Occurrence of the hydromedusa Moerisia cf. inkermanica (Hydrozoa, Moerisiidae) in the ballast water of oil tankers in the Gulf of Mexico

Abstract

The introduction of non-native species is a constant concern around the world since it represents one of the main threats to biodiversity, impacting negatively on native populations, some of them with commercial importance. Hence, monitoring these introductions is fundamental to the management and conservation of the biodiversity of a region. Herein, we report the presence of Moerisia cf. inkermanica in the ballast water of oil tankers loaded at the Cayo Arcas oil terminal. The taxonomy of Moerisia members is uncertain due to the lack of comprehensive morphological descriptions and the few molecular data available. So, we provide a detailed morphological comparison among its congeners. The taxonomic identity of the specimens was determined based on the length of the perradial lobes of the manubrium, the number of tentacles, and the features of their nematocyst rings. Some Moerisids are considered invasive in different localities of the world. However, this genus had not been reported in coastal ecosystems of the Gulf of Mexico over the years until now. Sampled tankers came from different ports of the region, mainly from the northern Gulf of Mexico. Therefore, we encourage systematic monitoring of these ecosystems to recognize the establishment of this species as invasive in the region, know its population dynamics over time, and evaluate the possible ecological impacts that could exert on native populations.

Introduction

The Gulf of Mexico is a semi-closed basin of the Atlantic Ocean that provides diverse ecosystem services related to its biodiversity, biological productivity, and geological features (Fautin et al., 2010). Among the ecosystem services that generate greater economic benefits are oil extraction and tourism (Shepard et al., 2013). Hence, maritime transport has been constant in the Gulf of Mexico throughout history (Botello et al., 1997), impacting some ecosystems due to the introduction of non-native species (Graham et al., 2003; Brockinton et al., 2022). In the last few years, the presence of some non-native invertebrates in the Gulf of Mexico has been reported; some examples include Phyllorhiza punctata (Graham et al., 2003; Ocaña-Luna et al., 2010), Blackfordia virginica (Ocaña-Luna et al., 2021), Tubastraea coccinea (Fenner and Banks, 2004; Derouen et al., 2020), Penaeus monodon (Wakida-Kusunoki et al., 2013), and the bryozoans Hippoporina indica, Arbopercula bengalensis, Sinoflustra annae, and Celleporaria pilaefera (McCann et al., 2007). Unfortunately, few studies have evaluated their potential economic and ecological impact in the region (Graham et al., 2003), so the status of their populations and their establishment as invasive species is uncertain.

The Hydromedusae of Moerisia Boulenger, 1908 distributes in tropical and template regions of the world, including continental water bodies (GBIF, 2024). Little is known about their taxonomy due to the lack of reports with detailed morphological descriptions and the few molecular data associated with these reports (Restaino et al., 2018), causing the taxonomic boundaries of the group to be uncertain (Rees, 1958; Calder, 2010; Nawrocki et al., 2010). This genus includes seven valid species (Schuchert, 2024), of which M. inkermanica Paltschikowa-Ostroumowa, 1925 and M. lyonsi Boulenger, 1908 are more frequently reported in the literature (e.g., Purcell et al., 1999; Ma and Purcell, 2005; Nascimento et al., 2019). M. inkermanica was described for the first time in the Bay of Sevastopol, Black Sea (Paltschikowa-Ostroumowa, 1925). Since then, it has been recorded in several localities around the world, mainly in the Atlantic Ocean (see Schuchert, 2010; Nogueira, 2012; Restaino et al., 2018). The nearest record to the Gulf of Mexico was in Barnegat Bay, New Jersey (as Moerisia sp. Restaino et al., 2018). This species is considered invasive in some localities (e.g., Nogueira, 2012; Killi et al., 2020), so having a record of its presence in a new region is fundamental to knowing the possible impacts that it could generate on the native biodiversity.

Reports about invasive hydrozoans are frequent around the world (e.g., Gonionemus vertens, Blackfordia virginica, Cordylophora caspia; Bardi & Marques, 2009; Folino-Rorem et al., 2009; Marchessaux et al., 2017). These reports are of importance since hydrozoans are key consumers of zooplankton, and under certain environmental conditions, they can generate massive local aggregations with high abundance (blooms), negatively impacting native populations, some with commercial importance (Rees and Gershwin, 2000). Thus, identifying the invasion pathways, vectors, and source localities is key to understanding their ecological impact and conducting correct management (Reusch et al., 2010). B. virginica and C. caspia are the only non-native hydrozoans recorded in the Gulf of Mexico, yet their invasion monitoring in coastal zones of the Gulf has been scarce (Rioja, 1959; López-Ochoterena and Madrazo-Garibay, 1989; Álvarez-Silva et al., 2003; Pruski and Miglietta, 2019; Ocaña-Luna et al., 2021). Moreover, other unrecorded non-native species likely exist in this region because of the constant maritime transport, the influence of ocean currents, and the scarcity of studies about coastal hydrozoans. Here, we report the occurrence of M. cf. inkermanica in the ballast water of oil tankers loaded at the Cayo Arcas oil terminal, giving a comprehensive morphological description through its comparison with its congeners.

Materials and methods

Zooplanktonic samples were obtained from 30 tankers (three tanks per tanker) loaded at the Cayo Arcas oil terminal between 18 June and 6 July 2005 (the Cayo Arcas oil terminal is used as a port for the tankers loading oil for exportation; Figure 1) conducting vertical trawls from the bottom to the surface of each tank (90 tanks) using a conical net of 30 cm in diameter and 300 μm of clear mesh. Sampling was initially intended to collect as many zooplanktonic groups as possible for morphological analyses, so the samples were fixed in a 10% formalin solution buffered with sodium borate. Then, the samples were analysed in the laboratory, sorting the specimens of Moerisia from the rest of the material. Standard measurements were recorded (i.e., the width and height of the umbrella and number of tentacles) of the best-preserved specimens (n = 29). Four specimens were deposited in the Regional collection of ‘Cnidarios del Golfo de México y Mar Caribe Mexicano’, based at the Universidad Nacional Autónoma de México, Facultad de Ciencias, Unidad Multidisciplinaria de Docencia e Investigación-Sisal, Yucatán (Catalogue numbers for two vials with three and one specimens: YUC-CC-254-11-001660, YUC-CC-254-11-001661). For each tanker, the port of origin was recorded. The depth of the tanks ranged between 1.7 and 20 m (8 m on average). Temperature (°C) and salinity (ups) were recorded in each tank with a multiparametric YSI-85 (±0.01) (Table 1). Additionally, we surveyed the available genetic data in GenBank (Clark et al., 2016) using the term ‘Moerisia’, assessing the locality where the samples were collected and the barcode marker used in order to provide a thorough summary of the available information (morphological and molecular) among the species of the genus.

Figure 1. Locations from where the tankers set sailed towards the Cayo Arcas oil terminal (star). Green dots indicate the locations from where the tankers transporting specimens of Moerisia cf. inkermanica Paltschikowa-Ostroumowa, 1925 set sailed.

Table 1. Physicochemical features of the ballast water and number of medusae recorded on each tanker. The ID corresponds to each tanker.

Results

SYSTEMATICS (according to Schuchert, 2024)
Class HYDROZOA Owen, 1843
Subclass HYDROIDOLINA Collins, 2000
Order ANTHOATHECATA Cornelius, 1992
Suborder CAPITATA Kühn, 1913 (sensu stricto)
Family MOERISIIDAE Poche, 1914
Moerisia cf. inkermanica Paltschikowa-Ostroumowa, 1925 (Figure 2)

Diagnosis

Moerisid with less than 32 but more than four moniliform tentacles, with rings of nematocysts arranged regularly on tentacles, with a terminal knob; manubrium short, cylindrical, lacking lips, with a quadrangular base and four long perradial lobes, with their distal parts swollen and pendant; gonads surrounding the manubrium and continuing over the perradial lobes.

Figure 2. Moerisia cf. inkermanica Paltschikowa-Ostroumowa, 1925. (A) Complete view of mature specimens; (B) Lateral view of the manubrium; (C) Aboral view of the manubrium and perradial lobes; (D-E) Umbrella margin indicating tentacles at different development stages; (F) Oval clasping bulbs; (G) Moniliform tentacle indicating the terminal nematocysts knob; (H) Desmonemes; (I) Stenoteles.

Description

Medusa with an umbrella slightly wider than high, 3.25 mm width (2 ± 4.5 mm, SD = 0.70), 3.06 mm height (2 ± 4.5 mm, SD = 0.57); mesoglea thick; manubrium slender, not extending beyond the half of the subumbrellar cavity, with a narrow mouth beset with nematocysts, and with appearance of four folded lips; the base of the manubrium is small and quadrangular, with four long perradial lobes, extending nearly to the umbrella margin in the most mature specimens, with their distal parts swollen and pendant; the proximal part of the lobes is divided longitudinally by a median groove that narrows in its distal part; gonads located on the manubrium, continuing over the perradial lobes; four thin radial canals; margin of umbrella simple, lacking statocysts, and with a marginal ring narrow; in some specimens, the presence of short tentacles-like or vesicles-like structures, arising directly from the umbrella margin were observed; velum thin, covering 1/3 of the subumbrellar cavity; marginal bulbs oval, slightly enlarged, tapering, and clasping the umbrella margin; 15–24 (usually 16) hollow tentacles, moniliform, with numerous nematocyst rings regularly arranged, bearing a terminal knob. Cnidome composed of stenoteles of two size classes and desmonemes; stenoteles of class 1 in the tentacles: 7–8 × 8–10 μm, stenoteles of class 2 in the mouth: 6–9 × 7–11 μm; desmonemes of tentacles: 4–5 × 5–7 μm; scarce desmonemes in the mouth: 4–5 μm.

Habitat

M. inkermanica usually inhabits brackish waters of shallow depths (Schuchert, 2010). Nevertheless, its wide distribution suggests good adaptability to physicochemical variations, reporting it in estuaries (Nascimento et al., 2019), lakes (Restaino et al., 2018), and marine environments (Killi et al., 2020) around the world. The polyps can tolerate 5–40 psu (%) salinity and temperatures from 0–30°C. They grow on reeds, pilings, and among polychaete tubes (Schuchert, 2012).

Remarks

The presence of ocelli is a diagnostic character at the family level (Bouillon et al., 2004; Schuchert, 2010). However, ocelli were not observed in the analysed specimens. We attribute the absence of ocelli to the deterioration of the specimens due to the age of the samples and the preservation method. In addition, the shape of the bulbs varied among the specimens, which can also be attributed to the preservation method. The length of the perradial lobes varied among the analysed specimens, likely due to the different development stages. Kramp (1938) mentioned the presence of statocysts in the umbrella margin of M. inkermanica, whereas Valkanov (1953) states that Kramp's interpretation corresponds to nematocyst capsules (Schuchert, 2010). We observed similar structures to the previously described, concluding that they are marginal tentacles with different developmental stages (Figure 2d, e).

Discussion

The morphological characteristics of the specimens analysed in this work match those reported for M. inkermanica (Kramp, 1959, 1961; Bouillon et al., 2004), except the cnidome reported by Schuchert (2010), which indicated four types of nematocysts. Due to the scarcity of morphological and molecular information for the members of Moerisia (Tables 2 and 3), we decided to tentatively recognize our specimens as M. cf. inkermanica. The variation in the cnidome could be considered a diagnostic character for discriminating among the species of Moerisia; yet, this information is poorly described for some species, so taxonomic studies describing this aspect are fundamental to improving the knowledge about the taxonomy of this group. The number of marginal tentacles and the length of the perradial lobes of the manubrium are the main characteristics differentiating among the medusae of Moerisia (Bouillon et al., 2004; Schuchert, 2010; Jankowski and Anokhin, 2019). In this sense, M. lyonsi is distinguished from M. inkermanica by the number of tentacles and their prominent nematocyst clusters (Kramp, 1961; Bouillon et al., 2004; Jankowski and Anokhin, 2019). Likewise, the polyp of M. lyonsi lacks podocysts (pedal disc), whereas that of M. inkermanica presents these structures (Bouillon et al., 2004; Jankowski and Anokhin, 2019). M. lyonsi is reported from Egypt (type locality) and in rivers from Virginia, U.S.A. (Calder and Burrell, 1967).

Table 2. Comparison of the morphological diagnostic features of the valid species within Moerisia Boulenger, 1908

Table 3. GenBank accession numbers for the specimens of Moerisia Boulenger, 1908 with molecular data and their locality

M. carine Bouillon, 1978 can be differentiated from M. inkermanica by its short perradial lobes, its marginal tentacles of different sizes (up to 16), and its mouth with well-defined lips and cnidome (Bouillon, 1978). Despite the perradial lobes of the specimens analysed in this study varied in length, no specimens with short lobes as described in M. carine were observed (Bouillon et al., 2004), except a juvenile with four tentacles. The polyp of M. carine is unknown, so a comprehensive morphological comparison with its congeners is not possible. This species is distributed in Papua New Guinea (type locality) and the Eastern Mediterranean (Schuchert, 2010).

The medusa of M. horii (Uchida and Uchida, 1929) resembles that of M. inkermanica (Uchida and Nagao, 1959), making it hard to recognize reliable morphological characteristics to discriminate between these species. Their main morphological differences are in the polyp stage. The polyp of M. horii is smaller, usually with more than 12 tentacles and up to 10 podocysts (Uchida and Nagao, 1959; Calder, 2010). In addition, three types of nematocysts are reported in M. horii, i.e., stenoteles, basitrichous isorhizas, and desmonemes, whereas the specimens of this study only had stenoteles and desmonemes, and those analysed by Schuchert (2010) presented two additional types, i.e., mastigophores and haplonemes?.

Three species of Moerisia are hard to differentiate among their congeners due to their incipient morphological descriptions, the scarcity of records, and the lack of knowledge about their polyp or medusa stages, i.e., M. pallasi (Derzhavin, 1912), M. gemmata (Ritchie, 1915), and M. gangetica Kramp, 1958. Morphological differences between M. pallasi and M. inkermanica are not evident in the medusa stage (Kramp, 1961; Schuchert, 2010). Unfortunately, since its first description in the Caspian Sea (Derzhavin, 1912), the morphological descriptions of M. pallasi have been scarce (e.g., Kramp, 1961), making it difficult to recognize its taxonomic boundaries. The polyp of M. pallasi is smaller than that of M. inkermanica and lacks podocysts, resembling that of M. lyonsi. However, the polyp of M. pallasi presents a greater number of tentacles (Derzhavin, 1912; Bouillon et al., 2004). M. gemmata was described based on the polyp stage, which is smaller than that of M. inkermanica and has up to two podocysts and two types of nematocysts, although both possess the same number of tentacles (Ritchie, 1915). The medusa of M. gemmata is unknown, so comprehensive morphological discrimination is complicated. M. gangetica was described and differentiated from M. lyonsi based on geographical grounds (Kramp, 1955). This species, however, is reported in nearby locations where M. inkermanica occurs, presenting similar characteristics in the medusa stage (Kramp, 1955). Moreover, the polyp stage of M. gangetica is unknown, making reliable morphological differentiation impossible. These three species have been suggested as conspecific of some of their congeners (Rees and Thursfield, 1965; Schuchert, 2010); however, this must be addressed with integrative approaches, considering morphological and molecular data of the species from their different type localities. Molecular data regarding Moerisids is scarce, and the available information is related to only two nominal species (M. inkermanica and M. lyonsi) coming from the USA, Brazil, and China. M. inkermanica is the best molecularly known species, although there exist specimens with no specific assignation, which could suggest other undescribed species (Table 3).

Since its first description from the bay of Sevastopol in the Black Sea, M. inkermanica has been reported in the Netherlands (Saraber, 1962), the Mediterranean Sea (Schuchert, 2010; Killi et al., 2020), India (Kramp, 1955), France (Bouillon et al., 1969), South Africa (Millard, 1975) and in different localities from Brazil (e.g., Nogueira and Oliveira, 2006; Nascimento et al., 2019; Teixeira-Amaral et al., 2021). Some works hypothesized that its introduction was through maritime transport (e.g., Saraber, 1962; Nascimento et al., 2019). Here, we proved this hypothesis for the Gulf of Mexico since the analysed specimens came from the ballast water of oil tankers. Hence, we encourage attention to the application of protocols that regulate the management of this type of water since other non-native species could be introduced. The presence of juvenile specimens in our samples suggests a budding process, which might explain the prevalence of the species after water exchange since the polyps can fixed on the walls of the tanks. Only the tankers coming from the ports of Baytown, Houston, Sunoil Nederland, Port Arthur (TX), Lake St. Charles (LA), and Pascagoula (MS) transported specimens of M. cf. inkermanica on their ballast water (Figure 1). Nevertheless, the presence of this species in other ports is not ruled out since we only sampled three tanks per tanker.

Studies monitoring hydrozoan diversity in the Gulf of Mexico are fragmentary. In the southern Gulf, diverse studies have been conducted since the collection of the specimens of this work (2005) reporting different hydrozoan species in coastal ecosystems but not reporting to M. inkermanica (e.g., Cortés-Lacomba et al., 2013; Gutiérrez-Aguirre et al., 2015; Ahuatzin-Hernández et al., 2020; López-Torres et al., 2023). In the northern Gulf, fewer studies have been carried out in this field, focusing on phylogenetic aspects (e.g., Pruski and Miglietta, 2019; Miglietta and Pruski, 2023). The monitoring hydrozoan diversity in nearby areas to the ports where tankers transporting M. cf. inkermanica set sail is scarce (e.g., Moore, 1962; Burke, 1975, 1976; Harrel, 2002; Pruski and Miglietta, 2019). M. inkermanica is considered an invasive species in some regions of the world (Killi et al., 2020), so its establishment in the Gulf of Mexico must be proved by monitoring the different coastal ecosystems of the region, analysing its abundance changes through the seasons of the year, and its impact on the native populations of the Gulf. Only then could it be recognized as an invasive species in this region. We encourage conducting more efforts in this way, aiming to have a better knowledge of the diversity of this group in the Gulf of Mexico, which is crucial to understanding the potential impacts on the native fauna and being able to apply correct management strategies to mitigate these impacts.