou), A. eumyarius (A. eumy), A. similis (A. simi), M. ferruginosa (M. ferr), T. equalis (T. equa), T. flexuosa (T. flex), T. gouldi (T. goul), T. granulosa (T. gran), T. obsoleta (T. obso), T. polygona (T. poly), T. sarsi (T. sars), T. succisa (T. succ).
3.1.4. Thyasira granulosa (Monterosato, 1874) Thyasira granulosa was found at 4 locations in Hordaland. It occurs at depths ranging from 535 m to 585 m in this study, which is well within the range of 100 m to 1300 m given for Norwegian waters in Oliver and Killeen (2002). Off the west coast of Shetland the species is recorded at a depth of 1800 m, but in samples taken at this depth T. granulosa can easily be confused with the bathyal species T. subcircularis (Oliver and Killeen, 2002). Ockelmann states in his notes that in Norway T. granulosa is only recorded off the west coast between Bergen (Hordaland) and Lofoten (Nordland). In this study the species was found in samples from the Hardanger fjord, which is located slightly south of Bergen, and a more southerly distribution cannot be excluded. T. granulosa seems to thrive in deeper waters and is intolerant to H2S (Fig. 1), preferring an environment with a high biodiversity
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and low organic content. Symbiotic bacteria are present in the gills, but T. granulosa might not be dependent on them for nutrition. 3.1.5. Thyasira equalis (Verrill and Bush, 1898) Thyasira equalis was found at 45 of the 81 stations and has a wide geographical distribution. In this study it is the third most numerous species and occurs at depths ranging from 27 m to 675 m. In other studies T. equalis has been recorded at a depth ranging from 10 m to 4734 m (Dufour, 2005). However, Oliver and Killeen (2002) express some uncertainty about the identity of shells with morphology similar to T. equalis retrieved from deeper waters (below 400 m). In this study T. equalis seems to thrive in deeper waters, preferring sediments with low organic content and little or no H2S, as well as a higher biodiversity, although we found it under a wide variety of conditions in Hordaland (Fig. 1). This indicates that T. equalis thrives in a less polluted environment. Table 1). This species is probably able to both suspension feed and obtain nutrition from chemo-autotrophic bacteria in the gills. 3.1.6. Thyasira obsoleta (Verrill and Bush, 1898) Thyasira obsoleta was found at 23 of the 81 stations at depths ranging from 40 m to 675 m. Oliver and Killeen (2002) report a depth range of 43 m to 1159 m for material from Norway and the Faroes while Payne and Allen (1991) give an overall depth range of 24 m to 2900 m. K.W. Ockelmann states in his unpublished notes that T. obsoleta is most common below 200 m and the findings in this study support this. The species seems to prefer well oxygenated, fine sediments (Table 1) with low organic content and does not tolerate H2S. In addition the species thrives in an environment with a high biodiversity (Fig. 1). This indicated that T. obsoleta prefers a less polluted environment. This species is a suspension feeder and symbiotic bacteria are absent in the gills (Dufour, 2005). 3.1.7. Axinulus croulinensis (Jeffreys, 1847) Axinulus croulinensis was found at 10 of the 81 stations and at depths ranging from 40 m to 224 m. Oliver and Killeen (2002) state that it is very common near some North Sea oil installations at 85 m to 220 m, although a much wider depth preference of 40 m to 3861 m is reported in Payne and Allen (1991) who also state that this is a common species in their samples. In Hordaland A. croulinensis has a more limited shallow distribution in well-oxygenated waters with low organic content and little or no H2S (Fig. 1). It prefers an environment with a high biodiversity (Fig. 1). Symbiotic bacteria are present in the gills of A. croulinensis, but to a lesser extent than in other species (Dufour, 2005) and the survival does not seem to be dependent on sulphides in the sediment. 3.1.8. Thyasira succisa (Jeffreys, 1876) Only two specimens of Thyasira succisa were found at two of the 81 stations, at depths of 225 m and 330 m. In the North Sea oil fields the species was recorded at depths ranging from 145 m to 220 m and not further south than 60°550 N (Oliver and Killeen, 2002). The most southerly location recorded in our study is at 59°480 N, although T. succisa has been found at locations as far south as the Mediterranean, at depths ranging from 73 m to 2813 m (Payne and Allen, 1991). The preferred habitat is fine and well oxygenated sediments (Table 1) although the basis for conclusion is only two specimens and might not be representative for the species. It is not known whether T. succisa possesses symbiotic bacteria in the gills. Payne and Allen (1991) state that the abfrontal tissue in the gills is poorly developed and Dufour (2005) suggests that the gills are not modified to house symbiotic bacteria which may therefore be absent in T. succisa.
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3.1.9. Axinulus eumyarius (Sars, 1870) Axinulus eumyarius was found at ten of the 81 stations, at depths ranging from 330 m to 675 m. The species seems to have a limited distribution in Hordaland, but large numbers were found at some stations. It is uncommon in the North Sea oil fields (recorded from one location off the coast of Norway) and the species has not been recorded elsewhere on the British Shelf (Oliver and Killeen, 2002). A depth range of 50 m to 1350 m is noted by K.W. Ockelmann in Norwegian waters (Oliver and Killeen, 2002), and Payne and Allen (1991) state that the species can occur from 42 m to 2663 m depth. A. eumyarius thrives in deeper waters and an environment with a high biodiversity (Fig. 1), preferring fine and well oxygenated sediments (Table 1) with low organic content, and it does not tolerate H2S. The species is a suspension feeder and symbiotic bacteria in the gills are absent (Dufour, 2005). 3.1.10. Mendicula ferruginosa (Forbes, 1844) Mendicula ferruginosa was found at 29 of the 81 examined stations, from 40 m to 675 m. The species is quite common and has a wide geographical, possibly cosmopolitan, range (Payne and Allen, 1991 Oliver and Killeen, 2002) It occurs at depths ranging from 200 m to 1850 m in the North Atlantic (Oliver and Killeen, 2002) but a more extensive depth range of 40 m to 4825 m is stated in Dufour (2005). M. ferruginosa seems to thrive in deeper waters and an environment with a high biodiversity (Fig. 1). The species seems to prefer well oxygenated sediments (Table 1) with low organic content and does not tolerate H2S. The species is a suspension feeder and lacks symbiotic bacteria in the gills (Dufour, 2005). 3.1.11. Adontorhina similis Barry and McCormack, 2007 Adontorhina similis was found at 18 of the 81 stations and has a limited distribution from 71 m to 585 m. Previous records of depth distribution include from 85 m to 161 m in the North Sea (Oliver and Killeen, 2002) or a more general range of 30 m to >2000 m as noted by K.W. Ockelmann (Oliver and Killeen, 2002). A. similis seems to thrive in deeper waters and in an environment with a high biodiversity (Fig. 1). The species seems to prefer well oxygenated sediments with low organic content and does not tolerate H2S (Fig. 1). According to Dufour (2005) A. similis (identified as Mendicula pygmaea) has no symbiotic sulphide oxidising bacteria. 3.1.12. Thyasira gouldi (Philippi, 1845) Thyasira gouldi were found in a single sample taken in the province of Møre and Romsdal. Although T. gouldi is regarded to be a circum boreal/arctic species, it is present at several locations around the British Isles (Oliver and Killeen, 2002). The species has previously also been recorded off the coast of Hordaland (K.W. Ockelmann, unpublished notes) and its absence in our samples is not explained. 4. Discussion The statistical analysis chosen to apply to the dataset collected in this study was the direct gradient analyses with unimodal modelling (CCA-Canonical Correspondence Analyses). This analysis recognises species distribution patterns related to environmental parameters best in regard to the collected dataset. Other methods for selecting environmental indicators, as for example the method presented by Pearson et al. (1983) demand a different dataset. The stations included in our study were not randomly selected, but are incorporated in environmental survey studies related to pollution and disturbance. Stations included in this study are around discharge points or investigations of polluted or disturbed
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areas mostly in shallower waters, and the reference stations with good environmental conditions are situated in deeper waters. H2S is only qualitatively measured. This has influenced the correlations of environmental factors on thyasirid distribution. High organic content usually results in anoxic conditions in the sediment, triggering the formation of hydrogen sulphide, and reduce the local biodiversity (Clark, 2003). Organic content and depth are only slightly negatively correlated. Temperature is thought not to influence the occurrence of Thyasiridae in Hordaland as the geographical area is limited and a latitudinal gradient is not present. A rather surprising result of this study was that in other studies T. flexuosa was seen exploiting sulphides in the sediments (Dando et al., 1994, 2004), but in this study T. flexuosa could not be related to organic enrichment even though species numbers were sufficient to create valid significant results. Although the species often occurs together with Thyasira sarsi and has symbiotic bacteria in the gills, it does not seem to be depending on organic enrichment for survival. Indeed the species are able to share environmental conditions as shallow waters, low salinity and a low biodiversity (Table 1), but organic enrichment and H2S content are not shared preferences (Fig. 1). In this study T. flexuosa seems to thrive in an environment with coarser sediments that are better oxygenated, which could indicate that the species simply prefers an environment with stronger currents. Further research is necessary to better define the ecological preferences of T. flexuosa. Thyasira sarsi, is the only thyasirid species which seems to thrive in an environment where the organic content is high, hydrogen sulphide is present, and the biodiversity is low. Several studies have shown that this species relies heavily on nutrition from symbiotic bacteria (Spiro et al., 1986; Dando et al., 1994, 2004), The distribution of thyasirids in this study is not determined by grain size, despite this being an important determinant of habitat for bivalves in general (Bertness et al., 2001). Depth seems to be much more important for the occurrence of these species, although depth is often correlated with fine sediments in fjords (Erlandsson, 2008). Species diversity of Thyasiridae might be a useful indicator of environmental conditions. Also single thyasirid species that seem to be quite common in environments with good conditions and lack symbiotic bacteria, as for example Mendicula ferruginosa, could be used as indicators. Thyasira sarsi was found to be a useful indicator of organic enrichment. A typical habitat for T. sarsi would be in shallow waters, organically enriched sediments, often containing H2S, with a low biodiversity. Low biodiversity together with the presence of T. sarsi may be a very good indicator of organic enrichment. Large densities of T. sarsi indicate the presence of large amounts of sulphides in the sediments, which indicates a high organic content. However, the occurrence of T. sarsi is, as with most opportunistic species, not always related to the organic content in the sediment, and such symbiotic species can also be found in sediments with low organic content and low or undetectable sulphide levels (Dufour, 2005 – see also Table 1), but not in large densities. In addition T. sarsi is a secondary coloniser after the opportunistic polychaetes and requires oxygen for its existence (Pearson and Rosenberg, 1978). T. sarsi population densities can therefore fluctuate much in sediments that can become depleted of oxygen (Dando and Spiro, 1993). As soon as oxygen is reintroduced large populations quickly become established with sulphide being oxidised at a high rate, and as the sediments become depleted for sulphides heterotrophic benthic species can colonise the area (Dando et al., 2004). After that T. sarsi populations decline not only due to the lack of sulphides, but also due to bioturbation by later colonisers that disrupts their tunnel systems and makes it more difficult to mine for sulphides (Dando et al., 2004).
In conclusion, the presence of T. sarsi usually indicates organic enrichment, but it is recommended to examine the characteristics of the whole benthic community (biodiversity) in order to confirm organic enrichment and pollution. The presence of Thyasira sarsi together with low biodiversity is a good indicator of organic enrichment. High thyasirid species diversity might be indicative of good environmental conditions. Further research should be conducted to better define the ecological preferences of thyasirid species, as some might be indicators of good environmental conditions, and the capability of Thyasira sarsi as an environmental engineer should be readily exploited. Acknowledgements We extend our gratitude towards Graham Oliver, Anders Warén, and Per Johannessen for help with identification. Karin Pittman is thanked for valuable comments on the manuscript. The work was funded by a student grant from the department of biology, University of Bergen, Norway (Marine Biodiversity research group). References Anonymous, 1980. Norwegian Standard NS 4764. Water analysis. Total residue and total fixed residue in water, sludge and sediment. Norsk Standardiseringsforbund. Barry, P.J., McCormack, G.P., 2007. Two new species of Adontorhina Berry, 1947 (Bivalvia: Thyasiridae) from the Porcupine Bank, off the west coast of Ireland. Zootaxa 1526, 37–49. Bertness, M.D., Gaines, S.D., Hay, M., 2001. Marine Community Ecology. Sinauer Associates Inc. Botnen, H., Heggøy, E., Vassenden, G., Johansen, P.-O., Johannessen, P.J., 2002. ‘‘Byfjordsundersøkelsen’’ overvåking av fjordene rundt Bergen – miljøundersøkelse i 2001. IFM Rapport 5, 1–158. Botnen, H.B., Vassenden, G., Hjohlman, S., Johansen, P.-O., Johannessen, P.J., 2000. ‘‘Byfjordundersøkelsen’’ overvåking fjordene rundt Bergen – miljøundersøkelse i 2000. IFM Rapport 13, 1–155. Buchanan, J.B., 1984. Sediment analysis. In: Holme, N.A., McIntyre, A.D. (Eds.), Methods for the Study of Marine Benthos. Blackwell Scientific Publications, Oxford, pp. 41–65. Clark, R.B., 2003. Marine Pollution, fifth ed. Oxford University Press. Dando, P.R., Ridgway, S.A., Spiro, B., 1994. Sulphide ‘mining’ by lucinid bivalve molluscs: demonstrated by stable sulphur isotope measurements and experimental models. Mar. Ecol. Prog. Ser. 107, 169–175. Dando, P.R., Southward, A.J., Southward, E.C., 2004. Rates of sediment sulphide oxidation by the bivlave mollusc Thyasira sarsi. Mar. Ecol. Prog. Ser. 208, 181– 187. Dando, P.R., Spiro, B., 1993. Varying nutritional dependence of the thyasirid bivalves Thyasira sarsi and T. equalis on chemo-autotrophic symbiontic bacteria, demonstrated by isotope ratios of tissue carbon and shell carbonate. Mar. Ecol. Prog. Ser. 92, 151–158. Dufour, S.C., 2005. Gill Anatomy and the Evolution of Symbiosis in the Bivalve Family Thyasiridae. Biol. Bull. 208, 200–212. Dufour, S.C., Felbeck, H., 2003. Sulphide mining by the superextensile foot of symbiotic thyasirid bivalves. Nature 426, 65–67. Erlandsson, C.P., 2008. Vertical transport of particulate organic matter regulated by fjord topography. J. Geophys. Res. 113, 1–13. Heggøy, E., Botnen, H., Vassenden, G., Johannessen, P., 2004a. Marinbiologisk miljøundersøkelser i Lundevågen-Humlevik, Tysnesvik-Gjerdsvik, SøreidvikBeltestadvågen og Gripnesvågen, Tysnes kommune 2004. IFM Rapport 5, 1–60. Heggøy, E., Vassenden, G., Botnen, H., Johannessen, P., 2004b. Inbiologisk miljøundersøkelse ved fusa Fiskeanlegg AS i Sævareidfjorden, Fusa kommune i 2004. IFM Rapport 7, 1–36. Heggøy, E., Johansen, P.-O., Halvorsen, G.A., Vassenden, G., Botnen, H., Johannessen, P., 2005a. Miljøundersøking i Lindås Kommune i 2004. Vestbio 3, 1–105. Heggøy, E., Johansen, P.-O., Vassenden, G., Botnen, H., Johannessen, P., 2005b. ‘‘Byfjordundersøkelsen’’ – overvåking av Fjordene Rundt Bergen i 2004. Vestbio 6, 1–194. Heggøy, E., Vassenden, G., Johannessen, P.J., 2005c. Marinbiologisk miljøundersøkelse av resipienter i Os kommune i 2005. Vestbio 8, 1–61. Heggøy, E., Vassenden, G., Johannessen, P.J., 2007. Marinbiologisk miljøundersøkelse av resipienter i Os kommune i 2006. Vestbio 1, 1–110. Hjohlman, S., Botnen, H., Johannessen, P.J., 2000. Resipientundersøkelse i Eggesbøstraumen, Herøy kommune, i 2000. IFM Rapport 12, 1–73. Hovgaard, P., 1973. A new system of sieves for benthic samples. Sarsia 53, 15–18. Johannessen, P.J., Risheim, I., Botnen, H.B., 1991. ‘‘Byfjordsundersøkelsen’’ overvåking av fjordene rundt Bergen 1990. IFM Rapport 11, 1–108. Johansen, P.-O., Hjohlman, S., Botnen, H.B., Johannessen, P.J., 2000. Overvåking av Statoil’s raffineri på Mongstad i 2000. IFM Rapport 9, 1–108. Johansen, P.-O., Vassenden, G., Botnen, H., Johannessen, P.J., 2001a. Undersøkelser av miljøforholdene ved Mjelstad restdeponi på Osterøy i 2001. IFM Rapport 18, 1–56.
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