journal article Open Access May 29, 2024

Individual diet variability shapes the architecture of Antarctic benthic food webs

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Abstract
AbstractAntarctic biodiversity is affected by seasonal sea-ice dynamics driving basal resource availability. To (1) determine the role of intraspecific dietary variability in structuring benthic food webs sustaining Antarctic biodiversity, and (2) understand how food webs and the position of topologically central species vary with sea-ice cover, single benthic individuals’ diets were studied by isotopic analysis before sea-ice breakup and afterwards. Isotopic trophospecies (or Isotopic Trophic Units) were investigated and food webs reconstructed using Bayesian Mixing Models. As nodes, these webs used either ITUs regardless of their taxonomic membership (ITU-webs) or ITUs assigned to species (population-webs). Both were compared to taxonomic-webs based on taxa and their mean isotopic values. Higher resource availability after sea-ice breakup led to simpler community structure, with lower connectance and linkage density. Intra-population diet variability and compartmentalisation were crucial in determining community structure, showing population-webs to be more complex, stable and robust to biodiversity loss than taxonomic-webs. The core web, representing the minimal community ‘skeleton’ that expands opportunistically while maintaining web stability with changing resource availability, was also identified. Central nodes included the sea-urchin Sterechinus neumayeri and the bivalve Adamussium colbecki, whose diet is described in unprecedented detail. The core web, compartmentalisation and topologically central nodes represent crucial factors underlying Antarctica’s rich benthic food web persistence.
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References
149
[1]
Elton, C. Animal Ecology (Macmillan Co, New York, NY, 1927).
[2]
[3]
Will a Large Complex System be Stable?

Robert M. May

Nature 1972 10.1038/238413a0
[4]
May, R. M. Stability and Complexity in Model Ecosystems (Princeton University Press, 1974).
[5]
Paine, R. T. Food webs: Linkage, interaction strength and community infrastructure. J. Anim. Ecol. 49, 667–685 (1980). 10.2307/4220
[6]
Consequences of changing biodiversity

F. Stuart Chapin III, Erika S. Zavaleta, Valerie T. Eviner et al.

Nature 2000 10.1038/35012241
[7]
Thompson, R. M. et al. Food webs: Reconciling the structure and function of biodiversity. Trends Ecol. Evol. 27, 689–697 (2012). 10.1016/j.tree.2012.08.005
[8]
Gibert, J. P. Temperature directly and indirectly influences food web structure. Sci. Rep. 9, 5312 (2019). 10.1038/s41598-019-41783-0
[9]
Rossi, L. et al. Antarctic food web architecture under varying dynamics of sea ice cover. Sci. Rep. 9, 1–13 (2019). 10.1038/s41598-019-48245-7
[10]
Sporta Caputi, S. et al. Seasonal food web dynamics in the Antarctic Benthos of Tethys Bay (Ross Sea): Implications for biodiversity persistence under different seasonal sea-ice coverage. Front. Mar. Sci. 7, 594454 (2020). 10.3389/fmars.2020.594454
[11]
McCormack, S. A. et al. Southern ocean food web modelling: Progress, prognoses, and future priorities for research and policy makers. Front. Ecol. Evol. 9, 624763 (2021). 10.3389/fevo.2021.624763
[12]
McMeans, B. C., McCann, K. S., Humphries, M., Rooney, N. & Fisk, A. T. Food web structure in temporally-forced ecosystems. Trends Ecol. Evol. 30, 662–672 (2015). 10.1016/j.tree.2015.09.001
[13]
Food Web Complexity and Community Dynamics

Gary A. Polis, Donald R. Strong

The American Naturalist 1996 10.1086/285880
[14]
Norkko, A. et al. Trophic structure of coastal Antarctic food webs associated with changes in sea ice and food supply. Ecology 88, 2810–2820 (2007). 10.1890/06-1396.1
[15]
Clark, G. F. et al. Light-driven tipping points in polar ecosystems. Glob. Change Biol. 19, 3749–3761 (2013). 10.1111/gcb.12337
[16]
Constable, A. J. et al. Climate change and Southern Ocean ecosystems I: How changes in physical habitats directly affect marine biota. Glob. Change Biol. 20, 3004–3025 (2014). 10.1111/gcb.12623
[17]
Calizza, E., Careddu, G., Sporta Caputi, S., Rossi, L. & Costantini, M. L. Time- and depth-wise trophic niche shifts in Antarctic benthos. PLoS ONE 13, e0194796 (2018). 10.1371/journal.pone.0194796
[18]
Gutt, J. Some, “driving forces” structuring communities of the sublittoral Antarctic macrobenthos. Antarct. Sci. 12, 297–313 (2000). 10.1017/s0954102000000365
[19]
Chown, S. L. et al. The changing form of Antarctic biodiversity. Nature 522, 431–438 (2015). 10.1038/nature14505
[20]
Rogers, A. D. et al. Antarctic futures: An assessment of climate-driven changes in ecosystem structure, function, and service provisioning in the Southern Ocean. Annu. Rev. Mar. Sci. 12, 87–120 (2020). 10.1146/annurev-marine-010419-011028
[21]
Pusceddu, A., Cattaneo-Vietti, R., Albertelli, G. & Fabiano, M. Origin, biochemical composition and vertical flux of particulate organic matter under the pack ice in Terra Nova Bay (Ross Sea, Antarctica) during late summer 1995. Polar Biol. 22, 124–132 (1999). 10.1007/s003000050399
[22]
Wing, S. R. et al. Contribution of sea ice microbial production to Antarctic benthic communities is driven by sea ice dynamics and composition of functional guilds. Glob. Change Biol. 24, 3642–3653 (2018). 10.1111/gcb.14291
[23]
Lizotte, M. P. The contributions of sea ice algae to Antarctic marine primary production. Am. Zool. 41, 57–73 (2001).
[24]
Dayton, P. K., Mordida, B. J. & Bacon, F. Polar marine communities. Integr. Comp. Biol. 34, 90–99 (1994).
[25]
Rooney, N. & McCann, K. S. Integrating food web diversity, structure and stability. Trends Ecol. Evol. 27, 40–46 (2012). 10.1016/j.tree.2011.09.001
[26]
Rosenblatt, A. E. & Schmitz, O. J. Climate change, nutrition, and bottom-up and top-down food web processes. Trends Ecol. Evol. 31, 965–975 (2016). 10.1016/j.tree.2016.09.009
[27]
Petchey, O. L., Beckerman, A. P., Riede, J. O. & Warren, P. H. Size, foraging, and food web structure. Proc. Natl. Acad. Sci. 105, 4191–4196 (2008). 10.1073/pnas.0710672105
[28]
Feiner, Z. S. et al. Individual and spatial variation are as important as species-level variation to the trophic complexity of a lentic food web. Ecol. Freshw. Fish 28, 516–532 (2019). 10.1111/eff.12472
[29]
Layman, C. A. et al. Applying stable isotopes to examine food-web structure: An overview of analytical tools. Biol. Rev. 87, 545–562 (2012). 10.1111/j.1469-185x.2011.00208.x
[30]
Sporta Caputi, S. et al. Changing isotopic food webs of two economically important fish in Mediterranean coastal lakes with different trophic status. Appl. Sci. 10, 2756 (2020). 10.3390/app10082756
[31]
Akçakaya, H. R. et al. Assessing ecological function in the context of species recovery. Conserv. Biol. 34, 561–571 (2020). 10.1111/cobi.13425
[32]
Mérillet, L. et al. Effects of life-history traits and network topological characteristics on the robustness of marine food webs. Glob. Ecol. Conserv. 34, e02048 (2022).
[33]
Robinson, B. J. O., Barnes, D. K. A., Grange, L. J. & Morley, S. A. The extremes of disturbance reduce functional redundancy: Functional trait assessment of the shallow Antarctic benthos. Front. Mar. Sci. 8, 797 (2022). 10.3389/fmars.2021.797112
[34]
Ings, T. C. et al. Ecological networks–beyond food webs. J. Anim. Ecol. 78, 253–269 (2009). 10.1111/j.1365-2656.2008.01460.x
[35]
Martinez, N. D. Effects of resolution on food web structure. Oikos 66, 403–412 (1993). 10.2307/3544934
[36]
Fulton, E. A., Smith, A. D. M. & Johnson, C. R. Effect of complexity on marine ecosystem models. Mar. Ecol. Prog. Ser. 253, 1–16 (2003). 10.3354/meps253001
[37]
Bates, M. L. et al. Construction of a trophically complex near-shore Antarctic food web model using the Conservative Normal framework with structural coexistence. J. Mar. Syst. 145, 1–14 (2015). 10.1016/j.jmarsys.2014.12.002
[38]
Moran, N. P., Wong, B. B. M. & Thompson, R. M. Weaving animal temperament into food webs: Implications for biodiversity. Oikos 126, 917–930 (2017). 10.1111/oik.03642
[39]
Johnson, S., Domínguez-García, V., Donetti, L. & Muñoz, M. A. Trophic coherence determines food-web stability. Proc. Natl. Acad. Sci. 111, 17923–17928 (2014). 10.1073/pnas.1409077111
[40]
Rubenstein, M. A. et al. Do empirical observations support commonly-held climate change range shift hypotheses? A systematic review protocol. Environ. Evid. 9, 10 (2020). 10.1186/s13750-020-00194-9
[41]
Steele, J. H. Assessment of some linear food web methods. J. Mar. Syst. 76, 186–194 (2009). 10.1016/j.jmarsys.2008.05.012
[42]
Thomaz, S. M. et al. Using space-for-time substitution and time sequence approaches in invasion ecology. Freshw. Biol. 57, 2401–2410 (2012). 10.1111/fwb.12005
[43]
Cucherousset, J. & Olden, J. D. Ecological impacts of nonnative freshwater fishes. Fisheries 36, 215–230 (2011). 10.1080/03632415.2011.574578
[44]
Costantini, M. L. et al. The role of alien fish (the centrarchid Micropterus salmoides) in lake food webs highlighted by stable isotope analysis. Freshw. Biol. 63, 1130–1142 (2018). 10.1111/fwb.13122
[45]
Influence of diet on the distribution of carbon isotopes in animals

Michael J. DeNiro, Samuel Epstein

Geochimica et Cosmochimica Acta 1978 10.1016/0016-7037(78)90199-0
[46]
STABLE ISOTOPES IN ECOSYSTEM STUDIES

Bruce J. Peterson, Brian Fry

Annual Review of Ecology and Systematics 1987 10.1146/annurev.es.18.110187.001453
[47]
Careddu, G. et al. Effects of terrestrial input on macrobenthic food webs of coastal sea are detected by stable isotope analysis in Gaeta Gulf. Estuar. Coast. Shelf Sci. 154, 158–168 (2015). 10.1016/j.ecss.2015.01.013
[48]
Sporta Caputi, S. et al. Trophic attractiveness for soil fauna of residues of Bt and near-isogenic maize: A C and N stable isotope-based study. Agric. Ecosyst. Environ. 329, 107868 (2022). 10.1016/j.agee.2022.107868
[49]
Calizza, E. et al. Climate-related drivers of nutrient inputs and food web structure in shallow Arctic lake ecosystems. Sci. Rep. 12, 2125 (2022). 10.1038/s41598-022-06136-4
[50]
McCutchan, J. H., Lewis, W. M., Kendall, C. & McGrath, C. C. Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102, 378–390 (2003). 10.1034/j.1600-0706.2003.12098.x

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Published
May 29, 2024
Vol/Issue
14(1)
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Funding
Ministero dell’Istruzione, dell’Università e della Ricerca Award: PNRA16_00291 (LR)
Cite This Article
Simona Sporta Caputi, Jerzy Piotr Kabala, Loreto Rossi, et al. (2024). Individual diet variability shapes the architecture of Antarctic benthic food webs. Scientific Reports, 14(1). https://doi.org/10.1038/s41598-024-62644-5