Marine Biodiversity

, Volume 39, Issue 1, pp 9–25

Small-scale spatial patterns of meiobenthos in the Arctic deep sea

Original Paper

Abstract

A variety of analytical techniques were used to quantify and describe small-scale (centimetre to decimetre) spatial patterns of meiofauna taxa, with emphasis on nematode species, at a bathyal site in the Arctic deep sea. Three cores (10-cm diameter) taken from the same multicorer were each subsampled as 12 contiguous subcores (1.2-cm diameter) for meiofauna and 16 contiguous subcores (0.9-cm diameter) for bacteria (eight subcores) and phytodetritus (chl a and phaeopigment concentration) (eight subcores). Coefficients of variation and the variance component from PERMANOVA were estimated to compare variability between cores (20–50 cm) versus within cores (≤10 cm). Both methods showed that spatial variation within cores contributed the main part of total heterogeneity for all parameters, while differences between cores were less important. To further investigate distribution patterns at this small scale (≤10 cm), indices of dispersion were calculated and autocorrelation analyses were performed on the complete data set. Abundances of nematodes, nauplii and 65.5% of the nematode species were significantly aggregated at the scale of subcores (2 cm). Nematode species aggregations were discordant on the small scale, suggesting that processes maintaining diversity in the deep sea can be expected to operate at scales smaller than 10 cm. Autocorrelograms suggested that nematode patch sizes were smaller than 4 cm2, while adult harpacticoid copepods and nauplii showed aggregations of ca. 9–25 cm2 and 64 cm2, respectively. Significant spatial autocorrelation at the core scale was also observed for 24 nematode species. These species were grouped in ten different spatial patterns according to their scale of heterogeneity. The spatial patterns observed for the meiobenthos were neither explained by the concentration of chloroplastic pigments nor by bacterial densities. Nevertheless, observations on nematode morphology suggest that morphological characters linked to their locomotion and feeding behaviour may be involved in pattern formation. Finally, our data provide evidence that studies based on few replicates to characterise large-scale or long-term patterns of deep-sea benthic communities may be confounded by inadequate assessment of small-scale variability.

Keywords

Small-scale heterogeneity Spatial distribution Autocorrelogram Deep-sea diversity Meiofauna Nematodes 

References

  1. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46 doi:10.1046/j.1442-9993.2001.01070.x CrossRefGoogle Scholar
  2. Anderson MJ (2005) PERMANOVA: a FORTRAN computer program for permutational multivariate analysis of variance. Department of Statistics, University of Auckland, New ZealandGoogle Scholar
  3. Andrew NL, Mapstone BD (1987) Sampling and the description of spatial patterns in marine ecology. Oceanogr Mar Biol Ann Rev 25:39–90Google Scholar
  4. Barnett PRO, Watson J, Conelly D (1984) A multiple corer for taking virtually undisturbed samples from shelf, bathyal and abyssal sediments. Oceanol Acta 7:399–408Google Scholar
  5. Bell SS, Watzin MC, Coull BC (1978) Biogenic structure and its effects on the spatial heterogeneity of meiofauna in a salt marsh. J Exp Mar Biol Ecol 35:99–107 doi:10.1016/0022-0981(78)90069-2 CrossRefGoogle Scholar
  6. Bergström U, Englund G, Bonsdorff E (2002) Small-scale spatial structure of Baltic Sea zoobenthos – inferring processes from patterns. J Exp Mar Biol Ecol 281:123–136 doi:10.1016/S0022-0981(02)00440-9 CrossRefGoogle Scholar
  7. Bernstein BB, Meador JP (1979) Temporal persistence of biological patch structure in an abyssal benthic community. Mar Biol (Berl) 51:179–183 doi:10.1007/BF00555197 CrossRefGoogle Scholar
  8. Bernstein BB, Hessler RR, Smith R, Jumars PA (1978) Spatial dispersion of benthic Foraminifera in the abyssal Central Pacific. Limnol Oceanogr 23:401–416Google Scholar
  9. Bett BJ, Vanreusel A, Vincx M, Soltwedel T, Pfannkuche O, Lambshead JPD, Gooday AJ, Ferrero T, Dinet A (1994) Sampler bias in the quantitative study of deep-sea meiobenthos. Mar Ecol Prog Ser 104:197–203 doi:10.3354/meps104197 CrossRefGoogle Scholar
  10. Blanchard GF (1990) Overlapping microscale dispersion patterns of meiofauna and microphytobenthos. Mar Ecol Prog Ser 68:101–111 doi:10.3354/meps068101 CrossRefGoogle Scholar
  11. Blome D, Schleier U, Bernem KHV (1999) Analysis of the small-scale spatial patterns of free-living marine nematodes from tidal flats in the East Frisian Wadden Sea. Mar Biol (Berl) 133:717–726 doi:10.1007/s002270050513 CrossRefGoogle Scholar
  12. Chapman MG, Underwood AJ (2008) Scales of variation of gastropod densities over multiple spatial scales: comparison of common and rare species. Mar Ecol Prog Ser 354:147–160 doi:10.3354/meps07205 CrossRefGoogle Scholar
  13. Clarke KR, Green RH (1988) Statistical design and analysis for a ‘biological effects’ study. Mar Ecol Prog Ser 46:213–226 doi:10.3354/meps046213 CrossRefGoogle Scholar
  14. Clarke KR, Chapman MG, Somerfield PJ, Needham HR (2006) Disperson-based weighting of species counts in assemblage analyses. Mar Ecol Prog Ser 320:11–27 doi:10.3354/meps320011 CrossRefGoogle Scholar
  15. Cliff AD, Ord JK (1973) Spatial autocorrelation. Pion, LondonGoogle Scholar
  16. Coull BC, Ellison RL, Fleeger JW, Higgins RP, Hope WD, Hummon WD, Rieger RM, Sterrer WE, Thiel H, Tietjen JH (1977) Quantitative estimates of the meiofauna from the deep sea off North Carolina, USA. Mar Biol (Berl) 39:233–240 doi:10.1007/BF00390997 CrossRefGoogle Scholar
  17. Decho AW, Castenholz RW (1986) Spatial patterns and feeding of meiobenthic harpacticoid copepods in relation to resident microbial flora. Hydrobiol 131:87–96 doi:10.1007/BF00008327 CrossRefGoogle Scholar
  18. Eckman J, Thistle D (1988) Small-scale spatial pattern in meiobenthos in the San Diego Trough. Deep-Sea Res 35:1565–1578 doi:10.1016/0198-0149(88)90103-3 CrossRefGoogle Scholar
  19. Findlay SEG (1981) Small-scale spatial distribution of meiofauna on a mud- and sandflat. Estuar Coast Shelf Sci 12:471–484 doi:10.1016/S0302-3524(81)80006-0 CrossRefGoogle Scholar
  20. Fleeger JW, Palmer MA, Moser EB (1990) On the scale of aggregation of meio-benthic copepods on a tidal mudflat. Marine Ecology 11:227–237CrossRefGoogle Scholar
  21. Fonseca G, Soltwedel T (2007) Deep-sea meiobenthic communities underneath the marginal ice zone off Eastern Greenland. Polar Biol 57:137–145Google Scholar
  22. Fortin MJ, Dale M (2005) Spatial analysis: a guide for ecologists. Cambridge University Press, CambridgeGoogle Scholar
  23. Gage JD (1977) Structure of the abyssal macrobenthic community in the Rockall Trough. In: Keegan BF, Ceidigh PO, Boaden PJS (eds) Biology of benthic organisms. Pergamon Press, OxfordGoogle Scholar
  24. Gallucci F, Netto SA (2004) Effects of the passage of cold fronts over a coastal site: an ecosystem approach. Mar Ecol Prog Ser 281:79–92 doi:10.3354/meps281079 CrossRefGoogle Scholar
  25. Gallucci F, Moens T, Vanreusel A, Fonseca G (2008) Active colonization of disturbed sediments by deep-sea nematodes: Evidence for the patch mosaic model. Mar Ecol Prog Ser 367:173–183 doi:10.3354/meps07537 CrossRefGoogle Scholar
  26. Giere O (1993) Meiobenthology: the microscopic fauna in aquatic sediments. Springer, BerlinGoogle Scholar
  27. Grassle JF, Sanders HL (1973) Life histories and the role of disturbance. Deep-Sea Res 20:643–659Google Scholar
  28. Grossmann S, Reichardt W (1991) Impact of Arenicola marina on bacteria in intertidal sediments. Mar Ecol Prog Ser 77:85–93 doi:10.3354/meps077085 CrossRefGoogle Scholar
  29. Hairston NG (1973) Ecology, selection and systematics. Breviora 414:1–21Google Scholar
  30. Hasemann C (2006) Kleinskalige Heterogentität in der arktischen Tiefsee: Einfluss kleiner Kaltwasser-Schwämme auf die Diversität benthischer Nematoden-Gemeinschaften. Ber Pol- Meeresforsch 527:1–323Google Scholar
  31. Heip C (1975) On the significance of aggregation in some benthic marine invertebrates. In: Harold Barnes (ed) Proceedings of the 9th European Marine Biology Symposium, Aberdeen University Press, Aberdeen, pp 527–538Google Scholar
  32. Heip C, Vincx M, Vranken G (1985) The ecology of marine nematodes. Oceanogr Mar Biol Ann Rev 23:399–489Google Scholar
  33. Hessler RR, Jumars PA (1974) Abyssal community analysis from replicate box cores in the central North Pacific. Deep-Sea Res 21:185–209Google Scholar
  34. Hewitt JE, Legendre P, McArdle BH, Thrush SF, Bellehumeur C, Lawrie SM (1997) Identifying relationships between adult and juvenile bivalves at different spatial scales. J Exp Mar Biol Ecol 216:77–98 doi:10.1016/S0022-0981(97)00091-9 CrossRefGoogle Scholar
  35. Hodda M (1990) Variation in estuarine littoral nematode populations over three spatial scales. Estuar Coast Shelf Sci 30:325–340 doi:10.1016/0272-7714(90)90001-8 CrossRefGoogle Scholar
  36. Hogue EW (1982) Sediment disturbance and the spatial distributions of shallow water meiobenthic nematodes on the open Oregon coast. J Mar Res 40:551–573Google Scholar
  37. Hoste E, Vanhove S, Schewe I, Soltwedel T, Vanreusel A (2007) Spatial and temporal variations in deep-sea meiofauna assemblages in the Marginal Ice Zone of the Arctic Ocean. Deep Sea Res Part I Oceanogr Res Pap 54:109–129 doi:10.1016/j.dsr.2006.09.007 CrossRefGoogle Scholar
  38. Jensen P (1981) Phyto-chemical sensitivity and swimming behaviour of the free-living marine nematode Chromadorita tenuis. Mar Ecol Prog Ser 4:203–206 doi:10.3354/meps004203 CrossRefGoogle Scholar
  39. Jumars PA (1975) Environmental grain and polychaete species diversity in a bathyal benthic community. Mar Biol (Berl) 30:253–266 doi:10.1007/BF00390748 CrossRefGoogle Scholar
  40. Jumars PA (1976) Deep-sea species diversity: does it have a characteristic scale? J Mar Res 34:217–246Google Scholar
  41. Jumars PA (1978) Spatial autocorrelation with RUM (remote underwater manipulator): vertical and horizontal structure of a bathyal benthic community. Deep-Sea Res 25:589–604 doi:10.1016/0146-6291(78)90615-X CrossRefGoogle Scholar
  42. Jumars PA, Eckman JE (1983) Spatial structure within deep-sea benthic communities. In: Rowe GT (ed) The sea. Wiley, New York, pp 399–452Google Scholar
  43. Jumars PA, Thistle D, Jones ML (1977) Detecting two-dimensional spatial structure in biological data. Oecologia 28:109–123 doi:10.1007/BF00345246 CrossRefGoogle Scholar
  44. Lambshead PJD, Boucher G (2003) Marine nematode deep-sea biodiversity—hyperdiverse or hype? J Biogeogr 30:475–485CrossRefGoogle Scholar
  45. Lambshead PJD, Brown CJ, Ferrero TJ, Mitchell NJ, Smith CR, Hawkins LE, Tietjen J (2002) Latitudinal diversity patterns of deep-sea marine nematodes and organic fluxes: a test from the central equatorial Pacific. Mar Ecol Prog Ser 236:129–135 doi:10.3354/meps236129 CrossRefGoogle Scholar
  46. Lee JJ, Tietjen JH, Mastropaolo C, Rubin H (1977) Food quality and the heterogeneous spatial distribution of meiofauna. Helgol Wiss Meeresunters 30:272–282 doi:10.1007/BF02207841 CrossRefGoogle Scholar
  47. Legendre P, Fortin MJ (1989) Spatial pattern and ecological analysis. Vegetatio 80:107–138 doi:10.1007/BF00048036 CrossRefGoogle Scholar
  48. Li J, Vincx M, Herman PMJ, Heip C (1997) Monitoring meiobenthos using cm-, m- and km-scales in the Southern Bight of the North Sea. Mar Environ Res 43:265–278 doi:10.1016/S0141-1136(96)00089-X CrossRefGoogle Scholar
  49. Manly BFJ (1997) Randomization, bootstrap and Monte Carlo methods in biology. Chapman and Hall, LondonGoogle Scholar
  50. McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–297Google Scholar
  51. Meyer-Reil LA (1983) Benthic response to sedimentation events during autumn to spring at a shallow water station in the Western Kiel Bight. Mar Biol (Berl) 77:247–256 doi:10.1007/BF00395813 CrossRefGoogle Scholar
  52. Moens T, Vincx M (1997) Observations on the feeding ecology of estuarine nematodes. J Mar Biol Assoc U K 77:211–227CrossRefGoogle Scholar
  53. Muthumbi AW, Vanreusel A, Duineveld G, Soetaert K, Vincx M (2004) Nematode community structure along the continental slope off the Kenyan coast, Western Indian Ocean. Intern Rev Hydrobiol 89:188–205 doi:10.1002/iroh.200310689 CrossRefGoogle Scholar
  54. Oden NL (1984) Assessing the significance of a spatial correlogram. Geogr Anal 16:1–16Google Scholar
  55. Palmer MA (1984) Invertebrate drift: behavioural experiments with intertidal meiobenthos. Mar Behav Physiol 10:235–253CrossRefGoogle Scholar
  56. Rice AL, Lambshead PJD (1994) Patch dynamics in the deep-sea benthos: the role of a heterogeneous supply of organic matter. In: Giller PS, Hildrew AG, Raffaelli DG (eds) Aquatic ecology: scale, pattern and process. 34th Symposium of the British Ecological Society, Blackwell, Oxford, pp 469–499Google Scholar
  57. Riemann F (1974) On hemisessile nematodes with flagelliform tails living in marine soft bottoms and on microtubes found in deep sea sediments. Mikrofauna Meeresb 40:1–15Google Scholar
  58. Rose A, Seifried S, Willen E, George KH, Veit-Köhler G, Bröhldick K, Drewes J, Moura G, Martinez 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 5:3–17 doi:10.1016/j.ode.2004.10.001 CrossRefGoogle Scholar
  59. Sandulli R, Pickney J (1999) Patch sizes and spatial patterns of meiobenthic copepods and benthic microalgae in sandy sediments: a microscale approach. J Sea Res 41:179–187 doi:10.1016/S1385-1101(98)00048-3 CrossRefGoogle Scholar
  60. Sawada M (1999) ROOKCASE: an Excel 97/2000 Visual basic (VB) add-in for exploring global and local spatial autocorrelation. Bull Ecol Soc Am 80:231–234 doi:10.1890/0012-9623(1999)080[0231:TT]2.0.CO;2 CrossRefGoogle Scholar
  61. Schoener TW (1974) Resource partitioning in ecological communities. Science 185:27–39 doi:10.1126/science.185.4145.27 PubMedCrossRefGoogle Scholar
  62. Schratzberger M, Whomersley P, Warr K, Bolam SG, Rees HL (2004) Colonisation of various types of sediment by estuarine nematodes via lateral infaunal migration: a laboratory study. Mar Biol (Berl) 145:69–78 doi:10.1007/s00227-004-1302-1 CrossRefGoogle Scholar
  63. Shuman FR, Lorenzen CF (1975) Quantitative degradation of chlorophyll by a marine herbivore. Limnol Oceanogr 20:580–586CrossRefGoogle Scholar
  64. Snedecor GW, Cochran WG (1980) Statistical methods, 7th edn. Iowa State University Press, AmesGoogle Scholar
  65. Snelgrove PVR, Smith CR (2002) A riot of species in an environmental calm: the paradox of the species-rich deep-sea floor. Oceanogr Mar Biol Ann Rev 40:322–342Google Scholar
  66. Sokal RR (1979) Ecological parameters inferred from spatial correlograms. In: Patil GP, Rosenzweig ML (eds) Contemporary quantitative ecology and related ecometrics. Statistical Ecology Series, vol. 12. International Co-operative Publishing House, Fairland, pp 167–196Google Scholar
  67. Sokal RR, Wartenberg D (1981) Space and population structure. In: Griffith D, Mckinnon R (eds) Dynamic spatial models. Sijthoff and Noordhoff, Alphen aan den Rijn, pp 186–213Google Scholar
  68. Somerfield PJ, Gage JD (2000) Community structure of the benthos in the Scottish Sea-lochs. IV. Multivariate spatial pattern. Mar Biol (Berl) 136:1133–1145 doi:10.1007/s002270000311 CrossRefGoogle Scholar
  69. Thistle D (1978) Harpacticoid dispersion patterns: implications for deep-sea diversity maintenance. J Mar Res 36:377–397Google Scholar
  70. Thistle D (1979) Harpacticoid copepods and biogenic structures: Implications for deep-sea diversity maintenance. In: Livingstone RJ (ed) Ecological processes in coastal and marine systems. Plenum, New York, pp 217–231Google Scholar
  71. Thistle D (2003) On the utility of metazoan meiofauna for studying the soft-bottom deep sea. Vie Milieu 53:97–101Google Scholar
  72. Thistle D, Sherman KM (1985) The nematode fauna of a deep-sea site exposed to strong near-bottom currents. Deep-Sea Res 32:1077–1088 doi:10.1016/0198-0149(85)90063-9 CrossRefGoogle Scholar
  73. Thistle D, Hilbig B, Eckman JE (1993) Are polychaetes sources of habitat heterogeneity for harpacticoid copepods in the deep-sea? Deep Sea Res Part I Oceanogr Res Pap 40:151–157 doi:10.1016/0967-0637(93)90058-B CrossRefGoogle Scholar
  74. 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 Oceanogr Res Pap 54:1008–1014 doi:10.1016/j.dsr.2007.03.002 CrossRefGoogle Scholar
  75. Thrush SF (1991) Spatial patterns in soft-bottom communities. Trends Ecol Evol 6:75–79 doi:10.1016/0169-5347(91)90178-Z CrossRefGoogle Scholar
  76. Thrush SF, Hewitt JE, Pridmore RD (1989) Patterns in the spatial arrangement of polychaetes and bivalves in intertidal sandflats. Mar Biol (Berl) 102:529–536 doi:10.1007/BF00438355 CrossRefGoogle Scholar
  77. Thrush SF, Pridmore RD, Hewitt JE (1994) Impacts on soft-sediment macrofauna: the effects of spatial variation on temporal trends. Ecol Appl 4:31–41 doi:10.2307/1942112 CrossRefGoogle Scholar
  78. Ugland KI, Gray JS, Ellingsen KE (2003) The species-accumulation curve and estimation of species richness. J Anim Ecol 72:888–897 doi:10.1046/j.1365-2656.2003.00748.x CrossRefGoogle Scholar
  79. Underwood AJ (1996) Spatial patterns of variability in density of intertidal populations. In: Floyd RB, Sheppard AW, De Barro PJ (eds) Frontiers of population ecology. CSIRO Publishing, Melbourne, pp 369–389Google Scholar
  80. Underwood AJ (1997) Ecological experiments: their logical design and interpretation using analysis of variance. Cambridge University Press, CambridgeGoogle Scholar
  81. Underwood AJ, Chapman MG (1996) Scales of spatial patterns of distribution of intertidal invertebrates. Oecologia 107:212–224 doi:10.1007/BF00327905 CrossRefGoogle Scholar
  82. Vanaverbeke J, Martinez-Arbizu P, Dahms HU, Schminke HK (1997) The metazoan meiobenthos along a depth gradient in the Arctic Laptev Sea with special attention to nematode communities. Polar Biol 18:391–401 doi:10.1007/s003000050205 CrossRefGoogle Scholar
  83. Volckaert F (1987) Spatial pattern of soft-bottom Polychaeta off Nova Scotia, Canada. Mar Biol (Berl) 93:627–639 doi:10.1007/BF00392800 CrossRefGoogle Scholar
  84. Warwick RM, Clarke KR (1993) Increased variability as a symptom of stress in marine communities. J Exp Mar Biol Ecol 172:215–226 doi:10.1016/0022-0981(93)90098-9 CrossRefGoogle Scholar
  85. Wieser W (1953) Die Beziehung zwischen Mundhöhlengestalt, Ernährungsweise und Vorkommen bei freilebenden marinen Nematoden. Arch Z 4:439–484Google Scholar

Copyright information

© Senckenberg, Gesellschaft für Naturforschung and Springer 2009

Authors and Affiliations

  1. 1.Alfred Wegener Institute for Polar and Marine ResearchBremerhavenGermany
  2. 2.Marine Biology Section, Biology DepartmentGhent UniversityGentBelgium

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