Red Sea host anemones
This study presents a multisource list that now includes eight host sea anemones in the Red Sea, seven of which have been described hosting A. bicinctus, and one (Cryptodendrum adhaesivum) that has been documented and suggested as a host (Dunn 1981, Chadwick and Arvedlund 2005, Emms et al. 2020) but was not confirmed as such in our surveys. Seven of the eight host anemones were directly observed in our visual surveys: Heteractis crispa, Heteractis aurora, Entacmaea quadricolor, Heteractis magnifica, Cryptodendrum adhaesivum, Stichodactyla mertensii, and Stichodactyla haddoni.
Our documentation of symbiosis between S. mertensii and S. haddoni with A. bicinctus resolves conflicting reports of their distribution along the coast of Saudi Arabia. Anecdotal reports (e.g., dive shop operators) from the Egyptian coast suggest C. adhaesivum may host A. bicinctus in some areas, but this symbiosis has not been documented in the literature nor in our survey effort – C. adhaesivum that we found in Saudi Arabia only harbored Dascyllus trimaculatus (Rüppell, 1829). Our results considerably revise the host anemone distributions and diversity in the Red Sea.
However, one purported Red Sea anemone species, S. gigantea, was not observed in our surveys, with or without fish symbionts. Further, we found no records containing photos or preserved specimens from the Red Sea in either the literature or databases reviewed. This calls into question previous reports of this species occurring in the Red Sea and other nearby localities, and warrants further discussion, particularly in light of widespread observations of a similar looking species, S. mertensii, and the potential for misidentification among all host carpet anemone species.
Red Sea and Indian Ocean Stichodactyla species
In contrast to most literature sources, observations of S. mertensii along the Saudi Arabian coastline indicate that the known range of this species should be expanded significantly northward to include the Red Sea. The next closest observation, according to OBIS, is approximately 2000 km south near Madagascar (OBIS 2020). Other sources cite East Africa as the northwestern boundary of its range (Fautin and Allen, 1992). Given the broad distance covered by recent observations of this species along the Saudi Arabian coastline, S. mertensii has likely been present in the Red Sea for several decades or longer, which is particularly interesting given the complete absence of the commonly reported carpet anemone species in the region, S. gigantea, on surveyed reefs. Our initial review found only eight Red Sea records of S. gigantea, all from one database (Fautin 2013), and none with associated photographs or specimens. Further, of those eight records, three report the “original scientific name” as Actinia (Isacmaea) gigantea. According to WoRMS, Isacmaea gigantea Hemprich & Ehrenberg has been synonymized with Stichodactyla gigantea (Daly and Fautin 2020a, 2020b); however, Actinia (Isacmaea) gigantea (Forsskäl) has been synonymized with Stichodactyla haddoni (Daly and Fautin 2020a, 2020b). To further confuse the matter, the “original scientific author” listed in the database is neither Hemprich & Ehrenber nor Forsskäl, but Saville-Kent, who described S. haddoni.
The nomenclature of S. mertensii and S. gigantea in the Red Sea is also conflicting and the physical appearances of S. mertensii, S. gigantea, and S. haddoni are all relatively similar, which may have led to published misidentifications in the Red Sea among these species. In Dunn’s seminal guide to anemonefishes and their distributions (Dunn 1981), there are two records of S. gigantea in association with A. bicinctus in the Red Sea: “Das Zusammenleben von Riffanemonen und Anemonfischen” (Schlichter 1968) and “Commensalism between fish and anemone” (Gohar 1948). Schlichter 1968 reports S. gigantea (identified as Discosoma giganteum, now synonymized with S. gigantea, Fautin 2013) from the Egyptian coastline, near Hurghada, and identifies the species based solely on the physical description of a “fleshy mouth and very short tentacles” (Schlichter 1968). No other descriptive information is provided, and the only photographs in Schlichter’s publication are of H. crispa. On its own, this description is at most inconclusive, however, the author goes on to describe the behavior of the anemones in question: “...when the anemones were touched a little more forcefully, they pulled back abruptly into the ground, and only a gentle depression in the sand indicated where they were to be found.” This behavior is an identifying characteristic of S. haddoni, which can and does retract completely into the sand, but is not reported as an identifying characteristic of S. gigantea (Fenner 2016, personal observations).
We have been unable to find any other conclusive records of S. gigantea in the Red Sea literature spanning the last 100 years, and the type specimen collected from the Red Sea (Forsskäl, 1775) was lost from the Coelenterates Collection at the Universitetets Zoologiske Museum in Copenhagen. Dunn (1981) reports, “Much of Forsskal’s (1775) original description, while accurate, is not diagnostic, but the extreme adhesiveness of the tentacles which may result in tearing the animal apart permits firm identification of his description with this species”. Adhesiveness is a relatively subjective and variable characteristic (e.g., S. mertensii and S. haddoni are both generally “adhesive”, and both S. haddoni and S. gigantea tentacles can tear off when touched); based on confirmed current survey data, review of past reports and misidentifications, and Forsskäl’s incomplete description, we consider it likely that misidentifications between these carpet anemone species go back to the type specimen from the Red Sea. It is, however, important to reiterate that we were not able to conduct surveys on the Egyptian coastline as part of this study. Instead, we re-examined past records and anemone photographs from this region. As such, we cannot completely rule out that S. gigantea may occur on the western coastline of the Red Sea in low abundance, and that historical identifications were correct. If this is the case, then the abundance of this species in the area has substantially declined, for unknown reasons.
Rigorous systematic and taxonomic revision will be required to formally disentangle the conflicting species descriptions within Stichodactyla, but we call into question Forsskäl as the taxonomic authority of S. gigantea. Rather, based on our anemone surveys throughout the Red Sea and updated distributions from global databases, we hypothesize that the identity of Forsskäl’s anemone description is most likely what is currently recognized as S. haddoni.
As a clownfish host, recent literature generally does not report S. haddoni as hosting A. bicinctus in the Red Sea (e.g., Emms et al. 2020). However, our surveys confirmed the association between these two species. As S. haddoni was found in both the southern and central Red Sea regions (and has possibly been observed in other Red Sea regions as indicated by OBIS misidentifications and non-scientific reports from Egypt), populations of this species may be widespread (albeit not very abundant) in the Red Sea. It is also possible that survey efforts in the region may have failed to thoroughly canvas suitable S. haddoni habitats; some reports indicate this species prefers sandy-bottom habitats in waters as deep as 40 m, and often far from heavily surveyed reef habitats (Attaran-Fariman and Javid 2015). During our surveys, this species typically occurred in sandy habitats from 9 to 13 m depth. The depth limitations of our surveys, however, limit our ability to comment on deeper distributions.
Similar to the previous discussion of S. mertensii and S. gigantea, S. haddoni and S. gigantea also look superficially similar. It is therefore possible that anemones identified as S. gigantea in this region were indeed S. haddoni, as discussed above in reference to Schlicter’s incorrect identifications. Conversely, other studies from the Red Sea likely incorrectly identified S. mertensii as S. haddoni, including one publication that listed 357 S. haddoni individuals in the Saudi Arabian Red Sea (Hobbs et al. 2013). Stichodactyla mertensii was considerably more abundant across all surveyed regions along the entire coastline of Saudi Arabia; unverifiable (no photographs or specimens) studies that report S. haddoni or S. gigantea in abundance on surveys in this region, and do not report S. mertensii, are likely incorrect in their identifications. Further, in other Indian Ocean regions, including South Africa, both S. mertensii and S. haddoni have been recently reported on surveys (Acuña and Griffiths 2004; Laird and Griffiths 2016); S. gigantea has not been reported.
In summary, the widespread documentation of S. mertensii from our surveys in the Saudi Arabian Red Sea and literature review results have three possible explanations: i) S. mertensii has experienced a recent range expansion into the Red Sea through the Gulf of Aden, ii) S. mertensii has been historically present in the Red Sea but not documented, or iii) host carpet anemone species in the Red Sea have been historically misidentified as S. gigantea. We consider the third scenario to be most likely. The large distance covered by recent observations (almost 2000 km of coastline) suggests that this species is not new in the Red Sea, ruling out a recent range expansion. As carpet anemone and clownfish pairs are highly visible, charismatic partnerships on coral reefs, we also find it unlikely that S. mertensii has been historically overlooked by studies in the Red Sea, especially in more frequently-visited reefs such as those in Egypt. In addition to our study’s documentation on the eastern coastline, recent photographs and unpublished citizen science records from Egypt and Sudan indicate S. mertensii is widely distributed on the western coastline of the Red Sea. Thus, it is likely that the conflicting nomenclature and similarity in morphological characteristics among carpet anemone species resulted in their historical misidentifications in the Red Sea. Determining the absence of a species in a large region is much more difficult than determining the presence of that same species; however, we consider it likely that S. gigantea is at least ecologically irrelevant in the Red Sea, and likely not present at all.
Heteractis crispa/Heteractis aurora morphological variability
Recent work that has used molecular techniques to resolve host anemone phylogenies (e.g. Titus et al. 2019) has indicated that Heteractis crispa and Heteractis aurora are closely related, and may be sister taxa. In the Red Sea, we observed a morphological gradient between these two species, with many anemones exhibiting overlapping phenotypes in Saudi Arabia (Fig. 4). In other parts of the western Indian Ocean, specimens have been observed and photographed by citizen science contributors that appear to illustrate morphological characteristics of these two species within the same individual. Neither species was particularly abundant at our survey localities, and these low population densities, combined with the morphological gradient we observed, may hint at ongoing hybridization. Future studies integrating genomic and morphological techniques are necessary to further disentangle whether these species hybridize, or if both H. crispa and H. aurora simply exhibit a wide degree of phenotypic variability (as seen in E. quadricolor).
Amphiprion bicinctus: generalist anemonefish
The host specificity of different clownfish species varies widely, from specialists (one associated host anemone, e.g., Amphiprion frenatus) to generalists (ten associated host anemones, e.g., Amphiprion clarkii). Some sources (e.g., WoRMS, FishBase) list as few as three species of host anemones for A. bicinctus, which is around the average host specificity for all 28 extant species of anemonefish. Based on this study, A. bicinctus is one of the most generalist clownfish: only Amphiprion clarkii has been documented in symbiosis with more host anemones. One other species, Amphiprion akindynos, is known to associate with seven host anemones, which is in the range of A. bicinctus’ host specificity--depending on two inconclusive anemone associations for A. bicinctus (C. adhaesivum and S. gigantea), the Red Sea clownfish is either the second or third most generalist clownfish species. Amphiprion bicinctus’ ability to use a diverse array of sea anemone microhabitats may be crucial in helping it adapt to future changing cnidarian communities in the Red Sea.