Abstract
Sun corals (Tubastraea spp.) have invaded the SW Atlantic coast in the 1980s, saturating vertical walls at heavily impacted areas. More recently, the boring bivalve Leiosolenus aristatus, another invasive species in the SW Atlantic, was found inhabiting sun corals. Here we show that Tubastraea tagusensis is the main coral host for L. aristatus at an extensively invaded island in Southeastern Brazil. Bivalve biomass adjusted to colony volume was similar between invasive T. tagusensis and native corals. However, when adjusted to colony basal area per reef space, bivalve density was exceptionally higher in sun corals, especially on vertical substrates or those with negative orientation. Therefore, sun corals constitute main doorways for borer bivalves at most invaded reefs. Moreover, and owing to the phaceloid colony morphology of T. tagusensis, boring bivalves reduce, on average, the contact area between sun corals and the substrate in 9.6% (SD = 9.9), ranging from 1 to 44%. Regardless of sampling site and reef inclination, the decrease of such surface contact area causes a drop of sun-coral adhesive strength (from 36 to 22 kgf), that can be described by a general exponential decay function, and explain the accumulation of coral debris at the bottom of invaded reefs. While possibly ceding space for native species in the reef community, dislodgment through bivalve infestation may eventually reduce intraspecific competition among sun-coral colonies and favor resettlement in alternative reef habitats, ultimately contributing to the ongoing invasive process.
Similar content being viewed by others
References
Abbott RT (1974) American seashells, 2nd edn. Van Nostrand Reinhold, New York, p 663
Acker KL, Risk MJ (1985) Substrate destruction and sediment production by the boring sponge, Cliona caribbaea on Grand Cayman Island. J Sediment Petrol 55:705–711
Babcock R, Mundy C (1996) Coral recruitment: Consequences of settlement choice for early growth and survivorship in two scleractinians. J Exp Mar Biol Ecol 206:179–201
Bak PM, Engel MS (1979) Distribution, abundance and survival of juvenile hermatypic corals (Scleractinia) and the importance of early life history strategies in the parent coral community. Mar Biol 54:341–352
Barbosa ACC, Vinagre C, Mizrahi D, Duarte RC, Flores AAV (2019a) Invasive sun corals and warming pose independent threats to the brain coral Mussismilia hispida in the Southwestern Atlantic. Mar Ecol Prog Ser 629:43–54
Barbosa ACC, Vinagre C, Mizrahi D, Flores AAV (2019b) Temperature driven secondary competence windows may increase the dispersal potential of invasive sun corals. Mar Biol 166:131
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
Bolognani Fantin AM, Bolognani L (1979) The pallial gland of Lithophaga lithophaga (L.): a histochemical and biochemical approach of the rock boring problem. Malacologia 18:587–590
Breves-Ramos A, Pimenta AD, de Széchy MTM, Junqueira AOR (2010) Mollusca, Bivalvia, Mytilidae, Myoforceps aristatus (Dillwyn, 1817): distribution and new record localities at Ilha Grande Bay, Brazil. Check List 6:408–409
Capel KCC, Toonen RJ, Rachid CTCC, Creed JC, Kitahara MV, Forsman Z, Zilberberg C (2017) Clone wars: asexual reproduction dominates in the invasive range of spp. (Anthozoa: Scleractinia) in the South-Atlantic Ocean. PeerJ 5:e3873
Carvalho LMV, Jones C, Liebmann B (2002) Extreme precipitation events in Southeastern South America and large-scale convective patterns in the South Atlantic Convergence Zone. J Clim 15:2377–2394
Castro CB, Pires D (2001) Brazilian coral reefs: what we already know and what is still missing. Bull Mar Sci 69:357–371
Creed JC (2006) Two invasive alien azooxanthellate corals, Tubastraea coccinea and Tubastraea tagusensis, dominate the native zooxanthellate Mussismilia hispida in Brazil. Coral Reefs 25:350
Creed JC, Fenner D, Sammarco PW, Cairns S et al (2017) The invasion of the azooxanthellate coral Tubastraea (Scleractinia: Dendrophylliidae) throughout the world: history, pathways and vectors. Biol Invasions 19:283–305
De Paula AF, Pires DO, Creed JC (2014) Reproductive strategies of two invasive sun corals (Tubastraea spp.) in the southwestern Atlantic. J Mar Biol Assoc UK 94:481–492
Donahue MJ (2004) Size-dependent competition in a gregarious porcelain crab Petrolisthes cinctipes (Anomura: Porcellanidae). Mar Ecol Prog Ser 267:219–231
Fernandes FC, Rapagnã LC, Bueno GBD (2004) Estudo da população do bivalve exótico Isognomon bicolor (C.B. Adams, 1845) (Bivalvia, Isonomonidae) na Ponta da Fortaleza em Arraial do Cabo - RJ. In: Silva JSV, Souza RCCL (eds) Água de Lastro e Bioinvasão. Interciência, Rio de Janeiro, pp 133–141
Genovese SJ, Witman JD (1999) Interactive effects of flow speed and particle concentration on growth rates of an active suspension feeder. Limnol Oceanogr 44:1120–1131
Glynn PW, Colley SB, Maté JL, Cortés J, Guzman HM, Bailey RL, Feingold JS, Enochs IC (2008) Reproductive ecology of the azooxanthellate coral Tubastraea coccinea in the Equatorial Eastern Pacific: part V. Dentrophylliidae Mar Biol 153:529–544
Gomes LEO, Correa LB, Bernardino AF (2014) New record of the non-native bivalve Myoforceps aristatus in SE Brazil. Strombus 21:10–14
Goreau TF, Hartman WD (1966) Sponge: effect on the form of reef corals. Science 151:343–344
Gosling E (2003) Bivalve molluscs: biology, ecology and culture. Fishing New Books, Blackwell Publishing, London, p 443
Green PT, O’Dowd DJ, Abbott KL, Jeffery M, Retallick K, Mac Nally R (2011) Invasional meltdown: invader-invader mutualism facilitates a secondary invasion. Ecology 92:1758–1768
Harriott VJ (1983) Reproductive seasonality, settlement, and post-settlement mortality of Pocillopora damicornis (Linnaeaus), at Lizard Island, Great Barrier Reef. Coral Reefs 2:151–157
Hoeksema BW, ten Hove HA (2017) The invasive sun coral Tubastraea coccinea hosting a native christmas tree worm at Curaçao, Dutch Caribbean. Mar Biodiv 47:59–65
Holstein TW, Hobmayer E, Technau U (2003) Cnidarians: an evolutionarily conserved model system for regeneration? Dev Dyn 226:257–267
Ignacio BL, López MS, Silva JSV (2012) Colonization plasticity of the boring bivalve Lithophaga aristata (Dillwyn, 1817) on the Southeastern Brazilian coast: considerations on its invasiveness potential. Aquat Invasions 7:475–482
Jaccarini V, Bannister WH, Micallef H (1968) The pallial glands and rock boring in Lithophaga lithophaga (Lamellibranchia, Mytilidae). J Zool 154:397–401
Kcc C, Creed JC, Kitahara MV (2020) Invasive corals trigger seascape changes in the southwestern Atlantic. Bull Mar Sci 96:217–218
Kefi FJ, Boubaker S, El Menif NT (2014) Relative growth and reproductive cycle of the date mussel Lithophaga lithophaga (Linnaeus, 1758) sampled from the Bizerte Bay (Northern Tunisia). Helgoland Mar Res 68:439
Kim K, Lasker HR (1997) Flow-mediated resource competition in the suspension feeding gorgonian Plexaura homomalla (Esper). J Exp Mar Biol Ecol 215:49–64
Kohler KE, Gill SM (2006) Coral Point Count with Excel extensions (CPCe): a Visual Basic program for the determination of coral and substrate coverage using random point count methodology. Comp Geosci 32:1259–1269
Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest package: tests in linear mixed effects models. J Stat Softw 82:1–26
Lages BG, Beatriz GF, Rezende CM, Pinto AC, Creed JC (2010) Chemical composition and release in situ due to injury of the invasive coral Tubastraea (Cnidaria, Scleractinia). Braz J Oceanogr 58:47–56
Lages BG, Fleury BG, Menegola C, Creed JC (2011) Change in tropical rocky shore communities due to an alien coral invasion. Mar Ecol Prog Ser 438:85–96
Lenth R (2019) emmeans: estimated marginal means, aka least-squares means. R package version 1.3.5. https:// CRAN.R-project.org/package=emmeans.
Lesson RP (1829) Histoire naturelle des oiseaux-mouches. Ouvrage orné de planches dessinées et gravées par les meilleurs artistes. Paris. Bertrand 223p.
Li B-H, Wu H-I, Zou G (2000) Self-thinning rule: a causal interpretation from ecological field theory. Ecol Modell 132:167–173
Lima KC, Satyamurty P (2010) Post-summer heavy rainfall events in Southeast Brazil associated with the South Atlantic Convergence Zone. Atmos Sci Lett 11:13–20
Lirman D (2000) Fragmentation in the branching coral Acropora palmata (Lamarck): growth, survivorship, and reproduction of colonies and fragments. J Exp Mar Biol Ecol 251:41–57
Lopes EP (2011) Leiosolenus aristatus (Dillwyn, 1817), new to the Cape Verde Islands (Mollusca, Bivalvia, Mytilidae). Zool Caboverdiana 2(2):71–73
Luz BLP, Capel KCC, Zilberberg C, Flores AAV, Migotto AE, Kitahara MV (2018) A polyp from nothing: the extreme regeneration capacity of the Atlantic invasive sun corals Tubastraea coccinea and T. tagusensis (Anthozoa, Scleractinia). J Exp Mar Biol Ecol 503:60–65
Luz BLP, Di Domenico M, Migotto AE, Kitahara MV (2020) Life-history traits of Tubastraea coccinea: reproduction, development, and larval competence. Ecol Evol 10:6223–6238
Mantelatto MC, Mourão GG, Migotto AE, Creed JC (2011) Range expansion of the invasive corals Tubastraea coccinea and Tubastraea tagusensis in the Southwest Atlantic. Coral Reefs 30:397
Mizrahi D, Navarrete AS, Flores AAV (2014a) Uneven abundance of the invasive sun coral over habitat patches of different orientation: an outcome of larval or later benthic processes? J Exp Mar Biol Ecol 452:22–30
Mizrahi D, Navarrete SA, Flores AAV (2014b) Groups travel further: pelagic metamorphosis and polyp clustering allow higher dispersal potential in sun coral propagules. Coral Reefs 33:443–448
Mizrahi D, Pereira SF, Navarrete AS, Flores AAV (2017a) Allelopathic effects on the sun-coral invasion: facilitation, inhibition and patterns of local biodiversity. Mar Biol 164:139
Mizrahi D, Kitahara MV, Barbosa ACC, Flores AAV (2017b) Possible interference competition involving established fish and a sun coral incursion. Mar Biodiv 47:369–370
Mizrahi D (2008) Influência da temperatura e luminosidade na distribuição da espécie invasora Tubastraea coccinea na região de ressurgência de Arraial do Cabo - RJ. MSc Dissertation, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil, 85 pp.
Moreira TSG, Creed JC (2012) Invasive, non-indigenous corals in a tropical rocky shore environment: no evidence for generalist predation. J Exp Mar Biol Ecol 438:7–13
Morton B (1993) How the ‘forceps’ of Lithophaga aristata (Bivalvia: Mytiloidea) are formed. J Zool 229:609–621
Nogueira JMM (2003) Fauna living in colonies of Mussismilia hispida (Verrill) (Cnidaria: Scleractinia) in four south-eastern Brazil Islands. Braz Arch Biol Technol 46:421–432
Paula A, Creed JC (2005) Spatial distribution and abundance of non-indigenous coral genus Tubastraea (Cnidaria, Scleractinia) around Ilha Grande, Brazil. Braz J Biol 65:661–673
De Paula AF (2007) Biologia reprodutiva, crescimento e competição dos corais invasores Tubastraea coccinea e Tubastraea tagusensis (Scleractinia: Dendrophylliidae) com espécies nativas. PhD Dissertation, Universidade Federal do Rio de Janeiro. Rio de Janeiro 87 pp.
R Core Team (2021) R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. https://www.R-project.org/.
Reimer AA (1976) Succession of invertebrates in vacant tests of Tetraclita stafactifera panamensis. Mar Biol 35:239–251
Rinkevich B, Loya Y (1985) Intraspecific competition in a reef coral: effects on growth and reproduction. Oecologia 66:100–105
Sammarco PW, Porter SA, Sinclair J, Genazzio M (2014) Population expansion of a new invasive coral species, Tubastraea micranthus, in the northern Gulf of Mexico. Mar Ecol Prog Ser 495:161–173
Scott PJB, Risk MJ (1988) The effect of Lithophaga (Bivalvia: Mytilidae) boreholes on the strength of the coral Porites lobata. Coral Reefs 7:145–151
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 21:1339–1350
Simberloff D, Von Holle B (1999) Positive interactions of nonindigenous species: invasional meltdown? Biol Invasions 1:21–32
Simone JRL, Gonçalves EP (2006) Anatomical study on Myoforceps aristatus, an invasive boring bivalve in S.E. Brazilian coast (Mytilidae). Pap Avulsos Zool 46:57–65
Smith LD (2011) Densities of the endolithic bivalve Lithophaga lessepsiana (Vaillant, 1865) in Pocillopora damicornis, Solitary Islands Marine Park, northern NSW, Australia. Molluscan Res 31:42–46
Smith LD, Hughes TP (1999) An experimental assessment of survival, re-attachment and fecundity of coral fragments. J Exp Mar Biol Ecol 235:147–164
Turner RD, Boss KJ (1962) The genus Lithophaga in the western Atlantic. Johnsonia 4:81–116
Valentich-Scott P, Dinesen GE (2004) Rock and coral boring Bivalvia (Mollusca) of the middle florida keys USA. Malacologia 46(2):339–354
Vermeij MJA, Fogarty ND, Miller MW (2006) Pelagic conditions affect larval behavior, survival, and settlement patterns in the Caribbean coral Montastraea faveolata. Mar Ecol Prog Ser 310:119–128
Vianna da Silva JS, Junqueira AOR, Fernandes FC, Leitão MS, Barbosa D, Bahia J (2007) Myoforceps aristatus (Dillwyn, 1817), mais um bivalve introduzido na Baía de Sepetiba/RJ. Anais do VIII Congresso de Ecologia do Brasil, Caxambu, 23–28 September 2007.
Vinagre C, Silva R, Mendonça V, Flores AAV, Baeta A, Marques JC (2018) Food web organization following the invasion of habitat-modifying Tubastraea spp. corals appears to favor the invasive borer bivalve Leiosolenus aristatus. Ecol Indic 85:1204–1209
Wanless RM, Scott S, Sauer WHH, Andrew TG, Glass JP, Godfrey B, Griffiths C, Yeld E (2010) Semi-submersible rigs: a vector transporting entire marine communities around the world. Biol Invasions 12:2573–2583
Wells JW (1982) Notes on Indo-Pacific Scleractinian Corals. Part 9. New corals from the Galápagos Islands. Pac Sci 36:211–219
Westoby M (1984) The self-thinning rule. Adv Ecol Res 14:167–225
Acknowledgements
Research fellowships were granted to D.M. (FAPESP post-doctoral fellow #2017/04904-2), R.C.D. (FAPESP post-doctoral fellow #2019/01934-3), A.A.V.F. (CNPq research fellow #315754/2021-4) and M.V.K. (CNPq research fellow #305274/2021-0). M.V.K. also acknowledges the support of the São Paulo Research Foundation (FAPESP grant #2021/06866-6). This is a contribution of the Research Centre for Marine Biodiversity of the University of São Paulo (NP – Biomar/USP).
Author information
Authors and Affiliations
Corresponding author
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
Mizrahi, D., Duarte, R.C., Kitahara, M.V. et al. Interactions between invaders: facilitation of boring bivalves leads to reduced adhesive strength of sun corals. Coral Reefs 42, 473–481 (2023). https://doi.org/10.1007/s00338-023-02358-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-023-02358-8