Haminoea cf. fusca (A. Adams, 1850 )

Aslam, Sadar, Oskars, Trond R., Siddiqui, Ghazala & Malaquias, Manuel António E., 2019, Beyond shells: first detailed morphological description of the mangrove-associated gastropod Haminoea cf. fusca (A. Adams, 1850) (Cephalaspidea, Haminoeidae), with a COI phylogenetic analysis, Zoosystema 41 (16), pp. 313-326 : 317-321

Haminoea cf. fusca (A. Adams, 1850)

( Figs 2 , 3 , 4 )

Bulla fusca A. Adams, 1850: 581 , pl. CXXIV, fig. 94.

Haminea (sic) fusca – Pilsbry 1895a: 360, pl. 40, figs 89, 90. — Kobelt 1896: 196, pl. 15, figs 14, 15.

Haminaea (sic) fusca – Bergh 1901: 266, pl. XIX, figs 4, 5, pl. XVIII, figs 44, 47.

Haloa fusca – Habe & Kira 1968: 137. Haminoea sp. – Strack 1998: 26, 28, pl. 1, fig. 6. — Ng & Sivasothi 2001. — Lozouet & Plaziat 2008: 65, pl. 34, figs 5, 6. — Riek 2013; 2014.

Haminoea cf. fusca – Gosliner et al. 2008: 27, fig. 3; 2015: 30, lower left figure.

Haloa vitrea – Hung 2013.

Haminoea tenera – Mujiono 2016: 47, fig. 4a, b.

Haminoea edmundsi Yonow & Jensen, 2018: 3 , fig. 2B, n. syn.

Haminoe (sic) exarata – Ullah et al. 2018: 129-132.

Haminoea fusca – Cobb 2018.

MATERIAL EXAMINED. — Pakistan. Balochistan Coast, Sindh Province, Hab River Delta (24°53’12.01’’N, 66°42’14.00’’E), 20 specimens (3 specimens dissected, 2 specimens sequenced), H, 3-7 mm, ZMBN 125424 .

TYPE LOCALITY. — Mindanao Island, the Philippines (A. Adams 1850).

DIAGNOSIS. — Animal pale yellowish-green to bright green; mantle transparent; cephalic shield, squarish, broad; shallowly bilobed. Widely spaced visible eyes. Hancock’s organ, simple small horizontal ridge. Shell, whitish translucent; dense, wavy spiral striae; periostracum light orange, darker within spiral striae. Aperture wide, slightly tapering apically. Columella deeply concave anteriorly. Columellar lip narrow. Clumellar lips separated from last whorl by narrow umbilical furrow. Outer lip rounded; shoulder rounded. Radular formula 30-35 × 10.1.1.1.10. Rachidian tooth tricuspid, cusps triangular, with rounded tips; central cusp larger, broader, lateral cusps reduced. Lateral teeth hook-shaped, smooth; inner lateral with broader cusp; outer laterals tapering outwardly. Gizzard plates with flat surface; ridges absent; central rachis present. Surface covered in small tightly arranged pointed rods; rods tapering in size outwardly, larger rods present on top of rachis. Male reproductive system compact, sparsely covered in soft warts; consisting of atrium, thick-walled fundus, thick seminal duct, and bulbous, nodulous prostate.

COI BARCODES. — MH638588 (TH81), MH638587 (TH82).

DISTRIBUTION. — In the Indian Ocean Haminoea cf. fusca is known in Pakistan (present study) and in the West Pacific from Singapore ( Ng & Sivasothi 2001), Mindanao, Bohol and Panglao Islands in the Philippines ( Adams 1850; Lozouet & Plaziat 2008; Gosliner et al. 2008; 2015), Lombok and Ambon Islands, Indonesia ( Strack 1998; Mujiono 2016; Yonow & Jensen 2018), Macau and Liyu Island, China ( Bergh 1901; Hung 2013), New South Wales, Australia ( Gosliner et al. 2008, 2015; Cobb 2018; Riek 2013, 2014).

DESCRIPTION

External morphology ( Figs 1B, C ; 3A )

Animal pale yellowish-green to bright green; mantle transparent, visceral mass reddish-brown. Cephalic shield, squarish, broad; shallowly bilobed, posterior cephalic shield extending over anterior part of shell. Eyes visible, widely spaced. Hancock’s organ simple, small, horizontal ridge. Parapodial lobes, thick, separated dorsally.Rounded pallial lobe, extending beyond apex.

Shell ( Fig. 3B )

Shell whitish-brown translucent, dense, wavy spiral striae throughout; periostracum light orange, darker in spiral striae; shape bulbous, rounded. Aperture broad anteriorly, tapering slightly posteriorly. Columella deeply concave anteriorly.

Columellar lip narrow. Narrow umbilical furrow separates lip form last whorl. Outer lip rounded; shoulder rounded.

Radula ( Fig. 3C )

Radular formula 30 × 10.1.1.1.10 (spc.TH81, H = 6.5 mm), 35 × 10.1.1.1.10 (spc. TH82, H = 7 mm). Rachidian tooth tricuspid, cusps triangular, with rounded tips; central cusp larger, lateral cusps reduced. Lateral teeth hook-shaped, smooth; inner lateral with broader cusp, outer laterals tapering outwardly.

Gizzard plates ( Fig. 3 D-F)

Flat surface, ridges absent. Rachis present. Surface covered in small tightly arranged pointed rods; rods tapering in size outwardly; larger worn rods on top of rachis.

Male reproductive system ( Fig. 4A, B )

Compact and sparsely covered in soft warts; formed by atrium, fundus (upper atrium), thick seminal duct, and a bulbous nodulous prostate. Atrium with thin walls. Fundus thick walled, externally looking as a rounded bulge ( Fig. 4A , arrow) internally with a distinct left lateral wall and right lateral wall. Walls separated by a narrow central groove, and both walls split by deep grooves. External seminal groove entering genital aperture and running along atrium upwards to the fundus, where it merges with the left lateral wall of the fundus. Seminal duct discharging into fundus apically. Two retractor muscles; one connected seminal duct to mantle, the other to lower region of atrium.

Egg-mass ( Figs 2D, E ; 3F )

Yellowish in colour, gelatinous, cylindrical-elongated, with short stalk attaching it to substrate. Egg-masses observed in February of 2016, 2017 and 2018 (SA, pers. obs.). First occurrences in late January and greatest abundance observed in mid-February before declining. Egg-masses mostly found in shallow submerged areas ( Fig. 2E ).

Ecology ( Fig. 2 )

Specimens were found between December 2017 and March 2018 on intertidal estuarine muddy-sandy flats (between the high- and mid-tidal zones) with oyster reefs formed by giant oysters Magallana gryphoides ( Schlotheim, 1820) , backwater oysters Magallana bilineata ( Röding, 1798) , green algae ( Ulva spp., Oedogonium sp.), and red algae ( Acanthophora sp., Gelidium sp.) (Aslam pers. obs.) ( Fig. 2C ).

REMARKS

Bergh (1901) did not differentiate between the prostate and the seminal duct in his study of H. fusca , yet, despite their resemblance these are discrete organs as demonstrated in the current study ( Fig. 4A ). Bergh (1901) described H. fusca as possessing a glans (penis) in the “penissack”, but like in all other known Haminoea of IWP origin (e.g. Er. Marcus & Burch 1965; Rudman 1971; Gosliner & Behrens 2006), H. fusca has no penis or penial papilla enveloped by a penial sheet, but instead a hollow atrium with a modified upper part here named “fundus” (sensu Er. Marcus & Burch 1965). The fundus has thick walls forming folds resembling a penial papilla ( Fig. 4B ).

The limited research available on the genus Haminoea and ambiguous original descriptions of most IWP species often hampered authors to identify correctly the species.For example, Strack (1998: Indonesia), Ng & Sivasothi (2001: Singapore), Lozouet & Plaziat (2008: the Philippines), Riek (2013, 2014: Australia) referred to H. fusca as Haminoea sp., whereas Hung (2013) has named it Haloa vitrea (from China) and Mujiono (2016) Haminoea tenera (from Indonesia). Both latter species are of doubtful taxonomic validity and are known only from their original descriptions. Ullah et al. (2018) tentatively named specimens from mangroves in Korangi and Sandspit, Pakistan as Haminoe exarata , which could corresponded to H. fusca , since Bullacta exarata (correct spelling and combination) is endemic to the China Sea.

Yonow & Jensen (2018) have recently described the species H. edmundsi from Ambon, Indonesia based on features of the external morphology, colouration, and shells (no anatomical details were included). The authors claim that the animal did not resemble any extant species of Haminoea , but the image included in the work is a perfect match with live images of H. fusca ( Gosliner et al. 2008; 2015; Hung 2013; Riek 2013, 2014, Mujiono 2016; Cobb 2018), and thus we here consider that H. edmundsi could be a junior synonym of H. fusca . However, the genetic distance found between the specimens from Pakistan and the one from the Philippines (COI uncorrected p -distance = 7.3-7.5%; Fig. 1 ) suggests the possible occurrence of cryptic species under the name Haminoea fusca , but this requires additional specimens covering the geography of the species in order to be properly tested.

At present in WoRMS (consulted 24.XI.2018) “Pease, 1863” is mentioned as the authority of Haminoea fusca , but this is a mistake originated from Habe & Kira (1968) and later repeated by Gosliner et al. (2008) and Willan & Tagaro (2010) the latter being cited as the information source by WoRMS as their source information.

Figures

FIG. 2. — A, Hab River delta, Sindh Province, Balochistan Coast, Pakistan, showing estuary and associated oyster reefs; B, Haminoea cf. fusca (A. Adams, 1850) in situ; arrows show faecal matter tracks over muddy substrate; C, H. cf. fusca in situ, amongst green algae; D, egg-mass in situ, attached to muddy substrate; E, egg-mass in situ, submerged during low tide. Photograph: S. Aslam.

FIG. 3. — Haminoea cf. fusca (A. Adams, 1850): A, live specimen,ex situ. Length c. 10 mm; B, shell, apertural view (left image) and adepertural view (right image), height, 7 mm; C, SEM, detail of radula with rachidian and first lateral teeth; D, lateral view of whole gizzard plate; E, SEM, dorsal surface of whole gizzard plate; F, SEM, detail of rodlets in dorsal part of gizzard plate. Scale bars: C, 20 µm; D, E, 100 µm; F, 2 µm.

FIG. 4. — Haminoea cf.fusca (A.Adams,1850):A, external view of male reproductive system,arrow denotes lateral bulge; B, detail of interior of atrium and fundus; C, figures modified from Bergh (1901: pl. 18, figs 44, 47, pl. 19, figs 4, 5), detail of radula with “a”: central rachidian (pl. 18, fig. 44); detail of surface of gizzard plate (pl. 18, fig. 47); male reproductive system, “a”: prostate (pl. 19, fig. 5); lateral view of gizzard plate (pl. 19, fig. 4); D, egg-mass. Abbreviations: as, atrium sheet; at, atrium; bc, body cavity; cg, central groove; fu, fundus; ga, genital aperture; llw, left lateral wall; lwg, grooves of lateral walls; pr, prostate; rlw, right lateral wall; rm, retractor muscles; sd, seminal duct; smg, seminal groove; w, soft warts. Scale bars: A, B, 0.5 mm; D, 1 cm.

FIG. 1. — Bayesian phylogenetic tree based on partial sequences of the COI gene.Figures on nodes are posterior probabilities,scale bar refer to branch lengths. Coloured squares refer to species that are Indo West Pacific in origin, whereas grey squares to Atlantic and eastern Pacific species. PP, 1. The specimen here used from the Philippines is depicted in Gosliner et al. 2015: 30, lower right.