Description of a new hydromedusa from the southwestern Atlantic Ocean, Bougainvillia pagesi sp. nov. (Cnidaria, Hydrozoa, Anthoathecata)

Introduction

Recently, in the southwestern Atlantic Ocean, hundreds of specimens of an unknown hydromedusa were collected in coastal waters and harbors. This species belongs to genus Bougainvillia, one of the most speciose among the Anthoathecata (see Bouillon & Boero 2000). This genus was established by Lesson, and its medusae are easy to recognize (Vannucci & Rees 1961; Schuchert 2007). Bougainvillia medusae possess four radially placed clusters of solid marginal tentacles, the tentacles of each cluster all alike, with four oral tentacles dichotomously branching, gonads on manubrium, with or without ocelli (Kramp 1961; Bouillon 1999; Bouillon & Boero 2000; Bouillon et al. 2004, 2006). The type species is Bougainvillia macloviana, first described as Cyanaea bougainvilli Lesson, 1830 (Vannucci & Rees 1961).

Vannucci & Rees (1961) revised the genus, recognizing 29 valid species, 20 of them with a known medusa stage. A more recent update by Bouillon & Boero (2000) recognizes 22 valid species. Subsequently, Xu & Huang (2004, 2006) and Xu et al. (2007a,2007b) described four new species, and Denitto et al. (2007) promoted a subspecies to species rank. In the World Hydrozoa Database (http://www.marinespecies.org/hydrozoa/) 51 names are listed, 31 considered valid, four of them – namely Bougainvillia balei Stechow, 1924, Bougainvillia crassa Fraser, 1938, Bougainvillia inaequalis Fraser, 1944 and Bougainvillia meinertiae Jäderholm, 1923 – only known from polyps. In total, 27 Bougainvillia medusae are currently known.

In the present study, a comparison of descriptions of all Bougainvillia medusae is made (Table 1), and a new species, Bougainvillia pagesi sp. nov., is described.

Material and Methods

A total of 3844 plankton samples were obtained from 25° to 55°S, between 1983 and 2008, using different nets (Biomoc, Bongo, Calvet, Motoda, Multinet, Nackthai, Pairovet or WP-2) with 200–500 μm mesh size. Most of the samples were collected by the Instituto Nacional de Investigación y Desarrollo Pesquero (INIDEP). In addition, 813 samples from South Brazil (~25–27°S) were obtained with bottom trawls, using shrimp fishing nets, 6–12 m wide and 1.5–3 cm in mesh size. These collections occurred monthly between late 1997 and 2009. More individuals were obtained from manual sampling (e.g. dip nets, snorkeling), and from others fishing gears, such as gill nets. All material was preserved in 4% formalin, usually after being anesthetized with menthol crystals. The nematocysts were identified from fixed medusae and only undischarged capsules were measured; the cnidome nomenclature followed Mariscal (1974).

The type material was deposited at the cnidarian collection of the Museu de Zoologia da Universidade de São Paulo (MZUSP), with additional paratypes deposited at the British Museum of Natural History (NHMUK), the Natural History Museum of Geneva (MHNG INVE), and the University of Salento Hydrozoan Collection (USHC). Most of the rest of the material is stored at the Cnidarian collection of the Zoology Department of the Paraná Federal University and the Medusozoa collection from Estación Costera Nágera (MedusAS), Universidad Nacional de Mar del Plata–INIDEP.

Results

Class Hydrozoa Huxley, 1856
Subclass Anthoathecata Cornelius, 1992
Order Filifera Kühn, 1913
Family Bougainvillidae Lütken, 1850
Genus Bougainvillia Lesson, 1836
Bougainvillia pagesi sp. nov. (Figs 1 and 2)

Material examined

826 specimens. Holotype: MZUSP 1480 (Fig. 1), specimen collected on 30 June 2009 with gill nets from Pontal do Paraná, Brazil (25°36′31″S, 48°22′26″W). Paratypes: MZUSP 0903, three specimens collected on 8 August 2003. MZUSP 0902, two specimens collected on 20 September 2003. All of them were sampled with shrimp fishing nets from Guaratuba, Paraná, Brazil (25°54′S, 38°3′W). MHNG INVE 74571, three specimens, NHMUK 2010.24-26, one medusa each and USHC 2010BOU.1, three specimens, all of them sampled by the Evaluation cruise CC 01/06 by INIDEP at Argentina at 7.5 m depth (37°30′S, 57°10′W) in 3 February 2006 with Bongo plankton net 200-μm mesh aperture.

Additional specimens

559 specimens from the south coast of Brazil (25°20′–26°04′S; 48°05′–48°35′W), collected with shrimp fishing nets and manual sampling and deposited at the Cnidarian collection of the Zoology Department of the Paraná Federal University; 252 specimens from the coast near Buenos Aires (Argentina, 36°16′–38°22′ S, 56°26′–57°45′ W), collected with a Bongo net and manual sampling and deposited at Medusozoa collection, Estación Costera Nágera, Universidad Nacional de Mar del Plata – INIDEP.

Etymology

The species was named in honor of Dr. Francesc Pagès (1962–2007), eminent hydrozoan researcher which gave the first author important assistance and encouragement in the early steps of this study.

Diagnosis

Bougainvillia medusa with globular umbrella and thick mesoglea; folded and voluminous gonads, hanging at perradial walls of the manubrium and along proximal part of the radial canals.

Description (based on several specimens, Figs 1 and 2)

Umbrella globular with round top, 3.3–18 mm wide and 3–20 mm high, usually slightly higher than wide. Mesoglea thick at apical region, representing c. 1/3 (20–47%) of total umbrelar height in preserved material; manubrium quadrate, short, without peduncle; mouth quadratic with slightly crenulated lips; oral tentacles with basal trunk usually short (up to half of total oral tentacles length), arising perradially above mouth rim, dichotomously branching three to five times, distal portion armed with nematocyst clusters; four simple radial canals; four folded hanging gonads, white in live material and very voluminous when developed, extending from perradial walls of the manubrium and along proximal part of radial canals. In a few (n = 3) small medusae sampled (<4 mm), the gonads were less developed, differing from others only by being much less voluminous and not folded; velum narrow; tentacular bulbs triangular and broad, with 7–16 short tentacles, typically 9–14; linear or crescent-shaped ocelli, black or red, located on the adaxial base of each tentacle.

Morphological variations

In four specimens from Brazil (of 565) one radial canal branched dichotomously once in the distal portion. None of the 261 medusa sampled from Argentina was a variant.

Cnidome

Marginal tentacles – desmonemes, undischarged capsule varying from 2.5 to 5.59 μm wide (mean ± SD = 4.55 ± 0.6, n = 70), and from 7.08 to 10.01 μm high (mean = 8.4 ± 0.83, n = 70). Oral tentacles – microbasic euryteles, undischarged capsules varying from 2.64 to 4.43 μm wide (mean = 3.56 ± 0.56, n = 32) and from 7.66 to 11.44 μm high (mean = 9.48 ± 1.03, n = 32); and small desmonemes with undischarged capsules smaller than 2 μm.

Biological notes

In Brazilian specimens around 5.5% of individuals were parasitized by one or two metacercariae of the genus Opechona (Digenea, Lepocreadiidae) and four animals had an unidentified nematode on their mesoglea.

Seasonality

On the Brazilian coast this medusa was collected throughout the year, but 88% of all individuals were caught in August and September (21% and 67%, respectively); this period corresponds to the transition between the austral winter and spring when the water temperature increases and usually is above 20° C. From Argentina the species was only collected during the austral summer (January–March) at temperatures of 19°–21°C.

Distribution

South Brazilian (~25–26°S) and Argentinean (~36–38°S) shallow coastal waters (Fig. 1).

Discussion

The specimens described correspond with the diagnosis of the genus Bougainvillia (Kramp 1961; Vannucci & Rees 1961; Bouillon & Boero 2000) and their characters show that it is a new species (Table 1).

The most distinctive character of Bougainvillia pagesi sp. nov. is the shape and position of the gonads, which are perradial like in Bougainvillia dimorpha Schuchert 1996; Bougainvillia lamellata Xu, Huang & Liu, 2007, Bougainvillia longistyla Xu & Huang 2004; Bougainvillia macloviana (Lesson, 1830) and Bougainvillia paraplatygaster Xu, Huang & Chen, 1991. However, none of them presents folded voluminous hanging gonads along the proximal part of the radial canals as B. pagesi sp. nov. (Figs 1 and 2b–d). Moreover, B. dimorpha is smaller and has round ocelli; B. lamellata is smaller, the oral tentacles branch only twice, it has fewer tentacles and no ocellus; B. longistyla has a long basal trunk in the oral tentacles, the bulbs are kidney-shaped with only four to six tentacles each and no ocellus; B. paraplatygaster has bulbs that are kidney-shaped and the oral tentacles are branched six to seven times; and B. macloviana has a well developed peduncle and 35–65 marginal tentacles arranged in a double row (Table 1). The shape of the ocelli and the tentacular bulbs of B. pagesi sp. nov. may resemble those of Bougainvillia platygaster (Haeckel, 1879). Both species differ in the shape and position of the gonads. The relatively larger size of B. pagesi sp. nov. compared with other Bougainvillia medusae is also remarkable. Although B. macloviana may reach up to 15 mm, B. pagesi sp. nov. is larger, up to 20 mm high (Table 1).

Despite the high number of planktonic samples analyzed (3844) that covered the entire Continental shelf of Argentina, Uruguay, and South Brazil, B. pagesi sp. nov. was only collected in three coastal ones and more individuals were obtained with demersal nets, gill nets and manual sampling along the coastal line. This coastal distribution could be the reason why the species did not appear in most plankton samples from the continental shelf. In subtropical waters (Brazil), the species was present throughout the year but it was mostly collected in late winter and early spring when temperatures were higher than 20°C. In temperate waters (Argentina), this medusa occurs only in summer when the temperature was 19–21°C. It was not recorded during the colder seasons. In temperate environments, species with metagenetic life cycles present a marked seasonality. During unfavorable periods they are represented by benthic stages with medusae release occurring in pulses constrained to shorter periods during favorable seasons (e.g. Calder 1990; Bavestrello et al. 2006). Among the well studied hydroid fauna of the region (see Genzano et al. 2009 for a review), no polyp stage could be linked or related to B. pagesi sp. nov. medusa. Resting stages could be involved in the life cycle of this species and further studies will be necessary to determine seasonal occurrence patterns, including resting stages, if any.