Research Article |
Corresponding author: Salinee Khachonpisitsak ( salineek@go.buu.ac.th ) Academic editor: Kai Horst George
© 2019 Woranop Sukparangsi, Ashitapol Pochai, Chinnakit Wongkunanusorn, Salinee Khachonpisitsak.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Sukparangsi W, Pochai A, Wongkunanusorn C, Khachonpisitsak S (2019) Discovery of Neonrosella vitiata (Darwin) and Newmanella spinosus Chan & Cheang (Balanomorpha, Tetraclitidae) from the Andaman Sea, eastern Indian Ocean. ZooKeys 833: 1-20. https://doi.org/10.3897/zookeys.833.30689
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In this present study, distantly related acorn barnacle species in the subfamily Newmanellinae (Cirripedia, Thoracica, Tetraclitidae), including Neonrosella vitiata (Darwin, 1854) and Newmanella spinosus Chan & Cheang, 2016, were discovered in the Andaman Sea of Thailand. Neo. vitiata can be readily distinguished from other newmanellids by shell plate and operculum morphology (external shell, tergum geometry, and pattern of parietal tube) and arthropodal characters (presence of basi-dorsal point at base of penis and triangular spines on cirri, setal type, and mouth parts). Both species were found to share overlapping territories on rocks at the rockweed zone, an area submerged under seawater most of the time throughout the year. This study highlights the first discovery of Neonrosella in the eastern Indian Ocean, whose ultrastructure compared to Newmanella is redescribed and illustrated here based on scanning electron microscopy.
Acorn barnacle, Cirripedia, Crustacea, Newmanellinae, Sessilia
The genus Neonrosella Jones, 2010 contains only one species, Neonrosella vitiata (Darwin, 1854). This species was placed and repositioned in different taxa of family Tetraclitidae. Originally, it was described in the genus Tetraclita Schumacher, 1817 belonging to subfamily Tetraclitinae Gruvel, 1903, as Tetraclita vitiata by
Later, a revision of species of the superfamily Tetraclitoidea Gruvel, 1903 was done by
Afterwards,
Recently, the subgenus Neonrosella was elevated to generic level by
The genus Newmanella was established by
A recent examination of acorn barnacle specimens from the Andaman Sea, southern Thailand, recognized two morphologically similar newmanellin species from the same area of the Na-Tai rocky shore (Phang-Nga Province); Neonrosella vitiata is new to Thailand and Newmanella spinosus is found next to Neo. vitiata at lowest low tide point. Both species are redescribed herein, based on shell plate morphology and arthropodal characters using scanning electron microscopy (SEM). This is also the first illustration of Neo. vitiata in its ultrastructure, providing clear observation of this barnacle for taxonomic identification. Both species are compared with the detailed redescription of New. radiata provided by
This study is based upon material collected from the Andaman Sea at Na-Tai rocky shore, Phang-Nga Province, southern Thailand, in March 2018. Samples were collected by hand picking and were transferred into plastic containers containing 95% ethanol. In the laboratory, specimens were transferred into clean 95% ethanol for storage. Specimens were examined under a compound microscope and stereomicroscope and later selected for dissection. All taxonomically important characters, shell plate morphology, and arthropodal characters were dissected and investigated with LEO 1450 VP scanning electron microscope on gold-coated specimens at Microscopic Center, Faculty of Science, Burapha University.
Specimens are preserved in 95% ethanol and have been deposited in the Zoological Collections of Burapha University, Thailand (ZCBUU).
The general terminology of the shell morphology and arthropodal characters follows
ZCBUU Zoological Collections of Burapha University, Thailand
Neonrosella vitiata (Darwin, 1854)
Tetraclita vitiata
Darwin, 1854: 340–341, Pl. 11, fig. 3a-e;
Tetraclita (Tetraclita) vitiata:
Newmanella vitiata
(Darwin, 1854) Yamaguchi, in
Yamaguchiella (Rosella) vitiata
(Darwin, 1854):
Yamaguchiella (Neonrosella) vitiata
(Darwin, 1854):
13 specimens, southern Thailand, Andaman Sea in the eastern Indian Ocean, Phang-Nga Province, Na-Tai District, Na-Tai rocky shore, 20 Mar 2018, A Pochai leg. ZCBUU-CP-024-036.
Parietes white with dark orange spots or longitudinal stripes. Tergum with broad spur. Area with lateral tergal depressor crests on basal margin long and carrying numerous and deep crests. Lateral scutal depressor crests numerous and deep. Cirrus II with equal rami. Cirrus III antenniform in both rami; lesser curvature with hook-like spines. Lesser curvature of cirrus IV without spines. Maxillule with two large spines and two smaller spines before notch; five pairs of spines and a cluster of 12 spines after notch. Mandible with five teeth; the third teeth tridentate; the fourth teeth quadridentate and the fifth teeth close to the fourth teeth; seven smaller setae on lower margin; without setae under inferior angle. Labrum with three canine-like teeth on each cutting margin. Penis with basi-dorsal point.
Peduncle absent. Body length 2–3 cm. Shell white with orange longitudinal lines; low conic; composed of four shell plates including one carina, two laterals, and one rostrum (Fig.
Shell plate and operculum morphology of Neonrosella vitiata (Darwin, 1854) A anterior view of shell B basal view of shell without body tissue C basal view of shell with body tissue intact D external view of individual shell plates (parietes) E internal view of individual shell plates F (left) close-up on external view of operculum (right) internal view of intact operculum G external view of operculum (one side of both tergum and scutum) H internal view of operculum (one side of both tergum and scutum) I–L tergum I external view J internal view K SEM of internal view L close-up on crests for lateral tergal depressor muscle M)–R) scutum M external view N internal view O SEM of internal view P close-up of crests at edge of basal margin (bm) close to occludent margin (om) Q close-up of crests for lateral scutal depressor muscle R close-up of articular ridge (ar).
Cirrus I with unequal rami; anterior ramus (20-segmented) length longer than that of posterior ramus (10-segmented), approximately 2.5 times (Fig.
SEM showing cirral morphology of Neonrosella vitiata (Darwin, 1854) A–E cirrus I A overview of cirrus I morphology B close-up at proximal region of cirrus I C serrulated seta on posterior side of protopod D serrulated seta on anterior ramus E serrulated seta on posterior ramus F–K cirrus II F overview of cirrus II morphology G posterior ramus H anterior ramus Iserrulated seta on posterior ramus J serrulated setae on anterior ramus K serrulated seta on anterior side of protopod L–U cirrus III L overview of cirrus III morphology M close-up on basipod and protopod N plumose seta on posterior side of basipod O plumose seta on anterior side of protopod P anterior seta on anterior ramus Q posterior seta on posterior ramus R posterior ramus S anterior ramus T close-up on posterior ramus showing spines on lesser curvature U close-up on anterior ramus showing spines on lesser curvature. Abbreviations: pr, protopod; bs, basipod; pos, posterior ramus; ant, anterior ramus. Scale bars in µm.
SEM showing cirral morphology of Neonrosella vitiata (Darwin, 1854) A–G cirrus IV A overview of cirrus IV morphology B close-up at basis and protopod C basipod with spines D greater curvature of both rami E close-up on spines on posterior ramus F lesser curvature of posterior ramus (1, 2 and 3 indicating first pair of long serrulated setae-longest, second pair of serrulated setae-second longest and third pair of simple setae-shortest, respectively) G lesser curvature of anterior ramus (number described as F) H–N cirrus V H overview of cirrus V morphology I proximal region showing greater curvature of both rami J close-up on greater curvature of posterior ramus carrying spines K basipod with spines L lesser curvature of anterior ramus M close-up on a segment on lesser curvature of anterior ramus showing type of setae (inset showing serrulated setae and number as described in F) N lesser curvature of posterior ramus (number as described in F) O–V cirrus VI O overview of cirrus VI morphology Q greater curvature of posterior ramus R greater curvature of both rami S basipod with spines T close-up on spines on posterior ramus U lesser curvature of anterior ramus V lesser curvature of posterior ramus (number described as F). Abbreviations: pr, protopod; bs, basipod; pos, posterior ramus; ant, anterior ramus. Scale bars in µm.
Maxilla bi-lobate; upper lobe covered with densely packed serrulated setae; lower lobe with a few serrulated setae carrying more packed setules (Fig.
SEM showing mouth parts of Neonrosella vitiata (Darwin, 1854) A–C maxilla A overview of maxilla morphology B serrulated setae on upper lobe C serrulated setae on lower lobe D–E maxillule D overview E spines and serrulated setae on inferior angle F–H mandible F overview of mandible morphology and inset showing close-up of lower margin G bidentate 2nd teeth H tridentate 3rd teeth, quadri-dentate 4th teeth and single 5th teeth I–L labrum I overview of labrum morphology of interior labrum and inset showing close-up of teeth on labrum J close-up of teeth on right side of labrum K close-up on teeth on left side of labrum L exterior side of labrum M–N mandibular palp M overview of mandibular palp morphology N serrulated setae on superior margin O–Q penis O overview of whole penis on side view and inset showing basi-dorsal point (arrow head) on base of the penis P close-up on apex of penis Q annulation along penis. Abbreviations: ul, upper lobe of maxilla; ll, lower lobe of maxilla. Scale bars in µm.
Neonrosella vitiata was collected only during the lowest tide (March) of the year and at the lowest littoral zone, an area submerged most of the time throughout the year. It was found on rocks covered with seaweed, densely packed green and red algae, hydroids, sponges, limpets, other acorn barnacles including Tetraclita species at the algal crust zone of the intertidal region. The barnacles were found mostly in solitary form, in connection with Newmanella spinosus, or with conspecifics as small colonies of only two or three individuals per colony.
Great Barrier Reef (Raine’s Islet), Australia (
Newmanella radiata (Bruguière, 1789). Additional species: New. hentscheli Kolosvary, 1942, New. kolosvaryi Ross & Perreault, 1999, New. spinosus Chan & Cheang, 2016.
Newmanella radiata.
Newmanella
sp.
Newmanella spinosus Chan & Cheang, 2016: 212–220, figs 9–15.
17 specimens, southern Thailand, Andaman Sea in the eastern Indian Ocean, Phang-Nga Province, Na-Tai District, Na-Tai rocky shore, 20 Mar 2018, A Pochai leg. ZCBUU-CP-007-023.
Parietes and opercular plates green on external and internal surfaces. External shell plate with numerous radiating or longitudinal lines extending from apex to base. Scutal margin of tergum with serrated teeth and broad spur with cutting edges. Cirrus II with equal rami and slight curvature of both rami carrying triangular spines. Basis of cirri IV–VI without spines. Greater curvature of both anterior ramus and posterior ramus of Cirrus IV with triangular spines. Mandible with five teeth, the third teeth bidentate, the fourth teeth with serrations and small teeth along the edge, and the fifth teeth sits on the middle of lower margin surrounded by other small spines. Labrum with four teeth on each cutting margin. Penis without basi-dorsal point.
Peduncle absent. Body length 2–3 cm. Shell green with longitudinal folds or lines from orifice toward base or radiating lines; low conic; composed of four shell plates including one carina, two laterals and one rostrum. Base calcareous with parietal tubes; three rows of irregular shape and size of parietal tubes (Fig.
Shell plate and operculum morphology of Newmanella spinosus Chan & Cheang, 2016 A anterior view of shell B basal view of shell with body tissue C external and anterior view of shell without body tissue D internal and basal view of shell plates showing parietal tubes E external view of parietes F internal view of parietes G close-up on orifice and exterior opercular plates H internal view of operculum without intact tissues I internal view (left) and external view (right) of tergum J internal view (left) and external view (right) of scutum.
Cirrus I with unequal rami; anterior ramus (21-segmented) length approx. twice as long as posterior ramus (10-segmented) (Fig.
SEM showing cirral morphology of Newmanella spinosus Chan & Cheang, 2016 A–H cirrus I A overview of cirrus I morphology B close-up at proximal region of cirrus I C close-up on posterior ramus D close-up on anterior ramus E apex of anterior ramus F serrulated setae on anterior ramus G serrulated setae on posterior ramus H plumose setae on posterior side of protopod I–P cirrus II I overview of cirrus II morphology J proximal region of cirrus II K serrulated and bidentate setae on greater curvature of posterior ramus L hook-like triangular spines on lesser curvature of posterior ramus M spines (asterisks) on lesser curvature of anterior ramus N close-up on apex on posterior ramus O serrulated setae on posterior ramus P serrulated and bidentate setae on anterior ramus Q–Y cirrus III Q overview of cirrus III morphology R slender spines on basipod S plumose setae on anterior side of basipod T hook-like triangular spines on lesser curvature of posterior ramus U hook-like triangular spines on lesser curvature of anterior ramus V greater curvature of anterior ramus with spines W serrulated setae and bidentate setae on posterior ramus X serrulated setae on anterior ramus Y bidentate setae on anterior ramus. Abbreviations: pr, protopod; bs, basipod; pos, posterior ramus; ant, anterior ramus. Scale bars in µm.
SEM showing cirral morphology of Newmanella spinosus Chan & Cheang, 2016 A–F cirrus IV A overview of cirrus IV morphology B close-up on proximal region of greater curvature C slender spines on greater curvature of posterior ramus D triangular spines on greater curvature of anterior ramus E close-up on basipod showing denticles without spine F lesser curvature of both rami showing two pairs of long serrulated setae and a pair of simple setae G–J cirrus V G overview of cirrus V morphology H greater curvature of posterior ramus showing spines I greater curvature of both rami (the other side) without spine J close-up on basipod without spine (only denticles) K–N Cirrus VI K overview of cirrus VI morphology L greater curvature of both rami M close-up on slender spines on greater curvature of anterior ramus N close-up on basipod without spine. Abbreviations: pr, protopod; bs, basipod; pos, posterior ramus; ant, anterior ramus. Scale bars in µm.
Maxilla bi-lobate; both lobes covered with serrulated setae (Fig.
SEM showing mouth parts of Newmanella spinosus Chan & Cheang, 2016 A–C maxilla A overview of maxilla morphology showing upper lobe (ul) and lower lobe (ll) B serrulated setae on upper lobe C serrulated setae on lower lobe D–E maxillule D overview of maxillule morphology E serrulated setae on inferior angle of maxillule F mandible (inset showing close up of third-fifth teeth of mandible) G–J labrum G exterior view of labrum H interior view of labrum I teeth on labrum (left margin from H) J teeth on labrum (right margin from H) K mandibular palp L close-up on superior side showing serrulated setae on mandibular palp M–P penis M overview of whole penis on side view and inset showing smooth dorsal side (dash line) on the base of the penis without basi-dorsal point N apex of penis carrying setae O penis with annulation P base of penis. Abbreviations: ul, upper lobe of maxilla; ll, lower lobe of maxilla. Scale bars in µm.
The specimens were collected only during the lowest tide (March) of the year at the lowest tide littoral zone, the same habitat as Neonrosella vitiata.
Western Pacific from Taiwan (type locality) and Philippines (
1 | Low-conic shell plate on calcareous base with four parietes; two layers of parietal tubes (inner laminar with radiating large tubes and outer laminar with three horizontal tubes) (Fig. |
Neonrosella vitiata |
– | Low-conic shell plate on calcareous base with four parietes; multiple layers of parietal tubes; cirrus IV with triangular spines (see Fig. |
2 |
2 | External shell plate white and longitudinal fold from apex to base without colour spots; tergum with narrow spur (see |
Newmanella radiata |
– | External shell plate green; scutal margin of tergum serrated (Fig. |
Newmanella spinosus |
The present study represents the first discovery of Neonrosella vitiata, sharing overlapping habitat with Newmanella spinosus in the Andaman Sea, eastern Indian Ocean. We previously reported a list of new record acorn barnacles in Thailand (the Gulf of Thailand and the Andaman Sea) and New. spinosus was also observed in the low-tide intertidal zone at Na-Tai District, Phang-Nga Province, southern Thailand (
Summary of shell plate morphology and anatomical characters used to diagnose Neonrosella vitiata from two morphologically related Newmanella species New. radiata and New. spinosus. Diagnostic characters to distinguish these three species are marked in bold.
Characters | Neonrosella vitiata (Darwin, 1854) |
Newmanella radiata (Bruguière, 1789) As redescribed in |
Newmanella spinosus Chan & Cheang, 2016 As redescribed in |
Shell plates | Low conical; white with irregular longitudinal dark orange/brownish stripes | Low conical; white with radiating lines | Low conical; green with radiating lines |
Parietal tube | Two layers: inner laminar with larger parietal tubes; outer laminar with three smaller parietal tubes between large parietal tubes from inner laminar | Two layers with irregular size of holes | Three layers |
Tergum | Broad spur with rounded tip; ten lateral depressor crests on long basal margin; scutal margin without serrated teeth | Narrow spur; 4–5 lateral depressor crests on basal margin; scutal margin without serrated teeth | Broad spur with cutting edge; 9–10 Lateral depressor crests on basal margin; scutal margin with serrated teeth |
Scutum | Triangular; height and width equal; deep and numerous lateral scutal depressor crests | Triangular; height and width equal; deep and numerous lateral scutal depressor crests | Triangular; height longer than width by 1.5 times; deep and numerous lateral scutal depressor crests |
Cirrus I | 1. Unequal rami; anterior ramus longer than posterior ramus 2.5 fold | 1. Unequal rami; anterior ramus longer than posterior ramus 2/3 fold | 1. Unequal rami; anterior ramus longer than posterior ramus |
2. Posterior ramus normal/not protuberant | 2. Posterior ramus protuberant | 2. Posterior ramus protuberant | |
Cirrus II | 1. Equal rami | 1. Unequal rami; posterior ramus longer 1.5 fold than anterior ramus | 1. Equal rami |
2. Greater/lesser curvature of both rami without triangular spines | 2. Greater/lesser curvature of both rami without triangular spines | 2. Lesser curvature of both rami with spines | |
Cirrus III | 1. Unequal rami; both antenniform | 1. Unequal rami; only posterior ramus antenniform | 1. Semi-equal rami; both antenniform |
2. Lesser curvature of anterior (only 7-segmented) and posterior rami (only 4-segmented) with triangular spines | 2. Lesser curvature of anterior (entire) and posterior rami (not 3 distal segments) with triangular spines | 2. Lesser curvature of anterior and posterior with triangular spines | |
3. Greater curvature of anterior ramus without spines | 3. Greater curvature of anterior ramus without spines | 3. Greater curvature of anterior ramus with spines | |
Cirrus IV–VI | Basis with triangular spines | Basis with triangular spines | Basis without triangular spines |
Cirrus IV | No triangular spines at greater curvature of anterior ramus | Triangular spines at greater curvature of anterior ramus | Triangular spines at greater curvature of anterior ramus |
Mandible | Five teeth: 1st(1)+2nd(2)+ 3rd(3)+4th(3-4/serrated) +5th(1)+7 small setae+3 larger setae at lower margin | Five teeth:1st(1)+2nd(2)+3rd(2)+4th(2/serrated)+5th(1)+16 setae at lower margin | Five teeth: 1st(1)+2nd(2)+3rd(2)+4th (1/serrated)+5th(1)+12 setae at lower margin |
Labrum | Three teeth on each side of cutting margin | Five teeth on each side of cutting margin | Two large teeth right side and five teeth on left side (in this study – 4 large teeth on right and left sides) |
Penis | Penis long and annulated with basi-dorsal point and at the tip of penis carrying two clusters of simple and long setae | Penis long and annulated without basi-dorsal point | Penis long and annulated without basi-dorsal point |
Neo. vitiata in this study exhibited some similarities in shell plate morphology to Tetraclita vitiata Darwin, 1854 found in Philippines and Indo-west Pacific water, as described in
Across all regions we examined in both the Gulf of Thailand and the Andaman Sea, Neo. vitiata was found only at the rocky shore-rockweed interface of the intertidal zone during the lowest tides, and the only one site for sample collection is Na-Tai, Phang-Nga. However, further investigations of more sampling areas at deeper depths of the intertidal zone are required and they may reveal a subtidal distribution of this species. In addition, the presence of Neo. vitiata in eastern Indian Ocean provides a possible scenario that before sea levels fluctuated by glaciation during the Pleistocene (e.g.,
This work was financially supported by the Research Grant of Burapha University through the National Research Council of Thailand (Grant no. 27/2560). We would like to express our heartfelt gratitude to Prof Frederick William Henry Beamish (Burapha University, Thailand) for his comments and reading through an earlier draft of this paper. We appreciate great review of this manuscript and careful consideration of correct taxonomic identification by Prof Benny KK Chan (Academia Sinica, Biodiversity Research Center, Taiwan). Thanks are due to the Microscopic Center, Faculty of Science, Burapha University for preparation of material for the SEM studies.