Research Article |
Corresponding author: Nicholas Wei Liang Yap ( cosmogony84@gmail.com ) Academic editor: James Reimer
© 2019 Nicholas Wei Liang Yap, Ria Tan, Clara Lei Xin Yong, Koh Siang Tan, Danwei Huang.
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:
Yap NWL, Tan R, Yong CLX, Tan KS, Huang D (2019) Sea anemones (Cnidaria, Actiniaria) of Singapore: redescription and taxonomy of Phymanthus pinnulatus Martens in Klunzinger, 1877. ZooKeys 840: 1-20. https://doi.org/10.3897/zookeys.840.31390
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Despite the ubiquity of sea anemones (Cnidaria: Actiniaria) in tropical ecosystems, our understanding of their biodiversity and taxonomy is limited. Here we re-establish the identity of an intertidal zooxanthellate species, Phymanthus pinnulatus Martens in Klunzinger, 1877. Originally described from a single preserved specimen in the Berlin Museum by CB Klunzinger, his brief footnote lacked crucial details to positively identify the species. Our redescription is based on more than 50 living individuals of P. pinnulatus collected from its type locality, Singapore. These were examined and compared with type materials of the species and its congeners. Specimens of P. pinnulatus differ from syntypes of species described as Phymanthus levis Kwietniewski, 1898 from Indonesia, as well as Phymanthus sansibaricus Carlgren, 1900 and Phymanthus strandesi Carlgren, 1900, both described from East Africa. Phymanthus pinnulatus was encountered on the lower intertidal, among coral rubble and between rocky crevices. It is vibrantly coloured and has 96 marginal tentacles with branching outgrowths along each, resulting in a ‘frilly’ appearance. The anemone has a flat expanded oral disc, with discal tentacles that are inconspicuous and reduced, unlike syntypes of its congeners. Details of its live appearance, musculature, and cnidom are also provided for the first time. Overall, types of cnidae and capsule sizes differ from other known species of Phymanthus documented elsewhere. It is inferred that P. pinnulatus has a wide distribution that extends eastwards from Singapore, as far as Ambon and the Torres Straits. Some individuals reported as Phymanthus muscosus Haddon and Shackleton, 1893 and Phymanthus buitendijki Pax, 1924 are probably P. pinnulatus. This morphological analysis provides new insights into the characters used to delimit P. pinnulatus, clarifies its geographical distribution, and contributes to an ongoing revision of the genus Phymanthus.
Actinoidea, Indo-Pacific, intertidal, Southeast Asia, zooxanthellae
Sea anemones (Cnidaria, Actiniaria) are ecologically successful invertebrates found in many tropical marine ecosystems. In spite of their ubiquity, few from the Indo-Pacific region have been subjected to rigorous taxonomic studies, and the identities of many species remain poorly defined (
Klunzinger’s footnote (1877) provided no further details or illustrations to support his description. Since then, the taxonomic validity of P. pinnulatus’ appearance has remained equivocal, with no illustrations or taxonomic work published thereafter to ascertain the identity of the species. Here we provide for the first time in over a century since
We encountered P. pinnulatus at the lower intertidal zone, where its lower column was buried in sand or wedged between crevices of silt covered rocks and/or coral rubble. These anemones were very conspicuous and common in the northern and southern shores of Singapore. They were also easily recognizable in the field because of the frilly and colourful appearance of its marginal tentacles.
Prior to this study, 25 anemones which are well known taxonomically were identified from Singapore (see
All anemones we report here were collected from Singapore over 16 years: between 2002 and 2018. Some animals were observed in situ and photographed; others were brought back to the laboratory for further study. Collected anemones were kept alive for at least one week. Details on their behaviour and appearance of the living animal were noted. Thereafter, the whole animal was fixed in 10% formalin. Internal morphology was examined in dissected specimens. Musculature of the anemones was visualized from 8-µm-thick histological sections stained with haematoxylin and eosin (
Unfired cnidae capsules were examined from tissues of the marginal tentacle tip, protuberances, discal tentacles, marginal projections, mid-column, actinopharynx, and mesenterial filaments. Cnidae were viewed at 1000 × magnification. We also examined discharged capsules from living specimens, to confirm identities of cnidae encountered (see
We examined the holotype of P. pinnulatum, kept as two separate lots—one at the Museum für Naturkunde Berlin (
To further establish the identity of P. pinnulatus and to delineate the species, available and accessible type material of its congeners were examined: Phymanthus buitendijki Pax, 1924 present at the Rijksmuseum van Natuurlijke Historie and Naturalis (
We relied on published descriptions of Phymanthus crucifer (Le Sueur, 1817), Phymanthus loligo (Hemprich & Ehrenberg in Ehrenberg, 1834), Phymanthus pulcher (Andrès, 1883) and Phymanthus rhizophorae (Mitchell, 1890) to obtain details of their appearance and morphological traits. The types of P. pulcher and P. rhizophorae could not be located (
While syntypes of both P. crucifer and P. loligo do exist and are present at the Museum of Zoology, Lund University (
Because uncertainty still lies with distinguishing the two genera of Phymanthidae (i.e., Phymanthus and Heteranthus; see
All new P. pinnulatus voucher specimens collected from Singapore for this study since 2002 were deposited in the Zoological Reference Collection, Lee Kong Chian Natural History Museum, National University of Singapore (
Phymanthus pinnulatum Martens in Klunzinger, 1877: 87 (original description).
Phymanthus pinnulatum:
Phymanthus pinnulatus:
(Fig.
Berlayer Creek (ZRC.CNI.1343 x4*), Big Sister’s Island (ZRC.CNI.0982 x1; ZRC.CNI.1103 x1*; ZRC.CNI.1163 x1*; ZRC.CNI.1045 x1*; ZRC.CNI.1347 x4*), Changi East Beaches (ZRC.CNI.1084 x1*; ZRC.CNI.1106 x1*), Chek Jawa (photographed but not collected), Cyrene Reef (ZRC.CNI.1089 x1*; ZRC.CNI.1112 x2*; ZRC.CNI.1145 x1*; ZRC.CNI.1342 x4*), East Coast Park Beaches (ZRC.CNI.1039 x1*; ZRC.CNI.1046 x1*; ZRC.CNI.1110 x1*), Kusu Island (ZRC.CNI.1162 x1*), Pulau Hantu (ZRC.CNI.0015 x1; BMNH1995.1006 x1; CASIZ161242 x1), Pulau Jong (BMNH1996.355 x1), Pulau Sekudu (ZRC.CNI.0738 x1), Pulau Semakau (ZRC.CNI.1031 x1*; ZRC.CNI.0318 x1; ZRC.CNI.0321 x1; ZRC.CNI.0322 x1; ZRC.CNI.0639 x1; ZRC.CNI.1098 x1*; ZRC.CNI.1361 x1*), Pulau Tekukor (ZRC.CNI.0993 x3*, of these only one has reduced protuberances; BMNH1996.313 x1; ZRC.CNI.1306 x1*), Sentosa (Tanjong Rimau) (ZRC.CNI.1345 x4*), St John’s Island (ZRC.CNI.0467 x1), Tanah Merah (photographed but not collected), Terumbu Bemban (ZRC.CNI.1223 x1*), Terumbu Pempang Tengah (ZRC.CNI.1028 x1*; ZRC.CNI.1029 x1*), Terumbu Raya (ZRC.CNI.1111 x1*), Terumbu Semakau (ZRC.CNI.0493 x1).
Map of Singapore where specimens of Phymanthus pinnulatus were collected for this study: 1, Berlayer Creek (1°15'56"N; 103°48'25"E); 2, Big Sisters’ Island (Pulau Subar Laut) (1°12'50"N; 103°50'05"E); 3, Changi East Beaches (1°18'45"N; 104°00'31"E); 4, Chek Jawa (1°24'25"N; 103°59'23"E); 5, Cyrene Reef (Terumbu Pandan) (1°15'28"N; 103°45'19"E); 6, East Coast Park Beaches (1°17'36"N; 103°53'46"E); 7, Kusu Island (Pulau Tembakul) (1°13'25"N; 103°51'39"E); 8, Pulau Hantu (1°13'35"N; 103°45'03"E); 9, Pulau Jong (1°12'54"N; 103°47'12"E); 10, Pulau Sekudu (1°24'19"N; 103°59'17"E); 11, Pulau Semakau (1°11'58"N; 103°45'31"E); 12, Pulau Tekukor (1°13'51"N; 103°50'18"E); 13, Sentosa (Tanjong Rimau) (1°14'47"N; 103°49'56"E); 14, St John’s Island (1°13'17"N; 103°50'55"E); 15, Tanah Merah (1°18'45"N; 103°59'34"E); 16, Terumbu Bemban (1°12'36"N; 103°44'27"E); 17, Terumbu Pempang Tengah (1°13'33"N; 103°43'50"E); 18, Terumbu Raya (1°12'46"N; 103°45'09"E); 19, Terumbu Semakau (1°12'46"N; 103°46'07"E).
Holotype, ZNB Cni 1324, collected by E. von Martens. A single specimen, 60 mm in length, flaccid, cut longitudinally, a slice of the distalmost margin and part of the proximal end missing, though a little of the pedal disc remains, cream-coloured entirely (Fig.
Holotype of Phymanthus pinnulatum Martens in Klunzinger, 1877 A entire specimen present at the Museum für Naturkunde, Berlin (
Usually encountered during low tide, with upper portion exposed, oral disc and marginal tentacles expanded (Fig.
Living specimens of Phymanthus pinnulatus, external morphology of oral end A expanded individual of green “banded” colour morph, in situ. Photograph by R Tan B an expanded slaty-green “plain” coloured individual, with extensive branching of its protuberances, in situ. Photograph by R Tan C a third colour morph with brilliant electric blue marginal tentacles, in situ. Photograph by NWL Yap D a partially contracted individual in situ, with its oral end protruding from the substratum; note longitudinal rows of verrucae along intermesenterial spaces, extending proximally from the oral end towards mid column, in situ. Photograph by R Tan.
96 in total; one individual with 98 (ZRC.CNI.1342). All of similar length, equal to oral disc radius or longer (Figs
Marginal tentacle and marginal projection appearance of Phymanthus pinnulatus A close-up of ramified protuberances of a living specimen. Photograph by NWL Yap B close-up of protuberances from a fixed specimen (ZRC.CNI.1345); note that finer details of protuberance branching are lost in preserved/fixed specimens, branching of protuberances now appear as knobs. Photograph by NWL Yap C a morphotype of that lacks ramified protuberances. Note that this individual (ZRC.CNI.1029) is atypical as it has lesser marginal tentacles, by which are also octo-ramously arranged. Photograph by NWL Yap. D a “smooth” tentacle morphotype, in situ. Photograph by R Tan E close-up of a marginal tentacle tip from a fixed specimen (ZRC.CNI.1342). Note absence of perforation at tip F close-up of a row of marginal projections of a fixed specimen (ZRC.CNI.1342). Note perforations (arrowed). Abbreviations: mt, marginal tentacles; mtt, marginal tentacle tip; p, protuberances. Photographs by NWL Yap.
Colour variable, from tan to translucent white. Distalmost end dark-brown. May appear whitish or cream-coloured in life, or with a light green tinge in preserved specimens. Distalmost end flared outwards when animal is expanded; mid-section uniform diameter; pedal end may spread outwards when animal is attached to a surface. Diameter of distalmost end greater than pedal disc. Marginal projections present along margin of distalmost end; may be inflated, perforated (Fig.
Outline round, flat when fully expanded; diameter 40 mm or greater. Colour in life grey to dark brown, with white markings flanking outwards; in fixed specimens, cream-coloured to translucent white. Discal tentacles present, arranged in radial rows extending from mouth to marginal tentacles, both endo- and exocoelic, numerous in a row (Fig.
Detail of the oral discs of Phymanthus pinnulatus, external morphology A top view of discal tentacles present on a live individual, arranged as radial rows between intermesenterial spaces, extending from the mouth towards the region of the marginal tentacles (ZRC.CNI.1361) B side view of discal tentacles of a living specimen; note the low and reduced elevation of tentacles (ZRC.CNI.1046) C faint and reduced radial rows of discal tentacles (arrowed) present on a recent, formalin-fixed specimen (ZRC.CNI.1345) D very reduced and barely noticeable remnants of discal tentacles (arrowed) present on the holotype (NRS76); note that this specimen was preserved before 1877. Abbreviations: m, mesenteries; mt, marginal tentacles. Photographs by NWL Yap.
Oval, flat, same colour as proximal section of column. Thin-walled, mesenterial insertions appear as radiating white lines. Strongly adherent; readily attaches to surfaces to follow contour of substratum.
Actinopharynx longitudinally pleated, extends proximally until mid-column. Oral and marginal stomata present. Mesenteries contain zooxanthellae, arranged in three orders. All 12 pairs of highest order complete, fertile and with filaments; two of these directives, each attached to a siphonoglyph. Mesenteries of second order incomplete, but all fertile with filaments, 12 pairs. In one individual (ZRC.CNI.0467) nine pairs of imperfect mesenteries were present in the second order. Twenty-four pairs of mesenteries small, without filaments and retractor pennon make up third order. All mesenteries, except smallest, extend to the proximal end. Sphincter muscle absent (Fig.
Internal musculature of Phymanthus pinnulatus A longitudinal section of ZRC.CNI.0321 at the margin, showing lack of marginal sphincter muscle. Fosse is indicated by a black star B cross-section of ZRC.CNI.0993. Note the presence of well-developed retractor muscles (white star), and oocytes. Abbreviations: a, actinopharynx; d, directives; mp, marginal projection; mt, marginal tentacle; pb, parietolbasilar muscle. Scale bar: 10 mm. Photographs by NWL Yap.
Spirocysts, basitrichs, microbasic p-mastigophores (Table
Singapore (
Cnidom of Phymanthus pinnulatus Martens in Klunzinger, 1877. Measurements in μm; size outliers of single capsules are presented in values within parentheses. Abbreviations: N = the number of specimens having that type of cnidae to total specimens examined; n = total number of capsules measured for each type. Letters in parentheses following cnidae type refer to its illustration in Fig.
Tissue | Cnidae | Phymanthus pinnulatus Martens in Klunzinger, 1877 | ||
Range length × range width | N | n | ||
Marginal tentacles | Spirocysts (A) | 13.5–26.5(27.5) × 2.0–4.2 | 9/9 | 91 |
Basitrichs (B) | 14.7–25.7(26.5) × 2.0–3.7(4.7) | 9/9 | 93 | |
Protuberances | Spirocysts (C) | (10.0)13.0–24.0 × 2.0–4.0 | 9/9 | 90 |
Basitrichs (D) | 11.0–21.0 × 2.0–3.0 | 9/9 | 100 | |
Discal tentacles | Spirocysts (E) | 14.0–26.0 × 2.0–4.5(5.0) | 9/9 | 90 |
Basitrichs (F) | (8.0)10.0–19.0 × 2.0–3.0 | 9/9 | 90 | |
Marginal pseudoacrorhagi | Basitrichs (G) | 12.0–17.0 × 2.0–3.0 | 9/9 | 100 |
Column | Basitrichs (H) | 13.0–23.1(25.0) × 2.0–3.7(4.2) | 9/9 | 100 |
Actinopharynx | Basitrichs (I) | 11.5–25.5 × 2.0–4.5 | 9/9 | 100 |
Microbasic p-mastigophores (J) | 14.7–25.7 × 4.0–7.9 | 9/9 | 88 | |
Mesenterial filaments | Small basitrichs (K) | 10.0–23.1 × 2.0–3.7 | 9/9 | 92 |
Large basitrichs (L) | (26.3)27.0–38.0 × (2.6)3.0–4.7 | 9/9 | 91 | |
Microbasic p-mastigophores (M) | 15.8–25.0 × (2.5)3.5–5.5(6.3) | 9/9 | 92 |
Of the 53 specimens collected in this study and those examined in situ, we encountered five individuals having reduced protuberances. These morphotypes were only encountered along the southern Singapore shores.
While
A feature that unites pieces of holotype (i.e.,
The inconspicuous and reduced form of discal tentacles in P. pinnulatus is distinct from its congeners depicted in primary scientific literature, and of type materials we studied. Those of P. crucifer, P. loligo, and P. rhizophorae are illustrated to be conspicuous and papilliform (see P. crucifer: Durden 1900: pl 10, fig 1; P. loligo:
On P. muscosus found nearby (i.e., Indonesia and northern Australia),
Discal tentacle form appeared to be consistent for all P. pinnulatus type and voucher materials examined here. We propose that this trait could be a stable character to help infer and define species boundaries for members of Phymanthus. As of writing, many members of this genus remain poorly described; whether the discal tentacle form is truly a useful trait to define species boundaries among members of Phymanthus warrants further study.
In this study, we report upon the cnidom of P. pinnulatus (Table
Intraspecific morphotypes of Phymanthus anemones have been widely documented in primary scientific literature, with reports focused on P. crucifer’s variable appearance of protuberances (see
Little is known about the biology and ecology of Phymanthus anemones. On reproduction,
As stated on the onset, the family Phymanthidae consists of two valid and extant genera, Phymanthus and Heteranthus (
However, in his diagnosis of Heteranthus,
In Table
Comparison of discal tentacle form, cnidom, and type localities of eight Phymanthus species. The symbol “×” indicates that the trait was found; “?” indicates that the trait was not examined in detail when the animal was first described and thereafter; a blank denotes that the trait was not observed from the species at all. Abbreviations: a, actinopharynx; c, column; pt, protuberances; dt, discal tentacles; mf, mesenterial filaments; mp, marginal projection; mt, marginal tentacles.
Morphological traits | Phymanthus species | |||||||||
pinnulatus | levis | strandesi | sansibaricus | crucifer | loligo | pulcher | rhizophorae | |||
Discal tentacle form | Papilliform | × | × | × | × | ? | × | |||
Conspicuous | × | × | × | × | × | ? | × | |||
Reduced | × | ? | ||||||||
As a stunted tentacle | × | ? | ||||||||
Cnidae | Basitrichs | a | × | × | × | × | × | ? | × | ? |
c | × | × | × | × | × | ? | × | ? | ||
pt | × | × | × | × | × | ? | ? | ? | ||
dt | × | × | × | × | × | ? | ? | ? | ||
mf | × | × | × | × | × | ? | × | ? | ||
mp | × | × | × | × | × | ? | ? | ? | ||
mt | × | × | × | × | × | ? | × | ? | ||
Microbasic p-masti-gophores | a | × | × | × | × | × | ? | ? | ||
c | × | ? | ? | |||||||
pt | ? | ? | ? | |||||||
dt | ? | ? | ? | |||||||
mf | × | × | × | × | × | ? | × | ? | ||
mp | × | ? | ? | ? | ||||||
mt | ? | ? | ||||||||
Microbasic b-masti-gophores | a | ? | ? | |||||||
c | ? | ? | ||||||||
pt | ? | ? | ? | |||||||
dt | ? | ? | ? | |||||||
mf | ? | × | ? | |||||||
mp | ? | ? | ? | |||||||
mt | ? | ? | ||||||||
Spirocysts | a | ? | × | ? | ||||||
c | ? | ? | ||||||||
pt | × | × | × | × | × | ? | ? | |||
dt | × | × | × | × | × | ? | ? | |||
mf | ? | ? | ||||||||
mp | ? | ? | ||||||||
mt | × | × | × | × | × | ? | × | ? | ||
Type locality | Singapore | Indonesia | East Africa | Caribbean | Red Sea | Mediterranean | Indonesia | |||
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The persistent and productive efforts of the “Anemone Army,” from 2002, led to many of the specimens listed in this study. We thank those involved for their continued assistance over many years, especially during very early morning fieldtrips. Permissions granted to examine types and voucher specimens were crucial to the success of this study. For this, NWL Yap thanks the personnel from each of the following institutions: (