Abstract
The Scotia Sea is a productive pelagic ecosystem in the Southern Ocean, which is rapidly changing as a consequence of global warming. Species range shifts are particularly evident, as sub-Antarctic species expand their range from North to South, potentially rearranging the structure of this ecosystem. Thus, studies are needed to determine the current extent of variation in food web structure between these two biogeographic regions of the Scotia Sea and to investigate whether the observed patterns are consistent among depth zones. We compiled a database of 10,888 feeding interactions among 228 pelagic taxa, underpinned by surveys and dietary studies conducted in the Scotia Sea. Network analysis indicated that the Northern Scotia Sea (NSS), relative to the Southern Scotia Sea (SSS), is more complex: with higher species richness (more nodes) and trophic interactions (more links) is more connected overall (greater connectance and linkage density). Moreover, the NSS is characterised by more groups of strongly interacting organisms (greater node clustering) than the SSS, suggesting a higher trophic specialisation of Antarctic compared to sub-Antarctic species. Depth also played a key role in structuring these networks, with higher mean trophic position and more dietary generalism in the mesopelagic and bathypelagic zones relative to the epipelagic zones. This suggests that direct access to primary producers is a key factor influencing the trophic structure of these communities. Our results suggest that under current levels of warming the SSS ecosystem will likely become more connected and less modular, resembling the current structure of the NSS.
Similar content being viewed by others
Data archiving
The full dataset used in this work is available at https://doi.org/10.5285/9F615353-C621-4216-865E-7D38A9B21E2C.
REFERENCES
Agusti S, Lubián LM, Moreno-Ostos E, Estrada M, Duarte CM. 2019. Projected changes in photosynthetic picoplankton in a warmer subtropical ocean. Front Mar Sci 5.
Álvarez-Berastegui D, Ciannelli L, Aparicio-González A, Reglero P, Hidalgo M, López-Jurado JL, Tintoré J, Alemany F. 2014. Spatial scale, means and gradients of hydrographic variables define pelagic seascapes of bluefin and bullet tuna spawning distribution. PloS ONE 9:e109338.
Angel MV. 2003. The pelagic environment of the open ocean. In: Tyler PA, Ed. Ecosystems of the World, Vol. 28 Ecosystems of the Deep Ocean. Amsterdam: Elsevier. pp 39–80.
Arai MN, Welch DW, Dunsmuir AL, Jacobs MC, Ladouceur AR. 2003. Digestion of pelagic Ctenophora and Cnidaria by fish. Can J Fish Aquat Sci 60:825–29.
Armour KC, Marshall J, Scott JR, Donohoe A, Newsom ER. 2016. Southern Ocean warming delayed by circumpolar upwelling and equatorward transport. Nature Geoscience 9:549–54.
Arrigo KR, Thomas DN. 2004. Large scale importance of sea ice biology in the Southern Ocean. Antarctic Science 16:471–86.
Atkinson A, Whitehouse MJ, Priddle J, Cripps GC, Ward P, Brandon MA. 2001. South Georgia, Antarctica: a productive, cold water, pelagic ecosystem. Marine Ecol Prog Ser 216:279–308.
Atkinson A, Hill SL, Pakhomov EA, Siegel V, Reiss CS, Loeb VJ, Steinberg DK, Schmidt K, Tarling GA, Gerrish L, Sailley SF. 2019. Krill (Euphausia superba) distribution contracts southward during rapid regional warming. Nat Clim Change 9:142–47.
Bersier LF, Banašek-Richter C, Cattin MF. 2002. Quantitative descriptors of food-web matrices. Ecology 83:2394–407.
Bascompte J, Melián CJ. 2005. Simple trophic modules for complex food webs. Ecology 86:2868–73.
Blois JL, Williams JW, Fitzpatrick MC, Jackson ST, Ferrier S. 2013. Space can substitute for time in predicting climate-change effects on biodiversity. Proc Natl Acad Sci USA 110:9374–79.
Boyce DG, Frank KT, Worm B, Leggett WC. 2015. Spatial patterns and predictors of trophic control in marine ecosystems. Ecol Lett 18:1001–11.
Brose U, Archambault P, Barnes AD, Bersier LF, Boy T, Canning-Clode J, Conti E, Digel C, Dissanayake A, Flores AAV, Fussman K, Gauzens B, Gray C, Häussler J, Hirt MR, Jacob U, Jochum M, Kéfi S, McLaughlin O, MacPherson MM, Latz E, Layer-Dobra K, Legagneux P, Yuanheng L, Madeira C, Martinez ND, Mendoça V, Mulder C, Navarrete SA, O’Gorman E, Ott D, Paula J, Perkins D, Piechnik D, Pokrovsky I, Raffaelli D, Rall BC, Rosenbaum B, Ryser R, Silva A, Sohlström EH, Sokolova N, Thompson MSA, Thompson RM, Vermandele F, Vinagre C, Wang S, Wefer JM, Williamns RJ, Wieters E, Woodward G, Iles AC. 2019. Predator traits determine food-web architecture across ecosystems. Nat Ecol Evol 3:919–27.
Bucklin A, Nishida S, Schnack-Schiel S, Wiebe PH, Lindsay D, Machida RJ, Copley NJ. 2010. A census of zooplankton of the global ocean. McIntyre A, Ed. Life in the world’s oceans: diversity, distribution, and abundance. Oxford: Blackwell. pp 247–265.
Cisewski B, Strass VH, Rhein M, Krägefsky S. 2010. Seasonal variation of diel vertical migration of zooplankton from ADCP backscatter time series data in the Lazarev Sea, Antarctica. Deep Sea Res Part I Oceanogr Res Papers 57:78–94.
Conley KR, Lombard F, Sutherland KR. 2018. Mammoth grazers on the ocean’s minuteness: a review of selective feeding using mucous meshes. Proc Roy Soc B Biol Sci 285:20180056.
Collins MA, Xavier JC, Johnston NM, North AW, Enderlein P, Tarling GA, Waluda CM, Hawker EJ, Cunningham NJ. 2008. Patterns in the distribution of myctophid fish in the northern Scotia Sea ecosystem. Polar Biol 31:837–51.
Csardi G, Nepusz T. 2006. The igraph software package for complex network research. Int J Comp Syst 1695.
Curtsdotter A, Binzer A, Brose U, de Castro F, Ebenman B, Eklöf A, Riede JO, Thierry A, Rall BC. 2011. Robustness to secondary extinctions: comparing trait-based sequential deletions in static and dynamic food webs. Basic Appl Ecol 7:571–80.
D’Alessandro S, Mariani S. 2021. Sifting environmental DNA metabarcoding data sets for rapid reconstruction of marine food webs. Fish and Fisheries (in press).
De Broyer C, Koubbi P, Griffiths HJ, Raymond B, Udekem d’Acoz C, Van de Putte AP, Danis B, David B, Grant S, Gutt J, Held C, Hosie G, Huettmann F, Post A, Ropert Coudert Y, Eds. 2014. Biogeographic Atlas of the Southern Ocean. Cambridge: Scientific Committee on Antarctic Research. p 510.
De Vargas C, Audic S, Henry N, Decelle J, Mahé F, Logares R, Lara E, Berney C, Le Bescot N, Probert I, Carmichael M, Poulain J, Romac S, Colin S, Aury JM, Bittner L, Chaffron S, Dunthorn M, Engelen S, Flegontova O, Guidi L, Horak A, Jaillon O, Lima-Mendez G, Lukes J, Malviya S, Morard R, Mulot M, Scalco E, Siano R, Vincent F, Zingone A, Dimier C, Picheral M, Searson S, Kandels-Lewis S, Acinas SG, Bork P, Bowler C, Gorsky G, Grimsley N, Hingamp P, Iudicone D, Not F, Ogata H, Pesant S, Raes J, Sieracki M, Speich S, Stemmann L, Sunagawa S, Weissenbach J, Wincker P, Karsenti E. 2015. Eukaryotic plankton diversity in the sunlit ocean. Science 348:1261605.
Desbruyères D, McDonagh EL, King BA, Thierry V. 2017. Global and full-depth ocean temperature trends during the early twenty-first century from argo and repeat hydrography. J Clim 30:1985–97.
Dunne JA, Williams RJ, Martinez ND. 2002a. Network structure and biodiversity loss in food webs: robustness increases with connectance. Ecol Lett 5:558–67.
Dunne JA, Williams RJ, Martinez ND. 2002b. Food-web structure and network theory: the role of connectance and size. Proc Natl Acad Sci USA 99:12917–22.
Dunne JA, Williams RJ, Martinez ND. 2004. Network structure and robustness of marine food webs. Mar Ecol Prog Ser 273:291–302.
Dunne JA, Williams RJ. 2009. Cascading extinctions and community collapse in model food webs. Proc Natl Acad Sci 364:1711–23.
Elton CS. 1927. Animal ecology. University of Chicago Press. 207 p.
Freer JJ, Tarling GA, Collins MA, Partridge JC, Genner MJ. 2019. Predicting future distributions of lanternfish, a significant ecological resource within the Southern Ocean. Div Distrib 25:1259–72.
Gilbert AJ. 2009. Connectance indicates the robustness of food webs when subjected to species loss. Ecol Indicat 9:72–80.
Gray C, Figueroa DH, Hudson LN, Ma A, Perkins D, Woodward G. 2015. Joining the dots: an automated method for constructing food webs from compendia of published interactions. Food Webs 5:11–20.
Gutt J, Bertler N, Bracegirdle TJ, Buschmann A, Comiso J, Hosie G, Isla E, Schloss IR, Smith CR, Tournadre J, Xavier JC. 2015. The Southern Ocean ecosystem under multiple climate change stresses an integrated circumpolar assessment. Global Change Biol 21:1434–53.
Hansen B, Bjornsen PK, Hansen PJ. 1994. The size ratio between planktonic predators and their prey. Limnol Oceanogr 39:395–403.
Hattab T, Leprieur F, Lasram FBR, Gravel D, Loc’h FL, Albouy C. 2016. Forecasting finescale changes in the food-web structure of coastal marine communities under climate change. Ecography 39(12):1227–37.
Hill SL, Keeble K, Atkinson A, Murphy EJ. 2012. A food web model to explore uncertainties in the South Georgia shelf pelagic ecosystem. Deep Sea Res Part II Topic Stud in Oceanogr 59:237–52.
Hudson LN, Reuman D, Emerson R. 2020. Cheddar: analysis and visualisation of ecological communities. R package version 0.1-636. https://github.com/quicklizard99/cheddar/
Hyrenbach KD, Forney KA, Dayton PK. 2000. Marine protected areas and ocean basin management. Aquat Conserv Mar Freshw Ecosyst 10:437–58.
Jacob U, Thierry A, Brose U, Arntz WE, Berg S, Brey T, Fetzer I, Jonsson T, Mintenbeck K, Möllmann C, Petchey OL, Riede JO, Dunne JA. 2011. The role of body size in complex food webs: a cold case. Adv Ecol Res 45:181–223.
Jordá G, Marbà N, Bennett S, Santana-Garcon J, Agusti S, Duarte CM. 2020. Ocean warming compresses the three-dimensional habitat of marine life. Nat Ecol Evol 4:109–14.
Kassen R. 2002. The experimental evolution of specialists, generalists, and the maintenance of diversity. J Evol Biol 15:173–90.
Kones JK, Soetaert K, van Oevelen D, Owino J. 2009. Are network indices robust indicators of food web functioning? A Monte Carlo approach. Ecol Modell 220:370–82.
Kortsch S, Primicerio R, Fossheim M, Dolgov AV, Aschan M. 2015. Climate change alters the structure of arctic marine food webs due to poleward shifts of boreal generalists. Proc Roy Soc B Biol Sci 282:20151546.
Kortsch S, Primicerio R, Aschan M, Lind S, Dolgov AV, Planque B. 2019. Food- web structure varies along environmental gradients in a high- latitude marine ecosystem. Ecography 42(2):295–308.
Kortsch S, Frelat R, Pecuchet L, Olivier P, Putnis I, Bonsdorff E, Ojaaver H, Jurgensone I, Strāķe S, Rubene G, Krūze E, Nordström MC. 2021. Disentangling temporal food web dynamics facilitates understanding of ecosystem functioning. J Animal Ecol 1–12.
Laigle I, Aubin I, Digel C, Brose U, Boulangeat I, Gravel D. 2018. Species traits as drivers of food web structure. Oikos 127:316–26.
Lopez-Lopez L, Genner M, Tarling G, Saunders R, O'Gorman E. 2020. Pelagic trophic network in the Scotia Sea (2006–2009) (Version 1.0). UK Polar Data Centre, Natural Environment Research Council, UK Research & Innovation
Lourenço S, Saunders RA, Collins M, Shreeve R, Assis CA, Belchier M, Watkins JL, Xavier JC. 2017. Life cycle, distribution and trophodynamics of the lanternfish Krefftichthys anderssoni (Lönnberg, 1905) in the Scotia Sea. Polar Biol 40:1229–45.
Mackey AP, Atkinson A, Hill SL, Ward P, Cunningham NJ, Johnston NM, Murphy EJ. 2012. Antarctic macrozooplankton of the southwest Atlantic sector and Bellingshausen Sea: baseline historical distributions (Discovery Investigations, 1928–1935) related to temperature and food, with projections for subsequent ocean warming. Deep Sea Res Part II Topic Stud Oceanogr 59:130–46.
Marshall NB. 1979. Deep sea biology: developments and perspectives. Garland: STMP Press. p 566.
May RM. 1972. Will a complex system be stable? Nature 238:824–7.
McCann K, Hastings A. 1997. Re-evaluating the omnivory-stability relationship in food webs. Proc Roy Soc B Biol Sci 264:1249–54.
Montoya JM, Solé RV. 2003. Topological properties of food webs: from real data to community assembly models. Oikos 102:614–22.
Murphy EJ, Watkins JL, Trathan PN, Reid K, Meredith MP, Thorpe SE, Johnston NM, Clarke A, Tarling GA, Colins MA, Forcada J, Shreeve RS, Atkinson A, Korb R, Whitehouse MJ, Ward P, Rodhouse PG, Enderlein P, Hirst AG, Martin AR, Hill SL, Staniland IJ, Pond DW, Briggs DR, Cunningham NJ, Fleming AH. 2007. Spatial and temporal operation of the Scotia Sea ecosystem: a review of large-scale links in a krill centred food web. Philos Trans Roy Soc Lond B Biol Sci 362:113–48.
Murphy EJ, Cavanagh RD, Drinkwater KF, Grant SM, Heymans JJ, Hofmann EE, Hunt GL, Johnston NM. 2016. Understanding the structure and functioning of polar pelagic ecosystems to predict the impacts of change. Proc Roy Soc B Biol Sci 283:20161646.
Newman ME, Girvan M. 2004. Finding and evaluating community structure in networks. Phys Rev E 69:026113.
Olmo Gilabert R, Navia AF, De La Cruz-Agüero G, Molinero JC, Sommer U, Scotti M. 2019. Body size and mobility explain species centralities in the Gulf of California food web. Commun Ecol 20:149–60.
Park J, Oh IS, Kim HC, Yoo S. 2010. Variability of SeaWiFs chlorophyll-a in the southwest Atlantic sector of the Southern Ocean: Strong topographic effects and weak seasonality. Deep Sea Res Part I Oceanogr Res Papers 57:604–20.
Pickett ST. 1989. Space-for-time substitution as an alternative to long-term studies. In: Likens GE, Ed. Long-term studies in ecology New York: Springer. pp. 110–135.
Poloczanska ES, Brown CJ, Sydeman WJ, Kiessling W, Schoeman DS, Moore PJ, Brander K, Bruno JF, Buckley LB, Burrows MT, Duarte CM, Halpern BS, Holding J, Kappel CV, O’Connor MI, Pandolfi JM, Parmesan C, Schwing F, Thompson SA, Richardson AJ. 2013. Global imprint of climate change on marine life. Nat Clim Change 3:919–25.
R Core Team. 2020. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.
Ramirez-Llodra EZ, Brandt A, Danovaro R, De Mol B, Escobar E, German CR, Levin LA, Martinez Arbizu P, Menot L, Buhl- Mortensen P, Narayanaswamy BE, Smith CR, Tittensor DP, Tyler PA, Vanreusel A, Vecchione M. 2010. Deep, diverse and definitely different: unique attributes of the world’s largest ecosystem. Biogeosciences 7:2851–99.
Raymond B. 2011. A circumpolar pelagic regionalisation of the Southern Ocean. Short note submitted to the CCAMLR Workshop on Marine Protected Areas held in Brest, France.
Reichardt J, Bornholdt S. 2006. Statistical mechanics of community detection. Phys Rev E 74:016110.
Rezende EL, Albert EM, Fortuna MA, Bascompte J. 2009. Compartments in a marine food web associated with phylogeny, body mass, and habitat structure. Ecol Lett 12(8):779–88.
Reynolds CS. 2008. A changing paradigm of pelagic food webs. Int Rev Hydrobiol 93:517–31.
Robison BH. 2004. Deep pelagic biology. J Exp Mar Biol Ecol 300:253–72.
Robison BH. 2009. Conservation of deep pelagic biodiversity. Conserv Biol 23:847–58.
Robinson C, Steinberg DK, Anderson TR, Aristegui J, Carlson CA, Frost JR, Ghiglione JF, Hernández-Leon S, Jackson GA, Koppelmann R, Quéguiner B, Ragueneau O, Rassoulzadegan F, Robison BH, Tamburini C, Tanaka T, Wishner KF, Zhang J. 2010. Mesopelagic zone ecology and biogeochemistry—a synthesis. Deep-Sea Res Part II 57:1504–18.
Saravia LA, Marina TI, De Troch M, Momo FR. 2019. Ecological Network assembly: how the regional meta web influence local food webs. bioRxivdoi: https://doi.org/10.1101/340430
Saunders RA, Collins MA, Foster E, Shreeve R, Stowasser G, Ward P, Tarling GA. 2014. The trophodynamics of Southern Ocean Electrona (Myctophidae) in the Scotia Sea. Polar Biol 37:789–807.
Saunders RA, Collins MA, Ward P, Stowasser G, Shreeve R, Tarling GA. 2015a. Distribution, population structure and trophodynamics of Southern Ocean Gymnoscopelus (Myctophidae) in the Scotia Sea. Polar Biol 38:287–308.
Saunders RA, Collins MA, Ward P, Stowasser G, Shreeve R, Tarling GA. 2015b. Trophodynamics of Protomyctophum (Myctophidae) in the Scotia Sea (Southern Ocean). J Fish Biol 87:1031–58.
Scotti M, Bondavalli C, Bodini A, Allesina S. 2009. Using trophic hierarchy to understand food web structure. Oikos 118:1695–702.
Schuetz JG, Mills KE, Allyn AJ, Stamieszkin K, Bris AL, Pershing AJ. 2019. Complex patterns of temperature sensitivity, not ecological traits, dictate diverse species responses to climate change. Ecography 42:111–24.
Smith- Ramesh LM, Moore AC, Schmitz OJ. 2017. Global synthesis suggests that food web connectance correlates to invasion resistance. Global Change Biol 23:465–73.
Stouffer DB, Bascompte J. 2011. Compartmentalization increases food-web persistence. Proc Natl Acad Sci USA 108:3648–52.
Strogatz SH. 2001. Exploring complex networks. Nature 410:268–76.
Tarling GA, Ward P, Atkinson A, Collins MA, Murphy EJ. 2012a. DISCOVERY 2010: Spatial and temporal variability in a dynamic polar ecosystem. Deep Sea Res Part II Topic Stud Oceanogr 59:1–13.
Tarling GA, Stowasser G, Ward P, Poulton AJ, Zhou M, Venables HJ, McGill RAR, Murphy EJ. 2012b. Seasonal trophic structure of the Scotia Sea pelagic ecosystem considered through biomass spectra and stable isotope analysis. Deep Sea Res Part II Topic Stud Oceanogr 59:222–36.
Tarling GA, Ward P, Thorpe SE. 2018. Spatial distributions of Southern Ocean mesozooplankton communities have been resilient to long-term surface warming. Global Change Biol 24:132–42.
Thompson RM, Brose U, Dunne JA, Hall RO, Hladyz S, Kitching RL, Martinez ND, Rantala H, Romanuk TN, Stouffer DB. 2012. Food webs: reconciling the structure and function of biodiversity. Trends Ecol Evol 27:689–97.
Tittensor DP, Mora C, Jetz W, Lotze HK, Ricard D, Berghe EV, Worm B. 2010. Global patterns and predictors of marine biodiversity across taxa. Nature 466:1098–101.
Troudet J, Grandcolas P, Blin A, Vignes-Lebbe R, Legendre F. 2017. Taxonomic bias in biodiversity data and societal preferences. Sci Rep 7:9132.
Ward P, Whitehouse M, Meredith M, Murphy E, Shreeve R, Korb R, Watkins J, Thorpe S, Woodd-Walker R, Brierley A, Cunningham N, Grant S, Bone D. 2002. The southern antarctic circumpolar current front: physical and biological coupling at South Georgia. Deep Sea Res Part I Oceanogr Res Papers 49:2183–202.
Ward P, Atkinson A, Venables HJ, Tarling GA, Whitehouse MJ, Fielding S, Collins MA, Korb R, Black A, Stowasser G, Schmidt K, Thorpe SE, Enderlein P. 2012. Food web structure and bioregions in the Scotia Sea: a seasonal synthesis. Deep Sea Res Part II Topic Stud Oceanogr 59:253–66.
Ward P, Tarling GA, Thorpe SE. 2018. Temporal changes in abundances of large calanoid copepods in the Scotia Sea: comparing the 1930s with contemporary times. Polar Biol 4:2297–310.
Watts DJ, Strogatz SH. 1998. Collective dynamics of ‘small-world’networks. Nature 393(6684):440–42.
Whitworth T III. 1980. Zonation and geostrophic flow of the Antarctic circumpolar current at Drake Passage. Deep Sea Res Part I Oceanogr Res Papers 27:497–507.
Whitehouse MJ, Meredith MP, Rothery P, Atkinson A, Ward P, Korb RE. 2008. Rapid warming of the ocean around South Georgia, Southern Ocean, during the 20th century: forcings, characteristics and implications for lower trophic levels. Deep Sea Res Part I Oceanogr Res Papers 55:1218–28.
Williams RJ, Martinez ND. 2004. Limits to trophic levels and omnivory in complex food webs: theory and data. Am Nat 163:458–68.
Williams RJ. 2010. Network3D Software. Cambridge, UK: Microsoft Research.
Woodward G, Benstead JP, Beveridge OS, Blanchard J, Brey T, Brown LE, Cross WF, Friberg N, Ings TC, Jacob U, Jennings S, Ledger ME, Milner AM, Montoya JM, O’Gorman E, Olesen JM, Petchey OL, Pichler DE, Reuman DC, Thompson MSA, Van Veen FJF, Yvon-Durocher G. 2010. Ecological networks in a changing climate. Adv Ecol Res 42:71–138.
Wootton KL. 2017. Omnivory and stability in freshwater habitats: Does theory match reality? Freshw Biol 62:821–32.
Yoon I, Williams RJ, Levine E, Yoon S, Dunne JA, Martinez ND. 2004. Webs on the Web (WoW): 3D visualization of ecological networks on the WWW for collaborative research and education. Proc IS&T/SPIE Symp Electron Imag vis Data Anal 5295:124–32.
ACKNOWLEDGEMENTS
We are grateful to the SeaDNA project team for the fruitful discussions during the development of this work, particularly to Laura Balcells and Stefano Mariani. We are also thankful to Jennifer Dunne, Susanne Kortsch, Lawrence N. Hudson, and Richard J. Williams, who kindly responded to our queries regarding methods for network analyses. We also acknowledge the work of the British Antarctic Survey during the Discovery project and, generally, the work of marine polar ecologists over recent decades; without their dedicated research, studies like ours would simply not be possible. The work was supported by NERC Highlight Topic Grant NE/N005937/1, awarded to M.J.G. and E.J.O.G. and a NERC Fellowship (NE/L011840/1) awarded to E.J.O.G.
Author information
Authors and Affiliations
Corresponding author
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
López-López, L., Genner, M.J., Tarling, G.A. et al. Ecological Networks in the Scotia Sea: Structural Changes Across Latitude and Depth. Ecosystems 25, 457–470 (2022). https://doi.org/10.1007/s10021-021-00665-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10021-021-00665-1