Our systematic surveys over a one-year period have demonstrated the presence of individuals of O. mirabilis at moderate to high abundances from Hollywood Beach to West Palm Beach, a distance along the coast of about 78 km. The clusters of high survey abundances immediately north and about 4 km south of the entrance to Port Everglades lend support to the hypothesized localized introduction of this exotic ophiuroid via high volume ship traffic (Glynn et al. 2020) as also proposed in several studies in Brazil (Hendler and Brugneaux, 2013; Bumbeer and Rocha, 2016; Mantelatto et al., 2016; Araújo et al., 2018; Lawley et al., 2018).
In just 20 years, individuals of O. mirabilis have colonized coastlines spanning more than 6,000 km of latitude (Tavares et al. 2021), from their first reported presence in southern Brazil (Hendler et al. 2012) northward along the South American coast to the Caribbean Sea (Hendler and Brugneaux 2013; Ferry et al. 2020) and southeastern Florida (Glynn et al. 2019). Their northern-most occurrence on the Florida east coast, observed on 28 September 2019, was at Deerfield Beach, 26.3184°N; 80.0998°W (Glynn et al. 2020). In the present study, individuals of O.mirabilis were found on a hydrozoan colony at Blue Heron Bridge, Riviera Beach, 26.7153°N; 80.0534°W on 20 October 2020, 44 km north of Deerfield Beach in a brackish environment. It is not known if this record represents migration over a one-year period or if the ophiuroids were already present there and un-reported. The near absence of shallow water octocorals in the vicinity of St. Lucie Inlet (Martin County), nearly 50 km north of Deerfield Beach (Jones et al. 2020) would not seem likely to inhibit a more northern range extension of individuals of O. mirabilis since this ophiuroid is known to associate with numerous other taxa in Florida (Glynn et al., 2020), Brazil (Bumbeer and Rocha, 2016; Mantelatto et al., 2016; Fortunato and Lôbo-Hajdu, 2021), and the eastern Pacific (Granja-Fernández et al., 2014). However, the present distributions of non-native western Atlantic and native eastern Pacific O. mirabilis are generally restricted to these amphiamerican tropical/subtropical biogeographic realms (Costello et al. 2017; Travares et al. 2020).
An ecological niche model analysis, employed by Derviche et al. (2021), based on current O. mirabilis distributions and abundances, predicted suitable western Atlantic habitats beyond present-day occurrences and widespread dispersion and range expansion in the future. They reported that the occurrence of O. mirabilis correlates chiefly with mean calcite concentration and mean sea surface temperature. If this prediction is realized the ophiuroid could colonize numerous suitable habitats in warm temperate southwestern and northwestern Atlantic environments. This would include range expansions to southeastern Brazil and to the Carolinian province along the east coast of the USA. Also included would be large areas of the Caribbean Sea and the northern Gulf of Mexico. Derviche and co-workers suggested that the calcite mineral would be required for ophiuroid skeletogenesis, especially during asexual fissiparity, and that physiological functions are impaired at mean sea temperatures less than 21.75 °C. These workers also noted increasing population densities of O. mirabilis from inner shelf to estuarine habitats at the Paranaguá estuarine complex in southern Brazil.
Marked variability occurred in epizoite densities in the 16 collections over the 19-month sampling period as reported in prior studies in southeast Florida (Glynn et al. 2020). For individuals of O. mirabilis and C. waltoni this is probably in part a reflection of the patchy occurrence and the sampling protocol for these species; the identical octocoral patches, colonies, and branches were not repeatedly sampled at the Dania Beach study site. The occurrence of individuals of Caprella penantis was sporadic, observed in only four collections. Aquarium observations revealed this amphipod to be highly mobile, moving quickly over a given octocoral branch, and often swimming and moving between branches. It is likely that this predatory amphipod naturally moves frequently among octocoral branches within and among colonies in search of prey.
Ophiuroids were not present on dead octocoral branches (Glynn et al. 2020). Their absence could offer a refuge for C. waltoni, however, the ctenophore was absent from dead branches as well. Dead branches are usually quickly colonized by algae and hydroids, a likely inhospitable habitat for mobile epizoites. Live octocoral host tissues bearing nematocysts, sclerites, and chemical defenses (Pawlik et al., 1987; Harvell and Fenical 1989; Yoffe et al., 2012) would provide an advantage in predator avoidance, thus offering a suitable microhabitat.
Since octocorals engage heavily in suspension feeding, capturing particulate organic matter (Lasker, 1981) and microzooplankton (Glynn et al. 2018a), the interference of polyp expansion by individuals of O. mirabilis was suggested to be a potentially significant threat against satisfying the trophic requirements of octocoral hosts (Araújo et al. 2018; Ferry et al. 2020), although a recent study suggests this may not be consequential (Glynn et al., 2021). From the current study -- which has demonstrated an inverse relationship in the abundance of ophiuroids and ctenophores in field collections, and decreasing ctenophore abundance in the presence of ophiuroids in a laboratory experiment -- it appears that the major effect of the exotic ophiuroid is on the displacement, by interference competition, of the cohabiting benthic ctenophore. This sort of negative impact on biodiversity is the predominant effect of marine invasive species in European seas (Katsanevakis et al. 2014). It is not yet known if O. mirabilis will negatively impact the abundances of octocoral hosts, but if this occurs then local biodiversity would be greatly diminished. Invasive azooxanthellate sun corals are displacing ecosystem engineers (e.g., reef-building corals and zoantharians) in Brazil, having a depressing effect on biodiversity, nearly two decades after their first sightings (Miranda et al., 2016; Luz and Kitahara, 2017). It is too early to determine the extent to which the ophiuroid will continue to affect C. waltoni, and perhaps begin to impact octocorals and other epizoites.
Several studies have described the kleptocommensal and kleptoparasitic trophic relationships of hydroids and other invertebrate epizoites associated with sponges, octocorals, bryozoans, and polychaete worms (e.g., Gotto, 1969; Puce et al., 2008). Bavestrello et al. (1996) observed caprellids seizing previously captured nauplii from hydroid polyps; a nudibranch grazing preferentially on hydroid polyps that previously ingested zooplankton, an example of the consumption of a prey item plus its ingested prey, was termed kleptopredation by Willis et al. (2017). The symbiotic status of the benthic ctenophore and its octocoral host is not clear since we have observed the ctenophore purloining food (unidentified organic detritus) captured by its host’s polyps, and octocoral polyps have been observed removing captured fish eggs from the tentacles of ctenophore epizoites (Glynn et al. 2018a). Further study is necessary to determine the significance of these trophic resources, the relative amounts garnered by the symbiotic partners, and how field conditions affect these interactions.
The alacrity with which individuals of Caprella penantis attacked, shredded and consumed relatively large fragments of benthic ctenophores suggests that this crustacean species is an occasional, if not frequent, predator of individuals of C. waltoni. No defensive responses by C.waltoni, such as rapid tentacle extension (Glynn et al., 2018b), were observed beyond slow fleeing movements, which were ineffective. From feeding observations conducted in northern Florida, Gulf of Mexico, Caine (1974) noted that individuals of C. penantis depended primarily on filter feeding and substrate scraping. Contrary to the observations of Caine (1974) and Paz-Rios et al. (2014) on the relative ineffectiveness of caprellids as predators, we observed that all individuals engaged in feeding moved quickly over octocorals, occasionally swimming, potentially in search of ctenophore prey. This is the first documented record of a ctenophore species consumed by a caprellid (Saunders, 1966; Sano et al., 2003; Guerra-García and Tierno de Figueroa, 2009). Most caprellids are detritivores, 86% in the global survey conducted by Guerra-García and Tierno de Figueroa (2009); however, several species are facultative and obligate predators, consuming sponges, polychaete worms, copepods and amphipods.
If the recent decline in abundance of C. waltoni, and local disappearance at some sites, is due primarily to O. mirabilis, then it is necessary to understand how this occurs. The ctenophores are exceedingly well camouflaged and typically quiescent when present on their octocoral hosts. Once a ctenophore has found a favorable perch for the extension of its ‘fishing’ tentacles, movement is infrequent. Our observations indicate that brittle star contact with individuals of C. waltoni is an irritation, often causing the ctenophores to move. We hypothesize that ctenophores on the move are more susceptible to dislodgment from their octocoral hosts. Dislodgment could occur during turbulent sea conditions, which are frequent off the southeast coast of Florida, or by fishes and other water column predators.
A notable report of a caprellid infestation and predation on gorgonian sea fans in North Sulawesi, Indonesia, revealed massive consumption of coenenchyme (octocoral tissues including epidermis, mesoglea and gastrodermis) and skeletal fragments resulting in total colony mortality in three species (Scinto et al., 2008). Octocoral colonies of Melithaea sp. were most severely affected, irreparably damaged within a week. The caprellid responsible for the sea fan mortality was Metaprotella sandalensis, a common species on Indo-Pacific coral reefs. The morphology of the feeding appendages (molar process and mandibular palp) are characteristic of caprellid predators and scrapers (Caine, 1977; Guerra-García and Tierno de Figueroa, 2009). Mean caprellid infestation densities were 8.5 ind cm-1 branch, equivalent to 85 individuals over a 10 cm-long branch (Scinto et al., 2008; C. Cerrano, pers. comm.). These densities are an order of magnitude higher than those observed in south Florida (Table 1). Such a severe predation event triggering the death of entire gorgonian colonies, would also result in the loss of the associated symbiont community.
Concluding remarks
The ophiuroid invasion of octocorals in southeast Florida is very recent, making it difficult to predict long-term effects. The apparent ongoing displacement of an endemic benthic ctenophore is the only negative effect thus far observed. No obvious signs of impairment to octocoral hosts are evident (Glynn et al., 2021). In light of the ophiuroids establishment in southeastern Brazil, over a period of about 20 years, its rapid and wide-ranging dispersal and possible repeated introductions, it is highly probable that it will continue to spread and become established throughout the western Atlantic warm water region where octocorals and other suitable substrata occur. Since the invasion of O. mirabilis in the western Atlantic region is so recent and still on-going, we urgently encourage continuing surveys to document its occurrence, abundance, and interactions with native species. Coastal and estuarine habitats with suitable environmental conditions in need of surveys and study are the Tropical Northwestern Atlantic province (wider Caribbean Sea) and the Warm Temperate Southwestern (southeastern Brazil) and Northwestern Atlantic (Northern Gulf of Mexico, Carolinian) provinces. Behavioral and experimental studies of alien brittle star interactions vis-a-vis native epizoites are especially encouraged and may shed light on control measures should these be needed. Cryptogenic C.penantis should also receive attention considering its predatory impacts on C. waltoni and other octocoral epizoites.