Diversity and community structure of harpacticoid copepods associated with cold-water coral substrates in the Porcupine Seabight (North-East Atlantic)
© Springer-Verlag and AWI 2009
Received: 12 March 2009
Accepted: 2 July 2009
Published: 1 August 2009
The influence of microhabitat type on the diversity and community structure of the harpacticoid copepod fauna associated with a cold-water coral degradation zone was investigated in the Porcupine Seabight (North-East Atlantic). Three substrate types were distinguished: dead fragments of the cold-water coral Lophelia pertusa, skeletons of the glass sponge Aphrocallistes bocagei and the underlying sediment. At the family level, it appears that coral fragments and underlying sediment do not harbour distinctly different assemblages, with Ectinosomatidae, Ameiridae, Pseudotachidiidae, Argestidae and Miraciidae as most abundant. Conclusions on assemblage structure and diversity of the sponge skeletons are limited as only two samples were available. Similarity analysis at species level showed a strong variation in the sediment samples, which did not harbour a distinctly different assemblage in opposition to the coral and sponge samples. Several factors (sediment infill on the hard substrates, mobility of the copepods, limited sample sizes) are proposed to explain this apparent lack of a distinct difference between the microhabitats. Coral fragments and sediment were both characterised by high species diversity and low species dominance, which might indicate that copepod diversity is not substantially influenced by hydrodynamical stress. The additive partitioning of species diversity showed that by adding locations species richness was greatly enhanced. The harpacticoid community in the cold-water coral degradation zone is highly diverse and includes 157 species, 62 genera and 19 families. Information from neighbouring soft-bottom regions is necessary to assess whether total species diversity is increased by the presence of these complex habitat-providing substrates.
Cold-water corals are arguably the most three-dimensionally complex habitats in the deep ocean, providing niches for many species (Roberts et al. 2006). Virtually all studies on cold-water coral reefs show that they sustain diverse macro- and megafaunal communities and that their biodiversity rivals the diversity of tropical zooxanthellate coral reefs (Rogers 1999; Henry and Roberts 2007; Roberts et al. 2008). Moreover, highest-diversity communities have been found within the dead and mixed live and dead coral framework of Lophelia pertusa (Linnaeus, 1758) reefs (Jensen and Frederiksen 1992; Mortensen et al. 1995; Freiwald et al. 2002). Potential explanations are that coral associates there find shelter and avoid being harmed or consumed by live coral polyps, the decreased competition with L. pertusa for suspended particles, or lower removal rates of larvae by L. pertusa (Cordes et al. 2008).
The associated metazoan meiofauna and nematofauna of L. pertusa reef degradation zones have recently been studied by Raes and Vanreusel (2005, 2006) in the Belgica Mound Province of the Porcupine Seabight (North-East Atlantic). Living coral is assumed not to be a suitable substrate for meiofauna, while the dead coral framework provides favourable surfaces especially for the meio-epifauna. Raes and Vanreusel (2006) found significantly different nematode assemblages associated with dead coral fragments, glass sponge skeletons and underlying sediment, and physical disturbance by bottom currents, substrate type, sediment infill and food availability were proposed as important structuring factors.
Harpacticoid copepods are generally the second most abundant taxon after the numerical dominant Nematoda in the deep-sea meiobenthos, and become even more important on the hard biogenic substrates of the cold-water coral degradation zone (Raes and Vanreusel 2005). The present study therefore investigates the associated harpacticoids of these L. pertusa reef degradation zones in the Belgica Mound Province. The spatial heterogeneity of biologically produced structures has already been suggested to affect distribution patterns of deep-sea harpacticoid species (Thistle and Eckman 1990), and we will examine here the importance of the different microhabitats of the coral degradation zone (i.e. dead fragments of L. pertusa, skeletons of the glass sponge Aphrocallistes bocagei Schultze, 1886 and underlying sediment) in structuring harpacticoid community composition and diversity. Furthermore, as the coral degradation zone undoubtedly represents great habitat heterogeneity, we will assess whether total species diversity is higher there than in the surrounding soft-bottom deep sea. A detailed account of the species composition in this coral degradation zone has been presented by Gheerardyn et al. (2009).
Materials and methods
Study area and sampling procedure
Depth, date, geographical position, and microhabitats sampled per boxcorer taken at the Porcupine Seabight, with harpacticoid density (as individuals/10 cm2 ± SD for sediment samples and individuals/100 ml for coral and sponge samples)
19 ± 7
4 ± 3
Granulometric characteristics of the underlying sediment at the coral degradation zone (data for box 1 and 2 are not available)
Median grain size (μm)
In the laboratory, each coral or sponge sample was rinsed thoroughly over 1 mm and 32 μm sieves to collect macro- and meiofauna, respectively. Volumes of all examined biogenic substrates were measured by immersion, as a proxy for surface area. Meiofauna from the sediment was extracted by density gradient centrifugation, using Ludox HS40 (specific density 1.18) as a flotation medium (Heip et al. 1985). Because sample volumes of the different substrate types could not readily be compared, per sample the first 200 randomly encountered copepods (or all copepods when less than 200 were present) were picked out and mounted in glycerine. All adult harpacticoids were identified to species using Lang (1948, 1965), Huys et al. (1996), Boxshall and Halsey (2004) and original species descriptions. Assignment of species to genera and families was in accordance with recent literature. The systematic status of Pseudotachidiidae Lang, 1936 and Rhynchothalestridae Lang, 1948 follows Willen (2000), the status of Miraciidae Dana, 1846 follows Willen (2000, 2002), and the status of Idyanthidae Lang, 1944, Neobradyidae Olofsson, 1917, and Zosimidae Seifried, 2003 follows Seifried (2003).
The non-parametric procedures multidimensional scaling (MDS) two-dimensional plot and one-way and two-way crossed analysis of similarity (ANOSIM) were used to compare sample similarity based on species composition (Clarke and Gorley 2001). Per boxcorer, copepods from the three sedimentcores were pooled and treated as one sediment sample. Per sample, data were standardised to relative abundance data and square root transformed prior to analysis. MDS was produced based on Bray–Curtis similarities between samples, calculated using the PRIMER5 software (Clarke and Gorley 2001).
Parametric (ANOVA) analyses of variance were performed with STATISTICA6 software. Bartlett’s and Cochran’s test were used to verify homogeneity of the variances prior to analysis. Rarefaction curves (Sanders 1968), calculated using the methods of Hurlbert (1971), were used to compare species richness. The equitability of the copepod fauna was studied based on species’ abundance distributions as k-dominance curves (Lambshead et al. 1983). The total species diversity (γ, as measured by species richness or a diversity index) found in a collection of samples can be additively partitioned into the average diversity within samples (α) and among samples (β) (Crist et al. 2003). In the present study, β-diversity is subdivided into β1-diversity which is due to the differences in microhabitat and β2-diversity generated by the differences in sampling sites. Additive partitioning of species diversity, as expressed by the Shannon-Wiener index H′ and N0 (Hill 1973), was conducted with PARTITION software (Veech et al. 2002; Crist et al. 2003), including sediment and coral samples.
Total number of Copepoda, Harpacticoida, harpacticoid adults, number of species and average number of adults per species within each sample
Number of harpacticoid adults
Number of species
Average number of adults per species
Harpacticoid community composition
Harpacticoid family composition per microhabitat in the cold-water coral degradation zone, based on pooled samples per microhabitat
Underlying sediment (%)
Coral fragments (%)
Sponge skeletons (%)
Harpacticoid genera (with a relative abundance of minimum 2% in at least one microhabitat) from the cold-water coral degradation zone, per microhabitat
Underlying sediment (%)
Coral fragments (%)
Sponge skeletons (%)
Neobradyidae gen. 1
Tetragonicipitidae gen. 1
Total number of genera
The hard substrates examined here prevented the use of multiple corer, which is considered the best device available for sampling of open-sea, soft-bottom sediments (Bett et al. 1994; Shirayama and Fukushima 1995). In the present study, the boxcorer may have caused sampling bias by washing away loose, light material containing associated fauna and also disturbance by its intrusion through the coral fragments. Considering this, we must be careful in interpreting trends in community structure and diversity based on these boxcorer samples. Nevertheless, the observed abundances in the underlying sediment are of a same order of magnitude as those found at a comparable depth along the nearby northwestern slope of the Porcupine Seabight (33 ± 15 harpacticoids/10 cm2 at 960 m depth, with multiple corer) by Pfannkuche (1985). Strict comparison with densities on the coral fragments and sponge skeletons was impossible because the exact surface area of these substrates had not been defined.
Harpacticoid copepod composition and microhabitat preferences
Although nature and structure of the examined microhabitats are different and the associated faunas likely experience different conditions (e.g. in terms of food supply and physical disturbance) (Raes and Vanreusel 2006), it appears that coral fragments and underlying sediment do not harbour distinctly different harpacticoid assemblages at family level. Five families (Ectinosomatidae, Ameiridae, Pseudotachidiidae, Argestidae and Miraciidae) were clearly abundant in each of the microhabitats. The high abundance of Pseudotachidiidae, and specifically of the mainly deep-sea genus Pseudomesochra, on the sponge skeletons might indicate a preference for this substrate, although the described species of this genus have before been reported exclusively in or on muddy sediments (Willen 1996; Vasconcelos et al. 2008). However, conclusions on the fauna of the sponge skeletons are limited as only two samples were collected. Similarity analysis at species level showed that sediment and (pooled) coral and sponge samples are separable to a limited degree. However, there is strong variation in the composition of the sediment samples, which clearly do not form a clustered group in opposition to the coral and sponge samples. This large variation might be attributed to the low number of individuals collected from the sediment samples, and also to the variation in sediment granulometry.
Especially in the inter- and subtidal, it has been shown that harpacticoids form remarkably specific associations (at familial, and in many cases also at generic and specific level) with particular habitat types (Hicks and Coull 1983). In the present study, there were only slight indications that certain taxa show a preference for a particular substrate. For example, the new species of Tetragonicipitidae, a family known as characteristic in every coarse shell-gravel assemblage (Hicks and Coull 1983), had a distinctly higher abundance in the underlying sediment. Representatives of Ameira and Pseudobradya seemed to show a preference for the (pooled) coral and sponge samples, although these genera are present in most marine habitats (Hicks and Coull 1983). Halophytophilus lopheliae appeared to show a preference for the underlying sediment. However, Halophytophilus and three other ectinosomatid genera with prehensile first legs found in the coral degradation zone (Bradyellopsis, Klieosoma and Peltobradya) generally do not occur in samples of the soft-bottom deep-sea floor (Gheerardyn et al. 2008). Their presence in the deep sea is exceptional and most likely due to the occurrence of the hard substrates of the coral degradation zone. It is conceivable that the prehensile first legs in these taxa permit an epifaunal life style on the hard biogenic substrata (Gheerardyn et al. 2008). Several factors might be responsible in explaining this apparent lack of a distinct difference between the microhabitats. The sediment infill between the coral branches and on the sponge skeletons could attract typical sediment-dwellers, which obscure the presence of true epifaunal taxa. Furthermore, close contact between the upper sediment layer and the overlying epibenthic structure can facilitate exchange of the highly mobile harpacticoids. Copepods typically reside in the upper sediment layers, and many are good swimmers capable of active emergence (Palmer 1988; Walters and Bell 1994; Thistle 2003), a behaviour which has been shown to exist in the deep sea (Thistle et al. 2007). However, high evenness in combination with the limited sample sizes may also be important in explaining the apparent lack of distinctly different assemblages. In deep-sea studies, it is a common problem that low animal abundance and high diversity make it difficult to detect spatial changes in community structure, and this is conceivably an important factor here as well. Nevertheless, as discussed by Gheerardyn et al. (2009), the presence of certain, typically epifaunal taxa indicates that the hard substrates of the coral degradation zone provide an exceptional habitat in the soft-bottom deep sea.
Harpacticoid diversity in the coral degradation zone
The harpacticoid community in the coral degradation zone of the Porcupine Seabight is highly diverse. We identified 157 species, 62 genera and 19 families from 860 individuals, which means that a different species is encountered in one out of every five individuals. Harpacticoids in the deep sea are characterised by high species diversity and low species dominance (Seifried 2004; Rose et al. 2005), and the assemblage in the Porcupine Seabight forms no exception to this. Even more, the value of ES (50) over the complete dataset of the coral degradation zone is 35.3, which is higher than reported values from deep-sea harpacticoid studies at western Atlantic (bathyal sites between Cape Lookout and Bermuda), eastern Pacific (Fieberling Guyot and San Diego Trough) and western Pacific (Sagami Bay) sites (Thistle 1978, 1998; Shimanaga et al. 2004; summarised in Shimanaga et al. (2004)). Contrary herewith, species diversity agrees well with values at comparable depths in the northern Gulf of Mexico (see Fig. 3 in Baguley et al. 2006; ES (30) in the Porcupine Seabight is 23.9). Comparison with values from these studies is, however, restricted because of the geographical and bathymetrical distance between the study sites, and differences in sampling procedure. The coral degradation zone undoubtedly provides a structurally more complex environment than normally encountered in the soft-bottom deep sea. At the moment, it is, however, difficult to assess the influence of this increased habitat complexity on total harpacticoid species diversity, because studies from nearby soft-bottom locations at similar depths are not available.
For the associated nematofauna, Raes and Vanreusel (2006) found that the community in the underlying sediment is significantly more diverse than on the coral fragments and sponge skeletons. They attributed this to increased habitat complexity and heterogeneity of the sediment (due to the presence of small biogenic structures), and higher disturbance by current activity for nematodes on both biogenic substrata. For the associated harpacticoids, it seems that the faunas of both underlying sediment and coral fragments are diverse and do not differ distinctly in terms of evenness. Thistle (1983) provided some evidence that differences in hydrodynamics may be less important for copepod diversity, which would explain this observation. However, because all rarefaction curves tend to converge at low abundances, no distinction between different richness patterns can be drawn if sample sizes are not sufficient (Tipper 1979) and this was likely to be the case with the sediment samples (none contained more than 50 adults). Furthermore, the observation of highest species richness in the underlying sediment (when samples are pooled according to microhabitat) should not be treated as conclusive, because pooling of replicates obscures the actual relationship between number of species and individuals at the sampling scale, and differences in heterogeneity among sites may then contribute to variation in diversity (Levin et al. 2001). The additive partitioning of species diversity showed that by adding locations species richness was greatly enhanced. The Shannon index showed these species to be rare, as most of the diversity was explained by α, which means that the same ‘common’ species occurred across the different locations. β-diversity, due to differences in microhabitat, was rather small as expressed by both measures.
Trends in species composition and diversity of the harpacticoids associated with different substrate types in the coral degradation zone were difficult to assess, mainly because of the rather small size of the sediment samples and the low number of sponge samples. However, first conclusions are that harpacticoid composition and diversity are not distinctly different between coral fragments and underlying sediment. These observations contrast with those of the associated nematofauna, for which distinctly different assemblages on the three microhabitats and clearly different trends in diversity between sediment and overlying biogenic substrates were found (Raes and Vanreusel 2006). Future samplings should focus on the difference between the harpacticoid fauna on cold-water coral mounds and the adjacent off-mound soft-bottom habitat, and take environmental characteristics, the exact surface area and habitat complexity of the biogenic substrates and the amount of sediment infill into account. Still, this study indicates that the substrates of the coral degradation zone sustain a harpacticoid fauna with high species diversity and low species dominance.
The authors want to thank Guy De Smet, Dr. Maarten Raes and Dr. Véronique Vanquickelberghe (Ghent University) for their sampling efforts and Bart Beuselinck, Danielle Schram and Annick Van Kenhove (Ghent University) for meiofauna extraction and granulometric analysis. The first and second authors acknowledge postdoctoral research grants from the Special Research Fund (Ghent University, BOF) and from the Fund for Scientific Research (FWO-Vlaanderen), respectively. This research was conducted within the framework of the HERMIONE project (EC Seventh Framework Research Programme), the national FWO Research Project G.0199.03 ‘A Comparative Study of the Meio-Epifauna Associated with Tropical and Cold-Water Coral Reefs’, the UGent-BOF-GOA research project 01GZ0705 ‘Biogeography and Biodiversity of the Sea’ and the MarBEF Network of Excellence ‘Marine Biodiversity and Ecosystem Functioning’, which is funded by the Sustainable Development, Global Change and Ecosystems Programme of the European Community’s Sixth Framework Programme (contract no. GOCE-CT-2003-505446). Prof. Dr. Jean-Pierre Henriet and co-workers from the Renard Centre of Marine Geology, as well as the crew of the R.V. Belgica, are acknowledged for a successful collaboration. Dr. D. Van Rooij is kindly thanked for making the map of the Porcupine Seabight.
- Baguley JG, Montagna PA, Lee W, Hyde LJ, Rowe GT (2006) Spatial and bathymetric trends in Harpacticoida (Copepoda) community structure in the northern Gulf of Mexico deep-sea. J Exp Mar Biol Ecol 330:327–341View ArticleGoogle Scholar
- Bett JB, Vanreusel A, Vincx M, Soltwedel T, Pfannkuche O, Lambshead PJD, Gooday AJ, Ferrero T, Dinet A (1994) Sampler bias in the quantitative study of deep-sea meiobenthos. Mar Ecol Prog Ser 104:197–203View ArticleGoogle Scholar
- Boxshall GA, Halsey SH (2004) Copepod orders and families. An introduction to Copepod diversity. Ray Society, LondonGoogle Scholar
- Clarke KR, Gorley RN (2001) PRIMER v5: User Manual/Tutorial. PRIMER-E, PlymouthGoogle Scholar
- Cordes EE, McGinley MP, Podowski EL, Becker EL, Lessard-Pilon S, Viada ST, Fisher CR (2008) Coral communities of the deep Gulf of Mexico. Deep-Sea Res Part I 55:777–787View ArticleGoogle Scholar
- Crist TO, Veech JA, Gering JC, Summerville KS (2003) Partitioning species diversity across landscapes and regions: a hierarchical analysis of α, β, and γ diversity. Am Nat 162:734–743View ArticlePubMedGoogle Scholar
- De Mol B (2002) Development of coral banks in Porcupine Seabight (SW Ireland): a multidisciplinary approach. PhD dissertation, Ghent UniversityGoogle Scholar
- De Mol B, Van Rensbergen P, Pillen S, Van Herreweghe K, Van Rooij D, McDonnell A, Huvenne V, Ivanov M, Swennen R, Henriet JP (2002) Large deep-water coral banks in the Porcupine Basin, southwest of Ireland. Mar Geol 188:193–231View ArticleGoogle Scholar
- Freiwald A, Hühnerbach V, Lindberg B, Wilson JB, Campbell J (2002) The Sula Reef complex, Norwegian shelf. Facies 47:179–200View ArticleGoogle Scholar
- Gheerardyn H, De Troch M, Vincx M, Vanreusel A (2009) Harpacticoida (Crustacea: Copepoda) associated with cold-water coral substrates in the Porcupine Seabight (NE Atlantic): species composition, diversity and reflections on the origin of the fauna. Sci Mar (in press)Google Scholar
- Gheerardyn H, Seifried S, Vanreusel A (2008) A new species of Halophytophilus Brian, 1919 (Copepoda: Harpacticoida: Ectinosomatidae) from cold-water corals in the Porcupine Seabight (NE Atlantic). Zootaxa 1761:1–16Google Scholar
- Heip C, Vincx M, Vranken G (1985) The ecology of marine nematodes. Oceanogr Mar Biol Annu Rev 23:399–489Google Scholar
- Henriet JP, De Mol B, Pillen S, Vanneste M, Van Rooij D, Versteeg W, Croker PF, Shannon PM, Unnithan V, Bouriak S, Chachkine P (1998) Gas hydrate crystals may help build reefs. Nature (Lond) 391:648–649View ArticleGoogle Scholar
- Henry L-A, Roberts JM (2007) Biodiversity and ecological composition of macrobenthos on cold-water coral mounds and adjacent off-mound habitat in the bathyal Porcupine Seabight, NE Atlantic. Deep-Sea Res Part I 54:654–672View ArticleGoogle Scholar
- Hicks GRF, Coull BC (1983) The ecology of marine meiobenthic harpacticoid copepods. Oceanogr Mar Biol Annu Rev 21:67–175Google Scholar
- Hill MO (1973) Diversity and evenness: a unifying notation and its consequences. Ecology 54:427–432View ArticleGoogle Scholar
- Hurlbert SH (1971) The nonconcept of species diversity: a critique and alternative parameters. Ecology 52:577–586View ArticleGoogle Scholar
- Huys R, Gee JM, Moore CG, Hamond R (1996) Marine and brackish water harpacticoid copepods. Part 1. Synopses of the British Fauna (New Series), vol 51. Field Studies Council, ShrewsburyGoogle Scholar
- Jensen A, Frederiksen R (1992) The fauna associated with the bank-forming deepwater coral Lophelia pertusa (scleractinaria) on the Faroe shelf. Sarsia 77:53–69Google Scholar
- Lambshead PJD, Platt HM, Shaw KM (1983) The detection of differences among assemblages of marine benthic species based on an assessment of dominance and diversity. J Nat Hist 17:859–874View ArticleGoogle Scholar
- Lang K (1948) Monographie der Harpacticiden, I & II. Håkan Ohlssons Boktryckeri, LundGoogle Scholar
- Lang K (1965) Copepoda Harpacticoidea from the Californian Pacific coast. Kungl Svenska Vetensk Akad Hand 10:1–560Google Scholar
- Levin LA, Etter RE, Rex MA, Gooday AJ, Smith CR, Pineda J, Stuart CT, Hessler RR, Pawson D (2001) Environmental influences on regional deep-sea species diversity. Annu Rev Ecol Syst 32:51–93View ArticleGoogle Scholar
- Mortensen PB, Hovland M, Brattegard T, Farestveit R (1995) Deep water bioherms of the scleractinian coral Lophelia pertusa (L.) at 64°N on the Norwegian shelf: structure and associated megafauna. Sarsia 80:145–158Google Scholar
- Palmer MA (1988) Dispersal of marine meiofauna: a review and conceptual model explaining passive transport and active emergence with implications for recruitment. Mar Ecol Prog Ser 48:81–91View ArticleGoogle Scholar
- Pfannkuche O (1985) The deep-sea meiofauna of the Porcupine Seabight and abyssal plain (NE Atlantic): population structure, distribution, standing stocks. Oceanol Acta 8:343–353Google Scholar
- Raes M, Vanreusel A (2005) The metazoan meiofauna associated with a coldwater coral degradation zone in the Porcupine Seabight (NE Atlantic). In: Freiwald A, Roberts JM (eds) Cold-water corals and ecosystems. Springer, Berlin Heidelberg, pp 821–847View ArticleGoogle Scholar
- Raes M, Vanreusel A (2006) Microhabitat type determines the composition of nematode communities associated with sediment-clogged cold-water coral framework in the Porcupine Seabight (NE Atlantic). Deep-Sea Res Part I 53:1880–1894View ArticleGoogle Scholar
- Roberts JM, Wheeler AJ, Freiwald A (2006) Reefs of the deep: the biology and geology of cold-water coral ecosystems. Science 312:543–547View ArticlePubMedGoogle Scholar
- Roberts JM, Henry L-A, Long D, Hartley JP (2008) Cold-water coral reef frameworks, megafaunal communities and evidence for coral carbonate mounds on the Hatton Bank, north east Atlantic. Facies 54:297–316View ArticleGoogle Scholar
- Rogers AD (1999) The biology of Lophelia pertusa (Linnaeus 1785) and other deep-water reef-forming corals and impacts from human activities. Internat Rev Hydrobiol 84:315–406Google Scholar
- Rose A, Seifried S, Willen E, George KH, Veit-Köhler G, Bröhldick K, Drewes J, Moura G, Martínez Arbizu P, Schminke HK (2005) A method for comparing within-core alpha diversity values from repeated multicorer samplings, shown for abyssal Harpacticoida (Crustacea: Copepoda) from the Angola Basin. Org Divers Evol 5:3–17View ArticleGoogle Scholar
- Sanders HL (1968) Marine benthic diversity: a comparative study. Am Nat 102:243–282View ArticleGoogle Scholar
- Seifried S (2003) Phylogeny of Harpacticoida (Copepoda): revision of “Maxillipedasphalea” and Exanechentra. Cuvillier, GöttingenGoogle Scholar
- Seifried S (2004) The importance of a phylogenetic system for the study of deep-sea harpacticoid diversity. Zool Stud 43:435–445Google Scholar
- Shimanaga M, Kitazato H, Shirayama Y (2004) Temporal patterns in diversity and species composition of deep-sea benthic copepods in bathyal Sagami Bay, central Japan. Mar Biol 144:1097–1110View ArticleGoogle Scholar
- Shirayama Y, Fukushima T (1995) Comparisons of deep-sea sediments and overlying water collected using multiple corer and box corer. J Oceanogr 51:75–82View ArticleGoogle Scholar
- Thistle D (1978) Harpacticoid dispersion patterns: implications for deep-sea diversity maintenance. J Mar Res 36:377–397Google Scholar
- Thistle D (1983) The stability-time hypothesis as a predictor of diversity in deep-sea soft-bottom communities: a test. Deep-Sea Res 30:267–277View ArticleGoogle Scholar
- Thistle D (1998) Harpacticoid copepod diversity at two physically reworked sites in the deep sea. Deep-Dea Res 45:13–24Google Scholar
- Thistle D (2003) Harpacticoid copepod emergence at a shelf site in summer and winter: implications for hydrodynamic and mating hypotheses. Mar Ecol Prog Ser 248:177–185View ArticleGoogle Scholar
- Thistle D, Eckman JE (1990) The effect of a biologically produced structure on the benthic copepods of a deep-sea site. Deep-Sea Res Part I 37:541–554View ArticleGoogle Scholar
- Thistle D, Sedlacek L, Carman KR, Fleeger JW, Barry JP (2007) Emergence in the deep sea: evidence from harpacticoid copepods. Deep-Sea Res Part I 54:1008–1014View ArticleGoogle Scholar
- Tipper JC (1979) Rarefaction and rarefiction—the use and abuse of a method in paleoecology. Paleobiology 5:423–434Google Scholar
- Vasconcelos DM, George KH, Santos PJP (2008) First record of the genus Pseudomesochra T. Scott (Harpacticoida: Pseudotachidiidae) in the South Atlantic with description of a deep-sea species: Pseudomesochra longiseta sp. nov. Zootaxa 1866:337–348Google Scholar
- Veech JA, Summerville KS, Crist TO, Gering JC (2002) The additive partitioning of species diversity: recent revival of an old idea. Oikos 99:3–9View ArticleGoogle Scholar
- Walters DG, Bell SS (1994) Significance of copepod emergence to benthic, pelagic and phytal linkages in a subtidal seagrass bed. Mar Ecol Prog Ser 108:237–249View ArticleGoogle Scholar
- Willen E (1996) Pseudomesochra T. Scott 1902 as a member of the Paranannopidae Por 1986 (Copepoda, Harpacticoida) with a description of three new species. Senckenb Marit 28:81–109View ArticleGoogle Scholar
- Willen E (2000) Phylogeny of the Thalestridimorpha Lang, 1944 (Crustacea, Copepoda). Cuvillier, GöttingenGoogle Scholar
- Willen E (2002) Notes on the systematic position of the Stenheliinae (Copepoda, Harpacticoida) within the Thalestridimorpha and description of two new species from Motupore Island, Papua New Guinea. Cah Biol Mar 43:27–42Google Scholar