Shifts in trait-based and taxonomic macrofauna community structure along a 27-year time-series in the south-eastern North Sea

English version

Autoři: Julia Meyer ^aff001; Ingrid Kröncke ^aff001
Působiště autorů: Marine Research, Senckenberg am Meer, Wilhelmshaven, Germany ^aff001; Institute for Chemistry and Biology of the Marine Environment, Benthic Ecology, Oldenburg, Germany ^aff002
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0226410

Souhrn

Current research revealed distinct changes in ecosystem functions, and thus in ecosystem stability and resilience, caused by changes in community structure and diversity loss. Benthic species play an important role in benthic-pelagic coupling, such as through the remineralization of deposited organic material, and changes to benthic community structure and diversity have associated with changes in ecosystem functioning, ecosystem stability and resilience. However, the long-term variability of traits and functions in benthic communities is largely unknown. By using abundance and bioturbation potential of macrofauna samples, taken along a transect from the German Bight towards the Dogger Bank in May 1990 and annually from 1995 to 2017, we analysed the taxonomic and trait-based macrofauna long-term community variability and diversity. Taxonomic and trait-based diversity remained stable over time, while three different regimes were found, characterised by changes in taxonomic and trait-based community structure. Min/max autocorrelation factor analysis revealed the climatic variables sea surface temperature (SST) and North Atlantic Oscillation Index (NAOI), nitrite, and epibenthic abundance as most important environmental drivers for taxonomic and trait-based community changes.

Klíčová slova:

Taxonomy – Community structure – Biodiversity – Nitrites – Sediment – Marine ecosystems – Surface temperature – Ecosystem functioning

Zdroje

1. Van Hoey G, Degraer S, Vincx M. Macrobenthic community structure of soft-bottom sediments at the Belgian Continental Shelf. Estuar Coast Shelf Sci. 2004;59(4):599–613.

2. Heip C, Craeymeersch J. Benthic community structures in the North Sea. Helgolander Meeresuntersuchungen. 1995;49(1):313–28.

3. Kröncke I, Reiss H, Eggleton JD, Aldridge J, Bergman MJN, Cochrane S, et al. Changes in North Sea macrofauna communities and species distribution between 1986 and 2000. Estuar Coast Shelf Sci. 2011;94(1):1–15.

4. Tittensor DP, Mora C, Jetz W, Lotze HK, Ricard D, Berghe EV, et al. Global patterns and predictors of marine biodiversity across taxa. Nature. 2010;466(7310):1098. doi: 10.1038/nature09329 20668450

5. Reiss H, Degraer S, Duineveld GCA, Kröncke I, Aldridge J, Craeymeersch JA, et al. Spatial patterns of infauna, epifauna, and demersal fish communities in the North Sea. ICES J Mar Sci. 2009;67(2):278–93.

6. Pianka ER. Latitudinal gradients in species diversity: a review of concepts. The American Naturalist. 1966;100(910):33–46.

7. Luck GW, Harrington R, Harrison PA, Kremen C, Berry PM, Bugter R, et al. Quantifying the contribution of organisms to the provision of ecosystem services. Bioscience. 2009;59(3):223–35.

8. Cardinale BJ, Duffy JE, Gonzalez A, Hooper DU, Perrings C, Venail P, et al. Biodiversity loss and its impact on humanity. Nature. 2012;486(7401):59. doi: 10.1038/nature11148 22678280

9. Brose U, Hillebrand H. Biodiversity and ecosystem functioning in dynamic landscapes. Philosophical Transactions of The Royal Society B. 2016;371(1694):20150267.

10. Cardinale BJ, Matulich KL, Hooper DU, Byrnes JE, Duffy E, Gamfeldt L, et al. The functional role of producer diversity in ecosystems. Am J Bot. 2011;98(3):572–92. doi: 10.3732/ajb.1000364 21613148

11. Loreau M. Biodiversity and ecosystem functioning: recent theoretical advances. Oikos. 2000;91(1):3–17.

12. Díaz S, Cabido M. Vive la difference: plant functional diversity matters to ecosystem processes. Trends in ecology & evolution. 2001;16(11):646–55.

13. Neumann H, Diekmann R, Kröncke I. Functional composition of epifauna in the south-eastern North Sea in relation to habitat characteristics and fishing effort. Estuar Coast Shelf Sci. 2016;169:182–94.

14. Dencker TS, Pecuchet L, Beukhof E, Richardson K, Payne MR, Lindegren M. Temporal and spatial differences between taxonomic and trait biodiversity in a large marine ecosystem: Causes and consequences. PLoS One. 2017;12(12):e0189731. doi: 10.1371/journal.pone.0189731 29253876

15. Solan M, Cardinale BJ, Downing AL, Engelhardt KAM, Ruesink JL, Srivastava DS. Extinction and ecosystem function in the marine benthos. Science. 2004;306(5699):1177–80. doi: 10.1126/science.1103960 15539601

16. Gamfeldt L, Hillebrand H, Jonsson PR. Multiple functions increase the importance of biodiversity for overall ecosystem functioning. Ecology. 2008;89(5):1223–31. doi: 10.1890/06-2091.1 18543617

17. Breine NT, De Backer A, Van Colen C, Moens T, Hostens K, Van Hoey G. Structural and functional diversity of soft-bottom macrobenthic communities in the Southern North Sea. Estuar Coast Shelf Sci. 2018;214:173–84.

18. van der Linden P, Patrício J, Marchini A, Cid N, Neto JM, Marques JC. A biological trait approach to assess the functional composition of subtidal benthic communities in an estuarine ecosystem. Ecol Indic. 2012;20:121–33.

19. Douglas EJ, Pilditch CA, Kraan C, Schipper LA, Lohrer AM, Thrush SF. Macrofaunal Functional Diversity Provides Resilience to Nutrient Enrichment in Coastal Sediments. Ecosystems. 2017;20(7):1324–36.

20. Weigel B, Blenckner T, Bonsdorff E. Maintained functional diversity in benthic communities in spite of diverging functional identities. Oikos. 2016;125(10):1421–33.

21. Wrede A, Dannheim J, Gutow L, Brey T. Who really matters: Influence of German Bight key bioturbators on biogeochemical cycling and sediment turnover. J Exp Mar Bio Ecol. 2017;488:92–101.

22. Gasbarro R, Wan D, Tunnicliffe V. Composition and functional diversity of macrofaunal assemblages on vertical walls of a deep northeast Pacific fjord. Mar Ecol Prog Ser. 2018;597:47–64.

23. Ashford OS, Kenny AJ, Barrio Froján CR, Bonsall MB, Horton T, Brandt A, et al. Phylogenetic and functional evidence suggests that deep-ocean ecosystems are highly sensitive to environmental change and direct human disturbance. Proceedings of the Royal Society B. 2018;285(1884):20180923. doi: 10.1098/rspb.2018.0923 30068675

24. Chapman AS, Tunnicliffe V, Bates AE. Both rare and common species make unique contributions to functional diversity in an ecosystem unaffected by human activities. Divers Distrib. 2018;24(5):568–78.

25. Nasi F, Nordström M, Bonsdorff E, Auriemma R, Cibic T, Del Negro P. Functional biodiversity of marine soft-sediment polychaetes from two Mediterranean coastal areas in relation to environmental stress. Mar Environ Res. 2018;137:121–32. doi: 10.1016/j.marenvres.2018.03.002 29551408

26. Törnroos A, Bonsdorff E, Bremner J, Blomqvist M, Josefson AB, Garcia C, et al. Marine benthic ecological functioning over decreasing taxonomic richness. J Sea Res. 2015;98:49–56.

27. Kokarev V, Vedenin A, Basin A, Azovsky A. Taxonomic and functional patterns of macrobenthic communities on a high-Arctic shelf: a case study from the Laptev Sea. J Sea Res. 2017;129:61–9.

28. Griffiths JR, Kadin M, Nascimento FJ, Tamelander T, Törnroos A, Bonaglia S, et al. The importance of benthic–pelagic coupling for marine ecosystem functioning in a changing world. Glob Chang Biol. 2017;23(6):2179–96. doi: 10.1111/gcb.13642 28132408

29. Salzwedel H, Rachor E, Gerdes D. Benthic macrofauna communities in the German Bight. Veröff Inst Meeresforsch Bremerh. 1985;20(2):199–267.

30. Rosenberg R. Benthic marine fauna structured by hydrodynamic processes and food availability. Neth J Sea Res. 1995;34(4):303–17.

31. Aller RC. The Effects of Macrobenthos on Chemical Properties of Marine Sediment and Overlying Water. In: McCall PL, Tevesz MJS, editors. Animal-Sediment Relations: The Biogenic Alteration of Sediments. Boston, MA: Springer US; 1982. p. 53–102.

32. Aller RC. Bioturbation and remineralization of sedimentary organic matter: effects of redox oscillation. Chem Geol. 1994;114(3–4):331–45.

33. Zhang W, Wirtz K. Mutual Dependence Between Sedimentary Organic Carbon and Infaunal Macrobenthos Resolved by Mechanistic Modeling. Journal of Geophysical Research: Biogeosciences. 2017(10):2509–26.

34. Solan M, Wigham BD, Hudson IR, Kennedy R, Coulon CH, Norling K, et al. In situ quantification of bioturbation using time-lapse fluorescent sediment profile imaging (f-SPI), luminophore tracers and model simulation. Mar Ecol Prog Ser. 2004;271:1–12.

35. Queirós AM, Birchenough SNR, Bremner J, Godbold JA, Parker RE, Romero-Ramirez A, et al. A bioturbation classification of European marine infaunal invertebrates. Ecol Evol. 2013;3(11):3958–85. doi: 10.1002/ece3.769 24198953

36. Meyer J, Nehmer P, Kröncke I. Shifting south-eastern North Sea macrofauna bioturbation potential over the past three decades: a response to increasing SST and regionally decreasing food supply. Mar Ecol Prog Ser. 2019;609:17–32.

37. Dauwe B, Herman PM, Heip C. Community structure and bioturbation potential of macrofauna at four North Sea stations with contrasting food supply. Mar Ecol Prog Ser. 1998;173:67–83.

38. Bremner J, Rogers S, Frid C. Methods for describing ecological functioning of marine benthic assemblages using biological traits analysis (BTA). Ecol Indic. 2006;6(3):609–22.

39. Bremner J, Rogers S, Frid C. Matching biological traits to environmental conditions in marine benthic ecosystems. J Mar Syst. 2006;60(3–4):302–16.

40. Gogina M, Morys C, Forster S, Gräwe U, Friedland R, Zettler ML. Towards benthic ecosystem functioning maps: Quantifying bioturbation potential in the German part of the Baltic Sea. Ecol Indic. 2017;73:574–88.

41. Kirby RR, Beaugrand G, Lindley JA. Synergistic Effects of Climate and Fishing in a Marine Ecosystem. Ecosystems. 2009;12(4):548–61.

42. Beaugrand G, Reid PC. Long‐term changes in phytoplankton, zooplankton and salmon related to climate. Glob Chang Biol. 2003;9(6):801–17.

43. Wernberg T, Bennett S, Babcock RC, de Bettignies T, Cure K, Depczynski M, et al. Climate-driven regime shift of a temperate marine ecosystem. Science. 2016;353(6295):169–72. doi: 10.1126/science.aad8745 27387951

44. van der Veer HW, Dapper R, Henderson PA, Jung AS, Philippart CJM, Witte JIJ, et al. Changes over 50 years in fish fauna of a temperate coastal sea: Degradation of trophic structure and nursery function. Estuar Coast Shelf Sci. 2015;155(0):156–66.

45. Goberville E, Beaugrand G, Edwards M. Synchronous response of marine plankton ecosystems to climate in the Northeast Atlantic and the North Sea. J Mar Syst. 2014;129:189–202.

46. Luczak C, Beaugrand G, Lindley JA, Dewarumez JM, Dubois PJ, Kirby RR. North Sea ecosystem change from swimming crabs to seagulls. Biol Lett. 2012;8(5):821–4. doi: 10.1098/rsbl.2012.0474 22764111

47. Reid PC, Edwards M. Long-term changes in the pelagos, benthos and fisheries of the North Sea. Senckenb Marit. 2001;31(2):107–15.

48. Kröncke I. Changes in Dogger Bank macrofauna communities in the 20th century caused by fishing and climate. Estuar Coast Shelf Sci. 2011;94(3):234–45.

49. Ghodrati Shojaei M, Gutow L, Dannheim J, Rachor E, Schröder A, Brey T. Common trends in German Bight benthic macrofaunal communities: Assessing temporal variability and the relative importance of environmental variables. J Sea Res. 2016;107, Part 2:25–33.

50. Heip C, Basford D, Craeymeersch JA, Dewarumez JM, Dörjes J, De Wilde P, et al. Trends in biomass, density and diversity of North Sea macrofauna. 1992;49(1):13–22.

51. Meyer J, Nehmer P, Moll A, Kröncke I. Shifting south-eastern North Sea macrofauna community structure since 1986: A response to de-eutrophication and regionally decreasing food supply? Estuar Coast Shelf Sci. 2018;213:115–27.

52. Burson A, Stomp M, Akil L, Brussaard CP, Huisman J. Unbalanced reduction of nutrient loads has created an offshore gradient from phosphorus to nitrogen limitation in the North Sea. Limnol Oceanogr. 2016;61(3):869–88.

53. Devictor V, Mouillot D, Meynard C, Jiguet F, Thuiller W, Mouquet N. Spatial mismatch and congruence between taxonomic, phylogenetic and functional diversity: the need for integrative conservation strategies in a changing world. Ecol Lett. 2010;13(8):1030–40. doi: 10.1111/j.1461-0248.2010.01493.x 20545736

54. Villéger S, Miranda JR, Hernández DF, Mouillot D. Contrasting changes in taxonomic vs. functional diversity of tropical fish communities after habitat degradation. Ecol Appl. 2010;20(6):1512–22. doi: 10.1890/09-1310.1 20945756

55. Törnroos A, Pecuchet L, Olsson J, Gårdmark A, Blomqvist M, Lindegren M, et al. Four decades of functional community change reveals gradual trends and low interlinkage across trophic groups in a large marine ecosystem. Glob Chang Biol. 2018.

56. Törnoos A, Olsson J, Gardmark A, Pécuchet L, Blomqvist M, Lindegren M, et al., editors. Long-term functional trends in Baltic Sea coastal macrofauna and fish. ICES Annual Science Conference 2015; 2015.

57. Kröncke I, Reiss H, Dippner JW. Effects of cold winters and regime shifts on macrofauna communities in shallow coastal regions. Estuar Coast Shelf Sci. 2013;119:79–90.

58. Beaugrand G, Conversi A, Chiba S, Edwards M, Fonda-Umani S, Greene C, et al. Synchronous marine pelagic regime shifts in the Northern Hemisphere. Philosophical Transactions of the Royal Society of London B: Biological Sciences. 2015;370(1659):20130272.

59. Meyer J, Kroencke I, Bartholomae A, Dippner JW, Schueckel U. Long-term changes in species composition of demersal fish and epibenthic species in the Jade area (German Wadden Sea/Southern North Sea) since 1972. Estuar Coast Shelf Sci. 2016;181:284–93.

60. Beare D, Batten S, Edwards M, Reid D. Prevalence of boreal Atlantic, temperate Atlantic and neritic zooplankton in the North Sea between 1958 and 1998 in relation to temperature, salinity, stratification intensity and Atlantic inflow. J Sea Res. 2002;48(1):29–49.

61. van Aken HM. Variability of the water temperature in the western Wadden Sea on tidal to centennial time scales. J Sea Res. 2008;60(4):227–34.

62. Schückel U, Kröncke I. Temporal changes in intertidal macrofauna communities over eight decades: A result of eutrophication and climate change. Estuarine Coastal and Shelf Science. 2013;117:210–8.

63. Schückel U, Kröncke I, Baird D. Linking long-term changes in trophic structure and function of an intertidal macrobenthic system to eutrophication and climate change using ecological network analysis. Mar Ecol Prog Ser. 2015;536:25–38.

64. Reiss H, Meybohm K, Kröncke I. Cold winter effects on benthic macrofauna communities in near- and offshore regions of the North Sea. Helgol Mar Res. 2006;60(3):224–38.

65. Neumann H, Ehrich S, Kröncke I. Effects of cold winters and climate on the temporal variability of an epibenthic community in the German Bight. Clim Res. 2008;37(2–3):241–51.

66. Beaugrand G. The North Sea regime shift: evidence, causes, mechanisms and consequences. Prog Oceanogr. 2004;60(2–4):245–62.

67. Dippner JW, Junker K, Kröncke I. Biological regime shifts and changes in predictability. Geophys Res Lett. 2010;37(24):L24701.

68. Scheffer M, Carpenter S, Foley JA, Folke C, Walker B. Catastrophic shifts in ecosystems. Nature. 2001;413(6856):591–6. doi: 10.1038/35098000 11595939

69. Dippner JW, Kröncke I. Ecological forecasting in the presence of abrupt regime shifts. J Mar Syst. 2015;150:34–40.

70. Hurrell JW. Decadal trends in the North Atlantic Oscillation: Regional temperatures and precipitation. Science. 1995;269(5224):676–9. doi: 10.1126/science.269.5224.676 17758812

71. Hurrell J. National Center for Atmospheric Research. The Climate Data Guide: Hurrell North Atlantic Oscillation (NAO) Index (station-based).

72. Capuzzo E, Lynam CP, Barry J, Stephens D, Forster RM, Greenwood N, et al. A decline in primary production in the North Sea over 25 years, associated with reductions in zooplankton abundance and fish stock recruitment. Glob Chang Biol. 2018;24(1):352–64.

73. Neumann H, Reiss H, Ehrich S, Sell A, Panten K, Kloppmann M, et al. Benthos and demersal fish habitats in the German Exclusive Economic Zone (EEZ) of the North Sea. Helgol Mar Res. 2013;67(3):445–59.

74. Neumann H, Ehrich S, Kröncke I. Spatial variability of epifaunal communities in the North Sea in relation to sampling effort. Helgol Mar Res. 2008;62(3):215–25.

75. Clarke K, Warwick R. An approach to statistical analysis and interpretation. Change in Marine Communities. 1994;2.

76. Zuur A, Ieno EN, Smith GM. Analysing ecological data. New York: Springer Science & Business Media; 2007. 672 p.

77. Legendre P, Dallot S, Legendre L. Succession of species within a community: chronological clustering, with applications to marine and freshwater zooplankton. The American Naturalist. 1985;125(2):257–88.

78. Pecl GT, Araújo MB, Bell JD, Blanchard J, Bonebrake TC, Chen I-C, et al. Biodiversity redistribution under climate change: Impacts on ecosystems and human well-being. Science. 2017;355(6332):eaai9214. doi: 10.1126/science.aai9214 28360268

79. Rockström J, Steffen W, Noone K, Persson Å, Chapin FS III, Lambin EF, et al. A safe operating space for humanity. Nature. 2009;461(7263):472. doi: 10.1038/461472a 19779433

80. Bremner J, Rogers S, Frid C. Assessing functional diversity in marine benthic ecosystems: a comparison of approaches. Mar Ecol Prog Ser. 2003;254:11–25.

81. MacArthur R. Fluctuations of animal populations and a measure of community stability. Ecology. 1955;36(3):533–6.

82. MacArthur R, Recher H, Cody M. On the relation between habitat selection and species diversity. The American Naturalist. 1966;100(913):319–32.

83. UNEP. United Nations Environment Programme—Convention on Biological Diversity. 1992.

84. ICES. Greater North Sea Ecoregion–Ecosystem overview—ICES. 2016.

85. OSPAR. Quality status report 2000, Region II—Greater North Sea: The Commission; 2000.

86. Hinz H, Prieto V, Kaiser MJ. Trawl disturbance on benthic communities: chronic effects and experimental predictions. Ecol Appl. 2009;19(3):761–73. doi: 10.1890/08-0351.1 19425437

87. Reiss H, Greenstreet SPR, Sieben K, Ehrich S, Piet GJ, Quirijns F, et al. Effects of fishing disturbance on benthic communities and secondary production within an intensively fished area. Mar Ecol Prog Ser. 2009;394:201–13.

88. Hiddink JG, Burrows MT, García Molinos J. Temperature tracking by North Sea benthic invertebrates in response to climate change. Glob Chang Biol. 2015;21(1):117–29. doi: 10.1111/gcb.12726 25179407

89. Cattiaux J, Vautard R, Cassou C, Yiou P, Masson‐Delmotte V, Codron F. Winter 2010 in Europe: a cold extreme in a warming climate. Geophys Res Lett. 2010;37(20).

90. Strayer D, Glitzenstein JS, Jones CG, Kolasa J, Likens GE, McDonnell MJ, et al. Long-term ecological studies: an illustrated account of their design, opera tion, and importance to ecology. Occasional Publication of The Institute of Ecosystem Studies. 1986;Number 2.

91. Goberville E, Beaugrand G, Sautour B, Treguer P, Team S. Climate-driven changes in coastal marine systems of western Europe. Mar Ecol Prog Ser. 2010;408:129–U59.

92. Birchenough SN, Reiss H, Degraer S, Mieszkowska N, Borja Á, Buhl‐Mortensen L, et al. Climate change and marine benthos: a review of existing research and future directions in the North Atlantic. Wiley interdisciplinary reviews: climate change. 2015;6(2):203–23.

93. Bonsdorff E, Blomqvist E, Mattila J, Norkko A. Long-term changes and coastal eutrophication. Examples from the Aland Islands and the Archipelago Sea, northern Baltic Sea. Oceanolica Acta. 1997;20(1):319–29.

94. Clare DS, Spencer M, Robinson LA, Frid CL. Explaining ecological shifts: the roles of temperature and primary production in the long‐term dynamics of benthic faunal composition. Oikos. 2017;126(8):1123–33.

95. Defriez EJ, Sheppard LW, Reid PC, Reuman DC. Climate change-related regime shifts have altered spatial synchrony of plankton dynamics in the North Sea. Glob Chang Biol. 2016;22(6):2069–80. doi: 10.1111/gcb.13229 26810148

96. Lenhart H-J, Mills DK, Baretta-Bekker H, Van Leeuwen SM, Van Der Molen J, Baretta JW, et al. Predicting the consequences of nutrient reduction on the eutrophication status of the North Sea. J Mar Syst. 2010;81(1–2):148–70.

97. Philippart CJ, Beukema JJ, Cadée GC, Dekker R, Goedhart PW, van Iperen JM, et al. Impacts of nutrient reduction on coastal communities. Ecosystems. 2007;10(1):96–119.

98. Künitzer A, Basford D, Craeymeersch JA, Dewarumez JM, Dörjes J, Duineveld GCA, et al. The benthic infauna of the North Sea: species distribution and assemblages. ICES J Mar Sci. 1992;49(2):127–43.

99. Sarker S. What explains phytoplankton dynamics? An analysis of the Helgoland Roads Time Series data sets: Jacobs University Bremen; 2018.

100. Creutzberg F, Wapenaar P, Duineveld G, Lopez Lopez N. Distribution and density of the benthic fauna in the southern North Sea in relation to bottom characteristics and hydrographic conditions. Rapports et Procès-Verbaux des Réunions du Conseil Permanent International pour l'Exploration de la Mer. 1984.

101. Reid PC, Hari RE, Beaugrand G, Livingstone DM, Marty C, Straile D, et al. Global impacts of the 1980s regime shift. Glob Chang Biol. 2016;22(2):682–703. doi: 10.1111/gcb.13106 26598217

102. Weijerman M, Lindeboom H, Zuur AF. Regime shifts in marine ecosystems of the North Sea and Wadden Sea. Mar Ecol Prog Ser. 2005;298:21–39.

103. Reid PC, de Fatima Borges M, Svendsen E. A regime shift in the North Sea circa 1988 linked to changes in the North Sea horse mackerel fishery. Fisheries Research. 2001;50(1):163–71.

104. Kröncke I, Neumann H, Dippner JW, Holbrook S, Lamy T, Miller R, et al. Comparison of biological and ecological long-term trends related to northern hemisphere climate in different marine ecosystems. Nat Conserv. 2019.

105. Pihl L. Food selection and consumption of mobile epibenthic fauna in shallow marine areas. Marine ecology Progress series. 1985;22(2):169–79.

106. Virnstein RW. The importance of predation by crabs and fishes on benthic infauna in Chesapeake Bay. Ecology. 1977;58(6):1199–217.

107. Neumann H, Diekmann R, Emeis KC, Kleeberg U, Moll A, Kroncke I. Full-coverage spatial distribution of epibenthic communities in the south-eastern North Sea in relation to habitat characteristics and fishing effort. Mar Environ Res. 2017;130:1–11. doi: 10.1016/j.marenvres.2017.07.010 28712824

108. Murray F, Douglas A, Solan M. Species that share traits do not necessarily form distinct and universally applicable functional effect groups. Mar Ecol Prog Ser. 2014;516:23–34.

109. Kristensen E, Delefosse M, Quintana CO, Flindt MR, Valdemarsen T. Influence of benthic macrofauna community shifts on ecosystem functioning in shallow estuaries. Frontiers in Marine Science. 2014;1.

110. Queirós AM, Stephens N, Cook R, Ravaglioli C, Nunes J, Dashfield S, et al. Can benthic community structure be used to predict the process of bioturbation in real ecosystems? Prog Oceanogr. 2015;137:559–69.

111. Kristensen E, Penha-Lopes G, Delefosse M, Valdemarsen T, Quintana CO, Banta GT. What is bioturbation? The need for a precise definition for fauna in aquatic sciences. Mar Ecol Prog Ser. 2012;446:285–302.

Shifts in trait-based and taxonomic macrofauna community structure along a 27-year time-series in the south-eastern North Sea

Souhrn

Klíčová slova:

Zdroje

PLOS One

Aktuální možnosti diagnostiky a léčby litiáz