ICES Journal of Marine Science: Journal du Conseil Advance Access originally published online on July 18, 2008
ICES Journal of Marine Science: Journal du Conseil 2008 65(8):1428-1435; doi:10.1093/icesjms/fsn116
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This article appears in the following ICES Journal of Marine Science issue: Marine Environmental Indicators: Utility in Meeting Regulatory Needs [View the issue table of contents]
The use of meiofauna diversity as an indicator of pollution in harbours
1 Department for the Study of Territory and Its Resources (DIPTERIS), University of Genoa, Corso Europa 26, 16132 Genoa, Italy
2 Department of Biology (DIBIO), University of Genoa, Viale Benedetto XV, 16132 Genova, Italy
Correspondence to M. Moreno: tel: +39 010 353 8069; fax: +39 010 353 8066; e-mail: moreno{at}dipteris.unige.it
Moreno, M., Vezzulli, L., Marin, V., Laconi, P., Albertelli, G., and Fabiano, M. 2008. The use of meiofauna diversity as an indicator of pollution in harbours. – ICES Journal of Marine Science, 65: 1428–1435.We assessed several meiofaunal indices in sediments of three Mediterranean harbours differing in environmental contamination to evaluate their usefulness as indicators of pollution and to identify those that best described environmental quality. In general, indicators based on meiofaunal taxa demonstrated a significant correlation with the concentration of contaminants, especially the polycyclic aromatic hydrocarbons (PAHs). Nematode genus-based indicators correlated with contaminant concentrations at similar levels of significance, suggesting that a high taxonomic resolution does not improve the information content of meiofauna diversity indicators for assessing the environmental quality in these harbours. Notably, environmental variables that affect meiofaunal and nematode assemblages (e.g. water depth, grain size, and food sources) demonstrated a low spatial and temporal variability in the harbours investigated and did not represent important confounding factors. We conclude that the application of meiofaunal and nematode indices can be a useful tool for assessing the environmental quality of harbour ecosystems.
Keywords: environmental indicators, harbour, meiofauna, nematodes
Received 23 November 2007; accepted 13 May 2008; advance access publication 18 July 2008.
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Introduction |
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Harbours, as a major interface between coastal cities and the sea, are often under heavy pressure from human activities and increasingly suffer from environmental risks linked to poor water and sediment quality (Estacio et al., 1997). These risks may be associated with the presence of toxic contaminants and/or with hypertrophy caused by the high input of organic-matter concentrations and the associated development of anoxia and bad odours. Typically, environmental disturbance in harbours varies considerably over small spatial scales, owing to various factors including the location and magnitude of pollution sources, river inputs, tidal regime, and water circulation (Moreno et al., 2008).
To improve the ecological status of harbour ecosystems, management must first be informed, through monitoring programmes, about the spatial variation in water and sediment quality. This type of knowledge can be enhanced through the use of environmental indicators that can be related to the pressure put upon these systems. The introduction of biological features in the assessment of environmental quality is an innovation of recent monitoring programmes, as required by the Water Framework Directive (WFD) of the European Union (2000/60/EC). Benthic communities are commonly considered to be sensitive to local pressure, because they should reflect an integrated response over time. In the WFD, specific indicators that reflect the abundance and diversity of macrofauna organisms have been proposed for assessing environmental quality of coastal systems (Borja et al., 2000; Simboura and Zenetos, 2002). However, in enclosed and stressed systems such as harbours, macrobenthic organisms are generally scarce and difficult to sample representatively, thereby providing little information that can be used effectively. In contrast, meiofaunal organisms appear to represent the only major metazoan component of the fauna in harbour sediments (Fichet et al., 1999). Moreover, because these small and abundant organisms are bound to the sediment throughout their life history (Suderman and Thistle, 2003) and are often sensitive to many toxicants (Coull and Chandler, 1992; Long, 1992; Guo et al., 2001), they are considered to be good candidate organisms for environmental quality assessment of harbours (e.g. Amjad and Gray, 1983; Lambshead, 1984; Shiells and Anderson, 1985; Lampadariou et al., 1997; Fichet et al., 1999; Suderman and Thistle, 2003; Vezzulli et al., 2003; Moreno et al., 2008).
We tested a number of widely used indicators on meiofauna and nematodes in sediments of three Mediterranean harbours that suffer different levels of pollution. The Shannon–Wiener diversity index (H’), Pielou evenness index (J’), the number of taxa/genera (S), the maturity index (MI), and the index of trophic diversity (ITD) were measured at different stations and during different periods in relation to the concentration and typology of the main environmental contaminants. Our main objective was to evaluate the use of meiofauna as an indicator of state and pollution effects by identifying the metrics that best describe the environmental quality and its spatial heterogeneity within harbour ecosystems.
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Material and methods |
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Sampling sites
Surface sediment samples (0–2 cm) were collected from the harbours of Genoa-Voltri, Portosole, and Marina degli Aregai, Italy, which are all located in the Ligurian Sea (northwest Mediterranean). Genoa-Voltri is a heavily polluted, commercial harbour covering an area of
34.5 ha with a depth of 7–12 m and sediment composed of fine sand and silt. Samples were collected on four occasions (June, July, and November 2002, and February 2003) at three stations representing the inner part of the harbour (Station I), the middle part (Station M), and the outer part (Station O) close to the open sea (Figure 1a). Portosole and Marina degli Aregai are both tourist marinas with areas of 16 and 18 ha, respectively, and sediment that is dominated by the fine-sand fraction. Portosole is located close to a commercial harbour (Sanremo) and has an average depth of 3–7 m. Marina degli Aregai has a depth of 3–12 m. In both harbours, samples were collected on two occasions (July 2005 and January 2006) at four stations (Stations 1–4; Figure 1b and c).
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At each station, six PVC-core (inner diameter, 3.6 cm) sediment samples were taken by scuba divers, three for the analysis of contaminants [protein, heavy metals, and polycyclic aromatic hydrocarbons (PAHs)] and three for meiofauna and nematodes. Heavy-metal concentrations were not determined for Genoa-Voltri. A detailed description of methods and results regarding contaminants can be found in Salvo et al. (2005), Fabiano et al. (2006), and Moreno et al. (2006, 2008). A summary of the results is presented in Table 1.
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Meiofauna
Samples were fixed with 4% buffered formaldehyde in filtered seawater. In the laboratory, all meiofaunal samples were rinsed with a gentle jet of fresh water over a 0.5 mm sieve to exclude macrofauna, decanted over a 38 µm sieve ten times, centrifuged three times with Ludox HS40 (specific density 1.18; Heip et al., 1985), and stained with Rose Bengal. Meiofauna were counted and identified at the major taxon level, using a stereomicroscope, and density was recalculated as abundance 10 cm–2. Diversity indices (H’, J’, and S) were calculated using the Primers routine (Clarke and Warwick, 1994). The nematode (Ne)–copepod (Co) ratio was also analysed, considering all (Ne:Co; Raffaelli and Mason, 1981) and epistrate-feeding nematodes only (Ne2A:Co; Warwick, 1981).
Nematodes
Nematodes were analysed from the surface layers (0–2 cm) of the three replicate cores. The first 100 nematodes were picked out using a fine pin under a stereomicroscope (magnification x40), transferred from formalin to glycerol through a series of ethanol–glycerol solutions, and mounted on slides in anhydrous glycerine, following the procedure described by Heip et al. (1985). Nematodes were identified at the genus level, using the pictorial keys of Platt and Warwick (1983, 1988), Warwick et al. (1998), and Steyaert et al. (2005). Diversity indices (H’, J’, and S) were calculated as for meiofauna. Nematode genera were also classified according to Wieser (1953) into four feeding groups to investigate the trophic structure of the community: selective (1A) and non-selective (1B) deposit-feeders, epistrate-feeders (2A), and predators/omnivores (2B). The ITD was calculated according to Heip et al. (1985), ranging from 0.25 (highest trophic diversity) to 1.0 (lowest trophic diversity). The MI uses the classification of nematode genera into "colonizers" (c; organisms with a high tolerance to disturbance events) and "persistents" (p; organisms with little colonizing capability and low tolerance of disturbance events). Based on their specific characteristics, all nematode genera have been distributed on a c–p scale ranging from 1 (for extreme colonizers) to 5 (for extreme persistent genera). MI was calculated as the weighted average of the c–p values of the individual genera according to Bongers et al. (1991).
Statistical analyses
Analysis of variance (ANOVA) was used to investigate whether or not the differences in abundance of meiofauna and nematodes among sampling stations and sampling times were significant. Before the analysis, normality of data was checked and, when necessary, data were transformed appropriately. The homogeneity of variance was assessed by Cochran’s test. Pearson's correlation analysis was carried out to test correlation among various indices and contaminant concentration.
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Results |
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Meiofauna
Total meiofaunal density in Genoa-Voltri harbour revealed significant differences between stations, with higher average densities at Station I (1403 ± 658 ind. 10 cm–2) than at Stations O and M (641 ± 410 and 290 ± 214 ind. 10 cm–2, respectively; ANOVA, p < 0.05). Assemblage structure was similar across stations, with a clear dominance of nematodes (on average 52%; Table 2). S, H’, and J’ were lower at Station M than at the other stations, although the Ne–Co and Ne2A–Co ratios were higher (Table 3).
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The Portosole marina revealed high densities of meiofauna, ranging from 1429 ± 83 (Station 1) to 2423 ± 146 ind. 10 cm–2 (Station 2), with no significant differences detected between stations (ANOVA). The meiofauna were dominated by nematodes (on average, 73%; Table 2). H’ and J’ indices were lower at the outer Station 4, although S was lower at the inner Station 1 (Table 3). The Ne–Co and Ne2A–Co ratios were higher at Stations 1 and 4.
Meiofaunal densities of Marina degli Aregai were highest at Station 2 in January (3288 ± 2185 ind. 10 cm–2) and lowest at Station 3 in July (338 ± 6 ind. 10 cm–2; ANOVA, p < 0.05). The taxa composition of the community is given in Table 2. H’ and J' indices revealed lower values at Station 3 and higher values at Station 4. In contrast, the higher S was found at Station 3. The Ne–Co and Ne2A–Co ratios revealed higher values at Station 3 and the lowest values at Station 4 (Table 3).
Clearly, there were no consistent trends in the various indicator values along the inner–outer gradient in any of the harbours. However, the three biodiversity indices (H’, J’, and S) were negatively correlated with the concentrations of total PAHs (p < 0.05), and S was positively correlated with the redox potential (Eh) values at the water–sediment interface, whereas all correlations with heavy metals were not significant (see Table 6 later). In contrast, the Ne–Co and Ne2A–Co ratios revealed a significant positive correlation with total heavy-metal concentrations, with Pb specifically, and with PAHs. Although no significant correlation was found between biodiversity indices and protein concentrations for all pooled data, a negative correlation was found for H’ and S in Genoa-Voltri harbour (n = 12; p < 0.05).
Nematodes
Nematodes represented the dominant group at all sampling stations, accounting on average for >60% of the total meiofaunal abundance in the three harbours (Table 2).
At Genoa-Voltri, 43 genera belonging to 21 families were identified (Table 4). The diversity indices (H’, J’, and S) were higher at Station O than at the other two stations (Table 5). MI values were similar across stations, with high percentages of nematodes with c–p values of 2 (60%; Table 4). Station I was characterized by a dominance of epistrate-feeders (2A: 46%) and selective-feeders (1A: 33%), Station M by a dominance of epistrate-feeders (2A: 33%), and non-selective-feeders (1B: 31%), whereas at Station O, the trophic groups were more evenly represented by epistrate-feeders (2A: 38%), selective-feeders (1A: 31%), and non-selective-feeders (1B: 28%). Despite these differences in food selection among the three stations, the ITD demonstrated similar values (Table 5).
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The assemblage at Portosole marina was represented by 46 genera belonging to 21 families (Table 4). S was lowest at Station 1 and highest at Station 3, whereas Station 4 displayed lower values of H’ and J’. MI values were similar at Stations 1, 2, and 4, and the minimum was observed at Station 3. In all, 60% of the community was characterized by a c–p value of 2 (Table 5). The dominant trophic group was formed by epistrate-feeders (2A: 59%), followed by non-selective deposit-feeders (1B: 24%; Table 4). The ITD was relatively low at Station 1 as a consequence of the high densities of predators found in July (2B: 27%; Tables 4 and 5).
The assemblage at Marina degli Aregai was characterized by 44 genera belonging to 19 families (Table 4). Station 2 exhibited relatively low values of S, H’, and J’, whereas the highest value of S was recorded at Station 1, and higher values of H’ and J’ were found at Station 3 (Table 5). MI values were consistently lower than at the other harbours at all stations. The dominant trophic group was represented by the non-selective deposit-feeders (1B: 61%), followed by the epistrate-feeders (2A: 23%). ITD was lowest at Station 1 (Table 5).
The H’, J’, and S indices revealed a significant negative correlation with PAHs, and also H’ with heavy metals (Table 6). MI was positively correlated with Pb concentrations, and the ITD index revealed negative correlations with PAHs and Cu concentrations (Table 6).
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Discussion |
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All three meiofaunal taxon-based diversity indicators revealed a significant correlation only with the concentration of PAHs, whereas the two nematode–copepod ratios revealed a correlation with PAHs and with total heavy-metal concentrations, specifically Pb. Although the use of the latter indices in relation to the environmental quality assessment appears to be controversial (Coull et al., 1981; Warwick, 1981; Lambshead, 1984; Shiells and Anderson, 1985), our results suggest that the Ne–Co ratio is potentially useful as an indicator of pollution in harbours. This might be explained by the low variability within and among the harbours studied in the environmental parameters that affect the Ne–Co ratio in coastal marine systems, such as water depth and sediment grain size (Warwick, 1981; Gee et al., 1985), and which therefore did not represent major confounding factors. Also, organic-matter concentrations of protein were relatively high in sediments at all stations (average = 2.5 mg g–1; Table 1), suggesting that food resources did not limit meiofaunal abundance and distribution. The lack of large spatio-temporal changes in food supply might explain the absence of significant correlations between any of the indicators and the concentrations of total protein, which represent the fraction of organic matter available for these benthic consumers (Vezzulli and Fabiano, 2006). Only in Genoa-Voltri harbour has a negative correlation between meiofaunal indices and protein content been found, which might be explained by the high levels of organic enrichment affecting oxygen concentrations in the sediment (Moreno et al., 2008).
The nematode genus-based diversity indicators vs. concentration of PAHs exhibited correlation coefficients that were comparable with those for meiofauna taxon-based indicators (Table 6). Therefore, the application of biodiversity indices based on higher taxonomic resolution does not seem to yield higher discriminatory power in evaluating environmental quality. The correlations with environmental contaminants observed for MI and ITD are difficult to interpret, because their sign is opposite to expectations (Heip et al., 1985; Bongers et al., 1991).
The presence of sensitive or tolerant meiofaunal taxa and nematode genera appears to be particularly informative in highlighting the state of sediment pollution and allows a better assessment of the spatial heterogeneity of environmental disturbance within each harbour. Generally, in heavily polluted sediments characterized by a low redox potential, the total meiofauna abundance was lower, and kinorhynchs and tanaids were absent (Table 2), whereas the nematode assemblage was dominated by the genera Terschellingia spp., Sabatieria spp. (pulchra group), Paracomesoma spp., and Daptonema spp. (Table 4). These nematode genera are typically found in organically rich, muddy sediment (Heip, et al., 1990; Schratzberger et al., 2006) and have been proposed to be representative of a community that is well adapted to disturbed conditions (Vanreusel, 1990). In particular, the genus Sabatieria survives low oxygen and high sulphide concentrations and often persists under conditions that are unsuitable for most other nematode species (Tietjen, 1980; Hendelberg and Jensen, 1993; Steyaert et al., 1999). In contrast, in harbour sediments characterized by lower levels of environmental pollution, meiofaunal abundance was higher, kinorhynchs and tanaids were present (Table 2), and nematodes were dominated by other genera, such as Desmodora spp. and Anticoma spp. (Table 4).
At a local scale, meiofaunal indicators revealed the least correlation with the concentration of contaminants in the least-polluted Marina degli Aregai, probably because of the even spread of the pollution pressure over the four sampling stations at this site. In contrast, most meiofauna and nematode diversity indices, as well as the nematode–copepod ratios at the Portosole marina, performed well in assessing the marked heterogeneity of pollution pressure within the harbour, identifying Stations 1 and 4 as the most polluted (Marin et al., 2008).
We conclude that the application of meiofaunal and nematode indices can be a useful tool for assessing the pollution pressure in harbour ecosystems, as long as there are no confounding factors, such as differences in water depth, grains size, and food sources that critically affect abundance and distribution of these creatures.
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Acknowledgements |
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We thank Tim J. Ferrero (Natural History Museum, London, UK) for help with nematode genus identification. The research was funded by the EU within the LIFE-Environment programme as Project: PHAROS: "Playgrounds, Harbours, and Research of Sustainability" (ENV/IT/00437).
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References |
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-
Amjad S., Gray J. S. Use of the nematode–copepod ratio as an index of organic pollution. Marine Pollution Bulletin (1983) 14:178–180.[CrossRef][Web of Science]
Bongers T., Alkemade R., Yeates G. W. Interpretation of disturbance induced maturity decrease in marine nematode assemblages by means of the maturity index. Marine Ecology Progress Series (1991) 76:135–142.[CrossRef][Web of Science]
Borja A., Franco J., Pérez V. A marine biotic index to establish the ecological quality of soft bottom benthos within European estuarine and coastal environments. Marine Pollution Bulletin (2000) 40:1100–1114.[CrossRef][Web of Science]
Clarke K. R., Warwick R. M. Change in Marine Communities: An Approach to Statistical Analysis and Interpretation. (1994) Plymouth, UK: Plymouth Marine Laboratory. 1–144.
Coull B. C., Chandler G. T. Pollution and meiofauna: field, laboratory and mesocosm studies. Oceanography and Marine Biology: an Annual Review (1992) 30:191–271.
Coull B. C., Hicks G. R. F., Wells J. B. J. Nematode-copepod ratios for monitoring pollution: a rebuttal. Marine Pollution Bulletin (1981) 12:378–381.[CrossRef][Web of Science]
Estacio F. J., García-Adiego E. M., Fa D. A., García-Gómez J. C., Daza J. L., Hortas F., Gómez-Ariza J. L. Ecological analysis in a polluted area of Algeciras Bay (southern Spain): external "versus" internal outfalls and environmental implications. Marine Pollution Bulletin (1997) 34:780–793.[CrossRef][Web of Science]
Fabiano M., Marin V., Moreno M., Paoli C., Vassallo P., Vezzulli L. Assessment of the environmental status of marina’s water and sediments. In: Guidelines: Environmental Quality and Tourism Development at a Local Level: New Ways Towards Governance (2006) LIFE04 ENV/IT/00437 Project: PHAROS. 40–46. http://www.lifepharos.it.
Fichet D., Boucher G., Radenac G., Miramand P. Concentration and mobilisation of Cd, Cu, Pb and Zn by meiofauna populations living in harbour sediment: their role in the heavy metal flux from sediment to food web. The Science of the Total Environment (1999) 243:263–272.[CrossRef][Medline]
Gee J. M., Warwick R. M., Schaanning M., Berge J. A., Ambrose W. G. Effects of organic enrichment on meiofaunal abundance and community structure in sublittoral soft sediments. Journal of Experimental Marine Biology and Ecology (1985) 91:247–262.[CrossRef][Web of Science]
Guo Y., Somerfield P. J., Warwick R. M., Zhang Z. Large-scale patterns in the community structure and biodiversity of the free living nematodes in the Bohai Sea, China. Journal of the Marine Biological Association of the UK (2001) 81:755–763.[CrossRef]
Heip C., Huys R., Vincx M., Vanreusel A., Smol N., Herman R., Herman P. M. J. Composition, distribution, biomass and production of North Sea meiofauna. Netherlands Journal of Sea Research (1990) 26:333–342.
Heip C., Vincx M., Vraken G. The ecology of marine nematodes. Oceanography and Marine Biology: an Annual Review (1985) 23:399–489.
Hendelberg M., Jensen P. Vertical distribution of the nematode fauna in coastal sediment influenced by seasonal hypoxia in the bottom water. Ophelia (1993) 37:83–94.[Web of Science]
Lambshead P. J. D. The nematode–copepod ratio. Some anomalous results from the Firth of Clyde. Marine Pollution Bulletin (1984) 15:256–259.[CrossRef][Web of Science]
Lampadariou N., Austen M. C., Robertson N., Vlachonis G. Analysis of meiobenthic community structure in relation to pollution and disturbance in Iraklion harbour, Greece. Vie et Milieu (1997) 47:9–24.
Long E. R. Ranges in chemical concentrations in sediment associated with adverse biological effects. Marine Pollution Bulletin (1992) 24:38–45.[CrossRef][Web of Science]
Marin V., Moreno M., Vassallo P., Vezzulli L., Fabiano M. Development of a multi step indicator-based approach (MIBA) for the assessment of environmental quality of harbours. ICES Journal of Marine Science (2008) 65:1436–1441.
Moreno M., Ferrero T. J., Gallizia I., Vezzulli L., Albertelli G., Fabiano M. An assessment of the spatial heterogeneity of environmental disturbance within an enclosed harbour through the analysis of meiofauna and nematode assemblages. Estuarine, Coastal and Shelf Science (2008) 77:565–576.[CrossRef]
Moreno M., Marin V., Paoli C., Vassallo P., Vezzulli L., Fabiano M. Indicators for the assessment of the environmental status of marina’s water and sediments (in Italian), Technical Annex (CD-ROM). In: Guidelines: Environmental Quality and Tourism Development at a Local Level: New Ways Towards Governance. (2006) LIFE04 ENV/IT/00437 Project: PHAROS. 110. http://www.lifepharos.it/pratiche/porti/fondali/Indicatori.pdf.
Platt H. M., Warwick R. M. A Synopsis of the Free-living Marine Nematodes. Part I. British Enoplids. (1983) Cambridge: Cambridge University Press. 306.
Platt H. M., Warwick R. M. A synopsis of the free-living marine nematodes. In: Part II. British Chromadorids (1988) 38. Brill and Backhuys. 502.
Raffaelli D. G., Mason C. F. Pollution monitoring with meiofauna, using the ratio of nematodes to copepods. Marine Pollution Bulletin (1981) 12:158–163.[CrossRef][Web of Science]
Salvo V. S., Gallizia I., Moreno M., Fabiano M. Fungal communities in PAH-impacted sediments of Genoa-Voltri harbour (NW Mediterranean, Italy). Marine Pollution Bulletin (2005) 50:553–559.[Web of Science][Medline]
Schratzberger M., Warr K., Rogers S. I. Patterns of nematode populations in the southwestern North Sea and their link to other components of the benthic fauna. Journal of Sea Research (2006) 55:113–127.[Medline]
Shiells G. M., Anderson K. J. Pollution monitoring using the nematode–copepod ratio. A practical application. Marine Pollution Bulletin (1985) 16:62–68.[CrossRef][Web of Science]
Simboura N., Zenetos A. Benthic indicators to use in ecological quality classification of Mediterranean soft bottom marine ecosystems, including a new biotic index. Mediterranean Marine Science (2002) 3:77–111.[Medline]
Steyaert M., Deprez T., Raes M., Bezerra T., Demesel I., Derycke S., Desmet G., et al. Electronic key to the free-living marine Nematodes. (2005) http://nemys.ugent.be/.
Steyaert M., Gamer N., Van Gansbeke D., Vincx M. Nematode communities from the North Sea: environmental controls on species diversity and vertical distribution within the sediment. Journal of the Marine Biological Association of the UK (1999) 79:253–264.[CrossRef]
Suderman K., Thistle D. Spills of fuel oil #6 and orimulsion can have indistinguishable effects on the benthic meiofauna. Marine Pollution Bulletin (2003) 46:49–55.[CrossRef][Web of Science][Medline]
Tietjen J. H. Population structure and species composition of the free-living nematodes inhabiting sands on the New York Bight Apex. Estuarine Coastal Marine Science (1980) 10:61–73.[CrossRef]
Vanreusel A. Ecology of the free-living marine nematodes from the Voordelta (Southern Bight of the North Sea): I. Species composition and structure of the nematodes communities. Les Cahiers de Biologie Marine (1990) 31:439–462.
Vezzulli L., Fabiano M. Sediment biochemical and microbial variables for the evaluation of trophic status along the Italian and Albanian Continental Shelves. Journal of the Marine Biological Association of the UK (2006) 86:27–37.[CrossRef]
Vezzulli L., Fabiano M., Granelli V., Moreno M. Influence of large spectrum environmental contamination on the micro-meiobenthic assemblages in harbour sediments of the Ligurian Sea: (W Mediterranean). Chemistry and Ecology (2003) 19:233–246.[CrossRef]
Warwick R. M. The nematode–copepod ratio and its use in pollution ecology. Marine Pollution Bulletin (1981) 12:329–333.[CrossRef][Web of Science]
Warwick R. M., Platt H. M., Somerfield P. J. A Synopsis of the Free-Living Marine Nematodes. In: Part III. Monhysterids (1998) 53. Field Studies Council. 296.
Wieser W. Die Beziehung zwischen Mundhöhlengestalt, Ernährungsweise und Vorkommen bei freilebenden marinen Nematoden. Eine ökologisch-morphologische Studie. Arkiv Zoologie (1953) 4:439–484.
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