The rise of a native sun coral species on southern Caribbean coral reefs

. In contrast with a general decline of Caribbean reef corals, a previously rare sun coral is increasing in abundance within shallow coral communities on Curac (cid:1) ao. This azooxanthellate scleractinian was identi ﬁ ed as Cladopsammia manuelensis, which has an amphi-Atlantic distribution. Over the last decade, C. manuelensis has increased abundance along the leeward coast of Curac (cid:1) ao (southern Caribbean) between depths of 4 and 30 m. This species was initially not noticed because it resembles the invasive coral Tubastraea coccinea , which was introduced to Curac (cid:1) ao from the Indo-Paci ﬁ c around 1940. However, in contrast to T. coccinea, C. manuelensis was previously only present on deeper reef sections ( > 70 m) of Caribbean reefs. Our observations illustrate how the sudden increase in abundance of a previously unnoticed, apparently cryptogenic species could result from natural dynamics on present-day reefs, but also could easily be mistaken for an invasive species. The ﬁ nding that deep reef sections can harbor species capable of colonizing shallower reef zones highlights the importance of thorough inventories of reef communities across large depth ranges, which can help us to discriminate between range increases of native species and the arrival of invasives.

Indo-Pacific corals of the genus Tubastraea (Scleractinia: Dendrophylliidae) have become introduced to the Caribbean for decades (Creed et al. 2017).Because their expanded tentacles appear like yellow, radiating sun rays, they are often named sun corals.So far, three Tubastraea species have been observed in the tropical and subtropical West Atlantic, most probably introduced as fouling organisms on ships and oil platforms (Creed et al. 2017).Unlike many other reef-building corals, Tubastraea species are not restricted to shallow depths as they lack symbiotic algae (zooxanthellae) and solely depend on planktonic food for nutrition (Goreau et al. 1971).
The first introduced Tubastrea species, T. coccinea Lesson, 1829, arrived in the Caribbean at Curac ßao and Puerto Rico around 1940 and subsequently expanded its range northward to Georgia (USA) and southward to southern Brazil (Cairns 2000, Creed et al. 2017).The second species, T. tagusensis Wells, 1982, has become widespread along the Brazilian coastline since 2002 (Creed et  and has recently been reported from the Gulf of Mexico (Figueroa et al. 2019).Both species form clumps of polyps with dark-and light-orange calyces, respectively (Mantelatto et al. 2011).The third introduced species, T. micranthus (Ehrenberg, 1834), has been observed as fouling benthos on oil rigs in the Gulf of Mexico since 2006 and possesses a branching morphology with green calyces and tentacles (Sammarco et al. 2010, Creed et al. 2017).Along the coastline of Brazil, the first two are now considered nuisance species because they outcompete native corals (dos Santos et al. 2013, Miranda et al. 2016).
During reef surveys (2014-2017) along the leeward side of Curac ßao (southern Caribbean), a previously unnoticed, but presently common sun coral species was observed at 23 out of 32 (72%) dive locations (Figs. 1, 2; Appendix S1: Table S1).Its sudden increase in abundance in shallow water at Curac ßao had already been described by Engelen et al. (2018), who identified the species as Rhizopsammia goesi (Lindstr€ om 1877).The new species looked very similar to co-occurring T. coccinea, because both species have distinctive yellow tentacles.However, under artificial light the color of the new species' calyces varies from gray to brick red or dark orange, which differs from the uniform dark orange commonly seen in T. coccinea (Fig. 1; Appendix S1).Young polyps of the newly seen species taper toward the base, where they bud off from the basis of older polyps (Fig. 1c-f, j) or from root-like stolons (Fig. 1a, d, k, l), which eventually form a basal plate (Fig. 1k).In between polyps, the basal plate may become overgrown by algae, disguising the coral's colonial architecture (Fig. 1g, l).Both species were commonly found on reefs, on shipwrecks, and underneath rocky overhangs: T. coccinea at 0.2-55 m depth and the new species at 4-30 m (Appendix S1).
Septa of the new species appear to be more pronounced than those of T. coccinea (Fig. 2a).In dead polyps (Fig. 2b), septa of the new species show a bifurcating pattern according to the Pourtal es plan (Cairns 1994), which does not occur in Tubastraea (Fig. 2c).The septal pattern and the presence of stolons indicate that this species belongs to either the genus Cladopsammia or Rhizopsammia, which are both phylogenetically closely related to Tubastraea (Cairns 2001, Arrigoni et al. 2014).Genetic information on Atlantic Cladopsammia and Rhizopsammia is currently not available, but a preliminary molecular analysis based on the mitochondrial marker cytochrome c oxidase subunit I (COI) revealed that the species found on Curac ßao is very closely related to both Cladopsammia gracilis (Milne Edwards & Haime, 1848) and Rhizopsammia wettsteini (Scheer & Pillai, 1983) from the Red Sea (A.-F.Hiemstra, unpublished data).The stolons of Cladopsammia merge into a basal plate (like in Fig. 1k) but not in Rhizopsammia; though this difference is hard to observe in juveniles (Cairns 2000, Cairns andKitahara 2012;Fig 1a) making young individuals of both genera almost impossible to identify.
In the Caribbean, two species are already present that fulfill aforementioned morphological characters and taxonomic relatedness to the species from the Red Sea: Cladopsammia manuelensis (Chevalier, 1966) and R. goesi (Lindstr€ om 1877).Both species occur at mesophotic depths or deeper.The bathymetric range of the amphi-Atlantic C. manuelensis is 70-366 m (Cairns 2000).Its earliest West Atlantic records (since 1958) are from the Gulf of Mexico, while specimens from Curac ßao were first collected with manned submersibles from 143 to 330 m depth in 2000 and 2013, respectively (https://collections.nmnh.si.ed u/search/iz/).Fossils of East Atlantic C. manuelensis were found in the Pleistocene of West Africa (Cairns 2000), and since there are several scleractinian coral species with a natural amphi-Atlantic distribution (Cairns 2000, Nunes et al. 2011), there is no reason to assume that this species was recently introduced in the western Atlantic.
Rhizopsammia goesi is a deep-water species native to the Caribbean: Museum specimens have been collected from 75 to 275 depth at St. Martin in the eastern Caribbean (Lindstr€ om 1877) and from 73 to 152 m depth in the Colombian Caribbean (Santodomingo et al. 2013), and it has been observed at depths exceeding 30 m in the Bahamas and Cayman Islands (Slattery and Lesser 2019).Rather than yet another introduced dendrophylliid, the new coral increasing in abundance within shallow-water coral communities is likely one of two species that are native to deep water in the Caribbean as already proposed by Engelen et al. (2018).However, in contrast to Engelen et al. (2018) and Hoeksema and ten Hove (2017), who identified the species as R. goesi, we identified the species as C. manuelensis ❖ www.esajournals.orgbased on the presence of a basal plate, which is visible in some of the larger specimens (Fig. 1; Appendix S1) but is absent in R. goesi (Cairns 2000).Previously, the basal plate was not noticed because corals were too young and it had not yet developed or because it was covered by algae.
Corals of C. manuelensis were recently also discovered in Haiti, where they were abundant  in particular on shipwrecks and underneath rocky overhangs, it was not found here (Hoeksema and van Moorsel 2016).The rise of C. manuelensis on shallow Curac ßaoan reefs and certain other islands within the Caribbean is remarkable considering the decrease in abundance of many other coral species in recent decades (de Bakker et al. 2016).Additional research is needed to find out what has caused the expansion of C. manuelensis on Caribbean coral reefs and how this relates to the ecological role and geographic expansion of sun coral species in the western Atlantic.Moreover, the present case indicates that in future studies on the origin of cryptogenic reef species, we should not only consider introductions from elsewhere, but also bathymetric range expansions of native species previously only recorded from greater depths.

Fig. S16 .
Fig. S16.Colony of C. manuelensis at Aruba (May 2019).About 100 colonies were observed at 51 reef sites in 5x30 m 2 transects at 10 m depth with each site 700 m from the next one along the entire leeward coast of Aruba in May 2019.