First record of the epiphyte sea anemone Bunodeopsis pelagica in the Mexican Atlantic

Abstract

Bunodeopsis pelagica is one of the few species of sea anemones known to be found in the floating algae of Sargassum spp. It has been reported in the North Atlantic, particularly in the Canary Islands and the coast of Jamaica. The present study is the first to report the occurrence of B. pelagica in the Mexican Atlantic, found as epiphyte on Sargassum natans off Alacranes reef (southern Gulf of Mexico) and in Puerto Morelos reef (Mexican Caribbean), revealing that this species is much more widespread than has been reported. Bunodeopsis pelagica is mainly distinguished from other species of Bunodeopsis by having simple minute protuberances on its column, while its congeners have larger and much more developed vesicular projections. With the record of B. pelagica, the number of known species of actiniarian sea anemones from the Mexican Atlantic increases to 23.

Introduction

Bunodeopsis pelagica (Quoy and Gaimard, 1833) is one of the few known sea anemone species that lives as an epibiont on drifting seaweeds of Sargassum spp. (Fisher, 1976). This species was originally described as Actinia pelagica in a short paragraph by Quoy and Gaimard (1833), as a very small yellowish form with long, large, pointed, dirty yellow tentacles with brownish spots, and with a characteristic violet ring around the mouth. In 1976, Fisher carried out a taxonomic redescription of this species, providing detailed information on its external and internal anatomy, as well as its cnidae. This species has been reported on Sargassum spp. off the coast of Jamaica (Fisher, 1976), but also as a benthic species in the rocky intertidal of the coast of Tenerife, in the Canary Islands, and in Madeira (Ocaña et al., 1991; Ocaña and den Hartog, 2002). Although it has been suggested that B. pelagica could be found throughout the Caribbean carried by floating Sargassum (Ocaña et al., 2007), there are no known previous published records of this species in other localities along the Caribbean Sea.

In the present study, we document the novel occurrence of B. pelagica in two locations in the Mexican Atlantic, being found on floating mats of Sargassum natans: off the coast of the Alacranes reef, in the Campeche Bank, southern Gulf of Mexico, and in the coast of Puerto Morelos reef, in the Mexican Caribbean. This species is taxonomically diagnosed and images of living specimens are provided. In addition, the external taxonomic characteristics that distinguish this species from its congeners are discussed.

Materials and methods

Thirty specimens of B. pelagica were collected from fresh pelagic Sargassum natans found off the coast of Desterrada Island, in the Alacranes reef (Campeche Bank, southern Gulf of Mexico) (22.52°N, 89.78°W) in June 2016, and five from S. natans collected in the coast of Puerto Morelos reef (Mexican Caribbean) (20.84°N, 86.87°W) in August 2020 (Figure 1). Living specimens were photographed, relaxed in 5% MgCl₂ seawater solution and then fixed in 10% seawater formalin. Morphological features and internal anatomy was examined following Fisher's (1976) description. Specimens were deposited in the Collection of the Gulf of Mexico and Mexican Caribbean Sea (registration code: YUC-CC-254-11-001309) of Unidad Multidisciplinaria de Docencia e Investigación en Sisal (UMDI-Sisal) at the Universidad Nacional Autónoma de México (UNAM).

Figure 1. Map of the southern Gulf of Mexico and Mexican Caribbean indicating the localities sampled in this study: red star indicates Alacranes coral reef location, blue star indicates Puerto Morelos reef location.

Results

All diagnostic features and body measures observed of the specimens examined agree well with the description of B. pelagica by Fisher (1976).

Order ACTINIARIA Hertwig, 1882
Suborder ENTHEMONAE Rodríguez & Daly in Rodríguez et al. (2014)
Superfamily METRIDIOIDEA Rodríguez & Daly in Rodríguez et al. (2014)
Family BOLOCEROIDIDAE Carlgren, 1924
Bunodeopsis pelagica (Quoy & Gaimard, 1833)
(Figures 2A and B)

Synonymy:

Figure 2. Bunodeopsis pelagica (Quoy and Gaimard, 1833): (A) specimen with oral disc and tentacles fully expanded, note the violet ring around the mouth; (B) specimens attached to Sargassum natans, note the simple protuberances in the column. Scale bars: 5 mm.

Actinia pelagica Quoy & Gaimard, 1833, pp. 146–147 (original description)
Anemonia pelagica Milne-Edwards, 1857, p. 235
Uncertain genus pelagica Quoy & Gaimard: Andres, 1883, pp. 578–579 nomen dubium
Bunodeopsis pelagica (Quoy & Gaimard, 1833): Fisher, 1976, pp. 103–110, 112–118

Short diagnosis: fully expanded oral disc and tentacles 3–7 mm in diameter in living specimens. Oral disc smooth, 2–4 mm in diameter, wider than column, transparent, with the insertions of the mesenteries clearly visible; mouth slit-like and raised, outlined by a thin violet ring (Figure 2A). Margin tentaculate. Tentacles irregularly arranged in 2–4 cycles (12–36 in number), long, slender, tapered, with numerous ridges containing batteries of nematocysts along their entire length; inner cycles of tentacles longer than outer ones, retractile and deciduous due to an endodermal sphincter muscle at their bases. Column cylindrical, widening towards the base, divided in capitulum and scapus. Capitulum smooth, transparent, with insertions of the mesenteries visible; scapus dark brown colour, translucent, with simple minute protuberances mainly on the lower half, arranged in longitudinal rows, creamy yellow in colour (Figure 2B). Cnidom: basitrichs, microbasic p-mastigophores and microbasic amastigophores.

Natural history: Bunodeopsis pelagica mostly lives on the floating seaweed Sargassum spp., although it has also been reported inhabiting on rocky substrate in the intertidal zone (Ocaña et al., 1991). A nudibranch mollusc, which also lives on the sea weed, feeds on B. pelagica (Fisher, 1976). This species is associated with endosymbiotic dinoflagellates of family Symbiodiniaceae Fensome, Taylor, Norris, Sarjeant, Wharton & Williams, 1993 (Fisher, 1976).

Distribution: Bunodeopsis pelagica has only been reported from the North Atlantic, now including Caribbean Sea, southern Gulf of Mexico and Canary Islands and Madeira (Quoy and Gaimard, 1833; Fisher, 1976; Ocaña et al., 1991; Ocaña and den Hartog, 2002; this study).

Taxonomic remarks: six valid species are currently known within the genus Bunodeopsis (Rodríguez et al., 2023a) (Table 1). Bunodeopsis pelagica has a violet ring around the mouth (Fisher, 1976; Ocaña et al., 1991), a feature shared with Bunodeopsis australis Haddon, 1898 (Haddon, 1898), and similar to the blue ring around the mouth reported for Bunodeopsis antilliensis Duerden, 1897 (Cairns et al., 1986).

Table 1. Comparison of some external anatomical characteristics between species of the genus Bunodeopsis

The main distinguishing characteristic of B. pelagica with its congeners lies in the minute protuberances on its scapus, in the lower half of its column, which are only thickened portions of the ectoderm, and are not true vesicles like those of the other members of the genus (Fisher, 1976) (see Figure 2B, Table 1). The vesicles of B. australis are of uniform size (Haddon, 1898), whereas those of B. antilliensis, Bunodeopsis globulifera (Duchassaing, 1850), Bunodeopsis strumosa Andrés, 1881 and Bunodeopsis medusoides (Fowler, 1888) are of unequal size and degree of development. Furthermore, the coloration of vesicles and tentacles also varies between these species (Table 1). In addition, B. medusoides is the only species of the genus reported with two siphonoglyphs (Cutress, 1979), while these structures are absent in the other species. Differences in cnidae arrangement and size ranges between species of the genus Bunodeopsis are difficult to assess, because different nomenclatures were probably used to classify the various types of cnidae. For example, Fisher (1976) and Carlgren (1952) report basitrichs in the tentacles of B. pelagica and B. strumosa, respectively, while Cutress (1979) reports microbasic b-mastigophores rather than basitrichs for B. medusoides, and none of these types of cnidocysts were reported in the tentacles of B. antilliensis (González-Muñoz et al., 2012). Similarly, some authors identify cnidocysts as microbasic amastigophores, while others mention them as microbasic p-mastigophores (Table 2). Furthermore, the studies by Carlgren (1952), Fisher (1976), Cutress (1979) and Chintiroglou and den Hartog (1995) do not include photographs or drawings of the different types of cnidocysts reported, so a proper comparison is not possible. Moreover, no information is known about the cnidae of B. australis. Table 2 summarizes the currently known information on the cnidocysts of the species within the genus Bunodeopsis. More studies on the types and size ranges of cnidocysts in all species of the genus Bunodeopsis are required in order to establish their differences and their specific characteristics.

Table 2. Cnidae comparison between species of genus Bunodeopsis

Discussion

The seaweed Sargassum spp. is known to provide habitat for a diverse community of animals and plants, which in turn support larger migratory species such as tunas, marlins, sharks, and turtles (Pendleton et al., 2014). These algae are carried by currents and normally arrive and accumulate on the coasts, but in low abundances and at irregular intervals (van Tussenbroek et al., 2017). However, since 2011 there has been an unprecedented massive influx of drifting Sargassum off the coasts of Caribbean countries, peaking between July and August 2015 (Rodríguez-Martinez et al., 2016; van Tussenbroek et al., 2017).

Some cnidarians are common members of the living invertebrate community that inhabit of drifting Sargassum spp., including several species of hydrozoans (e.g. Cunha and Jacobucci, 2010, Cunha et al., 2018; Mendoza-Becerril et al., 2020) and at least three species of sea anemones: Anemonia sargassensis Hargitt, 1908, Bartholomea annulata (Le Sueur, 1817), and B. pelagica (Carlgren and Hedgpeth, 1952; Fisher, 1976).

Although several taxonomic studies have been carried out on sea anemones in the Mexican Atlantic (e.g. González-Muñoz et al., 2012, 2013; De la Cruz-Francisco et al., 2016; De la Cruz-Francisco and González-Muñoz, 2019; Herrera-Bojórquez et al., 2020), the species B. pelagica had never been observed. Thus, we hypothesize that the recent encounter of this species could be related to this extraordinary massive arrival of large quantities of Sargassum spp. to the coasts of the Caribbean.

The specimens collected in both places in the Mexican Atlantic were found in floating Sargassum, which is the usual substrate for this species (Fisher, 1976), although in the Canary Islands it has also been reported as an epibiont of filamentous green algae, as well as on intertidal rocky substrate (Ocaña et al., 1991). Since this species can presumably colonize new biotopes and adapt to benthic life (Ocaña et al., 1991), there is a probability that it can establish itself locally and compete for space and resources with local populations. However, it would be premature to classify this species as potentially invasive, since its native origin is still unknown.

Although only five distributional records of B. pelagica are known to date, it can be assumed that its distribution range is linked to the distribution of the Sargassum algae, which in turn is dependent on sea currents. This floating marine brown macroalgae is commonly found in the surface waters of the northwestern Gulf of Mexico, the Sargasso Sea and the Caribbean Sea, but has also recently been reported in abundance along northeastern Brazil and western Africa, including the coasts of the Canary Islands and Cape Verde (Franks et al., 2016). Similarly, the distribution of A. sargassensis, another species of sea anemone that can be found in Sargassum (Fisher, 1976), overlaps greatly with the distribution of this macroalgae, including the Atlantic coast of the northern United States, the Gulf of Mexico and the Caribbean Sea, the northeast coast of Brazil and Cape Verde off the coast of Senegal (Rodríguez et al., 2023b). Therefore, it could be suggested that the distribution of B. pelagica is similar to that of A. sargassensis, that in both cases it is dependent on the distribution of Sargassum, and that the few records in its distribution could be due to the fact that this species has gone overlooked, probably due to its diminutive size. Either way, it is clear that B. pelagica is much more widespread than previously reported. This is the third species of the genus Bunodeopsis reported in the region, increasing the total number of known actiniarian species from the Mexican Atlantic to 23.