DOI: https://doi.org/10.3354/meps14948
copiedDeep-sea nematode community changes over two decades at HAUSGARTEN observatory (Fram Strait, Arctic Ocean)
- Jannik Schnier
- Thomas Soltwedel
- Katarzyna Grzelak
- Barbara Górska
- Jennifer Dannheim
- Vadim Mokievsky
- Pedro Martínez Arbizu
- Christiane Hasemann
ABSTRACT:
Over the past 2 decades, deep-sea nematode communities in the Arctic Ocean have undergone significant changes in structure and diversity, likely linked to shifting organic matter input and environmental conditions. Free-living nematodes were collected in 2000, 2004, 2009, 2014 and 2019 at 3 stations along a bathymetric transect (1300, 2500, 4000 m) at the Long-Term Ecological Research (LTER) observatory HAUSGARTEN, a region of the Arctic Ocean undergoing rapid environmental change. Nematodes were identified to genus level and their biomass size distribution was calculated. Sedimentary food indicators, i.e. chloroplastic pigments (phytodetritus) and bacterial abundance/biomass, were analysed as explanatory variables. Food availability changed over time, with initial chlorophyll a decline at shallower depths, followed by increasing total pigment concentrations and bacterial biomass at greater depths, especially at 4000 m. Nematode abundances declined significantly across all depths, most notably by ~75% at 1300 m. Multivariate analyses revealed progressive and significant shifts in community composition, influenced primarily by depth and with clear separation between early (2000) and late (2019) samples. Alpha diversity (EG(50), J‘, H‘(log2)) declined over time, remaining highest at 1300 m. Beta diversity based on genus exchange ratios showed high genus turnover (29-77%) and changes in dominance (12-55%), suggesting a combination of immigration and replacement of rare genera. Our findings indicate that long-term warming in surface waters and an accompanying shift in productivity are potentially reshaping deep-sea nematode communities, particularly at bathyal depths. This study highlights the value of sustained long-term time-series for understanding deep-sea benthic responses to climate change.
KEYWORDS
Alderkamp AC, Buma AGJ, van Rijssel M (2007) The carbohydrates of Phaeocystis and their degradation in the microbial food web. In: van Leeuwe MA, Stefels J, Belviso S, Lancelot C, Verity PG, Gieskes WWC (eds) Phaeocystis, major link in the biogeochemical cycling of climate-relevant elements. Springer, Dordrecht, p 99-118 Crossref
Anderson M, Gorley RN, Clarke KR (2008) Permanova+ for PRIMER: guide to software and statistical methods. Primer-E, Plymouth
Andrássy I (1956) Die Rauminhalts- und Gewichtsbestimmung der Fadenwürmer (Nematoden). Acta Zool Hung 2:1-5
Aphalo PJ (2022) ggpmisc: miscellaneous extensions to ‘ggplot2’. R package version 0.5.2. Link
Armenteros M, Quintanar-Retama O, Gracia A (2022) Depth-related patterns and regional diversity of free-living nematodes in the deep-sea Southwestern Gulf of Mexico. Front Mar Sci 9:1023996 Crossref
Baguley JG, Montagna PA, Hyde LJ, Rowe GT (2008) Metazoan meiofauna biomass, grazing, and weight-dependent respiration in the Northern Gulf of Mexico deep sea. Deep Sea Res II 55:2607-2616 Crossref
Bauerfeind E, Nöthig EM, Beszczynska A, Fahl K and others (2009) Particle sedimentation patterns in the eastern Fram Strait during 2000-2005: results from the Arctic long-term observatory HAUSGARTEN. Deep Sea Res I 56:1471-1487 Crossref
Beszczynska-Möller A, Fahrbach E, Schauer U, Hansen E (2012) Variability in Atlantic water temperature and transport at the entrance to the Arctic Ocean, 1997-2010. ICES J Mar Sci 69:852-863 Crossref
Bluhm BA, Ambrose WG Jr, Bergmann M, Clough LM and others (2011) Diversity of the Arctic deep-sea benthos. Mar Biodivers 41:87-107 Crossref
Bongers T (1990) The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia 83:14-19 Crossref PubMed
Børsheim KY, Bratbak G, Heldal M (1990) Enumeration and biomass estimation of planktonic bacteria and viruses by transmission electron microscopy. Appl Environ Microbiol 56:352-356 Crossref PubMed
Bratbak G (1985) Bacterial biovolume and biomass estimations. Appl Environ Microbiol 49:1488-1493 Crossref PubMed
Budéus G, Lemke P (2007) The expeditions ARKTIS-XX/1 and ARKTIS-XX/2 of the research vessel Polarstern in 2004. Alfred-Wegener-Institut für Polar- und Meeresforschung, Bremerhaven Crossref
Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial (Plymouth routines in multivariate ecological research). PRIMER-e, Plymouth
Coull BC (1999) Role of meiofauna in estuarine soft-bottom habitats. Aust J Ecol 24:327-343 Crossref
Danovaro R, Bianchelli S, Gambi C, Mea M, Zeppilli D (2009) a-, b-, g-, d- and e-diversity of deep-sea nematodes in canyons and open slopes of Northeast Atlantic and Mediterranean margins. Mar Ecol Prog Ser 396:197-209 Crossref
Danovaro R, Carugati L, Corinaldesi C, Gambi C, Guilini K, Pusceddu A, Vanreusel A (2013) Multiple spatial scale analyses provide new clues on patterns and drivers of deep-sea nematode diversity. Deep Sea Res II 92:97-106 Crossref
Dunn OJ (1961) Multiple comparisons among means. J Am Stat Assoc 56:52-64 Crossref
Fadeev E, Rogge A, Ramondenc S, Nöthig EM and others (2021) Sea ice presence is linked to higher carbon export and vertical microbial connectivity in the Eurasian Arctic Ocean. Commun Biol 4:1255 Crossref PubMed
GEBCO Bathymetric Compilation Group (2023) The GEBCO_2023 grid—a continuous terrain model of the global oceans and land. NERC EDS British Oceanographic Data Centre NOC Crossref
Gerlach SA (1978) Food-chain relationships in subtidal silty sand marine sediments and the role of meiofauna in stimulating bacterial productivity. Oecologia 33:55-69 Crossref PubMed
Graf G (1989) Benthic-pelagic coupling in a deep-sea benthic community. Nature 341:437-439 Crossref
Grzelak KA (2015) Structural and functional diversity of Nematoda at the Arctic deep-sea long-term observatory HAUSGARTEN (Fram Strait). PhD dissertation, Polish Academy of Sciences, Sopot
Grzelak K, Kotwicki L, Hasemann C, Soltwedel T (2017) Bathymetric patterns in standing stock and diversity of deep-sea nematodes at the long-term ecological research observatory HAUSGARTEN (Fram Strait). J Mar Syst 172:160-177 Crossref
Guden RM, Haegeman A, Ruttink T, Moens T, Derycke S (2024) Nematodes alter the taxonomic and functional profiles of benthic bacterial communities: a metatranscriptomic approach. Mol Ecol 33:e17331 Crossref PubMed
Hasemann C, Soltwedel T (2024) LTER HAUSGARTEN data on biogenic sediment compounds from 1999 to 2015. doi.org/10.17632/h8r8j3v59j.1 Crossref
Heip C, Vincx M, Vranken G (1985) The ecology of marine nematodes. Oceanogr Mar Biol Annu Rev 23:399-489
Hesterberg T (2022) resample: resampling functions. R package version 0.6. Link
Hillebrand H, Blasius B, Borer ET, Chase JM and others (2018) Biodiversity change is uncoupled from species richness trends: consequences for conservation and monitoring. J Appl Ecol 55:169-184 Crossref
Hoffmann K, Hassenrück C, Salman-Carvalho V, Holtappels M, Bienhold C (2017) Response of bacterial communities to different detritus compositions in Arctic deep-sea sediments. Front Microbiol 8:266 Crossref PubMed
Holm-Hansen O, Lorenzen CJ, Holmes RW, Strickland JDH (1965) Fluorometric determination of chlorophyll. ICES J Mar Sci 30:3-15 Crossref
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 I 54:109-129 Crossref
Hurlbert SH (1971) The nonconcept of species diversity: a critique and alternative parameters. Ecology 52:577-586 Crossref PubMed
Ingels J, Van den Driessche P, De Mesel I, Vanhove S, Moens T, Vanreusel A (2010) Preferred use of bacteria over phytoplankton by deep-sea nematodes in polar regions. Mar Ecol Prog Ser 406:121-133 Crossref
Ingels J, Billett DSM, Van Gaever S, Vanreusel A (2011) An insight into the feeding ecology of deep-sea canyon nematodes - results from field observations and the first in-situ 13C feeding experiment in the Nazaré Canyon. J Exp Mar Biol Ecol 396:185-193 Crossref
Jaccard P (1912) The distribution of the flora in the alpine zone. New Phytol 11:37-50 Crossref
Jensen P (1988) Nematode assemblages in the deep-sea benthos of the Norwegian Sea. Deep-Sea Res A 35:1173-1184 Crossref
Kassambara A (2023) ggpubr: ‘ggplot2’ based publication ready plots. R package version 0.6.1. Link
Kassambara A (2023) rstatix: pipe-friendly framework for basic statistical tests. R package version 0.7.2. Link
Klages M (2010) The expedition of the research vessel Polarstern to the Arctic in 2009 (ARK-XXIV/2). Alfred-Wegener-Institut für Polar- und Meeresforschung, Bremerhaven Crossref
Klenke M, Schenke HW (2002) A new bathymetric model for the central Fram Strait. Mar Geophys Res 23:367-378 Crossref
Knust R (2017) Polar research and supply vessel POLARSTERN operated by the Alfred-Wegener-Institute. J Large-Scale Res Facil 3:A119 Crossref
Krause G, Schauer U (2001) The expeditions ARKTIS XVI/1 and ARKTIS XVI/2 of the research vessel Polarstern in 2000. Alfred-Wegener-Institut für Polar- und Meeresforschung, Bremerhaven Crossref
Kruskal WH, Wallis WA (1952) Use of ranks in one-criterion variance analysis. J Am Stat Assoc 47:583-621 Crossref
Lalande C, Bauerfeind E, Nöthig EM, Beszczynska-Möller A (2013) Impact of a warm anomaly on export fluxes of biogenic matter in the eastern Fram Strait. Prog Oceanogr 109:70-77 Crossref
Metfies K (2020) The expedition PS121 of the research vessel POLARSTERN to the Fram Strait in 2019. Alfred-Wegener-Institut, Helmholtz-Zentrum für Polar- und Meeresforschung, Bremerhaven Crossref
Montagna PA (1995) Rates of metazoan meiofauna microbivory: a review. Vie Milieu 45:1-9
Nemys Eds. (2023) Nemys: World Database of Nematodes. nemys.ugent.be
Nöthig EM, Bracher A, Engel A, Metfies K and others (2015) Summertime plankton ecology in Fram Strait - a compilation of long- and short-term observations. Polar Res 34:23349 Crossref
Nöthig EM, Ramondenc S, Haas A, Hehemann L and others (2020) Summertime chlorophyll a and particulate organic carbon standing stocks in surface waters of the Fram Strait and the Arctic Ocean (1991-2015). Front Mar Sci 7:350 Crossref
Pfannkuche O, Thiel H (1988) Sample processing. In: Higgins RP, Thiel H (eds) Introduction to the study of meiofauna. Smithsonian Institution Press, Washington, DC, p 134-145
Pielou EC (1966) The measurement of diversity in different types of biological collections. J Theor Biol 13:131-144 Crossref
Platt HM, Warwick RM (1983) Freeliving marine nematodes. Part I: British Enoplids. Pictorial key to world genera and notes for the identification of British species. Cambridge University Press, Cambridge
Platt HM, Warwick RM (1988) Freeliving marine nematodes. Part II: British Chromadorids. Pictorial key to world genera and notes for identification of British species. Cambridge University Press, Leiden
Posit Team (2023) RStudio: integrated development environment for R. www.posit.co/ Link
QGIS Development Team (2009) QGIS Geographic Information System. Link
Qiu Y (2023) showtext: using fonts more easily in R graphs. R package version 0.9.7. Link
R Core Team (2023) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna Link
Ramirez-Llodra E, Meyer HK, Bluhm BA, Brix S and others (2024) The emerging picture of a diverse deep Arctic Ocean seafloor: from habitats to ecosystems. Elementa Sci Anthropocene 12:00140 Crossref
Ramondenc S, Iversen MH, Soltwedel T (2024) Long-term measurements reveal a 100-day lag between peaks in phytoplankton chlorophyll and benthic bacterial abundance in the Fram Strait. ICES J Mar Sci 81:1647-1654 Crossref
Rex MA, Etter RJ, Morris JS, Crouse J and others (2006) Global bathymetric patterns of standing stock and body size in the deep-sea benthos. Mar Ecol Prog Ser 317:1-8 Crossref
Riebesell U, Reigstad M, Wassmann P, Noji T, Passow U (1995) On the trophic fate of Phaeocystispouchetii (Hariot): VI. Significance of Phaeocystis-derived mucus for vertical flux. Neth J Sea Res 33:193-203 Crossref
Rishworth GM, Adams JB, Bird MS, Carrasco NK and others (2020) Cross-continental analysis of coastal biodiversity change. Philos Trans R Soc B 375:20190452 Crossref PubMed
Rudis B (2020) hrbrthemes: additional themes, theme components and utilities for ‘ggplot2’. R package version 0.8.7. Link
Sanders HL (1968) Marine benthic diversity: a comparative study. Am Nat 102:243-282 Crossref
Schewe I (2015) The expedition PS85 of the research vessel POLARSTERN to the Fram Strait in 2014. Alfred-Wegener-Institut, Helmholtz-Zentrum für Polar- und Meeresforschung, Bremerhaven Crossref
Schmidt-Rhaesa A (ed) (2014) Handbook of zoology. Gastrotricha, Cycloneuralia and Gnathifera. De Gruyter, Berlin Crossref
Schnier J, Hasemann C, Mokievsky V, Martínez Arbizu P, Soltwedel T (2023) Nematode communities along a bathymetric transect in the deep eastern Fram Strait (Arctic Ocean): interrelations between diversity, function and environment. Front Mar Sci 10:1271447 Crossref
Schnier J, Grzelak K, Hasemann C, Soltwedel T (2025) Data on nematode genus abundance and counts at LTER HAUSGARTEN from 2000 to 2009, 2010, 2014 and 2019. Crossref
Schnier J, Hasemann C, Soltwedel T (2025) Data on nematode genus, body size, biomass, feeding types, tail shapes and cp-values at LTER HAUSGARTEN from 2010, 2014 and 2019. Crossref
Schratzberger M, Ingels J (2018) Meiofauna matters: the roles of meiofauna in benthic ecosystems. J Exp Mar Biol Ecol 502:12-25 Crossref
Schwinghamer P (1981) Characteristic size distributions of integral benthic communities. Can J Fish Aquat Sci 38:1255-1263 Crossref
Schwinghamer P (1983) Generating ecological hypotheses from biomass spectra using causal analysis: a benthic example. Mar Ecol Prog Ser 13:151-166 Crossref
Shannon CE (1948) A mathematical theory of communication. Bell Syst Tech J 27:379-423 Crossref
Shimanaga M, Shirayama Y (2000) Response of benthic organisms to seasonal change of organic matter deposition in the bathyal Sagami Bay, central Japan. Oceanol Acta 23:91-107 Crossref
Smith CR, De Leo FC, Bernardino AF, Sweetman AK, Martínez Arbizu P (2008) Abyssal food limitation, ecosystem structure and climate change. Trends Ecol Evol 23:518-528 Crossref PubMed
Soetaert K, Heip C (1995) Nematode assemblages of deep-sea and shelf break sites in the North Atlantic and Mediterranean Sea. Mar Ecol Prog Ser 125:171-183 Crossref
Soltwedel T, Pfannkuche O, Thiel H (1996) The size structure of deep-sea meiobenthos in the North-Eastern Atlantic: nematode size spectra in relation to environmental variables. J Mar Biol Assoc UK 76:327-344 Crossref
Soltwedel T, Bauerfeind E, Bergmann M, Budaeva N and others (2005) HAUSGARTEN: multidisciplinary investigations at a deep-sea, long-term observatory in the Arctic Ocean. Oceanography 18:46-61 Crossref
Soltwedel T, Bauerfeind E, Bergmann M, Bracher A and others (2016) Natural variability or anthropogenically-induced variation? Insights from 15 years of multidisciplinary observations at the Arctic marine LTER site HAUSGARTEN. Ecol Indic 65:89-102 Crossref
Soltwedel T, Grzelak K, Hasemann C (2020) Spatial and temporal variation in deep-sea meiofauna at the LTER Observatory HAUSGARTEN in the Fram Strait (Arctic Ocean). Diversity 12:279 Crossref
Strugger S (1948) Fluorescence microscope examination of bacteria in soil. Can J Res 26:188-193 Crossref PubMed
Swoboda S, Krumpen T, Nöthig EM, Metfies K and others (2024) Release of ballast material during sea-ice melt enhances carbon export in the Arctic Ocean. PNAS Nexus 3:pgae081 Crossref PubMed
Teschke K, Kraan C, Kloss P, Andresen H and others (2022) CRITTERBASE, a science-driven data warehouse for marine biota. Sci Data 9:483 Crossref PubMed
Vanaverbeke J, Soetaert K, Vincx M (2004) Changes in morphometric characteristics of nematode communities during a spring phytoplankton bloom deposition. Mar Ecol Prog Ser 273:139-146 Crossref
Vanhove S, Wittoeck J, Desmet G, Van den Berghe B and others (1995) Deep-sea meiofauna communities in Antarctica: structural analysis and relation with the environment. Mar Ecol Prog Ser 127:65-76 Crossref
Vanhove S, Vermeeren H, Vanreusel A (2004) Meiofauna towards the South Sandwich Trench (750-6300 m), focus on nematodes. Deep Sea Res II 51:1665-1687 Crossref
Vihtakari M (2023) ggOceanMaps: plot data on oceanographic maps using ‘ggplot2’. R package version 2.2.0. Link
Warwick RM, Platt HM, Somerfield PJ (1998) Freeliving marine nematodes. Part III: Monhysterids. Pictorial key to world genera and notes for the identification of British species. The Linnean Society of London and the Estuarine and Coastal Sciences Association, Shrewsbury
Wei CL, Rowe GT, Escobar-Briones E, Boetius A and others (2010) Global patterns and predictions of seafloor biomass using random forests. PLOS ONE 5:e15323 Crossref PubMed
Wickham H, Averick M, Bryan J, Chang W and others (2019) Welcome to the tidyverse. J Open Source Softw 4:1686 Crossref
Wieser W (1960) Benthic studies in Buzzards Bay II. The meiofauna. Limnol Oceanogr 5:121-137 Crossref
Wilke CO (2020) cowplot: streamlined plot theme and plot annotations for ‘ggplot2’. R package version 1.2.0. Link
Wolf KKE, Hoppe CJM, Rehder L, Schaum E, John U, Rost B (2024) Heatwave responses of Arctic phytoplankton communities are driven by combined impacts of warming and cooling. Sci Adv 10:eadl5904 Crossref PubMed
Wolff T (1977) Diversity and faunal composition of the deep-sea benthos. Nature 267:780-785 Crossref
Wollenburg JE, Katlein C, Nehrke G, Nöthig EM and others (2018) Ballasting by cryogenic gypsum enhances carbon export in a Phaeocystis under-ice bloom. Sci Rep 8:7703 Crossref PubMed
Yentsch CS, Menzel DW (1963) A method for the determination of phytoplankton chlorophyll and phaeophytin by fluorescence. Deep-Sea Res Oceanogr Abstr 10:221-231 Crossref
Zeppilli D, Sarrazin J, Leduc D, Arbizu PM and others (2015) Is the meiofauna a good indicator for climate change and anthropogenic impacts? Mar Biodivers 45:505-535 Crossref
Jannik Schnier (Corresponding Author)
- Alfred Wegener Institute Helmholtz-Centre for Polar and Marine Research, Am Handelshafen 12, 27570 Bremerhaven, Germany
Thomas Soltwedel (Co-author)
- Alfred Wegener Institute Helmholtz-Centre for Polar and Marine Research, Am Handelshafen 12, 27570 Bremerhaven, Germany
Katarzyna Grzelak (Co-author)
- Institute of Oceanology, Polish Academy of Sciences, ul. Powstańców Warszawy 55, 81-712 Sopot, Poland
Barbara Górska (Co-author)
- Institute of Oceanology, Polish Academy of Sciences, ul. Powstańców Warszawy 55, 81-712 Sopot, Poland
Jennifer Dannheim (Co-author)
- Alfred Wegener Institute Helmholtz-Centre for Polar and Marine Research, Am Handelshafen 12, 27570 Bremerhaven, Germany
Vadim Mokievsky (Co-author)
- P.P. Shirshov Institute of Oceanology, Russian Academy of Sciences, Nakhimovsky prosp. 36, Moscow 117997, Russia
Pedro Martínez Arbizu (Co-author)
- German Centre for Marine Biodiversity Research (DZMB), Senckenberg am Meer, Südstrand 40, 26382 Wilhelmshaven, Germany
Christiane Hasemann (Co-author)
- Alfred Wegener Institute Helmholtz-Centre for Polar and Marine Research, Am Handelshafen 12, 27570 Bremerhaven, Germany
Handling Editor:
Deborah K. Steinberg, Gloucester Point, Virginia, USA
Reviewers:
T. Pereira, E. Baldrighi and 1 anonymous referee
Acknowledgements:
We greatly thank the RV ‘Polarstern’ captains, crews, cruise leaders and all other involved persons of the expeditions ARK-XVI, ARK-XX/1, ARK-XXIV/2, PS85, PS121 and all other HAUSGARTEN cruises, without whom our data set would not exist. We are much obliged to Anja Pappert and the deep-sea volunteers (FÖJ participants) for analysing the environmental parameters and for their assistance with sample preparation. Special thanks also to Jule Wirries, who patiently carried out size measurements for hundreds of nematodes that were examined in this study. We express our gratitude to Dorothee Hodapp, who kindly provided a detailed R markdown for the b-diversity analyses, which was a tremendous help. Many thanks also to Lilian Böhringer for the help with QGIS. Furthermore, we thank the 3 anonymous reviewers, whose critical input significantly improved this paper. This research did not receive any specific grant from funding agencies in the public, commercial or not-for-profit sectors. We explicitly acknowledge the support by the Open Access Publication Funds of the Alfred-Wegener-Institute Helmholtz-Centre for Polar and Marine Research. The present work is part of J.S.’s PhD thesis.
