Introduction
Bunodeopsis pelagica (Quoy and Gaimard, Reference Quoy and Gaimard1833) is one of the few known sea anemone species that lives as an epibiont on drifting seaweeds of Sargassum spp. (Fisher, Reference Fisher1976). This species was originally described as Actinia pelagica in a short paragraph by Quoy and Gaimard (Reference Quoy and Gaimard1833), 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, Reference Fisher1976), 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., Reference Ocaña, Fraga and García1991; Ocaña and den Hartog, Reference Ocaña and den Hartog2002). Although it has been suggested that B. pelagica could be found throughout the Caribbean carried by floating Sargassum (Ocaña et al., Reference Ocaña, Moro, Ortea, Espinosa and Caballer2007), 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 (Reference Fisher1976) 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).
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 (Reference Fisher1976).
Order ACTINIARIA Hertwig, 1882
Suborder ENTHEMONAE Rodríguez & Daly in Rodríguez et al. (Reference Rodríguez, Barbeitos, Brugler, Crowley, Grajales, Gusmão, Häussermann, Reft and Daly2014)
Superfamily METRIDIOIDEA Rodríguez & Daly in Rodríguez et al. (Reference Rodríguez, Barbeitos, Brugler, Crowley, Grajales, Gusmão, Häussermann, Reft and Daly2014)
Family BOLOCEROIDIDAE Carlgren, 1924
Bunodeopsis pelagica (Quoy & Gaimard, Reference Quoy and Gaimard1833)
(Figures 2A and B)
Synonymy:
Bunodeopsis pelagica (Quoy and Gaimard, Reference Quoy and Gaimard1833): (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, Reference Quoy and Gaimard1833, 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, Reference Quoy and Gaimard1833): Fisher, Reference Fisher1976, 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., Reference Ocaña, Fraga and García1991). A nudibranch mollusc, which also lives on the sea weed, feeds on B. pelagica (Fisher, Reference Fisher1976). This species is associated with endosymbiotic dinoflagellates of family Symbiodiniaceae Fensome, Taylor, Norris, Sarjeant, Wharton & Williams, 1993 (Fisher, Reference Fisher1976).
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, Reference Quoy and Gaimard1833; Fisher, Reference Fisher1976; Ocaña et al., Reference Ocaña, Fraga and García1991; Ocaña and den Hartog, Reference Ocaña and den Hartog2002; this study).
Taxonomic remarks: six valid species are currently known within the genus Bunodeopsis (Rodríguez et al., Reference Rodríguez, Fautin and Daly2023a) (Table 1). Bunodeopsis pelagica has a violet ring around the mouth (Fisher, Reference Fisher1976; Ocaña et al., Reference Ocaña, Fraga and García1991), a feature shared with Bunodeopsis australis Haddon, Reference Haddon1898 (Haddon, Reference Haddon1898), and similar to the blue ring around the mouth reported for Bunodeopsis antilliensis Duerden, Reference Duerden1897 (Cairns et al., Reference Cairns, den Hartog, Arneson, Sterrer and Schoepfer-Sterrer1986).
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, Reference Fisher1976) (see Figure 2B, Table 1). The vesicles of B. australis are of uniform size (Haddon, Reference Haddon1898), 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, Reference Cutress1979), 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 (Reference Fisher1976) and Carlgren (Reference Carlgren1952) report basitrichs in the tentacles of B. pelagica and B. strumosa, respectively, while Cutress (Reference Cutress1979) 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., Reference González-Muñoz, Simões, Sánchez-Rodríguez, Rodríguez and Segura2012). Similarly, some authors identify cnidocysts as microbasic amastigophores, while others mention them as microbasic p-mastigophores (Table 2). Furthermore, the studies by Carlgren (Reference Carlgren1952), Fisher (Reference Fisher1976), Cutress (Reference Cutress1979) and Chintiroglou and den Hartog (Reference Chintiroglou and den Hartog1995) 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.
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., Reference Pendleton, Krowicki, Strosser and Hallett-Murdoch2014). 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., Reference van Tussenbroek, Hernández-Arana, Rodríguez-Martínez, Espinoza-Avalos, Canizales-Flores, González-Godoy, Barba-Santos, Vega-Zepeda and Collado-Vides2017). 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., Reference Rodríguez-Martínez, van Tussenbroek, Jordán-Dahlgren, García-Mendoza, Quijano-Scheggia, Olivos-Ortiz and Núñez-Vázquez2016; van Tussenbroek et al., Reference van Tussenbroek, Hernández-Arana, Rodríguez-Martínez, Espinoza-Avalos, Canizales-Flores, González-Godoy, Barba-Santos, Vega-Zepeda and Collado-Vides2017).
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, Reference Cunha and Jacobucci2010, Cunha et al., Reference Cunha, Maruyama and Jacobucci2018; Mendoza-Becerril et al., Reference Mendoza-Becerril, Serviere-Zaragoza, Mazariegos-Villarreal, Rivera-Perez, Calder, Vázquez-Delfín, Freile-Pelegrín, Agüero and Robledo2020) and at least three species of sea anemones: Anemonia sargassensis Hargitt, 1908, Bartholomea annulata (Le Sueur, 1817), and B. pelagica (Carlgren and Hedgpeth, Reference Carlgren and Hedgpeth1952; Fisher, Reference Fisher1976).
Although several taxonomic studies have been carried out on sea anemones in the Mexican Atlantic (e.g. González-Muñoz et al., Reference González-Muñoz, Simões, Sánchez-Rodríguez, Rodríguez and Segura2012, Reference González-Muñoz, Simões, Tello-Musi and Rodríguez2013; De la Cruz-Francisco et al., Reference De la Cruz-Francisco, González-González and Morales-Quijano2016; De la Cruz-Francisco and González-Muñoz, Reference De la Cruz-Francisco, González-Muñoz, Granados-Barba, Ortiz-Lozano, González-Gandara and Salas-Monreal2019; Herrera-Bojórquez et al., Reference Herrera-Bojórquez, González-Muñoz, León-Deniz, Arjona-Torres and Sima-Álvarez2020), 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, Reference Fisher1976), 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., Reference Ocaña, Fraga and García1991). Since this species can presumably colonize new biotopes and adapt to benthic life (Ocaña et al., Reference Ocaña, Fraga and García1991), 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., Reference Franks, Johnson and Ko2016). Similarly, the distribution of A. sargassensis, another species of sea anemone that can be found in Sargassum (Fisher, Reference Fisher1976), 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., Reference Rodríguez, Fautin and Daly2023b). 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.
Acknowledgements
The authors acknowledge the Secretaría de Marina (SEMAR) and Comisión Nacional de Áreas Naturales Protegidas (CONANP) for their help with access to the reef systems. The authors thank Catalina M. Corona Hinojosa for the photograph in Figure 2A.
Author's contribution
R.G.-M., J.S.-R., N.S. and J.L.T.-M. collected the specimens and devised the idea for the present study. R.G.-M., J.L.T.-M. and F.H.A. examined specimens and made taxonomic identification of the species. R.G.-M. and F.H.A. wrote the manuscript with input from all authors.
Financial support
This research was funded by grants to N.S. from Harte Research Institute (Biodiversity of the Southern Gulf of Mexico) and CONABIO (NE018; Actualización del conocimiento de la diversidad de especies de invertebrados marinos bentónicos de aguas someras [<50 m] del sur del Golfo de México).
Conflict of interest
The authors declare none.
