Abstract
The attention towards non-native sea anemone introductions has been steadily increasing as multiple species are reported from new locations each year. However, a lack of monitoring efforts and difficulties associated with the detection and identification of these species may result in overlooking introductions in certain areas. In the southern hemisphere, one of these non-native species is Metridium senile, whose current taxonomic and invasion status in Argentina is unclear. Here, we pooled scientific and community records to shed light on the past, current and future invasion scenario of this species. First, we clarified the taxonomic and invasion status of suspected M. senile populations from Argentina by revising available morphological descriptions and attributes associated with non-native species. Then, we inferred and described the potential dispersal pattern in Argentina from the late 1890s to present day. Finally, we provided a forecast of the species potential distribution range in the Southwestern Atlantic Ocean, along the coast and in off-shore areas. Enough evidence suggests that M. senile is a non-native species that has successfully established in Argentina. This species has been mistakenly considered as native for decades due to taxonomic errors and historical and geographical gaps (i.e., pseudoindigenous species). Its current distribution range in Argentina covers over 2000 km of coastline with a southward expansion in recent years. Moreover, according to our forecasted potential distribution, this species can spread further and reach novel areas in coastal and off-shore locations. As M. senile combines multiple traits of a successful invader, monitoring efforts should be implemented to early detect or prevent its establishment in areas recently colonized or at risk.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data generated or analyzed during this study are included in this published article and its Supplementary Information files.
References
Acuña FH, Cortés J, Garese A, González-Muñoz R (2020) The sea anemone Exaiptasia diaphana (Actiniaria: Aiptasiidae) associated to rhodoliths at Isla del Coco National Park, Costa Rica. Rev Biol Trop 68:S283–S288. https://doi.org/10.15517/rbt.v68iS1.41191
Assis J, Tyberghein L, Bosch S et al (2018) Bio-ORACLE v2.0: extending marine data layers for bioclimatic modelling. Glob Ecol Biogeogr 27:277–284. https://doi.org/10.1111/geb.12693
Bachelet G, Simon-Bouhet B, Desclaux C, Garcia-Meunier P, Mairesse G, de Montaudouin X, Raigné H, Randriambao K, Sauriau PG, Viard F (2004) Invasion of the eastern Bay of Biscay by the nassariid gastropod Cyclope neritea: origin and effects on resident fauna. Mar Ecol Prog Ser 276:147–159. https://doi.org/10.3354/meps276147
Bailey SA, Brown L, Campbell ML et al (2020) Trends in the detection of aquatic non-indigenous species across global marine, estuarine and freshwater ecosystems: a 50-year perspective. Divers Distrib 26:1780–1797. https://doi.org/10.1111/ddi.13167
Battini N, Giachetti CB, Castro KL et al (2021) New invasive predator reduces the abundance of native prey in a cold-temperate marine fouling community. Aquat Conserv Mar Freshw Ecosyst 31:2842–2854. https://doi.org/10.1002/aqc.3681
Bravo G, Livore JP, Battini N et al (2021) Rocky reef biodiversity survey: Punta Pardelas, Argentina. Biodivers Data J 9:e72081. https://doi.org/10.3897/BDJ.9.e72081
Carlgren O (1899) Zoantharien. Hambg Magalhaensische Sammelreise 4:1–48
Carlgren O (1933) Zoantharia and actiniaria: the godthaab expedition 1928. Medd Gronland 79:1–55
Carlgren O (1936) Some west American sea anemones. J Wash Acad Sci 26:16–23
Carlgren O (1949) A survey of the Ptychodactiaria, Corallimorpharia and Actiniaria. Kungl Svenska Vetenskapsakademiens Handlingar, pp 1–121
Carlton JT (2003) Community assembly and historical biogeography in the North Atlantic Ocean: the potential role of human-mediated dispersal vectors. In: Jones MB, Ingólfsson A, Ólafsson E et al (eds) Migrations and dispersal of marine organisms. Springer, Dordrecht, pp 1–8
Carlton JT (2009) Deep invasion ecology and the assembly of communities in historical time. In: Rilov G, Crooks JA (eds) Biological invasions in marine ecosystems. Springer, Berlin Heidelberg, pp 13–56
Castro KL, Battini N, Giachetti CB et al (2021) Early detection of marine invasive species following the deployment of an artificial reef: Integrating tools to assist the decision-making process. J Environ Manag 297:113333. https://doi.org/10.1016/j.jenvman.2021.113333
Chapman JW, Carlton JT (1991) A test of criteria for introduced species: the global invasion by the isopod Synidotea laevidorsalis (Miers, 1881). J Crustac Biol 11:386–400. https://doi.org/10.2307/1548465
Chapman D, Pescott OL, Roy HE, Tanner R (2019) Improving species distribution models for invasive non-native species with biologically informed pseudo-absence selection. J Biogeogr 46:1029–1040. https://doi.org/10.1111/jbi.13555
den Hartog JC, Ates RML (2011) Actiniaria from Ria de Arosa, Galicia, northwestern Spain, in the Netherlands Centre for Biodiversity Naturalis, Leiden. Zool Meded 85:11–53
Derviche P, Saucsen A, Spier D, Lana P (2021) Distribution patterns and habitat suitability of the non-native brittle star Ophiothela mirabilis Verrill, 1867 along the Western Atlantic. J Sea Res 168:101994. https://doi.org/10.1016/j.seares.2020.101994
Dons C (1945) Norges strand fauna XXXII Hexakoraller. Kongelige nor Vidensk Selsk Forh 18:17–20
Dormann CF, Schymanski SJ, Cabral J et al (2012) Correlation and process in species distribution models: bridging a dichotomy. J Biogeogr 39:2119–2131. https://doi.org/10.1111/j.1365-2699.2011.02659.x
Fautin DG (2016) Catalog to families, genera, and species of orders Actiniaria and Corallimorpharia (Cnidaria: Anthozoa). Zootaxa 4145:1–449. https://doi.org/10.11646/zootaxa.4145.1.1
Fautin DG, Malarky L, Soberón J (2013) Latitudinal diversity of sea anemones (Cnidaria: Actiniaria). Biol Bull 224:89–98. https://doi.org/10.1086/BBLv224n2p89
Ghabooli S, Shiganova TA, Zhan A et al (2011) Multiple introductions and invasion pathways for the invasive ctenophore Mnemiopsis leidyi in Eurasia. Biol Invasions 13:679–690. https://doi.org/10.1007/s10530-010-9859-8
Giachetti CB, Battini N, Bortolus A et al (2019) Macropredators as shapers of invaded fouling communities in a cold temperate port. J Exp Mar Biol Ecol 518:151177. https://doi.org/10.1016/j.jembe.2019.151177
Gimenez LH, Brante A (2021) Do non-native sea anemones (Cnidaria: Actiniaria) share a common invasion pattern?—A systematic review. Aquat Invasions 16:365–390. https://doi.org/10.3391/ai.2021.16.3.01
Gimenez LH, Rivera RJ, Brante A (2022) One step ahead of sea anemone invasions with ecological niche modeling: potential distributions and niche dynamics of three successful invasive species. Mar Ecol Prog Ser 690:83–95. https://doi.org/10.3354/meps14044
Glon H, Haruka Y, Daly M, Nakaoka M (2019) Temperature and salinity survival limits of the fluffy sea anemone, Metridium senile (L.), in Japan. Hydrobiologia 830:303–315. https://doi.org/10.1007/s10750-018-3879-2
Glon H, Costa M, de Lecea A et al (2020a) First record of the plumose sea anemone, Metridium senile (Linnaeus, 1761), from the Falkland Islands. BioInvasions Rec 9:461–470. https://doi.org/10.3391/bir.2020.9.3.02
Glon H, Daly M, Carlton JT et al (2020b) Mediators of invasions in the sea: life history strategies and dispersal vectors facilitating global sea anemone introductions. Biol Invasions 22:3195–3222. https://doi.org/10.1007/s10530-020-02321-6
Glon H, Quattrini A, Rodríguez E et al (2021) Comparison of sequence-capture and ddRAD approaches in resolving species and populations in hexacorallian anthozoans. Mol Phylogenet Evol 163:107233. https://doi.org/10.1016/j.ympev.2021.107233
Glon H, Häussermann V, Brewin PE, Brickle P, Kong S, Smith ML, Daly M (2023) There and back again: the unexpected journeys of Metridium de Blainville, 1824 between the old oceans and throughout the modern world. Biol Bull. In press
Griffiths CL, Kruger LM, Smith CE (1996) First record of the sea anemone Metridium senile from South Africa. Afr Zool 31:157–158. https://doi.org/10.1080/02541858.1996.11448407
Haller S, Vezub JE (2018) Interoceanic connections of the 19th century Patagonian coast: maritime history background. Anuario IEHS 33:15–38
Hand C (1955) The sea anemones of Central California, Part III. The acontiarian anemones. Wasmann J Biol 13:186–251
Häussermann V (2004) Identification and taxonomy of soft-bodied hexacorals exemplified by Chilean sea anemones; including guidelines for sampling, preservation and examination. J Mar Biol Assoc UK 84:931–936. https://doi.org/10.1017/S0025315404010215h
Häussermann V (2006) Biodiversity of Chilean sea anemones (Cnidaria: Anthozoa): distribution patterns and zoogeographic implications, including new records for the fjord region. Investig Mar 34:23–35. https://doi.org/10.4067/s0717-71782006000200003
Häussermann V, Försterra G (2001) A new species of sea anemone from Chile, Anemonia alicemartinae n sp (Cnidaria: Anthozoa). An invader or an indicator for environmental change in shallow water? Org Divers Evol 1:211–224. https://doi.org/10.1078/1439-6092-00018
Häussermann V, Försterra G (2005) Distribution patterns of Chilean shallow-water sea anemones (Cnidaria: Anthozoa: Actiniaria, Corallimorpharia); with a discussion of the taxonomic and zoogeographic relationships between the actinofauna of the South East Pacific, the South West Atlantic and the Antarctic. Sci Mar 69:91–102. https://doi.org/10.3989/scimar.2005.69s291
Häussermann V, Försterra G (2009) Marine benthic fauna of Chilean patagonia. Nature in Focus, Santiago
Häussermann V, Molinet C, Díaz Gómez M et al (2022) Recent massive invasions of the circumboreal sea anemone Metridium senile in North and South Patagonia. Biol Invasions. https://doi.org/10.1007/s10530-022-02878-4
Hiscock K, Sharrock S, Highfield J, Snelling D (2010) Colonization of an artificial reef in south-west England—ex-HMS ‘Scylla.’ J Mar Biol Assoc UK 90:69–94. https://doi.org/10.1017/S0025315409991457
Hoffmann RJ (1976) Genetics and asexual reproduction of the sea anemone Metridium senile. Biol Bull 151:478–488. https://doi.org/10.2307/1540501
Holmes S, Callaway R (2021) Fouling communities and non-native species within five ports along the Bristol Channel, South Wales, UK. Estuar Coast Shelf Sci 252:107295. https://doi.org/10.1016/j.ecss.2021.107295
iNaturalist (2022) Available from https://www.inaturalist.org. Accessed 13 Jan 2022
Lauretta D, Rodríguez E, Penchaszadeh PE (2011) A new vermiform sea anemone (Anthozoa: Actiniaria) from Argentina: Harenactis argentina sp. nov. Zootaxa 3027:9–18. https://doi.org/10.11646/zootaxa.3027.1.2
Lombardi MR, Lesser MP (2010) The annual gametogenic cycle of the sea anemone Metridium senile from the gulf of maine. J Exp Mar Biol Ecol 390:58–64. https://doi.org/10.1016/j.jembe.2010.04.004
López-Farrán Z, Guillaumot C, Vargas-Chacoff L et al (2021) Is the southern crab Halicarcinus planatus (Fabricius, 1775) the next invader of Antarctica? Glob Change Biol 27:3487–3504. https://doi.org/10.1111/gcb.15674
Manuel RL (1981) British Anthozoa. Linnean Society of London and the Estuarine and Brackish-water Sciences Association. Academic Press, London
Martin JP, Garese A, Sar A, Acuña FH (2015) Fouling community dominated by Metridium senile (Cnidaria: Anthozoa: Actiniaria) in Bahía San Julián (southern Patagonia, Argentina). Sci Mar 79:211–221. https://doi.org/10.3989/scimar.04082.21a
Molinet C, Häussermann V, Astorga M, Barahona N, Espinoza K, Diaz M, Díaz P, Henríquez J, Matamala T, Soto D (2022) Population expansion of the invasive sea anemone Metridium senile in the spatial mesoscale of a sea urchin bed in north-western Patagonia. Biol Invasions. https://doi.org/10.1007/s10530-022-02965-6
Nelson ML, Craig SF (2011) Role of the sea anemone Metridium senile in structuring a developing subtidal fouling community. Mar Ecol Prog Ser 421:139–149. https://doi.org/10.3354/meps08838
Newcomer K, Flenniken MM, Carlton JT (2019) Home and away and home again: discovery of a native reproductive strategy of the globally invading sea anemone Diadumene lineata (Verrill, 1869) in a satellite population. Biol Invasions 21:1491–1497. https://doi.org/10.1007/s10530-019-01940-y
Olivier SR, Kreibhom de Paternoster I, Bastida R (1966) Estudios biocenóticos en las costas de Chubut (Argentina) I. Zonación biocenológica de Puerto Pardelas (Golfo Nuevo). Bol Inst Biol Mar 10:1–73
Östman C, Kultima JR, Roat C, Rundblom (2010a) Acontia and mesentery nematocysts of the sea anemone Metridium senile (Linnaeus, 1761) (Cnidaria: Anthozoa). Sci Mar 74(3):483–497. https://doi.org/10.3989/scimar.2010.74n3483
Östman C, Kultima JR, Wong SYG (2010b) Dart formation in nematocysts of the sea anemone Metridium senile (Linnaeus, 1761) (Cnidaria: Anthozoa). Sci Mar 74(3):499–510. https://doi.org/10.3989/scimar.2010.74n3499
Östman C, Kultima JR, Roat C (2010c) Tentacle cnidae of the sea anemone Metridium senile (Linnaeus, 1761) (Cnidaria: Anthozoa). Sci Mar 74(3):511–521. https://doi.org/10.3989/scimar.2010.74n3511
Patris S, Martin LE, Bell LJ, Dawson MN (2019) Expansion of an introduced sea anemone population, and its associations with native species in a tropical marine lake (Jellyfish Lake, Palau). Front Biogeogr 11:e41048. https://doi.org/10.21425/f5fbg41048
Pederson J, Carlton J, Bastidas C et al (2021) 2019 Rapid Assessment Survey of marine bioinvasions of southern New England and New York, USA, with an overview of new records and range expansions. BioInvasions Rec 10:227–237. https://doi.org/10.3391/bir.2021.10.2.01
Pereira AM, Silva MM, Mateus O (2022) First record of Phymactis papillosa (Lesson, 1830), a Pacific south sea anemone in European shores. J Mar Biol Assoc UK 102:1–4. https://doi.org/10.1017/S0025315422000571
R Core Team (2022) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.r-project.org/
Riemann-Zürneck K (1975) Actiniaria des südwestatlantik. Helgol Wiss Meeresunters 27:70–95. https://doi.org/10.1007/BF01611687
Robinson TB, Swart C (2015) Distribution and impact of the alien anemone Sagartia ornata in the West Coast National Park. Koedoe 57:1246. https://doi.org/10.4102/koedoe.v57i1.1246
Rodríguez E, Barbeitos M, Daly M et al (2012) Toward a natural classification: phylogeny of acontiate sea anemones (Cnidaria, Anthozoa, Actiniaria). Cladistics 28:375–392. https://doi.org/10.1111/j.1096-0031.2012.00391.x
Rodríguez E, Fautin D, Daly M (2022) World list of actiniaria. Available from https://www.marinespecies.org/. Accessed 8 June 2022
Roman J (2006) Diluting the founder effect: cryptic invasions expand a marine invader’s range. Proc R Soc B Biol Sci 273(1600):2453–2459. https://doi.org/10.1098/rspb.2006.3597
Sbrocco EJ, Barber PH (2013) MARSPEC: ocean climate layers for marine spatial ecology. Ecology 94:979–979. https://doi.org/10.1890/12-1358.1
Schwindt E, Carlton J, Orensanz J et al (2020) Past and future of the marine bioinvasions along the Southwestern Atlantic. Aquat Invasions 15:11–29. https://doi.org/10.3391/ai.2020.15.1.02
Stephenson TA (1935) The British sea anemones, vol II. The Ray Society, London
Thuiller W, Lafourcade B, Engler R, Araújo MB (2009) BIOMOD—a platform for ensemble forecasting of species distributions. Ecography 32:369–373. https://doi.org/10.1111/j.1600-0587.2008.05742.x
Tyberghein L, Verbruggen H, Pauly K et al (2012) Bio-ORACLE: a global environmental dataset for marine species distribution modelling. Glob Ecol Biogeogr 21:272–281. https://doi.org/10.1111/j.1466-8238.2011.00656.x
Watkins HV, Yan HF, Dunic JC, Côté IM (2021) Research biases create overrepresented “poster children” of marine invasion ecology. Conserv Lett 14:e12802. https://doi.org/10.1111/conl.12802
Zabin CJ, Zardus J, Pitombo FB et al (2007) A tale of three seas: consistency of natural history traits in a Caribbean-Atlantic barnacle introduced to Hawaii. Biol Invasions 9:523–544. https://doi.org/10.1007/s10530-006-9056-y
Zaixso HE, Sar AM, Lizarralde ZI, Martin JP (2017) Macrobenthic assemblages with presence of mytilids of San Julián bay (Southern Patagonia, Argentina). Rev Biol Mar Oceanogr 52:311–323. https://doi.org/10.4067/S0718-19572017000200010
Zamponi MO (1978) Sobre la anémona Paraisometridium pehuensis, gen. y sp. nov. (Actiniaria: Metridiidae). Neotropica 24:117–122
Acknowledgements
We appreciate the contribution of all the people who kindly provided Metridium senile reports on iNaturalist, especially Gonzalo Bravo (CENPAT, Argentina) and Mariano Rodriguez (Argentina Submarina). We thank Héctor Monsalve, Marcelo Mazza, Juan Ángel Allieri, and Uriel Szokolowicz for providing historical photographs and videos from which invaluable data was retrieved. We also thank Dr. Cristina Damborenea (Museo de La Plata, Argentina) for her kind support in the loan of the holotype specimen of Paraisometridium pehuensis; Dr. Mauricio Zamponi (UNMdP-Argentina, retired) for providing the histological sections of P. pehuensis paratypes; Dr. Sandra Fiori (IADO, Argentina) for kindly providing us information about the status of M. senile in Bahía Blanca; Dr. Evangelina Schwindt (CENPAT, Argentina) for her helpful insights that improved an early version of the manuscript; Julieta Coronel (ESCiMar, Argentina) for her Metridium senile drawing; and two anonymous reviewers whose feedback and suggestions improved the work.
Funding
This work was partially supported by grants from the Agencia Nacional de Promoción de la Investigación, el Desarrollo Tecnológico y la Innovación (PICT 2020–Serie A–01451), and from PADI Foundation (Project No. 68424) to RGM.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Taxonomic revision of morphological descriptions was revised and compared by RGM. Type material of Paraisometridium pehuensis was examined by RGM. Historical and current records were compiled and curated by LHG, NB and HG. Species distribution modeling was carried out by NB and LHG. The first draft of the manuscript was written by LHG and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no relevant financial or non-financial interests to disclose.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Gimenez, L.H., Battini, N., González-Muñoz, R. et al. Invader in disguise for decades: the plumose sea anemone Metridium senile in the Southwestern Atlantic Ocean. Biol Invasions 25, 2159–2173 (2023). https://doi.org/10.1007/s10530-023-03031-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-023-03031-5