Medusae and ctenophores from the Bahía Blanca Estuary and neighboring inner shelf (Southwest Atlantic Ocean, Argentina)

Abstract

An updated checklist of medusae and ctenophores is presented for the first time for the area comprised by the Bahía Blanca Estuary, the adjacent shelf El Rincón and Monte Hermoso beach, on the southwest coast of Buenos Aires province (Argentina). The area is highly productive and provides several ecosystem services including fishing and tourism. Updated information on the biodiversity of medusae and ctenophores species is essential for the study area, given that these species can affect ecosystem services. The list includes 23 hydromedusae, 3 scyphomedusae, and 3 ctenophores. Five hydromedusae (Halitiara formosa, Amphinema dinema, Aequorea forskalea, Clytia lomae and Halopsis ocellata) were firstly observed in this area. Three species of medusae, 2 hydromedusae (Olindias sambaquiensis and Liriope tetraphylla) and 1 scyphomedusae (Chrysaora lactea) pose a potential health risk, due to their toxicity to humans. Considering the size of the study area, the Bahía Blanca region has a comparatively high species richness of hydromedusae, higher than larger zones previously studied along the temperate SW Atlantic Ocean. The present report provides the baseline knowledge of gelatinous species for the Bahía Blanca region.

Introduction

Our knowledge of gelatinous fauna (medusae and ctenophores particularly) in the Argentine Sea has been much enhanced since major contributions by Ramírez and Zamponi (1981), Bouillon (1999), Mianzan (1999), Mianzan and Cornelius (1999), Genzano et al. (2008a) and Rodriguez (2012). However, the Bahía Blanca Estuary and its neighboring inner shelf is a still largely understudied area, in spite of the widely recognized ecosystem services that these coastal waters provide, such as wildlife support (Delhey and Petracci 2004; Hoffmeyer et al. 2009; Guinder et al. 2013) and fisheries production (Carozza and Fernández Aráoz 2009), as well as nutrient cycling and amelioration of heavy metal pollution (Negrin et al. 2016). These coastal waters are intensely used for fishing, recreational purposes, and provide space for industrial, port and commercial activities (Acha et al. 2004; Pizarro and Piccolo 2008). Several species of medusae and ctenophores have been reported in the region (Ramírez and Zamponi 1980; Hoffmeyer and Mianzan 2004), including species which may exert considerable predation pressure on fishing resources, mainly through consumption of larvae and juveniles, as well as competition for food (Mianzan and Sabatini 1985; Mianzan 1986a; Hoffmeyer 1990). Medusae species of public health concern such as Olindias sambaquiensis and Liriope tetraphylla have also been reported in high concentrations (Mianzan and Ramírez 1996; Mianzan et al. 2000, 2001). Species composition and ecological studies on medusae and ctenophores in the Bahía Blanca region were mainly conducted in the 1980’s (Mianzan and Sabatini 1985; Zamponi and Mianzan 1985; Mianzan 1986a, 1986b, 1989a, 1989b, 1989c; Mianzan and Zamponi 1988; Hoffmeyer 1990), but discontinued afterwards.

Given the potential impacts of gelatinous species on valuable ecosystem services, updated information on their biodiversity in the study area is essential. This work aims at compiling information on the species composition of medusae and ctenophores in the Bahía Blanca Estuary and its neighboring inner shelf. To do so, we considered earlier faunal lists and own unpublished data from plankton surveys.

Materials and methods

Study area

The study area is located in a temperate, semiarid zone in the southwestern Atlantic, Argentina (38°30′ - 41°S, ~60°W) (Fig. 1). According to the biogeographic division of the Argentine Sea based on its marine fauna (Balech and Ehrlich 2008), the study area represents the transition between the Rionegrine and Uruguayan Districts of the Argentine Province. In this work, we considered information on the biodiversity of medusa and ctenophore species from the Bahía Blanca Estuary (BBE), the associated sandy beaches of Monte Hermoso (MH) located north of the estuary, and the adjacent shelf El Rincón (ER) (Fig. 1). The BBE is a shallow, funnel shaped system, oriented NW/SE. The estuarine area comprises a dense arrangement of meandering channels and islands, surrounded by extensive intertidal mudflats and marshes (Pratolongo et al. 2013). The inner zone of the estuary is characterized by a shallow (~7 m depth) and vertically homogeneous water column, due to the strong tidal mixing and wind forcing (Popovich and Marcovecchio 2008). Turbidity and nutrient contents are typically high, with a strong seasonal pattern (Popovich and Marcovecchio 2008). ER, in the adjacent shelf, extends to the 50 m isobath (Acha et al. 2004). Within the ER area, low-salinity waters and sediments from the continent (Río Negro, Río Colorado and BBE), highly saline waters from the south (San Matías Gulf) and shelf waters of typically intermediate salinity combine to create oceanic fronts and circulation cells that favor retention mechanisms, creating an appropriate environment for successful larval fish development (Hoffmeyer et al. 2009; Acha et al. 2012; Delgado et al. 2015). Sandy beaches of MH and Pehuen Có are one of the most visited touristic destinations of Argentina (Vaquero et al. 2007). These beaches are transitional environments between estuarine shorelines and open beaches of Buenos Aires Province (Carcedo et al. 2015; Menéndez et al. 2016), and commonly receive significant amounts of estuarine sediments (Delgado et al. 2016).

Fig. 1

Study area located in the southwestern Atlantic, Argentina. The area comprised the Bahía Blanca Estuary, the adjacent shelf El Rincón and the surf beach of Monte Hermoso to the north. Numbers represent bathymetry expressed in meters. Samplings sites included in the checklist are shown (red circles = own sampling surveys, blue circles = literature sampling points)

Own data collection and literature review

We present own data from 89 plankton samples, collected in 33 sampling campaigns. Plankton sampling within the study area was performed in December 2012, and recurring monthly campaigns were carried out from April 2013 to May 2014, and from December 2014 to February 2015 (Fig. 1). To collect the samples, Hensen-like zooplankton nets were used (mouth diameters 30 and 40 cm, and mesh sizes 67, 200 and 500 μm) and also a modified RMT (Rectangular Midwater Trawl; mouth opening 2.25 m² and mesh size 1000), designed to capture a wider size range of gelatinous organisms. Hensen nets were used in oblique tows (bottom to surface) from a motorboat or ship moving at ~2 knots, during 7 min. The RMT net was deployed against the ebb tide current, during 20 min. Records of stranded individuals were also considered.

Gelatinous species were fixed using a solution of 4% formaldehyde in seawater and later identified following Mayer (1910), Kramp (1961), Bouillon (1999), Mianzan (1999), Mianzan and Cornelius (1999) and Bouillon et al. (2006). When necessary, the hydrozoan collection stored at the J. J. Nágera Biological Station (Universidad Nacional de Mar del Plata, Argentina) was consulted. Species which do not tolerate fixation (as the ctenophore Mnemiopsis leidyi) were immediately identified after capture. Photographic records of the collected species were obtained with a digital camera attached to a stereomicroscope, before their deposit in the Instituto Argentino de Oceanografia (IADO-CONICET). The bibliographical review was based on an exhaustive analysis of the regional literature on zooplankton published since the first scientific contributions in the 1970’s until 2015, including technical reports, PhD and Ms Thesis (Table 1).

Table 1 Review of medusae and ctenophores from the Bahía Blanca region (Argentina) based on own data and literature data. In each case, data related to study area and type of collection from own samples are highlighted in bold while those from literature are not highlighted; when both sources overlap, data are italic

Results

Species composition, richness and current observations

In all, 29 species were either found in our samples or reported by others in the study area (26 of Medusozoa and 3 of Ctenophora; Table 1). Among these, 16 species (55.2% of all gelatinous species) were recorded in our samples and also in the literature, eight species (27.6%) were only found cited in the literature, but they did not appear in our samples, and the remaining five species (17.2%) were found exclusively in our samples (Table 1).

Within Medusozoa, 23 species belong to the class Hydrozoa (88.5% of Medusozoa), distributed among the orders Anthomedusae (26%), with six families and six genera, Leptomedusae (52.2%), with five families and 12 genera, Limnomedusae (13%), with one family and three genera, and Trachymedusae (8.7%), with two families and two genera. Three of the species reported in Table 1, Proboscidactyla mutabilis, Mitrocomella frigida and Olindias sambaquiensis are considered endemic to the southwestern Atlantic. Species identified to genus level only included Obelia spp. (Hydrozoa, Leptothecata), for which medusa specimens cannot be reliably determined down to species level (Bouillon et al. 2006). However, when hydroids were found at the time of medusae, the nominal species O. longissima, O. dichotoma and O. bidentata were cited for the study area. Five hydrozoan species (2 Anthomedusae and 3 Leptomedusae), collected in our samples, were reported for the first time in the study area: Halitiara formosa (Fewkes 1882), Amphinema dinema (Péron and Lesueur, 1810), Aequorea forskalea (Péron and Lesueur 1810), Clytia lomae (Torrey 1909) and Halopsis ocellata (Agassiz, 1865) (Fig. 2). Their taxonomic descriptions are provided below. The record of H. ocellata in MH is, as far as we know, the northern record for the Southwestern Atlantic. With respect to A. forskalea, large numbers of adult and juvenile specimens were commonly observed in MH, either stranded on the beach or in coastal waters, during January 2014, and the massive occurrence repeated in February 2016.

Fig. 2

Photographs of the five hydromedusae species firstly observed in the study area. A) Adults of H. formosa, B1-2) Adults of A. dinema, C1) juvenile and C2-3) adults of A. forskalea, D1-2) adults of C. lomae, E1-2) adults of H. ocellata. C3 and E1-2 reproduced with the permission of Kåre Telnes (www.seawater.no)

Scyphozoa was represented by three species of the order Semaeostomeae, families Pelagiidae, Ulmaridae and Cyaneidae. Chrysaora lactea, Aurelia aurita and Drymonema gorgo were the only scyphozoans recorded in the area (Table 1). We did not find A. aurita ephyrae in our samples, although the use of this coastal area as a reproduction site had been suggested (Mianzan 1986a). Regarding C. lactea, ephyrae of this species were frequently found in our samples, mainly in BBE and ER.

The Phylum Ctenophora was represented by three species of the orders Lobata, Cydippida and Beroida (cf. Table 1). Mnemiopsis leidyi was found throughout the year, with higher concentrations during autumn and spring, mainly in channels within the BBE connected with island zones. Beroe ovata was also found in the estuary almost all year round, and aggregations of Pleurobrachia pileus were observed in the inner estuary during early spring.

Finally, three stinging species of public health concern were found in the area: the hydromedusae Olindias sambaquiensis and Liriope tetraphylla, and the scyphomedusa Chrysaora lactea. Regarding stinging species, a consistent summer trend was observed since 2013, characterized by decreasing numbers of O. sambaquiensis, and large amounts of L. tetraphylla (from 600 to more than 1000 ind.m⁻³).

Taxonomic descriptions of the species observed for the first time in the study area

Halitiara formosa Fewkes 1882

Umbrella about 3 mm high, pear-shaped, with solid apical projection about half as long as bell cavity, 4 straight radial canals; 4 long, hollow perradial marginal tentacles and 24–35 short, solid cirrus-like tentacles; mouth simple, cruciform; with or without mesenteries; “gonads” interradial, smooth, sometimes extending over mesenteries; without ocelli; cnidome, when known, with merotrichous isorhizae (Bouillon 1999; Bouillon et al. 2006) (Fig. 2 A).

Amphinema dinema Péron and Lesueur 1810

Umbrella up to 4 mm wide and 6 mm high with considerable conical, solid, apical projection, jelly of uniform thickness around top. Four undivided radial canals. Manubrium with broad base, cross-like in section, flask-shaped, almost as long as bell cavity. Mouth with four prominent, recurved lips. With eight simple adradial gonads, smooth, on manubrium wall only. Two perradial, hollow, marginal tentacles with large elongated conical basal bulbs; bulbs without ocelli. With 14–24 small marginal warts (Bouillon 1999) (Fig. 2 B1-2).

Aequorea forskalea Péron and Lesueur 1810

Flat umbrella, 14–32 mm in diameter. Short manubrium, mouth large, about half the diameter of umbrella. Numerous radial canals (usually 60–80, sometimes fewer, and up to 160). Tentacles with elongate conical bulbs, generally less numerous than radial canals but varying from half to the same number of them; 5–10 statocysts between successive radial canals. Gonads along almost the entire length of the radial canals (Nagata et al. 2014) (Fig. 2 C1-3).

Clytia lomae Torrey 1909

Umbrella 9–12 mm in diameter, about 4 times broader than high, thin. Gonads narrow, elongated along less than 1/2 of the distal part of radial canals; about 32 tentacles and some young bulbs. Manubrium short, cruciform; mouth with 4 slightly frilled lips; bulbs elongated; 1 (rarely 2) statocysts between successive tentacles (Bouillon 1999). Smaller medusae (umbrella 3–5 mm wide) have been observed in Argentine waters (Rodriguez 2012; this study) (Fig. 2 D1-2).

Halopsis ocellata Agassiz 1865

Umbrella 50–65 mm in diameter, about 4 times as wide as high, watch-glass-shaped; mesoglea thick toward centre; manubrium broad, flat, 1/5 of bell diameter, circular to star-shaped in outline; mouth with 4 fairly short lips; 12–16 radial canals in 4 groups branching usually within outline of manubrium; gonads linear, about 2/3 of radial canals; up to 450 marginal tentacles; 1 marginal cirrus between successive tentacles; about 80 statocysts (Bouillon 1999). Smaller medusae (umbrella up to 28 mm in diameter) have been observed in Argentine waters (Rodriguez 2012; this study) (Fig. 2 E1-2).

Discussion

Our study provides the first compiled list of medusae and ctenophores species of the Bahía Blanca region, adding five hydromedusae species that had not been previously reported for the area. We found a high richness of hydromedusae species compared to values reported along the temperate Southwestern Atlantic platform (Genzano et al. 2008a; Rodriguez 2012). Based on an exhaustive sampling carried out across the neritic region from 33° to 55°S, over 20 years, Genzano et al. (2008a) recognized 71 hydromedusae species. Our study area covers less than 3% of the area covered by Genzano et al. (2008a), but we found 32.4% of the total number of hydromedusae species detected by these authors, a disproportionally large richness for the small area considered.

Taking into account the transitional location of our study area and the hydromedusae faunal list by Rodriguez (2012), we found species that equally represent both the Rionegrin and Uruguayan biogeographic districts. According to Balech and Ehrlich (2008), the Argentine Province is essentially neritic, characterized by a marked biological heterogeneity due to the mix of subtropical and subantarctic waters. This combination of subtropical and subantartic elements also determines a low level of endemism for organisms in this region. The fundamentally neritic character of the Argentine Province is further reflected in the dominance of meroplanktonic species in the Bahía Blanca region (see Bouillon et al. 2006). Among hydromedusae, the meroplanktonic Leptomedusae showed the highest genus diversity followed by Anthomedusae, and only three species of hydromedusae considered endemic to the southwestern Atlantic were observed (Mianzan 1989c; Genzano et al. 2008a).

The species observed for the first time in the study area also belong to the orders Leptomedusae and Anthomedusae. Halitiara formosa, A. dinema and C. lomae were previously reported in the Argentine Sea south and north of our study area, while H. ocellata and A. forskalea were reported in austral waters (from 51° to 54°50′S and from 43° to 53°S, respectively). This later species was reported in Patagonian waters and there is only one record northward from our study area within the Argentine Sea (37°40′S-56°02′W) (Genzano et al. 2008a). The underlying causes of the massive occurrences of A. forskalea observed in MH during January 2014 and February 2016 are still unresolved. We hypothesize that changes in currents and wind patterns might have produced a recurrent advection of large numbers of individuals, but further studies are required to understand the origin of these mass occurrences. However it has to be also considered that jellyfish research in the study area has been neglected over the past 20 years, and the increasing sampling effort on gelatinous zooplankton throughout the last 5 years increased the proportion of findings related to gelatinous species.

Chrysaora lactea, A. aurita and D. gorgo were the only scyphozoans found in the study area (Mianzan 1989a, b; Schiariti et al. 2016; this study). Although we did not find A. aurita ephyrae in our samples, recently released ephyrae of this species were reported by Mianzan (1989a) who suggested the use of this coastal area as a reproduction site. Regarding C. lactea even though medusae are rather common and widespread, ephyrae have been rarely observed in plankton samples elsewhere (Mianzan 1989a, 1989b; Tronolone et al. 2002). In our samples, however, ephyrae of C. lactea were frequently found, which supports the suggestion by Mianzan (1989a) about the reproduction area for these scyphozoans. Polyps of C. lactea have never been found in nature (Morandini et al. 2004). Potential substrata for polyp settlement include docks, harbors, support structures of industries, dredged material storage piles, buoys, fouling fauna, native vegetation, rocky, muddy and sandy bottoms (Miyake et al. 2002; Morandini et al. 2004; Lucas et al. 2012), all of them available in the study area. Future research should include benthic surveys to explore the presence of benthic stages, and their association with natural and human-made substrates. Finally, the occurrence of D. gorgo is a rare event that reconfirms its geographical distributional range for these latitudes (Mianzan 1989a, 1989b). Information on its ecology and distribution is very scarce due to its sporadic occurrence and the few specimens available for study (Williams et al. 2001; Bayha and Dawson 2010).

Coastal ctenophores are a major macroplanktonic group in the Southwestern Atlantic (Mianzan 1999), that may dominate zooplankton abundance and biomass (Mianzan et al. 1996; Mianzan and Guerrero 2000). In our study area, aggregations of ctenophores were observed at different times and sites (Hoffmeyer 1983; Mianzan and Sabatini 1985; Mianzan 1986a; Hoffmeyer 1990, this study). The occurrences of M. leidyi, B. ovata, and P. pileus in our samples are in agreement with findings by Mianzan and Sabatini (1985) and Mianzan (1986a).

Regarding the three species of public health concern, O. sambaquiensis has been long considered the most problematic species in terms of its health consequences, as well as its detrimental effects on touristic development (Mianzan et al. 2001). It causes severe skin damage and pain (Kokelj et al. 1993). Adults range in size from 6 to 10 cm (Nagata et al. 2014) although specimens up to 21 cm were observed in our study area (Mianzan 1986a). This species has a clear seasonal pattern of high-density aggregations during the warmest months (Macchi et al. 1995; Mianzan and Ramírez 1996), and were reported in the area from October to April (Mianzan 1986a). In spite of its presence year after year, the asexual polyp phase of O. sambaquinsis remains unidentified, and little is known about its population dynamic and reproduction (Macchi et al. 1995; Chiaverano et al. 2004). Regarding our samples, immature stages were expected to be found in late spring, as well as adults in summer. Nevertheless, juveniles did not appear and observations of adults reduced to sporadic occurrence in the area. This is in accordance with the unusual trend observed since 2013, characterized by a disappearance of the high-density aggregations usually observed (Brendel AS, Dutto MS, Menéndez MC, Huamantinco Cisneros MA, Piccolo MC: Wind pattern variation in a SW Atlantic beach: An explanation for changes in the coastal occurrence of the medusa Olindias sambaquiensis, submitted). The large amounts of L. tetraphylla observed in summer, since 2014, have also raised concern. These aggregations which can cause severe pruritus and strong itching sensation in sensitive areas of human skin conform a locally-known phenomenon called “tapioca”, which was well documented on northern beaches in Argentina and Uruguay (Mianzan et al. 2000), but never reported in this geographic area or further south. Finally, Chrysaora lactea was the last stinging species found in the study area. It is one of the most common blooming scyphozoan along the entire South Western Atlantic coast (Mianzan and Cornelius 1999; Migotto et al. 2002; Schiariti et al. 2016). This species can cause mild to moderate local pain and burning sensation. Although less common, erythema and edema forming lesions were also reported (Marques et al. 2014).

The background list provided lays the foundation for the development of further investigations on gelatinous zooplankton in this highly relevant economic and biological coastal area. Benthic surveys are required to confirm the occurrence of polyps and to provide potential valuable information on the biology of the gelatinous species (e.g. life cycle) inhabiting this geographic region.