Pre-Lessepsian isotopic niche spaces: using paleoecological proxies to assess the impact of ongoing bioinvasions on fishes in the eastern Mediterranean Sea
Published:
Jun 3, 2025
Keywords:
marine historical ecology Lessepsian migrations bioinvasions stable isotopes isotopic niche space marine fish trophic ecology
Abstract
Ongoing bioinvasions of Lessepsian species via the Suez Canal have profoundly altered marine coastal ecosystems in the eastern Mediterranean. In response to these Lessepsian migrations, some indigenous fishes have been observed to have widened their trophic niches and diversified their foraging strategies. Effects of invasive taxa are further compounded by modern anthropogenic drivers such as overfishing, habitat degradation, and pollution. The scale and characteristics of these recent changes in trophodynamics for broader ichthyofaunal communities are poorly understood due to a lack of data predating Lessepsian migrations; paleoecological data is, therefore, essential. Here, we present a substantial body of new carbon (δ13C) and nitrogen (δ15N) isotopic data from Middle to Late Holocene archaeological fish collagen (n=137), combined with previously published results (n=44) to establish paleoecological baselines for the region. An emphasis is placed on groupers (Epinephelidae) due to their high ubiquity in Mediterranean archaeological contexts and importance to rocky reef ecosystems today. We demonstrate that modern, indigenous Mediterranean fish have expanded their trophic niches beyond their pre Lessepsian migrations baseline foraging ecology. Paleo data further show that fishes in middle and lower trophic levels have the highest degree of overlap in isotopic niche spaces, suggesting greater levels of competition for trophic resources. Our study highlights the importance of integrating data from historical ecological baselines into our assessments of bioinvasions and, more broadly, anthropogenically driven ecosystem alterations.
Article Details
- How to Cite
-
WINTER, R. M., DESIDERÁ, E., GUIDETTI, P., VON TERSCH, M., DEE, M., ALEXANDER, M., & ÇAKIRLAR, C. (2025). Pre-Lessepsian isotopic niche spaces: using paleoecological proxies to assess the impact of ongoing bioinvasions on fishes in the eastern Mediterranean Sea. Mediterranean Marine Science, early view. https://doi.org/10.12681/mms.40039
- Issue
- early view
- Section
- Early View_vol. 26, n. 3, 2025
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution Non-Commercial License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g. post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are permitted and encouraged to post their work online (preferably in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).
Downloads
Download data is not yet available.
References
Agiadi, K., Albano, P.G., 2020. Holocene fish assemblages provide baseline data for the rapidly changing eastern Mediterranean. The Holocene, 30 (10), 1438-1450.
Albeke, S.E., 2017. rKIN:(kernel) isotope niche estimation. See https://github. com/cran/rKIN (Accessed 04 January 2022).
Apostolaki, E.T., Vizzini, S., Santinelli, V., Kaberi, H., Andolina, C. et al., 2019. Exotic Halophila stipulacea is an introduced carbon sink for the Eastern Mediterranean Sea. Scientific Reports, 9 (1), 9643.
Bariche, M., Letourneur, Y., Harmelin-Vivien, M., 2004. Temporal fluctuations and settlement patterns of native and Lessepsian herbivorous fishes on the Lebanese coast (eastern Mediterranean). Environmental Biology of Fishes, 70, 81-90.
Bearhop, S., Adams, C.E., Waldron, S., Fuller, R.A., Macleod, H., 2004. Determining trophic niche width: a novel approach using stable isotope analysis. The Journal of Animal Ecology, 73 (5), 1007-1012.
Boudouresque, C.F., Blanfuné, A., Fernandez, C., Lejeusne, C., Pérez, T. et al., 2017. Marine biodiversity-warming vs. biological invasions and overfishing in the Mediterranean Sea: take care,’One Train can hide another’. MOJ Ecology & Environmental Sciences, 2 (4), 1-13.
Casale, P., Broderick, A.C., Camiñas, J.A., Cardona, L., Carreras, C. et al., 2018. Mediterranean sea turtles: current knowledge and priorities for conservation and research. Endangered Species Research, 36, 229-267.
Corrales, X., Ofir, E., Coll, M., Goren, M., Edelist, D. et al., 2017. Modeling the role and impact of alien species and fisheries on the Israeli marine continental shelf ecosystem. Journal of Marine Systems, 170, 88-102.
Dee, M.W., Palstra, S.W.L., Aerts-Bijma, A., Bleeker, M.O., de Bruijn, S. et al., 2020. Radiocarbon Dating at Groningen: New and Updated Chemical Pretreatment Procedures. Radiocarbon, 62 (1), 63-74.
de Kock, W., Hasler-Sheetal, H., Holmer, M., Tsapakis, M., Apostolaki, E.T., 2020. Metabolomics and traditional indicators unveil stress of a seagrass (Cymodocea nodosa) meadow at intermediate distance from a fish farm. Ecological Indicators, 109, 105765.
de Kock, W., Mackie, M., Ramsøe, M., Allentoft, M.E., Broderick, A.C. et al., 2023. Threatened North African seagrass meadows have supported green turtle populations for millennia. Proceedings of the National Academy of Sciences of the United States of America, 120 (30), e2220747120.
DeNiro, M.J., 1985. Postmortem preservation and alteration of in vivo bone collagen isotope ratios in relation to palaeodietary reconstruction. Nature, 317 (6040), 806-809.
Desse, J., Desse-Berset, N., 1999. Préhistoire du mérou. Marine Life, 9 (1), 19-30. Eckrich, C.A., Albeke, S.E., Flaherty, E.A., Bowyer, R.T., Ben-David, M., 2020. rKIN: Kernel-based method for estimating isotopic niche size and overlap. The Journal of Animal Ecology, 89 (3), 757-771.
Edelist, D., Rilov, G., Golani, D., Carlton, J.T., 2013. Restructuring the Sea: Profound shifts in the world’s most invaded marine ecosystem. Diversity, 19, 69-77.
Estes, J.A., Terborgh, J., Brashares, J.S., Power, M.E., Berger, J. et al., 2011. Trophic downgrading of planet Earth. Science, 333 (6040), 301-306.
Fanelli, E., Azzurro, E., Bariche, M., Cartes, J.E., Maynou, F., 2015. Depicting the novel Eastern Mediterranean food web: a stable isotopes study following Lessepsian fish invasion. Biological Invasions, 17 (7), 2163-2178.
Froese, R., Pauly, D., 2023. FishBase. www.fishbase.org
Fuller, B.T., Müldner, G., Van Neer, W., Ervynck, A., Richards, M.P., 2012. Carbon and nitrogen stable isotope ratio analysis of freshwater, brackish and marine fish from Belgian archaeological sites (1st and 2nd millennium AD). Journal of Analytical Atomic Spectrometry, 27 (5), 807-820.
Fuller, B.T., Van Neer, W., Linseele, V., De Cupere, B., Chahoud, J. et al., 2020. Fish δ13C and δ15N results from two Bronze/Iron Age sites (Tell Tweini & Sidon) along the Levantine coast. Journal of Archaeological Science: Reports, 29, 102066.
Galil, B.S., Goren, M., 2014. Metamorphoses: Bioinvasions in the Mediterranean Sea. p. 463-478. In: The Mediterranean Sea: Its history and present challenges. Goffredo, S., Dubinsky, Z. (Eds). Springer, Netherlands.
Garcia-Guixé, E., Subirà, M.E., Marlasca, R., Richards, M.P., 2010. δ13C and δ15N in ancient and recent fish bones from the Mediterranean Sea. Journal of Nordic Archaeological Science, 17, 83-92.
Gates, M.H., Gates, C., Redford, S., Eger, A.A., 2015. Excavations at Kinet Höyük and Hisn Al-Tinat. Hatay Arkeolojik Kazı ve Araştırmaları, 157-171.
Genz, H., 2010. Recent excavations at Tell Fadous-Kfarabida. Near Eastern Archaeology, 73 (2-3), 102-113.
Giakoumi, S., Pey, A., Thiriet, P., Francour, P., Guidetti, P., 2019. Patterns of predation on native and invasive alien fish in Mediterranean protected and unprotected areas. Marine Environmental Research, 150, 104792.
Givan, O., Edelist, D., Sonin, O., Belmaker, J., 2018. Thermal affinity as the dominant factor changing Mediterranean fish abundances. Global Change Biology, 24 (1), e80-e89.
Goren, M., Galil, B.S., 2005. A review of changes in the fish assemblages of Levantine inland and marine ecosystems following the introduction of non-native fishes. Zeitschrift Fur Angewandte Ichthyologie = Journal of Applied Ichthyology, 21 (4), 364-370.
Goren, M., Galil, B.S., Diamant, A., Stern, N., Levitt-Barmats, Y., 2016. Invading up the food web? Invasive fish in the southeastern Mediterranean Sea. Marine Biology, 163 (8), 180.
Grupe, G., Heinrich, D., Peters, J., 2009. A brackish water aquatic foodweb: trophic levels and salinity gradients in the Schlei fjord, Northern Germany, in Viking and medieval times. Journal of Archaeological Science, 36 (10), 2125-2144.
Guidetti, P., Baiata, P., Ballesteros, E., Di Franco, A., Hereu, B. et al., 2014. Large-scale assessment of Mediterranean marine protected areas effects on fish assemblages. PloS One, 9 (4), e91841.
Guiry, E.J., Needs-Howarth, S., Friedland, K.D., Hawkins, A.L., Szpak, P. et al., 2016. Lake Ontario salmon (Salmo salar) were not migratory: A long-standing historical debate solved through stable isotope analysis. Scientific Reports, 6, 36249.
Guiry, E.J., Szpak, P., 2021. Improved quality control criteria for stable carbon and nitrogen isotope measurements of ancient bone collagen. Journal of Archaeological Science, 132, 105416.
Guiry, E., Royle, T.C.A., Matson, R.G., Ward, H., Weir, T. et al., 2020. Differentiating salmonid migratory ecotypes through stable isotope analysis of collagen: Archaeological and ecological applications. PloS One, 15 (4), e0232180.
Haubrock, P.J., Balzani, P., Matsuzaki, S.I.S., Tarkan, A.S., Kourantidou, M. et al., 2021. Spatio-temporal niche plasticity of a freshwater invader as a harbinger of impact variability. The Science of the Total Environment, 777, 145947.
Hedges, R.E.M., Clement, J.G., Thomas, C.D., O’Connell, T.C., 2007. Collagen turnover in the adult femoral midshaft: Modeled from anthropogenic radiocarbon tracer measurements. American Journal of Physical Anthropology, 133 (2), 808-816.
Hutchinson, G.E., 1957. Cold spring harbor symposium on quantitative biology. Concluding Remarks, 22, 415. Kamlah, J., Sader, H.S. (Eds), 2019. Tell el-Burak (Vol. 45). Abhandlungen des Deutschen Palästina-Vereins, 113.
Kragten, J., 1994. Tutorial review. Calculating standard deviations and confidence intervals with a universally applicable spreadsheet technique. The Analyst, 119 (10), 2161-2165.
Longin, R., 1971. New method of collagen extraction for radiocarbon dating. Nature, 230 (5291), 241-242.
Loponte, D., Corriale, M.J., 2020. Patterns of resource use and isotopic niche overlap among guanaco (Lama guanicoe), pampas deer (Ozotoceros bezoarticus) and marsh deer (Blastocerus dichotomus) in the pampas. Ecological, paleoenvironmental and archaeological implications. Environmental Archaeology, 25 (4), 411-444.
Lorrain, A., Pethybridge, H., Cassar, N., Receveur, A., Allain, V. et al., 2020. Trends in tuna carbon isotopes suggest global changes in pelagic phytoplankton communities. Global Change Biology, 26 (2), 458-470.
Magozzi, S., Yool, A., Vander Zanden, H.B., Wunder, M.B., Trueman, C.N., 2017. Using ocean models to predict spatial and temporal variation in marine carbon isotopes. Ecosphere , 8 (5), e01763.
Misarti, N., Finney, B., Maschner, H., Wooller, M.J., 2009. Changes in northeast Pacific marine ecosystems over the last 4500 years: evidence from stable isotope analysis of bone collagen from archeological middens. Holocene, 19 (8), 1139-1151.
Morales-Muñíz, A., 2010. Inferences about prehistoric fishing gear based on archaeological fish assemblages. p. 25-53. In: Ancient Nets and Fishing Gear, Proceedings of the International Workshop on Nets and Fishing Gear in Classical Antiquity: A First Approach, Cádiz, 15-17 November 2007. Universidad de Cádiz, Servicio de Publicaciones.
Mumby, P.J., Harborne, A.R., Brumbaugh, D.R., 2011. Grouper as a natural biocontrol of invasive lionfish. PloS One, 6 (6), e21510.
Newsome, S.D., Martinez del Rio, C., Bearhop, S., Phillips, D.L., 2007. A niche for isotopic ecology. Frontiers in Ecology and the Environment, 5 (8), 429-436.
Özyurt, C.E., Perker, M., Ki̇yağa, V.B., Mavruk, S., Kayaalp, G.T., 2018. Biomass of some Lessepsian fish species in the soft bottoms of Iskenderun Bay (Northeast Mediterranean). Review of Hydrobiology, 11(1), 23-39.
Pauly, D., Christensen, V., Dalsgaard, J., Froese, R., Torres, F., Jr., 1998. Fishing down marine food webs. Science, 279 (5352), 860-863.
Por, F.D., 1971. One Hundred Years of Suez Canal ‒ A Century of Lessepsian Migration: Retrospect and Viewpoints. Systematic Biology, 20 (2), 138-159.
Prato, G., Guidetti, P., Bartolini, F., Mangialajo, L., Francour, P., 2013. The importance of high-level predators in marine protected area management: Consequences of their decline and their potential recovery in the Mediterranean context. Advances in Oceanography and Limnology, 4 (2), 176-193.
Rilov, G., 2016. Multi-species collapses at the warm edge of a warming sea. Scientific Reports, 6, 36897.
Rilov, G., Peleg, O., Yeruham, E., Garval, T., Vichik, A. et al., 2018. Alien turf: Overfishing, overgrazing and invader domination in south-eastern Levant reef ecosystems. Aquatic Conservation: Marine and Freshwater Ecosystems, 28 (2), 351-369.
Robinson, J.R., 2021. Investigating isotopic niche space: Using rKIN for stable isotope studies in archaeology. Journal of Archaeological Method and Theory, 29 (3), 831-861.
Sala, E., Kizilkaya, Z., Yildirim, D., Ballesteros, E., 2011. Alien marine fishes deplete algal biomass in the Eastern Mediterranean. PloS One, 6 (2), e17356.
Sandias, M., Müldner, G., 2015. Diet and herding strategies in a changing environment: Stable isotope analysis of Bronze Age and Late Antique skeletal remains from Ya’amūn, Jordan. Journal of Archaeological Science, 63, 24-32.
Schulze, T., Dörner H., Baade, U., Hölker, F., 2012. Dietary niche partitioning in a piscivorous fish guild in response to stocking of an additional competitor–The role of diet specialisation. Limnologica, 42 (1), 56-64.
Schutkowski, H., Ogden, A., 2011. Sidon of the Plain, Sidon of the Sea-reflections on Middle Bronze Age diet in the Eastern Mediterranean. Archaeology & History in Lebanon, 34- 35, 213-225.
Shapiro Goldberg, D., Rilov, G., Villéger, S., Belmaker, J., 2021. Predation Cues Lead to Reduced Foraging of Invasive Siganus rivulatus in the Mediterranean. Frontiers in Marine Science, 8, 678848.
Szpak, P., Metcalfe, J.Z., Macdonald, R.A., 2017. Best practices for calibrating and reporting stable isotope measurements in archaeology. Journal of Archaeological Science: Reports, 13, 609-616.
Tsadok, R., Zemah-Shamir, Z., Shemesh, E., Martinez, S., Ramon, D. et al., 2023. Dietary habits change of Lessepsian migrants’ fish from the Red Sea to the Eastern Mediterranean Sea. Aquatic Invasions, 18 (4), 521-531.
Turan, C., Uygur, N., İğde, M., 2017. Lionfishes Pterois miles and Pterois volitans in the North-eastern Mediterranean Sea: Distribution, Habitation, Predation and Predators. Natural and Engineering Sciences, 2 (1), 35-43.
van Klinken, G. J., 1999. Bone Collagen Quality Indicators for Palaeodietary and Radiocarbon Measurements. Journal of Archaeological Science, 26 (6), 687-695.
Vika, E., Theodoropoulou, T., 2012. Re-investigating fish consumption in Greek antiquity: results from δ13C and δ15N analysis from fish bone collagen. Journal of Archaeological Science, 39 (5), 1618-1627.
Vizzini, S., Sarà, G., Michener, R.H., Mazzola, A., 2002. The trophic role of the macrophyte Cymodocea nodosa (Ucria) Asch. in a Mediterranean saltworks: Evidence from carbon and nitrogen stable isotope ratios. Bulletin of Marine Science, 71 (3), 1369-1378.
Wheeler, A., Jones, A.K.G., 1989. Fishes. Cambridge manuals in archaeology. Reports from the EAU, York. Report, 94, 54.
Winter, R.M., de Kock, W., Palsbøll, P.J., Çakirlar, C., 2021. Potential applications of biomolecular archaeology to the ecohistory of sea turtles and groupers in Levant coastal antiquity. Journal of Archaeological Science, Reports, 36 (102872), 102872.
Winter, R., Desiderà, E., Guidetti, P., Vermeersch, S., Demirel, N. et al., 2022. Catch of the Day: Abundance and Size Data of Groupers (Epinephelidae) and Combers (Serranidae) from Middle to Late Holocene Levantine Archaeological Contexts. The Journal of Island and Coastal Archaeology, 17 (4).
Winter, R.M., de Kock, W., Mackie, M., Ramsøe, M., Desiderà, E. et al.,2023. Grouping groupers in the Mediterranean: Ecological baselines revealed by ancient proteins. Ecology and Evolution, 13 (10), e10625.
Yeakel, J.D., Bhat, U., Elliott Smith, E.A., Newsome, S.D., 2016. Exploring the Isotopic Niche: Isotopic Variance, Physiological Incorporation, and the Temporal Dynamics of Foraging. Frontiers in Ecology and Evolution, 4.
Zohar, I., Belmaker, M., 2005. Size does matter: methodological comments on sieve size and species richness in fishbone assemblages. Journal of Archaeological Science, 32 (4), 635-641.
