Establishment and proliferation under climate change: temperate tunicates in south-western Iceland
Joana Micael
A * , Pedro Rodrigues B , Alfonso A. Ramos-Esplá C and Sindri Gíslason A
+ Author Affiliations
- Author Affiliations
A Southwest Iceland Nature Research Centre, Garðvegur 1, 245 Suðurnesjabær, Iceland.
B Rif Field Station, Aðalbraut 16, 675 Raufarhöfn, Iceland.
C Research Marine Centre of Santa Pola (CIMAR), University of Alicante, E-03080 Alicante, Spain.
Marine and Freshwater Research 73(6) 803-811 https://doi.org/10.1071/MF21351
Submitted: 14 December 2021 Accepted: 4 April 2022 Published: 3 May 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Context: Botryllus schlosseri and Diplosoma listerianum are spreading along the south-western coast of Iceland. Both species are non-indigenous and originated from the temperate zone. In some geographic regions, these species have been associated with negative ecological and economic impacts. The proliferation of these colonial tunicates in newly colonised areas will benefit from the projected warming of sea-surface temperatures.
Aims: Owing to the influence of temperature in physiological processes of marine invertebrates, the determination of the temporal dynamic of breeding activity is crucial for operational field control actions aiming to keep population abundances below a density-dependent adverse effect.
Methods: Colonies of B. schlosseri and D. listerianum were collected during a 12-month period, in Sandgerði, south-western Iceland. The number of oocytes and larvae were counted.
Key results: This study showed that both species are present year-round in south-western Iceland. The release of larvae is more intense during the warmer months.
Conclusions: To control their population density levels, field actions should be applied during the winter months before the onset of sexual reproduction and recruitment.
Implications: In the light of the findings, it is now possible to suggest the best time for countermeasures for both species and optimise resources for marine management.
Keywords: breeding activity, Botryllus schlosseri, Diplosoma listerianum, invasive species, latitudinal pattern, proliferation, subarctic, warming seawater.
References
Arens, CJ, Paetzold, SC, Ramsay, A, and Davidson, J (2011). Pressurized seawater as an antifouling treatment against the colonial tunicates Botrylloides violaceus and Botryllus schlosseri in mussel aquaculture. Aquatic Invasions 6, 465–476.| Pressurized seawater as an antifouling treatment against the colonial tunicates Botrylloides violaceus and Botryllus schlosseri in mussel aquaculture.Crossref | GoogleScholarGoogle Scholar |
Bishop, JDD (1996). Female control of paternity in the internally fertilizing compound ascidian Diplosoma listerianum. I. Autoradiographic investigation of sperm movements in the female reproductive tract. Proceedings of the Royal Society of London. Series B: Biological Sciences 263, 369–376.
| Female control of paternity in the internally fertilizing compound ascidian Diplosoma listerianum. I. Autoradiographic investigation of sperm movements in the female reproductive tract.Crossref | GoogleScholarGoogle Scholar |
Brunetti, R (1974). Observations on the life cycle of Botryllus schlosseri (Pallas) (Ascidiacea) in the Venetian Lagoon. Bolletino di Zoologia 41, 225–251.
| Observations on the life cycle of Botryllus schlosseri (Pallas) (Ascidiacea) in the Venetian Lagoon.Crossref | GoogleScholarGoogle Scholar |
Brunetti, R, Marin, MG, and Bressan, M (1984). Combined effects of temperature and salinity on sexual reproduction and colonial growth of Botryllus schlosseri (Tunicata). Bolletino di Zoologia 51, 405–411.
| Combined effects of temperature and salinity on sexual reproduction and colonial growth of Botryllus schlosseri (Tunicata).Crossref | GoogleScholarGoogle Scholar |
Brunetti, R, Bressan, M, Marin, MG, and Libralato, M (1988). On the ecology and biology of Diplosoma listerianum (Milne Edwards, 1841) (Ascidiacea, Didemnidae). Vie Milieu/Life & Environment 38, 123–131.
Brunetti, R, Manni, L, Mastrototaro, F, Gissi, C, and Gasparini, F (2017). Fixation, description and DNA barcode of a neotype for Botryllus schlosseri (Pallas, 1766) (Tunicata, Ascidiacea). Zootaxa 4353, 29–50.
| Fixation, description and DNA barcode of a neotype for Botryllus schlosseri (Pallas, 1766) (Tunicata, Ascidiacea).Crossref | GoogleScholarGoogle Scholar | 29245522PubMed |
Bullard, SG, Lambert, G, Carman, MR, Byrnes, J, Whitlatch, RB, Ruiz, G, Miller, RJ, Harris, L, Valentine, PC, Collie, JS, Pederson, J, McNaught, DC, Cohen, AN, Asch, RG, Dijkstra, J, and Heinonen, K (2007). The colonial ascidian Didemnum sp. A: current distribution, basic biology and potential threat to marine communities of the northeast and west coasts of North America. Journal of Experimental Marine Biology and Ecology 342, 99–108.
| The colonial ascidian Didemnum sp. A: current distribution, basic biology and potential threat to marine communities of the northeast and west coasts of North America.Crossref | GoogleScholarGoogle Scholar |
Burighel, P, and Martinucci, GB (1994). Sexual reproduction in the compound ascidian Diplosoma listerianum (Tunicata). II. Sperm penetration through ovary wall and evidence of internal fertilization. Marine Biology 118, 499–510.
| Sexual reproduction in the compound ascidian Diplosoma listerianum (Tunicata). II. Sperm penetration through ovary wall and evidence of internal fertilization.Crossref | GoogleScholarGoogle Scholar |
Byrne, M, and Przeslawski, R (2013). Multistressor impacts of warming and acidification of the ocean on marine invertebrates’ life histories. Integrative and Comparative Biology 53, 582–596.
| Multistressor impacts of warming and acidification of the ocean on marine invertebrates’ life histories.Crossref | GoogleScholarGoogle Scholar | 23697893PubMed |
Carver, CE, Mallet, AL, and Vercaemer, B (2006). Biological synopsis of the colonial tunicates, Botryllus schlosseri and Botrylloides violaceus. Canadian Manuscript Report of Fisheries and Aquatic Sciences 2747, 1–50.
Chadwick-Furman, NE, and Weissman, IL (1995). Life histories and senescence of Botryllus schlosseri (Chordata, Ascidiacea) in Monterey Bay. The Biological Bulletin 189, 36–41.
| Life histories and senescence of Botryllus schlosseri (Chordata, Ascidiacea) in Monterey Bay.Crossref | GoogleScholarGoogle Scholar | 7654845PubMed |
Claar, DC, Edwards, KF, and Stachowicz, JJ (2011). Positive and negative effects of a dominant competitor on the settlement, growth, and survival of competing species in an epibenthic community. Journal of Experimental Marine Biology and Ecology 399, 130–134.
| Positive and negative effects of a dominant competitor on the settlement, growth, and survival of competing species in an epibenthic community.Crossref | GoogleScholarGoogle Scholar |
Dijkstra, J, Harris, LG, and Westerman, E (2007). Distribution and long-term temporal patterns of four invasive colonial ascidians in the Gulf of Maine. Journal of Experimental Marine Biology and Ecology 342, 61–68.
| Distribution and long-term temporal patterns of four invasive colonial ascidians in the Gulf of Maine.Crossref | GoogleScholarGoogle Scholar |
Fortunato, H (2015). Mollusks: tools in environmental and climate research. American Malacological Bulletin 33, 310–324.
| Mollusks: tools in environmental and climate research.Crossref | GoogleScholarGoogle Scholar |
Gasparini, F, Manni, L, Cima, F, Zaniolo, G, Burighel, P, Caicci, F, Franchi, N, Schiavon, F, Rigon, F, Campagna, D, and Ballarin, L (2015). Sexual and asexual reproduction in the colonial ascidian Botryllus schlosseri. Genesis 53, 105–120.
| Sexual and asexual reproduction in the colonial ascidian Botryllus schlosseri.Crossref | GoogleScholarGoogle Scholar | 25044771PubMed |
Gosseling M (2017) CORDEX climate trends for Iceland in the 21st century. Technical Report, Icelandic Meteorological Office, Reykjavik, Iceland.
Gröner, F, Lenz, M, Wahl, M, and Jenkins, SR (2011). Stress resistance in two colonial ascidians from the Irish Sea: the recent invader Didemnum vexillum is more tolerant to low salinity than the cosmopolitan Diplosoma listerianum. Journal of Experimental Marine Biology and Ecology 409, 48–52.
| Stress resistance in two colonial ascidians from the Irish Sea: the recent invader Didemnum vexillum is more tolerant to low salinity than the cosmopolitan Diplosoma listerianum.Crossref | GoogleScholarGoogle Scholar |
Grosberg, RK (1988). Life-history variation within a population of the colonial ascidian Botryllus schlosseri. I. The genetic and environmental control of seasonal variation. Evolution 42, 900–920.
| Life-history variation within a population of the colonial ascidian Botryllus schlosseri. I. The genetic and environmental control of seasonal variation.Crossref | GoogleScholarGoogle Scholar | 28581164PubMed |
IPCC (2014) ‘Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change.’ (Cambridge University Press: Cambridge, UK)
Lafargue, F (1975). Révision taxonomique des Didemnidae des côtes de France (Ascidies composées). Description des espèces de Banyuls-sur-Mer. Genre Lissoclinum. Genre Diplosoma. Vie et Milieu/Life & Environment 25, 289–309.
Lambert, CC, and Lambert, G (1998). Non-indigenous ascidians in southern California harbors and marinas. Marine Biology 130, 675–688.
| Non-indigenous ascidians in southern California harbors and marinas.Crossref | GoogleScholarGoogle Scholar |
Lawrence, AJ, and Soame, JM (2004). The effects of climate change on the reproduction of coastal invertebrates. Ibis 146, 29–39.
| The effects of climate change on the reproduction of coastal invertebrates.Crossref | GoogleScholarGoogle Scholar |
Lejeusne, C, Bock, DG, Therriault, TW, MacIsaac, HJ, and Cristescu, ME (2011). Comparative phylogeography of two colonial ascidians reveals contrasting invasion histories in North America. Biological Invasions 13, 635–650.
| Comparative phylogeography of two colonial ascidians reveals contrasting invasion histories in North America.Crossref | GoogleScholarGoogle Scholar |
L’Hardy, J-P (1962). Observations sur le peuplement epiphyte des lames de Laminaria saccharina (Linne) Lamouroux, en Baie de Morlaix (Finistère). Cahiers de Biologie Marine 3, 115–127.
Lo Bianco, S (1909). Notizie biologiche riguardanti specialmente il periodo di maturiti sessuale degli animali del golfo di Napoli. Mittheilungen aus der Zoologischen Station zu Neapel 19, 513–761.
Lockwood, JL, Cassey, P, and Blackburn, TM (2009). The more you introduce the more you get: the role of colonization pressure and propagule pressure in invasion ecology. Diversity and Distributions 15, 904–910.
| The more you introduce the more you get: the role of colonization pressure and propagule pressure in invasion ecology.Crossref | GoogleScholarGoogle Scholar |
Lord, JP (2017). Impact of seawater temperature on growth and recruitment of invasive fouling species at the global scale. Marine Ecology 38, e12404.
| Impact of seawater temperature on growth and recruitment of invasive fouling species at the global scale.Crossref | GoogleScholarGoogle Scholar |
Ma KCK (2012) Population dynamics of a non-indigenous colonial ascidian tunicate in a subarctic harbour. MSc Thesis, Memorial University of Newfoundland, St John’s, Newfoundland and Labrador, Canada.
Ma, KCK, Simard, N, Stewart-Clark, SE, Bernier, RY, Nadeau, M, and Willis, J (2016). Early detection of the non-indigenous colonial ascidian Diplosoma listerianum in eastern Canada and its implications for monitoring. Management of Biological Invasions 7, 365–374.
| Early detection of the non-indigenous colonial ascidian Diplosoma listerianum in eastern Canada and its implications for monitoring.Crossref | GoogleScholarGoogle Scholar |
Ma, KCK, Goodwin, C, and Cooper, JA (2018). Second record of Diplosoma listerianum (Milne-Edwards, 1841) five years after and 280 kilometres from the site of the first record in Nova Scotia. BioInvasions Records 7, 159–163.
| Second record of Diplosoma listerianum (Milne-Edwards, 1841) five years after and 280 kilometres from the site of the first record in Nova Scotia.Crossref | GoogleScholarGoogle Scholar |
Mackenzie, AB (2011). Biological synopsis of the compound sea squirt (Diplosoma listerianum). Canadian Manuscript Report of Fisheries and Aquatic Sciences 2966, 1–18.
Mayor, DJ, Sommer, U, Cook, KB, and Viant, MR (2015). The metabolic response of marine copepods to environmental warming and ocean acidification in the absence of food. Scientific Reports 5, 13690.
| The metabolic response of marine copepods to environmental warming and ocean acidification in the absence of food.Crossref | GoogleScholarGoogle Scholar | 26364855PubMed |
Millar, RH (1952). The annual growth and reproductive cycle in four ascidians. Journal of the Marine Biological Association of the United Kingdom 31, 41–61.
| The annual growth and reproductive cycle in four ascidians.Crossref | GoogleScholarGoogle Scholar |
Millar RH (1970) ‘British ascidians, Tunicata: Ascidiacea; keys and notes for the identification of the species.’ Synopses of the British Fauna, NS 1. (Academic Press: London, UK)
Millar RH (1971) The biology of ascidians. In ‘Advances in marine biology. Vol. 9’. (Eds FS Russell, M Yonge) pp. 1–100. (Academic Press)
| Crossref |
Miller, AW, and Ruiz, GM (2014). Arctic shipping and marine invaders. Nature Climate Change 4, 413–416.
| Arctic shipping and marine invaders.Crossref | GoogleScholarGoogle Scholar |
Montanari, M, and Relini, G (1970). Fouling di zone inquinate. Osservazioni nel porto di Genova: Idrozoi e Ascidiacei. Pubblicazioni Stazione Zoologica Napoli 38, 34–54.
Nandakumar, K (1996). Importance of timing of panel exposure on the competitive outcome and succession of sessile organisms. Marine Ecology Progress Series 131, 191–203.
| Importance of timing of panel exposure on the competitive outcome and succession of sessile organisms.Crossref | GoogleScholarGoogle Scholar |
Occhipinti-Ambrogi, A (2007). Global change and marine communities: alien species and climate change. Marine Pollution Bulletin 55, 342–352.
| Global change and marine communities: alien species and climate change.Crossref | GoogleScholarGoogle Scholar | 17239404PubMed |
Pérez-Portela, R, Arranz, V, Rius, M, and Turon, X (2013). Cryptic speciation or global spread? The case of a cosmopolitan marine invertebrate with limited dispersal capabilities. Scientific Reports 3, 3197.
| Cryptic speciation or global spread? The case of a cosmopolitan marine invertebrate with limited dispersal capabilities.Crossref | GoogleScholarGoogle Scholar | 24217373PubMed |
Polk, P (1962). Bijdrage tot de kenntnis der mariene fauna van de belgische kust. II. Waarnemingen aangaande het voorkomen en de voortplanting van Botryllus schlosseri (Pallas, 1766). Natuurwetenschappelijk Tijdschrift 44, 21–28.
Ramos-Esplá AA (2016) Iceland, between boreal and arctic waters: benthic Tunicata (Chordata: Ascidiacea). In ‘Proceedings of mares conference: marine ecosystems health and conservation. 1–5 February 2016, Olhão, Portugal’. (ICRI)
Ramos-Esplá, AA, Micael, J, Halldórsson, HP, and Gíslason, S (2020). Iceland: a laboratory for non-indigenous ascidians. BioInvasions Records 9, 450–460.
| Iceland: a laboratory for non-indigenous ascidians.Crossref | GoogleScholarGoogle Scholar |
Reem, E, Douek, J, and Rinkevich, B (2022). A critical deliberation of the ‘species complex’ status of the globally spread colonial ascidian Botryllus schlosseri. Journal of the Marine Biological Association of the United Kingdom , .
| A critical deliberation of the ‘species complex’ status of the globally spread colonial ascidian Botryllus schlosseri.Crossref | GoogleScholarGoogle Scholar |
Rinkevich, B, Porat, R, and Goren, M (1998). Ecological and life history characteristics of Botryllus schlosseri (Tunicata) populations inhabiting under surface shallow-water stones. Marine Ecology 19, 129–145.
| Ecological and life history characteristics of Botryllus schlosseri (Tunicata) populations inhabiting under surface shallow-water stones.Crossref | GoogleScholarGoogle Scholar |
Ryland, JS, and Bishop, JDD (1990). Prevalence of cross-fertilization in the hermaphroditic compound ascidian Diplosoma listerianum. Marine Ecology Progress Series 61, 125–132.
| Prevalence of cross-fertilization in the hermaphroditic compound ascidian Diplosoma listerianum.Crossref | GoogleScholarGoogle Scholar |
Sabbadin, A (1955). Il ciclo biologica di Botryllus schlosseri (Pallas) (Ascidiacea) nella Laguna di Venezia. Archo Oceanography Limnology 10, 217–230.
Sæmundsson Þ, Björnsson G (2021) ‘Almanak fyrir Ísland 2021’, (Háskóli Íslands: Reykjavík, Iceland) Available at http://almanak.is/
Saito, Y, and Okuyama, M (2003). Studies on Japanese botryllid ascidians. IV. A new species of the genus Botryllus with a unique colony shape, from the vicinity of Shimoda. Zoological Science 20, 1153–1161.
| Studies on Japanese botryllid ascidians. IV. A new species of the genus Botryllus with a unique colony shape, from the vicinity of Shimoda.Crossref | GoogleScholarGoogle Scholar | 14578576PubMed |
Shanmao, C, Congyao, Z, Guofan, Z, and Yujing, W (1998). Study on species composition of fouling organisms on mariculture cages. Journal of Dalian Fisheries 13, 15–21.
Stachowicz, JJ, Terwin, JR, Whitlatch, RB, and Osman, RW (2002). Linking climate change and biological invasions: ocean warming facilitates nonindigenous species invasions. Proceedings of the National Academy of Sciences of the United States of America 99, 15497–15500.
| Linking climate change and biological invasions: ocean warming facilitates nonindigenous species invasions.Crossref | GoogleScholarGoogle Scholar | 12422019PubMed |
Stubbings, HG, and Houghton, DR (1964). The ecology of Chichester Harbour, S. England, with special reference to some fouling species. Internationale Revue der gesamten Hydrobiologie und Hydrographie 49, 233–279.
| The ecology of Chichester Harbour, S. England, with special reference to some fouling species.Crossref | GoogleScholarGoogle Scholar |
Vance, T, Lauterbach, L, Lenz, M, Wahl, M, Sanderson, RA, and Thomason, JC (2009). Rapid invasion and ecological interactions of Diplosoma listerianum in the North Sea, UK. Marine Biodiversity Records 2, e59.
| Rapid invasion and ecological interactions of Diplosoma listerianum in the North Sea, UK.Crossref | GoogleScholarGoogle Scholar |
Westerman E (2007) Impacts of changing water temperatures on the life histories of two invasive ascidians in the Gulf of Maine: Botryllus schlosseri and Botrylloides violaceus. MSc Thesis, University of New Hampshire, Durham, NH, USA.
Westerman, EL, Whitlatch, R, Dijkstra, JA, and Harris, LG (2009). Variation in brooding period masks similarities in response to changing temperatures. Marine Ecology Progress Series 391, 13–19.
| Variation in brooding period masks similarities in response to changing temperatures.Crossref | GoogleScholarGoogle Scholar |
Yund, PO, and McCartney, MA (1994). Male reproductive success in sessile invertebrates: competition for fertilizations. Ecology 75, 2151–2167.
| Male reproductive success in sessile invertebrates: competition for fertilizations.Crossref | GoogleScholarGoogle Scholar |
Yund, PO, and Stires, A (2002). Spatial variation in population dynamics in a colonial ascidian (Botryllus schlosseri). Marine Biology 141, 955–963.
| Spatial variation in population dynamics in a colonial ascidian (Botryllus schlosseri).Crossref | GoogleScholarGoogle Scholar |
Yund, PO, Marcum, Y, and Stewart-Savage, J (1997). Life-history variation in a colonial ascidian: broad-sense heritabilities and tradeoffs in allocation to asexual growth and male and female reproduction. The Biological Bulletin 192, 290–299.
| Life-history variation in a colonial ascidian: broad-sense heritabilities and tradeoffs in allocation to asexual growth and male and female reproduction.Crossref | GoogleScholarGoogle Scholar | 28581869PubMed |
Zhan, A, Briski, E, Bock, DG, Ghabooli, S, and MacIsaac, HJ (2015). Ascidians as models for studying invasion success. Marine Biology 162, 2449–2470.
| Ascidians as models for studying invasion success.Crossref | GoogleScholarGoogle Scholar |
