Two new Eirenidae medusae species were collected on the Amazonian coast, Eutima marajoara n. sp. and Helgicirrha angelicae n. sp. The former differs from other species of the genus by the gonads extending along almost the entire length of the subumbrellar portion of the radial canals but not connected to the ring canal, up to 40 marginal tentacles with conical bulbs and 48 marginal warts, lateral cirri and adaxial papillae on some marginal warts and tentacular bulbs. Helgicirrha angelicae n. sp. differs from other species of the genus by the gonads on the middle portion of the radial canals with medusa buds, the short gastric peduncle, up to 20 marginal tentacles, some with adaxial papillae, up to three marginal warts and two statocysts between successive tentacles, and lateral cirri both on tentacle bulbs and marginal warts.
RESUMEN
En la costa amazónica se recolectaron dos nuevas especies de medusas Eirenidae, Eutima marajoara n. sp. y Helgicirrha angelicae n. sp. La primera se diferencia de otras especies del género por las gónadas que se extienden a lo largo de casi toda la longitud de la porción subumbrellar de los canales radiales, pero no conectados al canal circular, hasta 40 tentáculos marginales con bulbos cónicos y 48 verrugas marginales, cirros laterales y papilas adaxiales en algunas verrugas marginales y bulbos tentaculares. Helgicirrha angelicae n. sp. se diferencia de otras especies del género por las gónadas en la porción media de los canales radiales con yemas de medusa, pedúnculo gástrico corto, hasta 20 tentáculos marginales, algunos con papilas adaxiales, hasta tres verrugas marginales y dos estatocistos entre tentáculos sucesivos, lateral cirros tanto en bulbos de tentáculos como en verrugas marginales.
Hydromedusae from the family Eirenidae Haeckel, 1879 are easily distinguished from other Leptothecata by the presence of a distinct gastric peduncle and closed statocysts (Bouillon et al. 2006). In some Eirenidae genera there are eight statocysts (rarely 12) while in others there are an indefinite number, but always more than eight in adult medusae (Bouillon 1984, 1999, Bouillon et al. 2006). Among those with eight statocysts, Eutima McCrady, 1859 differs from Eugymnanthea Palombi, 1936 by the adult medusae with tentacles and from Eutimalphes Haeckel, 1879, Eutonina Hartlaub, 1897 and Neotima Petersen, 1962 by the presence of lateral cirri on marginal warts and/or tentacles (Bouillon 1999, Bouillon et al. 2006). In the second case, Helgicirrha Hartlaub, 1909 differs from Eirene Eschscholtz, 1829, Tima Eschscholtz, 1829 and Phialopsis Torrey, 1909 by the presence of lateral cirri on tentacular bulbs and from Irenium Haeckel, 1879 by the gonads restricted to the subumbrellar part of the radial canals (Bouillon 1999, Bouillon et al. 2006).
Currently there are 22 valid species described in the genus Eutima and 11 (one with a temporary name) in Helgicirrha in the World Register of Marine Species(Schuchert 2020). Althoughthe general shape of the umbrella, gastric peduncle and manubrium may help with identification,species in the two genera are mainly distinguished by the shape and position of the gonads, the number of marginal structures and presence/absence of adaxial papillae or excretory pores (Kramp 1961, Bouillon 1984). This is not an easy assignment since most species show a high level of intraspecific variability (Tables 1, 2), which has not been described in detail, particularly when in juvenile and/or not fully developed specimens.
Comparison of main characters of the valid medusae species of the genus Eutima. ND, no data.
Species
Umbrella
Tentacles
Warts
Gonads
Papillae
Peduncle
Distribution
Reference
Eutima marajoara n. sp.
Up to 9.5 mm with thin mesoglea
Up to 40
Up to 48
Subumbrella
Present
1/4 of umbrella diameter
North Brazil
This study
Eutima cirrhifera (Kakinuma, 1964)
Up to 9.8 mm
8
24-49
Subumbrella
Absent
Small
Japan
Kakinuma, 1964, Bouillon 1984
Eutima coerulea (Agassiz, 1862)
Up to 10 mm, mesoglea thick at apex
32
96
Restricted to peduncle
Absent
1/2 of umbrella diameter, tapering
Bahamas, Florida, Tortuga
Kramp 1961, Bouillon 1999
Eutima commensalis Santhakumari, 1970
Up to 5.9 mm
8
48-80
Subumbrella
Absent
Small
Indian, Arabian Sea
Santhakumari 1970, Bouillon 1984
Eutima curva Browne, 1905
Up to 25 mm, with thick mesoglea
4
120-140
Restricted to peduncle
Absent
Long, pyramidal above
Indo-Pacific, China Sea
Kramp 1961, Bouillon and Barnett 1999
Eutima diademata (Kramp, 1959)
Up to 15 mm, almost hemispherical
8
50-80
8: 4 on radial canals, 4 on peduncle
Absent
Long
Indo-Pacific
Kramp 1959, Guo et al. 2008
Eutima gegenbauri (Haeckel, 1864)
Up to 20 mm, hemispherical
8 to 16
60-80
8: 4 on radial canals, 4 on peduncle
Present
Very long
Mediterranean, European Atlantic, Australia, China Sea
Kramp 1961, Bouillon 1984
Eutima gentiana (Haeckel, 1879)
Up to 8 mm, higher than wide
8
16
Restricted to peduncle
Absent
Very long
Canary Islands, China Sea
Kramp 1961, Bouillon 1984
Eutima gracilis (Forbes and Goodsir, 1853)
Up to 13 mm, with thick mesoglea
2 or 4
40-80
Restricted to peduncle
Absent
Long and narrow, with conical base
Mediterranean, European Atlantic, West Africa
Kramp 1961, Bouillon 1999
Eutima hartlaubi Kramp, 1958
Up to 15 mm, flatter than hemispherical
12 to 14
32
8: 4 on radial canals, 4 on peduncle
Absent
1/2 of umbrella diameter
Djibouti, Nicobar, Aden Gulf, Indian
Kramp 1958, Bouillon 1984
Eutima japonica Uchida, 1925
Hemispherical
8
16
Subumbrella, part of peduncle
Absent
Small
Japan, North Pacific
Kramp 1961, Bouillon 1984
Eutima levuka (Agassiz and Mayer, 1899)
Up to 15 mm
8
100
8: 4 on radial canals, 4 on peduncle
Absent
1 1/2 of umbrella diameter
Indo-Pacific, China Sea
Kramp 1961, Bouillon 1984
Eutima longigonia Bouillon, 1984
Up to 88 mm, flatter than hemispherical
8
64-80
Restricted to peduncle
Absent
= umbrella diameter
Papua New Guinea
Bouillon 1984
Eutima mira McCrady, 1859
Up to 30 mm, as broad as wide
4
~100
8: 4 on radial canals, 4 on peduncle
Absent
Long, tapering
Indo-Pacific, Brazil, Northeast Atlantic, China Sea
Kramp 1961, Bouillon 1999
Eutima modesta (Hartlaub, 1909)
Up to 8 mm, flat
16
16+
Subumbrella
Absent
1/2 of umbrella diameter
Djibouti, Aden Gulf
Kramp 1961, Bouillon 1984
Eutima mucosa Bouillon, 1984
Up to 15 mm, flat
8
56-80
Subumbrella
Absent
1/2 of umbrella diameter
Papua New Guinea
Bouillon 1984
Eutima neucaledonia Uchida, 1964
Up to 9 mm, flat
8
48-56
Subumbrella
Absent
= umbrella diameter
New Caledonia
Uchida 1964, Bouillon 1984
Eutima orientalis (Browne, 1905)
Up to 6 mm
4
60-80
8: 4 on radial canals, 4 on peduncle
Absent
2x umbrella diameter
Sri Lanka
Kramp 1968
Eutima sapinhoa Narchi and Hebling, 1975
Up to 4 mm, slightly higher than wide
4
28
Subumbrella
Absent
= umbrella diameter
Brazil
Narchi and Hebling 1975, Bouillon 1984
Eutima suzannae Allwein, 1967
5.7 mm, wider than high
8
32
Subumbrella
Present
1/2 of umbrella diameter
North Carolina
Allwein 1967, Bouillon 1984
Eutima variabilis McCrady, 1859
ND
20 (4 longer)
36
8: 4 on radial canals, 4 on peduncle
Absent
1-1.5 of umbrella height
East USA, China Sea
Kramp 1961, Bouillon 1984
Eutima taiwanensis Xu, Huang and Guo, 2019
Up to 12 mm, hemispherical
12-16
80-120
8: 4 on radial canals, 4 on peduncle
Absent
Long
Taiwan Strait
Guo et al. 2019
Comparison of main characters of the valid medusae species of the genus Helgicirrha. ND, no data.
Species
Width
Umbrella
Tentacles
Marginal warts
Statocysts
Helgicirrha angelicae n. sp.
Up to 8.5 mm
Flatter than hemispherical, with thin mesoglea
Up to 20
1-3 between successive tentacles
Generally 1 between successive tentacles
Helgicirrha brevistyla Xu and Huang, 1983
Up to 16 mm
Higher than hemispherical
28-54
0-2 between successive tentacles
1-2 between successive tentacles
Helgicirrha cari (Haeckel, 1864)
Up to 50 mm
Flatter than hemispherical, with thin mesoglea
Up to 60
Up to 100
Up to 100
Helgicirrha cornelii Bouillon, 1984
Up to 9 mm
Flatter than hemispherical, with thick mesoglea in centre
16
16 small rudimentary bulbs and 32 small protuberances
16
Helgicirrha danduensis (Bigelow, 1904)
Up to 25 mm
Flatter than hemispherical, somewhat conical
32
About 17
32
Helgicirrha gemmifera Bouillon, 1984
Up to 5 mm
Almost flat, with thin mesoglea
4
11-15
8-16
Helgicirrha irregularis Bouillon, Boero and Seghers, 1988
Up to 20 mm
Flatter than hemispherical, with thin mesoglea
16-180
Up to 80, 0-8 between successive tentacles
18
Helgicirrha malayensis (Stiasny, 1928)
Up to 20 mm
With thin mesoglea
30-140
Variable
1- between tentacles
Helgicirrha medusifera (Bigelow, 1909)
Up to 8 mm
Moderately high
Up to 21
As numerous as the tentacles in small medusae, fewer in larger specimens
1 between successive tentacles
Helgicirrha ovalis Huang, Xu, Lin and Guo, 2010
Up to 6.5 mm
Flatter than hemispherical, with thin mesoglea
8
1-2 between successive tentacles
2-3 between successive tentacles
Helgicirrha weaveri Allwein, 1967
Up to 25 mm
Almost hemispherical, with moderately thick mesoglea
Up to 14
4-6 between successive tentacles
1 between successive tentacles
Helgicirrha sinuatus Xu, Huang and Du, 2012
12-22 mm
Flatter than hemispherical
16-24
3-5 between successive tentacles
3-4 between successive tentacles
Species
Adaxial papillae and/or excretory pores
Gonads
Helgicirrha angelicae n. sp.
Some bulbs and warts with papillae
Linear, in the middle portion of radial canals, with medusa buds
Helgicirrha brevistyla Xu and Huang, 1983
ND
Elongated, from near the base of peduncle to near the umbrella margin
Helgicirrha cari (Haeckel, 1864)
Pores present
Linear, from near the base of peduncle to near the umbrella margin
Helgicirrha cornelii Bouillon, 1984
Absent
Linear, beginning in the middle part of the canal and posteriorly extending distally, but never reaching the margin
Helgicirrha danduensis (Bigelow, 1904)
ND
Spindle-shaped, occupying the distal 2/3 of the canals
Helgicirrha gemmifera Bouillon, 1984
Absent
In the middle portion of radial canals, with medusa buds
Helgicirrha irregularis Bouillon, Boero and Seghers, 1988
Absent
Sinuous, extending from the base of the peduncle to the distal quarter or radial canals
Helgicirrha malayensis (Stiasny, 1928)
ND
Long, extending from inwards, sometimes continuing along upper part of peduncle
Helgicirrha medusifera (Bigelow, 1909)
Pores on papillae
Cylindrical, on distal third of the radial canals (not reaching the umbrella margin), with medusa buds
Helgicirrha ovalis Huang, Xu, Lin and Guo, 2010
ND
Oval, in the middle of radial canals
Helgicirrha weaveri Allwein, 1967
Pores on tentacle bulbs and marginal warts
Narrow, from near the base of peduncle to near the umbrella margin
Helgicirrha sinuatus Xu, Huang and Du, 2012
Pores on tentacle bulbs and marginal warts
Sinuous, occupying the distal 2/3 or 1/3 of the canals
Species
Peduncle
Manubrium
Distribution
Reference
Helgicirrha angelicae n. sp.
Prismatic, about 1/4 of umbrella diameter
Small, with 4 lips
North Brazil
This study
Helgicirrha brevistyla Xu and Huang, 1983
About 1/6 of umbrella diameter
Quadratic with four slightly folded lips
China
Xu and Huang 1983
Helgicirrha cari (Haeckel, 1864)
Variable
Variable
North Sea, Adriatic, Mediterranean, Benguela Current, Mexican Caribbean
Kramp 1961, Pagès et al. 1992, Bouillon 1999
Helgicirrha cornelii Bouillon, 1984
Less than 11/5 of umbrella diameter
With evident lips
Papua New Guinea
Bouillon 1984
Helgicirrha danduensis (Bigelow, 1904)
Long, reaching well beyond umbrella margin
1/2 as long as the peduncle, with evident lips
Maldive islands
Bigelow 1904
Helgicirrha gemmifera Bouillon, 1984
About 1/4 of umbrella diameter
Long, without apparent lips
Papua New Guinea
Bouillon 1984
Helgicirrha irregularis Bouillon, Boero and Seghers, 1988
Cylindrical, about 3/4 of umbrella diameter
Short, with developed and scalloped lips
Papua New Guinea
Bouillon et al. 1988
Helgicirrha malayensis (Stiasny, 1928)
Conical
Short
Papua New Guinea, Java Sea, Madras, India, China
Kramp 1961, Bouillon et al. 1988
Helgicirrha medusifera (Bigelow, 1909)
Conical, about 1/4 of umbrella diameter
Short with 4 simple lips
Pacific coast of Mexico, Arabian Sea, Bay of Bengal, Taiwan strait
Bigelow 1909, Vannucci and Santhakumari 1969, Wang et al. 2013
Helgicirrha ovalis Huang, Xu, Lin and Guo, 2010
Short
Prismatic with four lips
Taiwan Strait
Huang et al. 2010
Helgicirrha weaveri Allwein, 1967
About 1/4 of umbrella diameter
Small with curved lips
North Carolina, USA
Allwein 1967
Helgicirrha sinuatus Xu, Huang and Du, 2012
Very long
Small and square
Beibu Gulf (China)
Du et al. 2012
Specimens from two Eirenidae species were found in a scientific expedition along the Amazonian coast of northern Brazil (Araujo et al. 2017, Tosetto et al. 2019). Species of the family are typically coastal and/or estuarine, often occurring in high abundance (Canché-Canché and Castellanos-Osorio 2005, Morales-Ramírez and Nowaczyk 2006, Mediseh et al. 2017). This aspect, associated with the high feeding rates of pelagic cnidarians (Hays et al. 2018), may place them as significant predators in these environments. The specimens found clearly belonged to the genera Eutima and Helgicirrha because of the characteristics explained above, but did not fit in any of the currently known species. Thus, the objective of this work is to describe Eutima marajoara n. sp. and Helgicirrha angelicae n. sp. In addition, the main characteristics of all species described in both genera are compiled and compared (Tables 1, 2).
MATERIALS AND METHODS
Specimens were obtained from samples collected in October 2012 at Marajó Bay and along the Amazonian coast, northern Brazil (Fig. 1), with oblique hauls from near bottom to the surface, using a Bongo net with 120 and 300 µm mesh and 0.3 and 0.6 m mouth opening, respectively. The material was fixed with 4% formaldehyde buffered with sodium tetraborate (0.5 g l–1). 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 Coleção de Invertabrados Paulo Young from Universidade Federal da Paraíba (CIPY). All applicable international, national and institutional guidelines for the care and use of animals were followed.
Sample sites for Eutima marajoara n. sp. (circles) and Helgicirrha angelicae n. sp. (diamond) along the Amazonian coast. “H” indicates holotype locality.
In the laboratory, specimens were measured and the number of marginal structures per quadrant was counted under an optical microscope. We considered each quadrant separately in order to test for individual variability and to alleviate the problem that some specimens had quadrants with parts of the margin damaged and structures missing. Relationships between umbrella diameter and number and ratio of marginal structures were modelled with linear regressions with Statsoft Statistica 10 software.
RESULTS
Eutima marajoara n. sp. A, oral view of the holotype; B, paratype; C, detail of a tentacular bulb with lateral cirri; D, schematic representation of adult specimen.
Class Hydrozoa Owen, 1843
Subclass Hydroidolina Collins, 2000
Order Leptothecata Cornelius, 1992
Family Eirenidae Haeckel, 1879
Genus Eutima McCrady, 1859
Etymology. Specimens were collected in the waters of Marajó Bay in northern Brazil. Marajoara refers to the native society that inhabited the area before European occupation and gave name to the bay.
Diagnosis.Eutima medusa with gonads restricted to subumbrella, extending along almost entire length of subumbrellar portion of radial canals. Approximately 32 (up to 40) marginal tentacles with conical bulbs and 32 (up to 48) marginal warts. Some marginal warts and tentacular bulbs with lateral cirri and a few with adaxial papillae.
Description (based on several specimens). Umbrella flat, ranging from 1.5 to 9.2 mm wide, with thin mesoglea. Manubrium tubular with folded lips. Narrow prismatic gastric peduncle, about 1/4 of umbrella diameter in length. Gonads restricted to subumbrella, linear, extending along almost entire length of subumbrellar portion of radial canals but not connected to ring canal and gastric peduncle (Fig. 2A, B). Approximately 32 (up to 40) marginal tentacles with conical bulbs in adult medusae. Up to 48 marginal warts in different sizes, usually two or three between successive tentacles in small medusae, fewer in larger specimens (as shown by the increase in the ratio between tentacles and warts, Fig. 3). Up to eight statocysts. Some warts and bulbs with lateral cirri (Fig 2C) and a few with adaxial papillae (Fig. 2D). Velum narrow.
Eutima marajoara n. sp. and Helgicirrha angelicae n. sp. relationship between mean number of marginal structures per umbrella quadrant and umbrella diameter. Symbols are mean+SD for each individual; symbols without error bars indicate that data from a single quadrant were available; dotted lines are the result of linear regressions (Table 3).
Development. Positive significant (p<0.05) relationships were observed between umbrella diameter and mean number of marginal tentacles, warts, ratio between tentacles and warts and statocysts per umbrella quadrant (Table 3, Fig. 3). Positive values of b coefficient indicate the number of tentacles and warts increases with medusa development (Table 3). While smaller specimens (1.5~2 mm) had one or two tentacles and two to four warts on each quadrant, individuals of intermediate sizes around 5 mm had approximately four tentacles and six warts per quadrant (note some individuals had up two 11 warts per quadrant in this stage) and bigger ones (~9 mm) had up to 10 tentacles and 12 warts per quadrant (Fig. 3). Positive values of b coefficient of tentacles/warts ratio also indicate that warts are relatively more abundant in juveniles (Fig. 3). Although the relationship between umbrella diameter and statocyst number was significant (p value almost 0.05, very close to the threshold limit of significance), the low value of the b coefficient indicates that the number of statocysts does not increase with medusa development, as was expected because species of Eutima are considered to have a fixed number of statocysts (Table 3, Fig. 3).
Summary and coefficients (a, b) of linear regression relating umbrella diameter and mean number of marginal structures per umbrella quadrant (number of structures = a + b * umbrella diameter) in Eutima marajoara n. sp. and Helgicirrha angelicae n. sp. (n, number of specimens analysed; a, intercept; b, inclination; p values <0.05 are considered significant).
n
F
p
a
b
Eutima marajoara
Tentacles
49
197.21
<0.0001
0.5
0.87
Marginal warts
49
56.14
<0.0001
2.62
0.76
Tentacles/warts ratio
49
13.03
<0.0001
0.51
0.05
Statocysts
47
4.07
0.0496
1.11
0.06
Helgicirrha angelicae
Tentacles
18
152.39
<0.0001
0.33
0.56
Marginal warts
17
25.69
<0.0001
-0.1
0.87
Tentacles/warts ratio
17
1.76
0.21
1.08
-0.05
Statocysts
15
24.77
<0.0001
0.3
0.45
Ecological notes. Specimens were found in estuarine waters (8 m bottom depth) of the Marajó Bay, mouth of Pará and Amazon Rivers, at 28.3°C temperature and 18.2 salinity throughout the water column.
Helgicirrha angelicae n. sp. A, oral view of the holotype; B, detail of the tentacular bulb with lateral cirri; C, detail of a gonad with medusa buds; D, schematic representation of adult specimen.
Genus Helgicirrha Hartlaub, 1909 Helgicirrha angelicae n. sp.
(Fig. 4)
Etymology. This species is named after Professor Maria Angélica Haddad, one of the pioneers of hydrozoan studies in Brazil whose passion encouraged generations of students.
Diagnosis. Helgicirrha medusa with gonads on middle portion of radial canals, with medusa buds. Short gastric peduncle. Up to 20 marginal tentacles, some with adaxial papillae. Generally one to three marginal warts and one statocyst between successive tentacles. Lateral cirri on tentacle bulbs and some marginal warts.
Description (based on several specimens). Umbrella flatter than a hemisphere, ranging from 0.8 to 8.5 mm wide, with thin mesoglea. Small manubrium, mouth with four short simple lips. Short and narrow prismatic gastric peduncle, about 1/4 of umbrella width in length. Linear gonads on middle portion of radial canals, with developing medusa buds (Fig. 4A, C). Up to 20 marginal tentacles with conical bulbs. Up to 28 marginal warts in different sizes, usually one to three between successive tentacles. Lateral cirri on tentacle bulbs and some marginal warts (Fig. 4B). Generally one statocyst between successive tentacles. Some bulbs with adaxial papillae. Velum narrow.
Development. Positive significant (p<0.05) relationships were observed between umbrella diameter and mean number of marginal tentacles, warts, and statocysts per umbrella quadrant (Table 3, Fig. 3). Positive values of b coefficient indicate that the number of tentacles, warts and statocysts increase with medusa development (Table 3). Smaller specimens (~1 mm) had one perradial tentacle, one or no interradial warts and one statocyst in each quadrant. Intermediate stages (~4.5 mm) had around three tentacles, four warts and 2.5 statocysts per quadrant and bigger specimens (6~8 mm) had up to six tentacles, seven warts and five statocysts per quadrant (Table 3, Fig. 3). Ratios between tentacles and warts were not significantly correlated with umbrella diameter.
Ecological notes. Specimens were found in neritic waters over a reef system (30-65 m bottom depth) under the influence of the Amazon River plume with water column temperature ranging from 24.9°C to 27.9°C and salinity from 31.1 to 36.3.
DISCUSSION
Genera of the family Eirenidae are mainly distinguished by the number of statocysts, the position of the gonads and the presence of marginal structures such as, cirri, warts and adaxial papillae (Bouillon et al. 2006). Eutima and Helgicirrha species always have lateral cirri on the tentacle bulbs and/or marginal warts, and some species of both genera have adaxial papillae and gonads restricted to the subumbrella (Bouillon 1984, Bouillon et al. 2006, Schuchert 2017), as do the specimens found in this study. However, Eutima species have eight statocysts (rarely 12) in adult medusae and Helgicirrha always has more than eight and up to an indefinite number (Bouillon 1984, Bouillon et al. 2006). The number of statocysts is the main character distinguishing the two genera (the absence of excretory pores in Eutima is controversial and will be discussed later) and was used to assign the genera of the two species discussed herein. However, when the medusae development was observed, smaller specimens of both had fewer statocysts (Fig. 3C, G), and observations based on these individuals, associated with the fragility of these organisms (marginal structures are frequently lost in net trawls and/or formalin fixation), could lead to misidentification. These observations reinforce the need to examine fully developed specimens and to characterize their ontogenetic development for accurate identification and to elucidate the taxonomy of complex families such as Eirenidae.
Distinctive characters of Eutima marajoara n. sp. are the gonads restricted to the subumbrella, the adaxial papillae on few marginal warts and/or tentacle bulbs and the large number of marginal tentacles. Among the other seven species described in the genus with gonads restricted to the subumbrella, only Eutima suzannae Allwein, 1967 also have adaxial papillae (Table 1). However, unlike in E. marajoara n. sp., in E. suzannae papillae are restricted to the marginal warts. Other differences are the longer gastric peduncle in E. suzannae and the number of tentacles and marginal warts. While E. marajoara have up to 40 (usually 32 in adults) tentacles and 1 to 3 warts between successive tentacles, E. suzannae have only eight tentacles and four warts between them (Allwein 1967). Moreover, the high number of tentacles in E. marajoara n. sp. is noteworthy. While most species in the genus have eight or four tentacles, only E. marajoara n. sp. and Eutima coerulea (Agassiz, 1862) have more than 20. However, in E. coerulea the gonads are restricted to the peduncle, unlike in our specimens (Table 1).
The original description of Eutima included species without papillae (McCrady 1859). A few years later Octorchis Haeckel, 1864 was described (Haeckel 1864), differing from Eutima mainly in the presence of adaxial papillae in Octorchis and their absence in Eutima (e.g. Russell 1953). Subsequent studies considered both as subgenera within the genus Eutima (Kramp 1961, Bouillon 1984). Currently the subgenus rank fell out of use and all species previously considered Octorchis are included within Eutima (Schuchert 2020), which now encompasses eirenids with eight statocysts and lateral cirri, with or without papillae (Kramp 1961, Bouillon 1984, Schuchert 2020; Table 1). One open question is whether these papillae do possess an excretory pore, which would be necessary to regard them as excretory papillae (as mentioned in recent diagnoses, e.g. Bouillon and Boero 2000, Bouillon et al. 2006), because this is hard to verify and requires detailed histological observations (Schuchert 2017).
Only the hydroid stage and newly released medusa are known in Eutima ostrearum (Mattox and Crowell, 1951). Hydroids of this species were found inhabiting the mantle cavity of oysters in an estuarine system in Puerto Rico (Mattox and Crowell 1951). Due to the close geographic location and similar habitat (e.g. estuarine waters), E. marajoara n. sp. could be the adult medusa of E. ostrearum. Future studies based on molecular data from both localities and on hydroids inhabiting the Marajó Bay are necessary to answer this question. However, newly released E. ostrearum of up to 3 mm displayed no lateral cirri and had no sign of a gastric peduncle (Mattox and Crowell 1951). Although these characters may develop later in the medusa ontogeny, they differ from our smaller specimens within the same size range (1.5-3 mm), which already had lateral cirri and a small but clearly visible peduncle. These differences suggest they are different species.
Specimens of Helgicirrha angelicae n. sp. have linear gonads located in the middle portion of the radial canals. Shape and position of gonads are important characters forthe taxonomy of Helgicirrha and other Eirenidae medusae (e.g. Bouillon 1984, Bouillon et al. 1988, Huang et al. 2010). Indeed, the gonadal position was helpful to distinguish the present specimens from Helgicirrha brevistyla Xu and Huang, 1983, Helgicirrha cari (Haeckel, 1864), Helgicirrha danduensis (Bigelow, 1904), Helgicirrha irregularis Bouillon, Boero and Seghers, 1988, Helgicirrha malayensis (Stiasny, 1928), Helgicirrha medusifera (Bigelow, 1909), Helgicirrha weaveri Allwein, 1967 and Helgicirrha sinuatus Xu, Huang and Du, 2012, which have gonads in other positions than the middle portion of the radial canals (see Table 2 and reference therein). Among the remaining species, Helgicirrha cornelii Bouillon, 1984, Helgicirrha gemmifera Bouillon, 1984 and Helgicirrha ovalis Huang, Xu, Lin and Guo, 2010, unlike our specimens, do not have adaxial papillae either on the tentacular bulbs or on the marginal warts. In addition, they are distinct from the current specimens in the lower number of tentacles and shape of the gonads in the case of H. ovalis and H. cornelii (Table 2). Unlike in Eutima, species of Helgicirrha may or may not have excretory pores either on papillae (e.g. H. medusifera) or directly on the bulbs and warts (e.g. H. weaveri); however, pores were not observed on H. angelicae papillae.
The presence of medusa buds on every gonad of all adult specimens of H. angelicae n. sp. is also an outstanding character that is useful to distinguish it from all other species but H. gemmifera and H. medusifera. As cited above, the former is quite different from H. angelicae n. sp. However, H. medusifera differs mainly in the position of the gonads, which are located on the distal third of the radial canals (Table 2), while in our specimens they are in the middle (Fig. 3). The large number of specimens found in our samples allowed us to observe the complete development of medusae, and in any case the gonads approached the ring canal or were even located on the distal region of the radial canals, while in H. medusifera they are clearly very close to it (Bigelow 1909). The different geographical distribution of the two species (the western Atlantic and the eastern Pacific) also argues against the possibility that they are morphological variations of the same species. Furthermore, in adult medusaeof H. medusifera most marginal warts turn into developed bulbs with tentacles and few warts are present (Bigelow 1909), and this is not the case for H. angelicae n. sp. because the number of warts increased with medusa development in similar proportion to the tentacles (Fig. 3). Future studies based on molecular data of both species could completely elucidate this question.
Among the 177 samples analysed, covering the northern Brazilian continental shelf and adjacent equatorial Atlantic oceanic waters (see Fig. 1 from Tosetto et al. 2019), both species had very restricted distributions. Currently, E. marajoara n. sp. has been found only in the waters of Marajó Bay, an estuarine environment (18.2 salinity) located in the mouth of the Pará and Amazon rivers, and is perhaps an endemic species to the area. H. angelicae n. sp. was restricted to coastal waters under the influence of the Amazon River plume. Knowledge on the zooplankton community inhabiting waters of the Amazonian coast is still scarce (Boltovskoy and Valentin 2018). Recently, this unique ecosystem has attracted attention from scientific and public society because of the presence of hard-bottom reefs (Moura et al. 2016) and oil exploitation in the area (Silva Junior and Magrini 2014), which may lead to significant impacts and losses in the rich, but still poorly known, biodiversity in the area.
ACKNOWLEDGEMENTS
We are grateful to the Brazilian National Institute of Science and Technology for Tropical Marine Environments, the Brazilian Research Network on Global Climate Change and European Integrated CARBOCHANGE for funding the Camadas Finas III survey for their support and to all the scientific team on board. We thank the CNPq (Brazilian National Council for Scientific and Technological Development), which provided a PhD scholarship to E.G.T. (grant 140897/2017-8) and a Research Scholarship to S.N.L.
REFERENCESAllweinJ.North American Hydromedusae from Beaufort, North Carolinae1967130117136AraujoM.NoriegaC.Hounsou-gboG.A.A Synoptic Assessment of the Amazon River-Ocean Continuum during Boreal Autumn: From Physics to Plankton Communities and Carbon Flux20178118https://doi.org/10.3389/fmicb.2017.01358BigelowH.B.Medusae from the Maldive Islands190439245269BigelowH.B.The Medusae. Reports on the scientific results of the expedition to the eastern tropical pacific, in charge of Alexander Agassiz, by the U. S. Fish Commission steamer "Albatross" from October, 1904, to March, 1905. XVI1909371243BoltovskoyD.ValentinJ.L.Overview of the History of Biological Oceanography in the Southwestern Atlantic, with Emphasis on PlanktonHoffmeyerM.S.SabatiniM.E.2018New YorkSpringer Science+Business Media334https://doi.org/10.1007/978-3-319-77869-3_1BouillonJ.Hydroméduses de la Mer de Bismark (Papouasie Nouvelle-Guinée. Partie IV: Leptomedusae (Hydrozoa-Cnidaria)1984125112BouillonJ.HydromedusaeBoltovskoyD.1999LeidenBackhuys Publishers424512BouillonJ.BarnettT.J.1999WellingtonNational Institute of Water and Atmospheric Research (NIWA)136BouillonJ.BoeroF.Synopsis of the families and genera of the hydromedusae of the world, with a list of the worldwide species20002447296BouillonJ.GraviliC.PagèsF.2006ParisMuséum national d’Histoire naturelle591BouillonJ.MedelM.D.PagèsF.Fauna of the Mediterranean Hydrozoa2004685438https://doi.org/10.3989/scimar.2004.68s25BouillonJ.SeghersG.BoeroF.Notes additionnelles sur les méduses de Papouasie Nouvelle-Guinée (Hydrozoa, Cnidaria). III19885225253Canché-CanchéV.E.Castellanos-OsorioI.Medusas (Cnidaria) de la Bahía de la Ascensión, Quintana Roo, México (1997)2005156572DuF.XuZ.HuangJ.Studies on the medusae (Cnidaria) from the Beibu gulf in the Northern South China Sea, with description of three new species201237506519GuoD.XuZ.HuangJ.Two new species of Eirenidae from the coast of southeast China2008276166GouF.XuZ.HuangJ.Two new hydrozoan species from the Taiwan Strait, China (Cnidaria: Hydrozoa: Leptothecata)201943185190HaeckelE.Beschreibung neuer Craspedoter Medusen aus dem Golfe von Nizza18641326342HaysG.C.DoyleT.K.HoughtonJ.D.R.A Paradigm Shift in the Trophic Importance of Jellyfish?201833874884https://doi.org/10.1016/j.tree.2018.09.001HuangJ.XuZ.LinM.Two new species of Leptomedusae from Taiwan Strait and its adjacent waters, China2010498790KakinumaY.A new commensal hydrozoan, Eugymanthea cirrhifera n. sp. from Hachinohe1964125157KrampP.L.Hydromedusae in the Indian museum195853339376KrampP.L.Some new and little-known Indo-Pacific medusae1959121223259KrampP.L.Synopsis of the medusae of the World1961401469https://doi.org/10.1017/S0025315400007347KrampP.L.1968Carlsberg FoundationCopenhagen200MattoxN.T.CrowellS.A new commensal hydroid of the mantle cavity of an oyster1951101162170https://doi.org/10.2307/1538383McCradyJ.Gymnopthalmata of Charleston Harbor18591103221MedisehS.D.KoochaknejadE.DehmourdiL.M.Jellyfish of Khuzestan coastal waters and their impact on fish larvae populations201716422430Morales-RamírezA.NowaczykJ.El zooplancton gelatinoso del Golfo Dulce, Pacífico de Costa Rica, durante la transición de la estación lluviosa a la seca 1997-1998200654201223MouraR.L.Amado-FilhoG.M.MoraesF.C.An extensive reef system at the Amazon River mouth20162111https://doi.org/10.1126/sciadv.1501252NarchiW.HeblingN.J.The life cycle of the commensal hydromedusa Eutima sapinhoa n. sp.1975307378https://doi.org/10.1007/BF00393755PagèsF.GiliJ.-M.BouillonJ.Medusae (Hydrozoa, Scyphozoa, Cubozoa) of the Benguela Current (Southeastern Atlantic)1992561164RussellF.S.1953LondonCambridge University Press530SanthakumariV.The life cycle of Eutima commensalis sp. nov. (Eutimidae, Hydromedusae)19705113118https://doi.org/10.1007/BF00352594SchuchertP.Systematic notes on some leptomedusa species with a description of Neotima galeai n. spec. (Hydrozoa, Cnidaria)2017124351375SchuchertP.2020http://www.marinespecies.orgSilva JuniorO.M.MagriniA.Exploração de Hidrocarbonetos na Foz do Rio Amazonas: Perspectivas de Impactos Ambietais no Âmbito das Áreas Ofertadas na 11o Rodada de Licitações da Agência Nacional do Petroléo20142146158https://doi.org/10.17551/2358-1778/geoamazonia.v2n4p146-158TosettoE.G.Neumann-LeitãoS.Nogueira JúniorM.Sampling planktonic cnidarians with paired nets: Implications of mesh size on community structure and abundance20192204853https://doi.org/10.1016/j.ecss.2019.02.027UchidaT.Some medusae from New Caledonia196412109112https://doi.org/10.5134/175348VannucciM.SanthakumariV.New records of hydromedusae from the shelf area off the Kerala Coast1969114043WangC.HuangJ.XuZ.One new species and one new record species of Eirenidae form the Taiwan Strait201338762764XuZ.HuangJ.On the Hydromedusae, Siphonophora, Scyphomedusae and Ctenophora from the Jiulong River Estuary of Fujian, China1983299110