Doctoral Programme on Marine Ecosystem Health and Conservation
 PhD Subject Catalogue Fifth Edition - 2014
Invasive corals of the genus Tubastraea on Caribbean coral reefs: comparison between new and past invaders.
PhD Code: MARES_14_18:
  • Host institute 1: P5 - University of Algarve
  • Host institute 2: P3 - University of Bologna
  • Host institute 3: CARMABI, Curaçao Netherlands Antilles ; Vienna University, Austria ; CNRS Universite de Nice Sophia antipolis; P24 - Australian Institute of Marine Science
Research fields:
  • T3 - Biological Invasions
  • Ester Serrão
  • Marco Abbiati
  • Prof Herndl Gerhard -
  • Mark Vermeij (Carmabi, Curacao) ; Olivier Thomas (Nice, France)
Contact Person and email: Aschwin Engelen -

Subject description
Marine ecosystems are increasingly impacted by natural and anthropogenic disturbances and changes. Biological invasions are recognized as one of the major threats to marine and coastal ecosystems due to the potential of these invasive species to locally or regionally displace native key stone species, change biodiversity, alter species interactions, ecosystem performance, modify habitat and have severe economic costs (Carlton and Geller 1993, Vitousek et al. 1996, Sala et al. 2000, Pimentel et al. 2000, Cacbelos et al 2012, Engelen et al. 2013).
Biological invasions in tropical marine habitats are probably far less common than in temperate regions, yet not necessary less harmful as has become clear with the recent introduction of the lion fish (Pterois volitans) in the Caribbean (Albins & Hixon 2013). In contrast to temperate reefs tropical coral reefs are dominated by zooxanthellate corals, which are assumed to have a fitness advantage in oligotrophic transparent waters. Surprisingly, azooxanthelate corals of the genus Tubastraea from the Pacific seem to be successfully invading Caribbean coral reefs. Natural reef communities may be negatively impacted if this invader thrives and outcompetes native Caribbean species.
In this perspective the first invader was the azooxanthellate scleractinian coral, Tubastraea coccinea, orange cup coral, which was first documented at two Caribbean reefs (Curaçao, the location of our partner CARMABI, and Puerto Rico) in 1943 (Vaughan and Wells 1943). Over the last decades, range expansions have extended to reefs throughout the Caribbean. Over the last decade Tubastraea coccinea was shown to be a prolific hermaphroditic brooding scleractinian coral (Harrison and Wallace, 1990) capable of producing larvae through sexual and asexual means (Ayre and Resing, 1986) and commonly producing new asexual colonies through runner formation (Vermeij, 2005). This species can dominate with population sizes that exclude native sessile organisms, likely reducing the species diversity and recruitment potential of native species within this community. However, the species is only found in cryptic habitats, where it hardly interacts directly with any major reefbuilding scleractinian.
More recently, two additional Pacific Tubastraea species have been detected in the Atlantic: Tubastrae. micranthus in the Gulf of Mexico (Sammarco et al 2010) and Tubastrae tagusensis in Brazil (Creed 2006). In contrast to T. coccinea, T. tagusensis in Brazil caused tissue necrosis and partial mortality of native corals due to contact with the invader (Creed 2006) as this species is non-cryptic colonizing on top of reefs. Invasive Tubastraea could facilitate algal overgrowth as it kills or makes native coral tissue retreat, which provides the opportunity for especially turf algae to move in, strengthening the displacement of native corals. In addition, closely related corals have potent chemical compounds suggesting that these invasive Tubastraea benefit from these to escape predation and increase competitive advantage, such as by killing new recruits of native corals (Koh and Sweatman 2000, Cachet et al. 2013). In the beginning of this year we have detected T. tagusensis in considerable amounts on several reefs around Curaçao, where T. coccinea was originally introduced. We propose to use these invasive corals as model organisms to test three (invasion) theories and obtain sufficient scientific background for a conservation and MPA management plan.
1) Communities in the introduced range of invaders can have a resistance or resilience to invaders. This can be due to a) the strong competition and interaction among natives and the limitation of resources available for new colonizers and/or b) the presence of predators that can exert a top down control on the invader (Enemy Release Hypothesis; Vermeij et al 2009). We hypothesize that colonization by invasive corals will be stronger on more degraded and less protected reefs compared to MPAs. In addition, in this case the native predator of Tubastraea, the gastropod Epitonium billeeanum, has not been documented in the Caribbean or Gulf of Mexico. Therefor we hypothesize that due to the absence of native predators Tubastraea can reach higher growth rates in the introduced range than in their native range. There are however other Epitonium species in the Caribbean for which it needs to be tested whether they have the potential to control Tubastraea invasions to a certain extent.
2) A genetic paradox exists in invasion biology: how can invaders whom genetic variation must have been reduced by the relative few individuals introduced be so successful? One possible explanation is that multiple introductions from different origins of the native range can lead to introduced populations that are genetically richer than their native counterparts and hence have elevated adaptive capacities (Kolbe et al 2004). Our recent results on the invasive seaweed however clearly indicate that invaders can be very successful even with very limited genetic variation (Viard et al unpublished). Invasive species form very good model species to investigate the importance of genetic diversity and drift for the success of a species, which at the same time will enable us to reconstruct invasion and trace introduction(s). In this context we hypothesize that the Tubastraea in the introduced range is genetically less diverse and differentiated than in their native range due to limited number of introductions.
3) The relative new hologenome theory states that each organism also comprises an associated microbial community that contributes to the overall fitness of the host (Rosenberg et al 2007). So, the holobiont rather than the individual organism (host) is the subject of natural selection. Bacteria play important roles in corals (Herndl & Velimirov 1986, Frade et al 2008, Rowher et al 2002, Ainsworth et al 2010, Garren & Azam 2012) and as such invasive corals form interesting model organisms to study the structure and function of coral associated prokaryotic communities. We hypothesise that coral associated prokaryotic communities enable their host to adapt and acclimate to the new environmental conditions encountered during invasion and even participate in the constitutive or induced chemical defense of the host. At the same time invasive species can potentially act as vectors of dispersal for (beneficial and pathogenic) bacteria new to the introduced range and as such affect the gene pool and metabolic pathways available to microbes on coral reefs.
This PhD project based on the hypotheses stated will be combine field and molecular ecology. In order to make it feasible within the 3 year funding the consortium of collaborators has already initiated the technical testing of the approaches that will be implemented in the project. Genetic barcodes have been developed and tested for Tubastraea, DNA has been collected for molecular marker development and we are in the process of obtaining the first insights in the microbiome of the two invasive corals species. With still 1.5 years ahead before the candidate will start we are sure that the technical aspects will be controlled and that the candidate can build upon the first obtained insights.
  • Ainsworth TD, Thurber RV, & Gates RD (2010) The future of coral reefs: a microbial perspective. Trends in Ecology & Evolution 25(4):233-240.
  • Albins MA, Hixon MA (2013) Worst case scenario: potential long-term effects of invasive predatory lionfish (Pterois volitans) on Atlantic and Caribbean coral-reef communities. Environ Biol Fish 96:1151-1157.
  • Ayre DJ, Resing JM (1986) Sexual and asexual production of planulae in reef corals. Mar Biol 90:187–190.
  • Cacabelos E, Engelen AH, Mejia A, Arenas F (2012) Comparison of the assemblage functioning of estuary systems dominated by the seagrass Zostera noltii versus the invasive drift alga Gracilaria vermiculophylla. Journal of Sea Research 72:99-105.
  • Cachet N, Loffredo L, Ocaña Vicente O, Thomas OP (2013) Chemical diversity in the scleractinian coral Astroides calycularia. Phytochemistry Letters 6: 2005-208.
  • Carlton JT, Geller JB (1993) Ecological roulette - the global transport of nonindigenous marine organisms. Science 261: 78-82.
  • 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.
  • Engelen AH, Primo AL, Cruz T, Santos R (2013) Faunal differences between the invasive brown macroalga Sargassum muticum and competing native macroalgae. Biological Invasions 15:171-183.
  • Frade PR, De Jongh F, Vermeulen F, Van Bleijswijk J, & Bak RPM (2008) Variation in symbiont distribution between closely related coral speciesover large depth ranges. Molecular Ecology 17(2):691-703.
  • Garren M & Azam F (2012) New directions in coral reef microbial ecology. Environmental Microbiology 14(4):833-844.
  • Harrison PL, Wallace CC (1990) Reproduction, dispersal and recruit- ment of scleractinian corals. In: Dubinsky Z (ed) Coral reefs, eco- systems of the world 25. Elsevier, Amsterdam, pp. 133–207.
  • Herndl GJ & Velimirov B (1986) Microheterotrophic Utilization of Mucus Released by the Mediterranean Coral Cladocora-Cespitosa. Marine Biology 90(3):363-369.
  • Koh EGL, Sweatman H (2000) Chemical warfare among scleractinians: bioactive natural products from Tubastraea faulkneri Wells kill larvae of potential competitors JEMBE 251: 141-60.
  • Kolbe JJ et al (2004) Genetic variation increases during biological invasion by a Cuban lizard. Nature 431: 177-181.
  • Pimentel D, Lach L, Zuniga R, Morrison D (2000) Environmental and economic costs of nonindigenous species in the United States. Bioscience 50: 53-65.
  • Rohwer F, Seguritan V, Azam F, & Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Marine Ecology-Progress Series 243:1-10.
  • Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I (2007) The role of microorganisms in coral health, disease and evolution. Mature Reviews Microbiology 5: 355-362.
  • Sala OE, Chapin FS, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, Huber-Sanwald E, Huenneke LF, Jackson RB, Kinzig A, Leemans R, Lodge DM, Mooney HA, Oesterheld M, Poff NL, Sykes MT, Walker BH, Walker M, Wall DH (2000) Biodiversity - global biodiversity scenarios for the year 2100. Science 287: 1770-4.
  • Sammarco PW, Porter SA, Cairns SD (2010) A new coral species introduced into the Atlantic Ocean – Tubastraea micranthus (Ehrenberg 1834) (Cnidaria, Anthozoa, Scleractina): An invasive threat? Aquatic Invasions 5(2): 131-140.
  • Vaughan TW, Wells JW (1943) Revision of the suborders, families, and genera of the Scleractinia. Geol Soc Am Spec Pap. 44: 1-363.
  • Vermeij MJA (2005) A novel growth strategy allows Tubastrea coccinea to escape small-scale adverse conditions and start over again. Coral Reefs 24: 442.
  • Vermeij MJA, Smith TB, Dailer ML, Smith CM (2009) Release from native herbivores facilitates the persistence of invasive marine algae: a biogeographical comparison of the relative contribution of nutrients and herbivory to invasion success. Biol. Invasions 11:1463-1474.
  • Vitousek PM, Dantonio CM, Loope LL, Westbrooks R (1996) Biological invasions as global environmental change. Am Sci. 84: 468-78.

Expected outcomes
We expect the candidate will be able to produce 5 publications with the putative titles: 
  •  Importance of reef health for the resistance and resilience to biological invasions (CARMABI & Ualg) 
  • Microbial community composition and function associated with the invasive coral Tubastraea: a role in invasions in the Caribbean? (Vienna University & Ualg) 
  • Coral predators as potential control on invasive coral populations in the native but not in introduced range: enemy release hypothesis (AIMS & CARMABI) 
  • Chemical diversity and induction in invasive cupcorals (CARMABI, Ualg & CNRS Universite de Nice) 
  • Testing of genetic paradox in invasive corals: a wide-geographic population biology approach on Tubastraea spp. (Ualg & CARMABI) 
These publications should be able to demonstrate that: healthier reefs with less bare substrate available and more oligotrophic water conditions are less prone to colonisation and proliferation of invaders; associated microbiomes are involved in the invasiveness and perhaps invasion impact; lack of predators in the introduced range plays an important role also in coral invasions on the short-term (invasion start); invaders benefit strongly from their chemical capacities during invasions; genetic bottlenecks do not limit invasion potential. Finally, we hope to demonstrate that previous invasions can be used to predict how new invasions will develop. 
We expect to provide the isolation of new microbes, characterization of new chemical compounds, new invasion biology insights for implementation in conservation and MPA management. The candidate will be embedded in a top level consortium of partners where each of the partners will cover the research costs associated to its expertise and project contribution.

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