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Temperature-driven secondary competence windows may increase the dispersal potential of invasive sun corals

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Abstract

Invasive sun corals exhibit outstanding development plasticity during early ontogenesis, which may greatly affect the pelagic duration of propagules and hence their dispersal potential. Remarkably, a small proportion of larvae may not directly settle on the benthic habitat, but metamorphose to planktonic polyps. We show the latter may settle successfully, eventually opening a secondary competence window (SCW). Based on local conditions (Southeast Brazil), delayed SCWs were confirmed at average summer (26 °C) and, especially, at heat-wave (30 °C) temperature, allowing an escape response from habitats where larval mortality rates are high and mass-mortality events of colonies, later on, more likely. Despite a higher frequency of pelagic metamorphosis, no SCWs were observed at average winter (22 °C) and cold-front (19 °C) conditions. Climate change may thus favor large-scale dispersal of competent pelagic polyps and further extensions of the leading range edge to subtropical and warm temperate regions where temperature conditions (ca. 22 °C) for propagule survival and settlement success are best.

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References

  • Barbosa ACC, Vinagre C, Mizrahi D, Duarte RC, Flores AAV (2019) Invasive sun corals and warming pose independent threats to the brain coral Mussismilia hispida in the Southwestern Atlantic. Mar Ecol Prog Ser. https://doi.org/10.3354/meps13110

    Article  Google Scholar 

  • Bassim KM, Sammarco PW (2003) Effects of temperature and ammonium on larval development and survivorship in a scleractinian coral (Diploria strigose). Mar Biol 142:241–252

    Article  CAS  Google Scholar 

  • Bruno JF, Selig ER, Casey KS, Page CA, Willis BL, Harvell CD, Sweatman H, Melendy AM (2007) Thermal stress and coral cover as drivers of coral disease outbreaks. PLoS Biol 5:1220–1227

    Article  CAS  Google Scholar 

  • Capel KCC, Migotto AE, Zilberberg C, Kitahara MV (2014) Another tool towards invasion? Polyp ‘‘bail-out’’ in Tubastraea coccinea. Coral Reefs 33:1165

    Article  Google Scholar 

  • Connolly SR, Baird AH (2010) Estimating dispersal potential for marine larvae: dynamic models applied to scleractinian corals. Ecology 91(12):3572–3583

    Article  Google Scholar 

  • Cowen RK, Paris CB, Srinivasan A (2006) Scaling of connectivity in marine populations. Science 311:522–527

    Article  CAS  Google Scholar 

  • Creed JC, Fenner D, Sammarco PW, Cairns S, Capel KCC, Junqueira AOR, Cruz I, Miranda RJ, Carlos-Júnior LA, Mantelatto MC, Oigman-Pszczol SS (2016) The invasion of the azooxanthellate coral Tubastraea (Scleractinia: Dendrophylliidae) throughout the world: history, pathways and vectors. Biol Invasions 19:283–305

    Article  Google Scholar 

  • Dahms HU (1995) Dormancy in the Copepoda—an overview. Hydrobiologia 306:199–211

    Article  Google Scholar 

  • de Paula AF, Creed JC (2004) Two species of the coral Tubastraea (Cnidaria, Scleractinia) in Brazil: a case of accidental introduction. Bull Mar Sci 74:175–183

    Google Scholar 

  • dos Santos LAH, Ribeiro FV, Creed JC (2013) Antagonism between invasive pest corals Tubastraea spp. and the native reef-builder Mussismilia hispida in the southwest Atlantic. J Exp Mar Biol Ecol 449:69–76

    Article  Google Scholar 

  • Drent J (2002) Temperature responses in larvae of Macoma balthica from a northerly and southerly population of the European distribution range. J Exp Mar Biol Ecol 275:117–129

    Article  Google Scholar 

  • Fenner D, Banks K (2004) Orange cup coral Tubastraea coccinea invades Florida and the Flower Garden Banks, Northwestern Gulf of Mexico. Coral Reefs 23:505–507

    Google Scholar 

  • Garrabou J, Perez T, Sartoretto S, Harmelin JG (2001) Mass mortality event in red coral Corallium rubrum populations in the Provence region (France, NW Mediterranean). Mar Ecol Prog Ser 217:263–272

    Article  Google Scholar 

  • Hadfield MG, Carpizo-Ituarte EJ, del Carmen K, Nedved BT (2001) Metamorphic competence, a major adaptive convergence in marine invertebrate larvae. Am Zool 41(5):1123–1131

    Google Scholar 

  • Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshwater Res 50:839–866

    Google Scholar 

  • Hughes TP, Kerry JT, Baird AH, Connolly SR, Dietzel A, Eakin CM, Heron SF, Hoey AS, Hoogenboom MO, Liu G, McWilliam MJ, Pears RJ, Pratchett MS, Skirving WJ, Stella JS, Torda G (2018) Global warming transforms coral reef assemblages. Nature 556:492–496

    Article  CAS  Google Scholar 

  • IPCC (2013) Climate change 2013: the physical science basis. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) Contribution of Working Group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, p 1535

    Google Scholar 

  • Kendall MS, Poti M, Wynne TT, Kinlan BP, Bauer LB (2013) Consequences of the life history traits of pelagic larvae on interisland connectivity during a changing climate. Mar Ecol Prog Ser 489:43–59

    Article  Google Scholar 

  • Keshavmurthy S, Fontana S, Mezaki T, Gonzalez LdC, Chen CA (2014) Doors are closing on early development in corals facing climate change. Sci Reports 4:5633

    Article  CAS  Google Scholar 

  • Kinlan BP, Gaines SD (2003) Propagule dispersal in marine and terrestrial environments: a community perspective. Ecology 84:2007–2020

    Article  Google Scholar 

  • Krug PJ (2001) Bet-hedging dispersal strategy of a specialist marine herbivore: a settlement dimorphism among sibling larvae of Alderia modesta. Mar Ecol Prog Ser 213:177–192

    Article  Google Scholar 

  • Luz BPL, Kitahara MV (2017) Could the invasive scleractinians Tubastraea coccinea and T. tagusensis replace the dominant zoantharian Palythoa caribaeorum in the Brazilian subtidal? Coral Reefs 36:875

    Article  Google Scholar 

  • Mizrahi D, Navarrete SA, Flores AAV (2014) Groups travel further: pelagic metamorphosis and polyp clustering allow higher dispersal potential in sun coral propagules. Coral Reefs 33:443–448

    Article  Google Scholar 

  • Mizrahi D, Pereira SF, Navarrete AS, Flores AAV (2017) Allelopathic effects on the sun-coral invasion: facilitation, inhibition and patterns of local biodiversity. Mar Biol 164:139

    Article  Google Scholar 

  • Munday PL, Leis JM, Lough JM, Paris CB, Kingsford MJ, Berumen ML, Lambrechts J (2009) Climate change and coral reef connectivity. Coral Reefs 28:379–395

    Article  Google Scholar 

  • O’Connor MI, Bruno JF, Gaines SD, Halpern BS, Lester SE, Kinlan BP, Weiss JM (2007) Temperature control of larval dispersal and the implications for marine ecology, evolution and conservation. PNAS 104(4):1266–1271

    Article  Google Scholar 

  • Park K-A, Chung JY (1999) Spatial and temporal scale variations of sea surface temperature in the East Sea using NOAA/AVHRR data. J Oceanogr 55:171–288

    Article  Google Scholar 

  • PBMC (2012) Sumário Executivo do Volume 1—Base Científica das Mudanças Climáticas. Contribuição do Grupo de Trabalho 1 para o 1o Relatório de Avaliação Nacional do Painel Brasileiro de Mudanças Climáticas. Volume Especial para a Rio + 20. PBMC, Rio de Janeiro, Brasil, p 34

  • Pineda J, DiBacco C, Starczak V (2005) Barnacle larvae in ice: survival, reproduction, and time to postsettlement metamorphosis. Limnol Oceanogr 50:1520–1528

    Article  Google Scholar 

  • Piraino S, De Vito D, Schmich J, Bouillon J, Boero F (2004) Reverse development in Cnidaria. Can J Zool 82:1748–1754

    Article  Google Scholar 

  • Randall CJ, Szmant AM (2009) Elevated temperature reduces survivorship and settlement of the Caribbean scleractinian coral, Favia fragum (Esper). Coral Reefs 28:537–545

    Article  Google Scholar 

  • Richmond RH (1985) Reversible metamorphosis in coral planula larvae. Mar Ecol Prog Ser 22:181–185

    Article  Google Scholar 

  • Riegl B, Piller WE (2003) Possible refugia for reefs in time of environmental stress. Int J Earth Sci 92:520–531

    Article  Google Scholar 

  • Robitzch VSN, Lozano-Cortes D, Kandler NM, Salas S, Berumen ML (2016) Productivity and sea surface temperature are correlated with the pelagic larval duration of damselfishes in the Red Sea. Mar Pollut Bull 105:566–574

    Article  CAS  Google Scholar 

  • Shanks AL, Grantham BA, Carr MH (2003) Propagule dispersal distance and the size and spacing of marine reserves. Ecol Appl 13(1):S159–S169

    Article  Google Scholar 

  • Silva R, Vinagre C, Kitahara MV, Acorsi I, Mizrahi D, Flores AAV (2019) Sun coral invasion of shallow rocky reefs: effects on mobile invertebrate assemblages in Southeastern Brazil. Biol Invasions 21(4):1339–1350

    Article  Google Scholar 

  • Soares MO, Davis M, Carneiro PBM (2018) Northward range expansion of the invasive coral (Tubastraea tagusensis) in the southwestern Atlantic. Mar Biodiv 48:1651–1654

    Article  Google Scholar 

  • Sokal RR, Rohlf FJ (2012) Biometry, 4th edn. W.H. Freeman and Company, New York

    Google Scholar 

  • Toonen RJ, Pawlik JR (2001) Foundations of gregariousness: a dispersal polymorphism among the plankton larvae of a marine invertebrate. Evolution 55(12):2439–2454

    Article  CAS  Google Scholar 

  • Underwood AJ (1997) Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press, Cambridge

    Google Scholar 

Download references

Acknowledgements

We thank two reviewers for their insightful comments on a previous manuscript version. We are also grateful to CEBIMar technicians Joseilto Medeiros de Oliveira and Eduardo Honuma for their assistance in the collection of coral colonies. This research was funded by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil), through the Research Program “Ciência sem Fronteiras”, as a Special Visiting Researcher Fellowship (PVE) to CV (# 400614/2014-6), and also for granting a PhD fellowship to ACCB (CNPq # 159822/2015-7). CV also acknowledges a researcher position, and respective project grant (UID/MARE/04292/2019), supported by the Fundação para a Ciência e a Tecnologia (Portugal). This is a contribution of the Research Centre for Marine Biodiversity of the University of São Paulo (NP-Biomar/USP).

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Authors and Affiliations

  1. Center for Marine Biology, University of São Paulo (CEBIMar-USP), São Sebastião, Brazil

    Andreia C. C. Barbosa & Augusto A. V. Flores

  2. Marine and Environmental Sciences Centre (MARE), Faculdade de Ciências, Universidade de Lisboa, Campo Grande, 1749-016, Lisbon, Portugal

    Catarina Vinagre

  3. Oceanographic Institute, University of São Paulo (IO-USP), São Paulo, Brazil

    Damián Mizrahi

Authors
  1. Andreia C. C. Barbosa
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  2. Catarina Vinagre
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  3. Damián Mizrahi
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  4. Augusto A. V. Flores
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Corresponding author

Correspondence to Andreia C. C. Barbosa.

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Conflict of interest

This study was funded by CNPq; Conselho Nacional de Desenvolvimento Científico e Tecnológico; Grants # 400614/2014-6 and # 159822/2015-7. The authors declare that they have no conflict of interest.

Ethical approval

The collection of coral colonies was authorized by the highest national authority, Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio), through the Sistema de Autorização e Informação em Biodiversidade (SISBIO); license # 49750-1. All applicable international, national, and/or institutional guidelines for sampling, care, and experimental use of animals were followed. Experiments were also carried out with minimal stress to individuals to meet ethical standards and to ensure the validity of observations.

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Communicated by C. Voostra.

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Barbosa, A.C.C., Vinagre, C., Mizrahi, D. et al. Temperature-driven secondary competence windows may increase the dispersal potential of invasive sun corals. Mar Biol 166, 131 (2019). https://doi.org/10.1007/s00227-019-3580-7

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