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High localised diversity of Halimeda (Chlorophyta: Bryopsidales) in a tropical marine park from Pahang, Malaysia
Regional Studies in Marine Science 31 (2019) 100773
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High localised diversity of Halimeda (Chlorophyta: Bryopsidales) in a tropical marine park from Pahang, Malaysia ∗
Natasha Arina, Mohammad Rozaimi , Nur Farah Ain Zainee Centre for Earth Sciences and Environment, Faculty of Science and Technology, Universiti Kebangsaan, Malaysia, 43600 UKM Bangi, Selangor, Malaysia
highlights • • • •
There were up to five Halimeda species within the surveyed channel. It is uncommon to find such high species richness in a small localised area. Halimeda borneensis was the most common species. Halimeda taenicola is a new record for the eastern coast of Peninsular Malaysia.
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Article history: Received 18 January 2019 Received in revised form 29 July 2019 Accepted 29 July 2019 Available online 1 August 2019 Keywords: Calcareous macroalgae Morphology Biogeographical distribution Southeast asia
a b s t r a c t The chlorophyte genus Halimeda is common in tropical waters but gaps still exist in the understanding of the biogeographical distributions of its species in Southeast Asia, particularly in Malaysia. During a study into the ecological functioning of reefs in a marine park (the Sembilang–Seri Buat group of islands, Pahang, Malaysia) along the eastern coast of Peninsular Malaysia, a previously unreported community of sand-dwelling Halimeda was discovered on a shallow reef flat (water depths of 12 m). We randomly collected 63 individuals and identified them using defining morphological and anatomical characteristics. The collection consisted of Halimeda borneensis, H. discoidea, H. macroloba, H. opuntia, and H. taenicola. Halimeda borneensis was the most collected (52 individual explants) in our study site. We report that H. taenicola is a new record for the eastern coast of Peninsular Malaysia, which is also a first biogeographical report of this species for the area spanning the Gulf of Thailand and towards the coastal areas to the east of Singapore. This study together with past records on Halimeda in the immediate surroundings show a total of six Halimeda species in the area, a localised coastal diversity uncommon to this part of the South China Sea. © 2019 Elsevier B.V. All rights reserved.
1. Introduction Halimeda is a genus of chlorophyte, which can be found in tropical and subtropical regions (El-Manawy and Shafik, 2008). Halimeda diversity is widely reported from the Atlantic Ocean, Pacific Ocean and Western Indian Ocean (Kooistra et al., 2002; Verbruggen and Kooistra, 2004; Verbruggen et al., 2005a,b), but its occurrences in the Eastern Pacific Ocean is relatively underexplored. In Southeast Asia, Halimeda distribution is centred in the Eastern Indian Ocean as well as the Andaman Sea (Pongparadon et al., 2015; Phang et al., 2016). Species are distributed along biogeographic barriers, which prevent the dispersal of genetic material between the regions (Pongparadon et al., 2015). Different regions influence the variations in different Halimeda sections and species including factors such as habitat depth, ∗ Corresponding author. E-mail address: [email protected] (M. Rozaimi). https://doi.org/10.1016/j.rsma.2019.100773 2352-4855/© 2019 Elsevier B.V. All rights reserved.
substrata, light intensity, wave action and currents (Pongparadon et al., 2015). In addition, these limitations are caused by various interacting features such as niche, morphological characteristics, reproductive behaviour and physiological traits (Verbruggen et al., 2009). Long-term survival and adaptation as well as species’ tolerances determine the niche characteristics of Halimeda (Verbruggen et al., 2009). Marine biogeographic barriers such as the Sunda Shelf Barrier restrict the continuity of Halimeda species occurrences between the Western Pacific Ocean and the tropical Indian Ocean (Pongparadon et al., 2015). In Peninsular Malaysia, the western and eastern coasts are affected by the southwest monsoon and northeast monsoon, respectively (Masseran and Razali, 2016; Kok et al., 2017). Species dispersal is impacted by these monsoons due to changes in current and circulation patterns along the South China Sea (Phang et al., 2016) for the eastern coast, and the Malacca Strait for the western coast. Halimeda species are mostly found in shallow waters, which are usually supersaturated with calcium carbonate (Granier, 2012)
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N. Arina, M. Rozaimi and N.F.A. Zainee / Regional Studies in Marine Science 31 (2019) 100773
Fig. 1. Location of the study site marked with an ‘X’ (right). Numbers on the map (left) refer to zonal classification in the appended table and described in the text.
and are either sand-dwelling or rock-dwelling (Hillis-Colinvaux, 1980; Verbruggen et al., 2006). Halimeda are mostly found in reefs (Perry et al., 2016), and a mutual relationship exists with the coral community. In Malaysia, most coral reefs are located in marine parks (Mustapha et al., 2014; Xin et al., 2016) and therefore the presence of Halimeda contributes to the biodiversity and ecological functioning within these areas. They serve as prominent primary producers, a source of food and habitats, and are major contributors to reef formation (Castro-Sanguino et al., 2016; Ximenes et al., 2017). Halimeda species are known to be resilient to grazing as their highly calcified tissues contain halimedatrial, which discourages herbivory (Hay et al., 1994; Hendri et al., 2015). Halimeda species have mineralised skeletons, which secretes calcareous layers on the outside of the cytoplasmic envelope (Granier, 2012). The relatively rapid growth of calcified layers and high turnover rates make these macroalgae major contributors of sediments in reef construction in the form of aragonite deposition (Pongparadon et al., 2015; Ximenes et al., 2017). After senescence, Halimeda mainly yields carbonate sand from their tissue segments (Verbruggen et al., 2009; Xu et al., 2015). These segments provide sediments that contribute to longterm biogenic deposits in the reef environment (Freile et al., 1995). To date, there are 44 species of Halimeda species known worldwide (Guiry and Guiry, 2019). In the South China Sea, there are 20–30 species of Halimeda within the waters of Malaysia, Thailand, Vietnam, Singapore, Philippines, and Indonesia (Phang et al., 2016). Challenges abound in the identification of Halimeda species due to similarities in morphological characteristics and therefore a definitive list of the species present would provide a basis in understanding the ecology and the biogeography of this genus in Southeast Asia. Especially in Malaysia, the genetic connectivity of Halimeda in dispersal is not widely investigated and species occurrences show sparse distribution. In this paper, we describe the Halimeda species found during a study into the ecological functioning of Halimeda in Seri Buat Island, where an unreported community of Halimeda was discovered. We then placed those species in the context of the biogeographical distribution of Halimeda along the western coast of the South China Sea to provide insights into their occurrences in the region.
2. Materials and methods Sampling activities were carried out in April 2018 in a sheltered channel located between Sembilang and Seri Buat Islands (Fig. 1). This channel is about 2–3 km long and shallow with certain portions of sandy elevated areas exposed during low tide. Sediments consist of coral rubble and the average coral coverage was reported to be approximately 44% (Aikanathan and Wong, 1994). During the field assessment, a total number of 63 Halimeda specimens were collected randomly from within this channel at shallow water depths (∼1–2 m) during low tide. Whole thallus (Fig. 2), including below-ground organs were carefully removed from the substrate, placed in plastic bags and transported to the laboratory for further analysis. Specimen identification was carried out by defining external morphological and anatomical characteristics. External traits included the specimen height, segment size, segment shape, basal segment size, structure of margin, surface texture, colour, segment thickness, branching type, and holdfast type. The type of sediment that was attached to the holdfast was also recorded. For anatomical identification, a small segment of Halimeda tissue was decalcified using 20% hydrochloric acid (after Bandeira-Pedrosa et al., 2004). The tissues were then stained with Lactophenol cotton blue stain to distinguish the utricle and medullary filaments. The stained surface, in both longitudinal and cross-sectional views, were observed under a stereo microscope (magnification of 100x and 400x). The characteristics of the utricle and medullary filaments were observed after the decalcified segment was dissected. Species identification was then completed through construction of dichotomous keys based on these characteristics. These characteristics were then compared to existing keys from other studies (Sundararajan et al., 1999; Bandeira-Pedrosa et al., 2004; El-Manawy and Shafik, 2008; Dijoux et al., 2012; Pongparadon et al., 2015) to reaffirm the species identity. 3. Results The 63 specimens collected in this study were identified to be five species based on morphological and anatomical characteristics. These were Halimeda borneensis, H. discoidea, H. macroloba, H. opuntia, and H. taenicola. Halimeda borneensis was the most collected (52 individuals from two morphotypes), followed by H. macroloba and H. discoidea with seven and two individuals, respectively. The least-common species were H. opuntia and
N. Arina, M. Rozaimi and N.F.A. Zainee / Regional Studies in Marine Science 31 (2019) 100773
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50–65 µm in length. Medullary filaments slender, 30–35 µm in breadth with minor branching. Nodal fusions arise from five fused medullary filaments.
Fig. 2. Naturally growing Halimeda at the study site.
H. taenicola (1 individual each). Identification keys for these five species were constructed based on the morphological and anatomical characteristics observed and is explained as follows: Key to Halimeda species 1 1
Segment size large, more than 1.5 cm wide and 1 cm height . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ..H. macroloba Segment size small, less than 1 cm wide and 0.5 cm height . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ... 2
2 2
Segment margin entire for whole plant. . . H. taenicola Segment margin varying from entire, sinuous or undulated . . . . . . . . . . . . ..... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .... 3
3
Segment shape reniform to flabellate with shallowly-lobed surface.... . . . . . . . . . . . . . . . . . H. discoidea Segment shape trilobed to heart-shaped with deeply-lobed surface . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
3
4 4
Segment branching regular, dichotomous and elongated . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . ... H. opuntia Segment branching irregular, polychotomous and form bushy habit . . . . . . . . . . . . . . . . . . . . . . . . . . . H. borneensis
The distinct characteristics of surface view, utricle and medullary filament for each species are illustrated in Fig. 3, and the thallus morphology in Fig. 4. The descriptions of each Halimeda species found in the sampling location are as follows: Halimeda borneensis W.R. Taylor, 1975 – morphotype A Description: Thallus erect forming thick clumps, long and large bulbous holdfast. Vertical growth up to 7 cm, moderately heavy calcification with dark green colour. Segments generally small, 0.5– 1.0 cm in breadth and 0.4–0.6 cm in length. Basal segments subterete to terete, varying from cylindrical to subcylindrical. Segments varying in shape, obovate, cuneate, heart-shaped or trilobed with sinuous to undulated margins. Segment thickness consistent from base to the terminal of thallus. Branching pattern elongated forming a bushy habit. Cortex consisting of three layers of inflated utricles with regular branching pattern. Utricles in surface view arranged in irregular polygons. Primary utricles obovate to cuneate, 9–15 µm in breadth and 10–25 µm in length. Secondary utricles elliptical, 35–45 µm in breadth and 45–55 µm in length. Tertiary utricles truncate, 55–70 µm in breadth and
Halimeda borneensis W.R. Taylor, 1975 – morphotype B Description: Thallus erect, single or gregarious, vertical growth up to 8 cm, arising from large bulbous holdfast about 3–4 cm in length. Moderately heavy calcification with dark green colour. Basal segment flabellate, consisting of two to three fused twisted segments, 0.3– 0.9 cm in breadth and 0.4–0.6 cm in length, with slightly distinct rib-like structure, irregular shape that varies from trilobe, ovate, oval, cuneate and reniform. Segment thickness decreases from base to the terminal portion of thallus. Upper margin deeply lobed with undulated surface. Branching pattern elongated and irregularly polychotomous. Utricles in surface view arranged in irregular polygons. Cortex consisting three layers of cylindricalinflated utricles. Primary utricles short-cylindrical, up to 8–10 µm in breadth and 10–15 µm in length. Secondary utricles cylindrical, 10–18 µm in breadth and 14–20 µm in length. Tertiary utricles elliptical, 25–40 µm in breadth and 30–45 µm in length. Medullary filaments thin, 25–35 µm in breadth, with trichotomous branching in close proximity to each other. Nodal fusions arise from four to five fused medullary filaments. Halimeda discoidea Decaisne, 1842 Description: Plants erect, arise from bulbous holdfast about 3–4 cm long. Thallus forming cushion-like clumps, tufted or loose in habit. Vertical growth up to 7 cm. Heavily calcified segment; yellowish green colour. Basal segments subcylindrical, subcuneate or subterete, discoidal to reniform with flattened smooth surface up to 0.6–1.2 cm in breadth and 0.5–0.6 cm in length. Margins generally entire to shallowly-lobed. Branching usually irregular, either trichotomous or polychotomous from one large segment. Utricles in surface view arranged in regular polygons. Cortex of segment composed of two layers of large and inflated utricles. Utricles large and inflated with regular polygonal shape. Secondary utricles subglobular, 90–120 µm in breadth and 110–150 µm in length, supporting four to five primary utricles, cylindrical, 10– 18 µm in breadth and 10–20 µm in length. Medullary filaments large, 45–55 µm in breadth with less densely branched. Nodal fusions arise from medullary filaments paired in groups of three. Halimeda macroloba Decaisne, 1841 Description: Thallus whitish green, highly calcified, solitary, erect, growth up to 15 cm. Holdfast large bulbous, extending to 5 cm long. Basal segment compressed, flabellate to cuneate, arising from single segment. Segment size about 1.5–2.3 cm in breadth and 1.0–1.5 cm in length, flabellate to reniform, with upper margin shallowly to deeply lobed with undulated surface. Branching pattern irregular polychotomous forming fan-shaped plant. Utricles in surface view arranged in irregular hexagons. Cortex consisting of four layers of utricles. Primary utricles cylindrical-elongated, 8–10 µm in breadth and 20–25 µm in length. Secondary utricles elliptical to obovate, 15–20 µm in breadth and 18–25 µm in length. Tertiary utricles elliptical, 22–35 µm in breadth and 40– 55 µm in length. Medullary filament large, 40–55 µm in breadth. Diameter of medullary filament decreases with constriction at the base of branching. Nodal fusions arise from two to three fused medullary filaments.
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N. Arina, M. Rozaimi and N.F.A. Zainee / Regional Studies in Marine Science 31 (2019) 100773
Fig. 3. Anatomical characteristics of Halimeda species.
Fig. 4. The shape of segments and thalli ramification of Halimeda species: (A) H. taenicola; (B) H. borneensis (morphotype A); (C) H. borneensis (morphotype B); (D) H. opuntia; (E) H. macroloba; (F) H. discoidea.
Halimeda opuntia (Linnaeus) J.V. Lamouroux, 1816 Description: Thallus erect, forming either solitary or thick clumps, spreading laterally from several small rhizoidal holdfast. Plant vertical growth up to 15 cm, light calcification with light green colour. Segments generally small, 0.2–0.5 cm breadth and 0.2–0.3 cm in length, and regular in size throughout the thallus. Basal segment irregular, varying from cylindrical to subcylindrical. Segments with distinct rib, reniform, oblong, heart-shaped or trilobed with shallowly- to deeply-lobed margin, sometimes twisted or crenulated. Branching pattern either elongated or densely-branching
that form bushy habit. Utricles in surface view arranged in irregular polygons. Cortex consisting four to five layers of elongated utricles with irregular branching pattern. Primary utricles shortcylindrical, up to 6–10 µm in breadth and 10–15 µm in length. Secondary utricles oblanceolate, 10–15 µm in breadth and 18– 20 µm in length. Tertiary utricles narrow-truncate, 12–20 µm in breadth and 55–75 µm in length. Fourth layer of utricles cylindrical, 13–18 µm in breadth and 25–30 µm in length. Medullary filaments densely branched, thin, up to 30–40 µm in breadth with less constrictions at branch and main axis is thins towards the lower branch. Nodal fusions arise from medullary filaments paired in groups of two to three.
N. Arina, M. Rozaimi and N.F.A. Zainee / Regional Studies in Marine Science 31 (2019) 100773
Halimeda taenicola W.R. Taylor, 1950 Description: Thallus erect, compact, vertical growth up to 7 cm, arising from small bulbous holdfast. Calcification light with dark green colour. Consists of more than one basal segments that are subcuneate or subcylindrical. Segments varying from lower to the terminal part of thallus. Lower part of thallus about 0.2–0.4 cm in breadth and 0.2–0.3 cm in length, size of segment decreases towards terminal ends. Thallus shape is mixed from the lower segment to the terminal segment; cuneate, subcuneate and ovate, with entire margin. Branching is polychotomous, numerous and elongated. Utricles in surface view arranged in regular polygons. Cortex consisting of three layers of elongated utricles. Primary utricles cylindrical, 8–12 µm in breadth and 15–20 µm in length. Secondary utricles narrow-elliptical, 10–15 µm in breadth and 30–35 µm in length. Tertiary utricles truncate, 30–45 µm in breadth and 50–65 µm in length. Medullary filaments up to 30–45 µm in breadth and have numerous constrictions at the main axis. Nodal fusions arise from medullary filaments paired in groups of three to four. 4. Discussion Detailed observations through morphological and anatomical characteristics classified the Halimeda specimens into five species, which are H. borneensis, H. discoidea, H. macroloba, H. taenicola, and H. opuntia. Although this study was restricted to only one locality, insights into the regional biogeography of Halimeda can be contextualised from this list of previously unreported records. At the study site, Halimeda were found in sandy patches of the coral reefs and all specimens had bulbous holdfasts typical of sand-dwellers. Among these species, H. borneensis was the most dominant, and we report that H. taenicola is a new record for the eastern coast of Peninsular Malaysia. At present, including findings from this study, there has been a total of 10 Halimeda species found in Malaysia (Table 1). In general, the western coast of Peninsular Malaysia has higher diversity compared to the eastern side of the Peninsular coast. The land mass of the Thai-Malay Peninsular limits the sea connectivity between the Indian and Pacific Oceans and therefore is clearly a barrier to population dispersal for Halimeda between the two coasts. Previous studies reported that H. discoidea, H. macroloba, H. opuntia and H. tuna were present on the eastern Peninsular coast while the same species, as well as H. cuneata, H. stuposa and H. taenicola, were present on the western Peninsular coast (Zainee et al., 2018). In recent Halimeda records in waters bordering Malaysia, the average number of species in the designated zones 1 to 14 (Fig. 1) is 4 to 5 (Table 1). The diversity of species found in our study site is therefore above-average but not the highest in this region. To date, it still stands that the highest localised Halimeda diversity (10 species; Table 1) among these zones was in the Riau Archipelago while in Malaysia it is in Sabah waters. In the latter, H. macrophysa and H. velasquezii were restricted to Borneo and are unlikely to be found on the peninsular coasts. To the south of the peninsular, H. gracilis and H. papyracea have been reported in Singapore waters (Pham et al., 2011) and, due to its proximity, it is possible that future surveys in the southern parts of Peninsular Malaysia may find the same species. The high diversity of Halimeda in the channel that formed a relatively small sandy area at the study site shows an apparent hotspot for members of this genus. Xu et al. (2015) described that Halimeda is highly adaptive to variable environmental conditions in the tropics, and high species diversity in the study area suggests the suitability of macro-ecological conditions for
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these Halimeda species in establishing populations. Species tolerances to varying environmental conditions are based on their morphological, reproductive and physiological traits (Verbruggen et al., 2009). H. discoidea, H. macroloba, H. opuntia and H. tuna can be considered cosmopolitan Halimeda species due to their widespread occurrence in the waters of the South China Sea. This is in contrast to the uncommon species of H. taenicola. Based on Phang et al. (2016) and Nguyen et al. (2013), H. taenicola was reported in Vietnamese waters and it was only recently that this species was reported in Malaysia, specifically on the northern coast of Sabah and off Langkawi Island (Zainee et al., 2018). The reasons for the rarity of this species in Malaysia are still unclear, although it is often found around the Pacific islands (e.g., Verbruggen et al., 2009; Tsuda et al., 2015). Observations of H. borneensis collected from the study site confirms earlier reports by Pongparadon et al. (2015) that described its occurrence off Pulau Tinggi, a marine park located relatively close to the study site. The specimens found in the Sembilang– Seri Buat channel reveals two contrasting morphotypes (Figs. 3 and 4) that are susceptible to possible misidentifications as different species (Verbruggen et al., 2005a; Dijoux et al., 2012; Pongparadon et al., 2015). The traits of morphotype A are similar to specimens of H. borneensis described by Taylor (1975). The second morphotype (B) has very similar traits to H. simulans, which is reported to be biogeographically restricted to the Atlantic basin (Verbruggen et al., 2005a). Molecular-level analysis of H. simulans-like specimens found in the Indo-pacific region demonstrated consistency with H. borneensis typification (H. Verbruggen, personal communication). Although modelled distribution showed the possible presence of H. simulans in Indopacific waters (Verbruggen et al., 2009), the current body of evidence suggests a low likelihood of H. simulans’ distribution in Malaysia. To date, no H. simulans-like specimen collected from Malaysia have been identified through molecular means as done for specimens elsewhere (Verbruggen et al., 2005a; Dijoux et al., 2012). Thus, future work to clarify the identification of cryptic Halimeda at the species level would require molecular studies to avoid misidentification. It is noteworthy that other recent inventories of Halimeda (Table 1) did not report this species along the eastern coast of Peninsular Malaysia. According to Verbruggen et al. (2009), Halimeda biogeography provides a strong phylogenetic imprint, which can demonstrate the connectivity among the populations of individual species. Pongparadon et al. (2015) added that during the northeast monsoon, the currents bring Halimeda spores from Borneo towards the eastern coast of Peninsular Malaysia, which increases the species richness and is therefore a factor in species partitioning as well as genetic differentiation of Halimeda. These hypotheses may be well founded since there were records of H. borneensis spanning south-eastern Peninsular Malaysia, the Riau Archipelago (though reported as H. simulans, Table 1) and Borneo. There is a good correlation for most Halimeda species between molecular-based 18 S rDNA and ITS region identification with several morphological traits (Kooistra et al., 2002). The cryptic nature of some species, however, may warrant further discrimination approaches to provide a definitive species identification. Nonetheless, our detailed morphometric observations were sufficient to distinguish Halimeda species, which allowed us to report the five species found in the channel between the Sembilang and Seri Buat Islands. Although this discovery, in addition to previous studies, indicates the localised diversity in the vicinity of the study site is up to six species, it is not the highest; but is still uncommon for this part of the South China Sea. Studies such as that reported here provide insights into the biogeography of Halimeda in the region. Further research that increases survey effort, especially in underexplored coral reefs, may demonstrate if a continuous distribution and population connectivity of Halimeda exists along the coasts bordering the South China Sea.
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N. Arina, M. Rozaimi and N.F.A. Zainee / Regional Studies in Marine Science 31 (2019) 100773
Table 1 Halimeda diversity classified through regional zonation: (1) Upper Gulf of Thailand; (2) Upper Andaman; (3) Lower Gulf of Thailand; (4) Lower Andaman; (5) North-western Peninsular Malaysia; (6) Eastern Peninsular Malaysia; (7) Western Peninsular Malaysia; (8) South-eastern Peninsular Malaysia; (9) Southern Malaysia; (10) Singapore; (11) Sarawak; (12) North-western Sabah; (13) Northern Sabah; and (14) Riau Archipelago. Halimeda incrassata had been reported from Singapore and the Riau Archipelago but Pongparadon et al. (2015) and Verbruggen et al. (2006) suggested its distribution is limited to the Altantic basin and is therefore omitted from the list. No
Species
Thai-Malay Peninsular 1
1 2
3 4 5 6
7
8 9
10 11
Section Halimeda Halimeda cuneata Halimeda discoidea
Section Rhipsalis Halimeda borneensis
X
X
X
X
7
8
X
X
9
10
11
X
12
13
14
X
X X
X
X
X
X X
X
X X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
Halimeda melanesica Halimeda stuposa
X
Section Pseudo-opuntia Halimeda gracilis
15 16 17
Section Opuntia Halimeda copiosa Halimeda minima Halimeda opuntia
X
X
This study; Zainee et al. (2018), Pongparadon et al. (2015), Pham et al. (2011) and Liao et al. (2004) Liao et al. (2004)
Pham et al. (2011)
X
X
X
X
X
X
X
X
X
X
X
Pham et al. (2011) and Liao et al. (2004)
X
Liao et al. (2004) Pongparadon et al. (2015) This study; Zainee et al. (2018), Pongparadon et al. (2015), Pham et al. (2011) and Liao et al. (2004) Pongparadon et al. (2015) Zainee et al. (2018)
X
X
Undetermined Section Halimeda papyracea
X 7
This study; Zainee et al. (2018)a , Pongparadon et al. (2015) and Liao et al. (2004)a Liao et al. (2004)
Pongparadon et al. (2015)
X
1
Zainee et al. (2018) This study; Pongparadon et al. (2015), Zainee et al. (2018), Pham et al. (2011) and Liao et al. (2004) Pongparadon et al. (2015) Zainee et al. (2018) and Liao et al. (2004) This study; Zainee et al. (2018) Zainee et al. (2018), Pham et al. (2011) and Liao et al. (2004)
Zainee et al. (2018)
X
X X
Halimeda renschii Halimeda velasquezii
Species total a
6
X
14
20
5
Reference
X
X
13
18 19
4
X X
X
Section Micronesicae Halimeda micronesica Halimeda fragilis
12
3
X
Halimeda gigas Halimeda macrophysa Halimeda taenicola Halimeda tuna
Halimeda cylindracea Halimeda macroloba
2
Malaysian Borneo, Riau Archipelago
1
4
8
2
5
6
4
7
Pham et al. (2011) 1
5
9
9
10
Reported H. borneensis as H.simulans. See text for elaboration.
Acknowledgements We thank Norfarzana Mohd Zahari for field work assistance, Dr. Heroen Verbruggen for sharing insights into the taxonomy of Halimeda, and Dr. Rose Norman for constructive comments in improving the final version of the manuscript. This research was supported by Universiti Kebangsaan Malaysia through the Research University grant UKM-GUP-2018-031. We also thank and acknowledge the approval from the Marine Park Department of Malaysia (research permit number JTLM 630-7 Jld 9 (71)) to undertake this study. References Aikanathan, S., Wong, F.H., 1994. Marine Park Island Management Conceptual Plan for Peninsular Malaysia. WWF Project MYS256/93. l36 pp.
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Sundararajan, M., Rajendran, M., Kaliaperumal, N., Kalimuthu, S., 1999. Studies on species of Halimeda from Lakshadweep. Seaweed Res. Utilization 21, 161–169. Taylor, W.R., 1975. A new species of Halimeda from Malaysia. Contrib. Univ. Michigan Herbarium 11, 81–83. Tsuda, R.T., Vroom, P.S., Page-Albins, K.N., Giuseffi, L., 2015. Marine benthic algae from seamounts along the Mariana Islands, Western Pacific. Micronesica 4, 1–19. Verbruggen, H., De Clerck, O., Kooistra, W.H.C.F., Coppejans, E., 2005a. Molecular and morphometric data pinpoint species boundaries in Halimeda section Rhipsalis (Bryopsidales, Chlorophyta). J. Phycol. 41 (3), 606–621. http://dx. doi.org/10.1111/j.1529-8817.2005.00083. Verbruggen, H., De Clerck, O., N’Yeurt, A.D.R., Spalding, H., Vroom, P.S., 2006. Phylogeny and taxonomy of Halimeda incrassata, including descriptions of h. kanaloana and h. heteromorpha spp. nov. (Bryopsidales, Chlorophyta). Eur. J. Phycol. 41 (3), 337–362. http://dx.doi.org/10.1080/09670260600709315. Verbruggen, H., De Clerck, O., Schils, T., Kooistra, W.H.C.F., Coppejans, E., 2005b. Evolution and phylogeography of Halimeda section Halimeda (Bryopsidales, Chlorophyta). Mol. Phylogenet. Evol. 37 (3), 789–803. http://dx.doi.org/10. 1016/j.ympev.2005.06.015. Verbruggen, H., Kooistra, W.H.C.F., 2004. Morphological characterization of lineages within the calcified tropical seaweed genus Halimeda (Bryopsidales, Chlorophyta). Eur. J. Phycol. 39 (2), 213–228. http://dx.doi.org/10.1080/ 0967026042000202163. Verbruggen, H., Tyberghein, L., Pauly, K., Vlaeminck, C., Nieuwenhuyze, K. Van, Kooistra, W.H.C.F., Leliaert, F., de Clerck, O., 2009. Macroecology meets macroevolution: Evolutionary niche dynamics in the seaweed Halimeda. Global Ecol. Biogeogr. 18 (4), 393–405. http://dx.doi.org/10.1111/j.14668238.2009.00463. Ximenes, C.F., Cassano, V., de Fátima de Oliveira-Carvalho, M., BandeiraPedrosa, M.E., Gurgel, C.F.D., Verbruggen, H., Pereira, S.M.B., 2017. Systematics of the genus Halimeda (Bryopsidales, Chlorophyta) in Brazil including the description of Halimeda jolyana sp. nov. Phycologia 56 (4), 369–381. http://dx.doi.org/10.2216/16-77.1. Xin, L.H., Adzis, K.A.A., Hyde, J., Cob, Z.C., 2016. Growth performance of acropora formosa in natural reefs and coral nurseries for reef restoration. AACL Bioflux 9 (5), 1090–1100. Xu, H., Zhao, X., Eberli, G.P., Liu, X., Zhu, Y., Cai, Y., Luo, W., Yan, G., Zhang, B., Shi, J., 2015. Biogenic carbonate formation and sedimentation in the Xisha Islands: evidences from living Halimeda. Acta Oceanol. Sin. 34 (4), 62–73. http://dx.doi.org/10.1007/s13131-015-0584-0. Zainee, N.F.A., Ismail, A., Taip, M.E., Ibrahim, N., Ismail, A., 2018. Diversity, distribution and taxonomy of Malaysian marine algae, Halimeda (Halimedaceae, Chlorophyta). Malayan Nat. J. 70 (2), 211–219.
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Regional Studies in Marine Science journal homepage: www.elsevier.com/locate/rsma
High localised diversity of Halimeda (Chlorophyta: Bryopsidales) in a tropical marine park from Pahang, Malaysia ∗
Natasha Arina, Mohammad Rozaimi , Nur Farah Ain Zainee Centre for Earth Sciences and Environment, Faculty of Science and Technology, Universiti Kebangsaan, Malaysia, 43600 UKM Bangi, Selangor, Malaysia
highlights • • • •
There were up to five Halimeda species within the surveyed channel. It is uncommon to find such high species richness in a small localised area. Halimeda borneensis was the most common species. Halimeda taenicola is a new record for the eastern coast of Peninsular Malaysia.
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Article history: Received 18 January 2019 Received in revised form 29 July 2019 Accepted 29 July 2019 Available online 1 August 2019 Keywords: Calcareous macroalgae Morphology Biogeographical distribution Southeast asia
a b s t r a c t The chlorophyte genus Halimeda is common in tropical waters but gaps still exist in the understanding of the biogeographical distributions of its species in Southeast Asia, particularly in Malaysia. During a study into the ecological functioning of reefs in a marine park (the Sembilang–Seri Buat group of islands, Pahang, Malaysia) along the eastern coast of Peninsular Malaysia, a previously unreported community of sand-dwelling Halimeda was discovered on a shallow reef flat (water depths of 12 m). We randomly collected 63 individuals and identified them using defining morphological and anatomical characteristics. The collection consisted of Halimeda borneensis, H. discoidea, H. macroloba, H. opuntia, and H. taenicola. Halimeda borneensis was the most collected (52 individual explants) in our study site. We report that H. taenicola is a new record for the eastern coast of Peninsular Malaysia, which is also a first biogeographical report of this species for the area spanning the Gulf of Thailand and towards the coastal areas to the east of Singapore. This study together with past records on Halimeda in the immediate surroundings show a total of six Halimeda species in the area, a localised coastal diversity uncommon to this part of the South China Sea. © 2019 Elsevier B.V. All rights reserved.
1. Introduction Halimeda is a genus of chlorophyte, which can be found in tropical and subtropical regions (El-Manawy and Shafik, 2008). Halimeda diversity is widely reported from the Atlantic Ocean, Pacific Ocean and Western Indian Ocean (Kooistra et al., 2002; Verbruggen and Kooistra, 2004; Verbruggen et al., 2005a,b), but its occurrences in the Eastern Pacific Ocean is relatively underexplored. In Southeast Asia, Halimeda distribution is centred in the Eastern Indian Ocean as well as the Andaman Sea (Pongparadon et al., 2015; Phang et al., 2016). Species are distributed along biogeographic barriers, which prevent the dispersal of genetic material between the regions (Pongparadon et al., 2015). Different regions influence the variations in different Halimeda sections and species including factors such as habitat depth, ∗ Corresponding author. E-mail address: [email protected] (M. Rozaimi). https://doi.org/10.1016/j.rsma.2019.100773 2352-4855/© 2019 Elsevier B.V. All rights reserved.
substrata, light intensity, wave action and currents (Pongparadon et al., 2015). In addition, these limitations are caused by various interacting features such as niche, morphological characteristics, reproductive behaviour and physiological traits (Verbruggen et al., 2009). Long-term survival and adaptation as well as species’ tolerances determine the niche characteristics of Halimeda (Verbruggen et al., 2009). Marine biogeographic barriers such as the Sunda Shelf Barrier restrict the continuity of Halimeda species occurrences between the Western Pacific Ocean and the tropical Indian Ocean (Pongparadon et al., 2015). In Peninsular Malaysia, the western and eastern coasts are affected by the southwest monsoon and northeast monsoon, respectively (Masseran and Razali, 2016; Kok et al., 2017). Species dispersal is impacted by these monsoons due to changes in current and circulation patterns along the South China Sea (Phang et al., 2016) for the eastern coast, and the Malacca Strait for the western coast. Halimeda species are mostly found in shallow waters, which are usually supersaturated with calcium carbonate (Granier, 2012)
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Fig. 1. Location of the study site marked with an ‘X’ (right). Numbers on the map (left) refer to zonal classification in the appended table and described in the text.
and are either sand-dwelling or rock-dwelling (Hillis-Colinvaux, 1980; Verbruggen et al., 2006). Halimeda are mostly found in reefs (Perry et al., 2016), and a mutual relationship exists with the coral community. In Malaysia, most coral reefs are located in marine parks (Mustapha et al., 2014; Xin et al., 2016) and therefore the presence of Halimeda contributes to the biodiversity and ecological functioning within these areas. They serve as prominent primary producers, a source of food and habitats, and are major contributors to reef formation (Castro-Sanguino et al., 2016; Ximenes et al., 2017). Halimeda species are known to be resilient to grazing as their highly calcified tissues contain halimedatrial, which discourages herbivory (Hay et al., 1994; Hendri et al., 2015). Halimeda species have mineralised skeletons, which secretes calcareous layers on the outside of the cytoplasmic envelope (Granier, 2012). The relatively rapid growth of calcified layers and high turnover rates make these macroalgae major contributors of sediments in reef construction in the form of aragonite deposition (Pongparadon et al., 2015; Ximenes et al., 2017). After senescence, Halimeda mainly yields carbonate sand from their tissue segments (Verbruggen et al., 2009; Xu et al., 2015). These segments provide sediments that contribute to longterm biogenic deposits in the reef environment (Freile et al., 1995). To date, there are 44 species of Halimeda species known worldwide (Guiry and Guiry, 2019). In the South China Sea, there are 20–30 species of Halimeda within the waters of Malaysia, Thailand, Vietnam, Singapore, Philippines, and Indonesia (Phang et al., 2016). Challenges abound in the identification of Halimeda species due to similarities in morphological characteristics and therefore a definitive list of the species present would provide a basis in understanding the ecology and the biogeography of this genus in Southeast Asia. Especially in Malaysia, the genetic connectivity of Halimeda in dispersal is not widely investigated and species occurrences show sparse distribution. In this paper, we describe the Halimeda species found during a study into the ecological functioning of Halimeda in Seri Buat Island, where an unreported community of Halimeda was discovered. We then placed those species in the context of the biogeographical distribution of Halimeda along the western coast of the South China Sea to provide insights into their occurrences in the region.
2. Materials and methods Sampling activities were carried out in April 2018 in a sheltered channel located between Sembilang and Seri Buat Islands (Fig. 1). This channel is about 2–3 km long and shallow with certain portions of sandy elevated areas exposed during low tide. Sediments consist of coral rubble and the average coral coverage was reported to be approximately 44% (Aikanathan and Wong, 1994). During the field assessment, a total number of 63 Halimeda specimens were collected randomly from within this channel at shallow water depths (∼1–2 m) during low tide. Whole thallus (Fig. 2), including below-ground organs were carefully removed from the substrate, placed in plastic bags and transported to the laboratory for further analysis. Specimen identification was carried out by defining external morphological and anatomical characteristics. External traits included the specimen height, segment size, segment shape, basal segment size, structure of margin, surface texture, colour, segment thickness, branching type, and holdfast type. The type of sediment that was attached to the holdfast was also recorded. For anatomical identification, a small segment of Halimeda tissue was decalcified using 20% hydrochloric acid (after Bandeira-Pedrosa et al., 2004). The tissues were then stained with Lactophenol cotton blue stain to distinguish the utricle and medullary filaments. The stained surface, in both longitudinal and cross-sectional views, were observed under a stereo microscope (magnification of 100x and 400x). The characteristics of the utricle and medullary filaments were observed after the decalcified segment was dissected. Species identification was then completed through construction of dichotomous keys based on these characteristics. These characteristics were then compared to existing keys from other studies (Sundararajan et al., 1999; Bandeira-Pedrosa et al., 2004; El-Manawy and Shafik, 2008; Dijoux et al., 2012; Pongparadon et al., 2015) to reaffirm the species identity. 3. Results The 63 specimens collected in this study were identified to be five species based on morphological and anatomical characteristics. These were Halimeda borneensis, H. discoidea, H. macroloba, H. opuntia, and H. taenicola. Halimeda borneensis was the most collected (52 individuals from two morphotypes), followed by H. macroloba and H. discoidea with seven and two individuals, respectively. The least-common species were H. opuntia and
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50–65 µm in length. Medullary filaments slender, 30–35 µm in breadth with minor branching. Nodal fusions arise from five fused medullary filaments.
Fig. 2. Naturally growing Halimeda at the study site.
H. taenicola (1 individual each). Identification keys for these five species were constructed based on the morphological and anatomical characteristics observed and is explained as follows: Key to Halimeda species 1 1
Segment size large, more than 1.5 cm wide and 1 cm height . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ..H. macroloba Segment size small, less than 1 cm wide and 0.5 cm height . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ... 2
2 2
Segment margin entire for whole plant. . . H. taenicola Segment margin varying from entire, sinuous or undulated . . . . . . . . . . . . ..... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .... 3
3
Segment shape reniform to flabellate with shallowly-lobed surface.... . . . . . . . . . . . . . . . . . H. discoidea Segment shape trilobed to heart-shaped with deeply-lobed surface . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
3
4 4
Segment branching regular, dichotomous and elongated . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . ... H. opuntia Segment branching irregular, polychotomous and form bushy habit . . . . . . . . . . . . . . . . . . . . . . . . . . . H. borneensis
The distinct characteristics of surface view, utricle and medullary filament for each species are illustrated in Fig. 3, and the thallus morphology in Fig. 4. The descriptions of each Halimeda species found in the sampling location are as follows: Halimeda borneensis W.R. Taylor, 1975 – morphotype A Description: Thallus erect forming thick clumps, long and large bulbous holdfast. Vertical growth up to 7 cm, moderately heavy calcification with dark green colour. Segments generally small, 0.5– 1.0 cm in breadth and 0.4–0.6 cm in length. Basal segments subterete to terete, varying from cylindrical to subcylindrical. Segments varying in shape, obovate, cuneate, heart-shaped or trilobed with sinuous to undulated margins. Segment thickness consistent from base to the terminal of thallus. Branching pattern elongated forming a bushy habit. Cortex consisting of three layers of inflated utricles with regular branching pattern. Utricles in surface view arranged in irregular polygons. Primary utricles obovate to cuneate, 9–15 µm in breadth and 10–25 µm in length. Secondary utricles elliptical, 35–45 µm in breadth and 45–55 µm in length. Tertiary utricles truncate, 55–70 µm in breadth and
Halimeda borneensis W.R. Taylor, 1975 – morphotype B Description: Thallus erect, single or gregarious, vertical growth up to 8 cm, arising from large bulbous holdfast about 3–4 cm in length. Moderately heavy calcification with dark green colour. Basal segment flabellate, consisting of two to three fused twisted segments, 0.3– 0.9 cm in breadth and 0.4–0.6 cm in length, with slightly distinct rib-like structure, irregular shape that varies from trilobe, ovate, oval, cuneate and reniform. Segment thickness decreases from base to the terminal portion of thallus. Upper margin deeply lobed with undulated surface. Branching pattern elongated and irregularly polychotomous. Utricles in surface view arranged in irregular polygons. Cortex consisting three layers of cylindricalinflated utricles. Primary utricles short-cylindrical, up to 8–10 µm in breadth and 10–15 µm in length. Secondary utricles cylindrical, 10–18 µm in breadth and 14–20 µm in length. Tertiary utricles elliptical, 25–40 µm in breadth and 30–45 µm in length. Medullary filaments thin, 25–35 µm in breadth, with trichotomous branching in close proximity to each other. Nodal fusions arise from four to five fused medullary filaments. Halimeda discoidea Decaisne, 1842 Description: Plants erect, arise from bulbous holdfast about 3–4 cm long. Thallus forming cushion-like clumps, tufted or loose in habit. Vertical growth up to 7 cm. Heavily calcified segment; yellowish green colour. Basal segments subcylindrical, subcuneate or subterete, discoidal to reniform with flattened smooth surface up to 0.6–1.2 cm in breadth and 0.5–0.6 cm in length. Margins generally entire to shallowly-lobed. Branching usually irregular, either trichotomous or polychotomous from one large segment. Utricles in surface view arranged in regular polygons. Cortex of segment composed of two layers of large and inflated utricles. Utricles large and inflated with regular polygonal shape. Secondary utricles subglobular, 90–120 µm in breadth and 110–150 µm in length, supporting four to five primary utricles, cylindrical, 10– 18 µm in breadth and 10–20 µm in length. Medullary filaments large, 45–55 µm in breadth with less densely branched. Nodal fusions arise from medullary filaments paired in groups of three. Halimeda macroloba Decaisne, 1841 Description: Thallus whitish green, highly calcified, solitary, erect, growth up to 15 cm. Holdfast large bulbous, extending to 5 cm long. Basal segment compressed, flabellate to cuneate, arising from single segment. Segment size about 1.5–2.3 cm in breadth and 1.0–1.5 cm in length, flabellate to reniform, with upper margin shallowly to deeply lobed with undulated surface. Branching pattern irregular polychotomous forming fan-shaped plant. Utricles in surface view arranged in irregular hexagons. Cortex consisting of four layers of utricles. Primary utricles cylindrical-elongated, 8–10 µm in breadth and 20–25 µm in length. Secondary utricles elliptical to obovate, 15–20 µm in breadth and 18–25 µm in length. Tertiary utricles elliptical, 22–35 µm in breadth and 40– 55 µm in length. Medullary filament large, 40–55 µm in breadth. Diameter of medullary filament decreases with constriction at the base of branching. Nodal fusions arise from two to three fused medullary filaments.
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Fig. 3. Anatomical characteristics of Halimeda species.
Fig. 4. The shape of segments and thalli ramification of Halimeda species: (A) H. taenicola; (B) H. borneensis (morphotype A); (C) H. borneensis (morphotype B); (D) H. opuntia; (E) H. macroloba; (F) H. discoidea.
Halimeda opuntia (Linnaeus) J.V. Lamouroux, 1816 Description: Thallus erect, forming either solitary or thick clumps, spreading laterally from several small rhizoidal holdfast. Plant vertical growth up to 15 cm, light calcification with light green colour. Segments generally small, 0.2–0.5 cm breadth and 0.2–0.3 cm in length, and regular in size throughout the thallus. Basal segment irregular, varying from cylindrical to subcylindrical. Segments with distinct rib, reniform, oblong, heart-shaped or trilobed with shallowly- to deeply-lobed margin, sometimes twisted or crenulated. Branching pattern either elongated or densely-branching
that form bushy habit. Utricles in surface view arranged in irregular polygons. Cortex consisting four to five layers of elongated utricles with irregular branching pattern. Primary utricles shortcylindrical, up to 6–10 µm in breadth and 10–15 µm in length. Secondary utricles oblanceolate, 10–15 µm in breadth and 18– 20 µm in length. Tertiary utricles narrow-truncate, 12–20 µm in breadth and 55–75 µm in length. Fourth layer of utricles cylindrical, 13–18 µm in breadth and 25–30 µm in length. Medullary filaments densely branched, thin, up to 30–40 µm in breadth with less constrictions at branch and main axis is thins towards the lower branch. Nodal fusions arise from medullary filaments paired in groups of two to three.
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Halimeda taenicola W.R. Taylor, 1950 Description: Thallus erect, compact, vertical growth up to 7 cm, arising from small bulbous holdfast. Calcification light with dark green colour. Consists of more than one basal segments that are subcuneate or subcylindrical. Segments varying from lower to the terminal part of thallus. Lower part of thallus about 0.2–0.4 cm in breadth and 0.2–0.3 cm in length, size of segment decreases towards terminal ends. Thallus shape is mixed from the lower segment to the terminal segment; cuneate, subcuneate and ovate, with entire margin. Branching is polychotomous, numerous and elongated. Utricles in surface view arranged in regular polygons. Cortex consisting of three layers of elongated utricles. Primary utricles cylindrical, 8–12 µm in breadth and 15–20 µm in length. Secondary utricles narrow-elliptical, 10–15 µm in breadth and 30–35 µm in length. Tertiary utricles truncate, 30–45 µm in breadth and 50–65 µm in length. Medullary filaments up to 30–45 µm in breadth and have numerous constrictions at the main axis. Nodal fusions arise from medullary filaments paired in groups of three to four. 4. Discussion Detailed observations through morphological and anatomical characteristics classified the Halimeda specimens into five species, which are H. borneensis, H. discoidea, H. macroloba, H. taenicola, and H. opuntia. Although this study was restricted to only one locality, insights into the regional biogeography of Halimeda can be contextualised from this list of previously unreported records. At the study site, Halimeda were found in sandy patches of the coral reefs and all specimens had bulbous holdfasts typical of sand-dwellers. Among these species, H. borneensis was the most dominant, and we report that H. taenicola is a new record for the eastern coast of Peninsular Malaysia. At present, including findings from this study, there has been a total of 10 Halimeda species found in Malaysia (Table 1). In general, the western coast of Peninsular Malaysia has higher diversity compared to the eastern side of the Peninsular coast. The land mass of the Thai-Malay Peninsular limits the sea connectivity between the Indian and Pacific Oceans and therefore is clearly a barrier to population dispersal for Halimeda between the two coasts. Previous studies reported that H. discoidea, H. macroloba, H. opuntia and H. tuna were present on the eastern Peninsular coast while the same species, as well as H. cuneata, H. stuposa and H. taenicola, were present on the western Peninsular coast (Zainee et al., 2018). In recent Halimeda records in waters bordering Malaysia, the average number of species in the designated zones 1 to 14 (Fig. 1) is 4 to 5 (Table 1). The diversity of species found in our study site is therefore above-average but not the highest in this region. To date, it still stands that the highest localised Halimeda diversity (10 species; Table 1) among these zones was in the Riau Archipelago while in Malaysia it is in Sabah waters. In the latter, H. macrophysa and H. velasquezii were restricted to Borneo and are unlikely to be found on the peninsular coasts. To the south of the peninsular, H. gracilis and H. papyracea have been reported in Singapore waters (Pham et al., 2011) and, due to its proximity, it is possible that future surveys in the southern parts of Peninsular Malaysia may find the same species. The high diversity of Halimeda in the channel that formed a relatively small sandy area at the study site shows an apparent hotspot for members of this genus. Xu et al. (2015) described that Halimeda is highly adaptive to variable environmental conditions in the tropics, and high species diversity in the study area suggests the suitability of macro-ecological conditions for
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these Halimeda species in establishing populations. Species tolerances to varying environmental conditions are based on their morphological, reproductive and physiological traits (Verbruggen et al., 2009). H. discoidea, H. macroloba, H. opuntia and H. tuna can be considered cosmopolitan Halimeda species due to their widespread occurrence in the waters of the South China Sea. This is in contrast to the uncommon species of H. taenicola. Based on Phang et al. (2016) and Nguyen et al. (2013), H. taenicola was reported in Vietnamese waters and it was only recently that this species was reported in Malaysia, specifically on the northern coast of Sabah and off Langkawi Island (Zainee et al., 2018). The reasons for the rarity of this species in Malaysia are still unclear, although it is often found around the Pacific islands (e.g., Verbruggen et al., 2009; Tsuda et al., 2015). Observations of H. borneensis collected from the study site confirms earlier reports by Pongparadon et al. (2015) that described its occurrence off Pulau Tinggi, a marine park located relatively close to the study site. The specimens found in the Sembilang– Seri Buat channel reveals two contrasting morphotypes (Figs. 3 and 4) that are susceptible to possible misidentifications as different species (Verbruggen et al., 2005a; Dijoux et al., 2012; Pongparadon et al., 2015). The traits of morphotype A are similar to specimens of H. borneensis described by Taylor (1975). The second morphotype (B) has very similar traits to H. simulans, which is reported to be biogeographically restricted to the Atlantic basin (Verbruggen et al., 2005a). Molecular-level analysis of H. simulans-like specimens found in the Indo-pacific region demonstrated consistency with H. borneensis typification (H. Verbruggen, personal communication). Although modelled distribution showed the possible presence of H. simulans in Indopacific waters (Verbruggen et al., 2009), the current body of evidence suggests a low likelihood of H. simulans’ distribution in Malaysia. To date, no H. simulans-like specimen collected from Malaysia have been identified through molecular means as done for specimens elsewhere (Verbruggen et al., 2005a; Dijoux et al., 2012). Thus, future work to clarify the identification of cryptic Halimeda at the species level would require molecular studies to avoid misidentification. It is noteworthy that other recent inventories of Halimeda (Table 1) did not report this species along the eastern coast of Peninsular Malaysia. According to Verbruggen et al. (2009), Halimeda biogeography provides a strong phylogenetic imprint, which can demonstrate the connectivity among the populations of individual species. Pongparadon et al. (2015) added that during the northeast monsoon, the currents bring Halimeda spores from Borneo towards the eastern coast of Peninsular Malaysia, which increases the species richness and is therefore a factor in species partitioning as well as genetic differentiation of Halimeda. These hypotheses may be well founded since there were records of H. borneensis spanning south-eastern Peninsular Malaysia, the Riau Archipelago (though reported as H. simulans, Table 1) and Borneo. There is a good correlation for most Halimeda species between molecular-based 18 S rDNA and ITS region identification with several morphological traits (Kooistra et al., 2002). The cryptic nature of some species, however, may warrant further discrimination approaches to provide a definitive species identification. Nonetheless, our detailed morphometric observations were sufficient to distinguish Halimeda species, which allowed us to report the five species found in the channel between the Sembilang and Seri Buat Islands. Although this discovery, in addition to previous studies, indicates the localised diversity in the vicinity of the study site is up to six species, it is not the highest; but is still uncommon for this part of the South China Sea. Studies such as that reported here provide insights into the biogeography of Halimeda in the region. Further research that increases survey effort, especially in underexplored coral reefs, may demonstrate if a continuous distribution and population connectivity of Halimeda exists along the coasts bordering the South China Sea.
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N. Arina, M. Rozaimi and N.F.A. Zainee / Regional Studies in Marine Science 31 (2019) 100773
Table 1 Halimeda diversity classified through regional zonation: (1) Upper Gulf of Thailand; (2) Upper Andaman; (3) Lower Gulf of Thailand; (4) Lower Andaman; (5) North-western Peninsular Malaysia; (6) Eastern Peninsular Malaysia; (7) Western Peninsular Malaysia; (8) South-eastern Peninsular Malaysia; (9) Southern Malaysia; (10) Singapore; (11) Sarawak; (12) North-western Sabah; (13) Northern Sabah; and (14) Riau Archipelago. Halimeda incrassata had been reported from Singapore and the Riau Archipelago but Pongparadon et al. (2015) and Verbruggen et al. (2006) suggested its distribution is limited to the Altantic basin and is therefore omitted from the list. No
Species
Thai-Malay Peninsular 1
1 2
3 4 5 6
7
8 9
10 11
Section Halimeda Halimeda cuneata Halimeda discoidea
Section Rhipsalis Halimeda borneensis
X
X
X
X
7
8
X
X
9
10
11
X
12
13
14
X
X X
X
X
X
X X
X
X X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
Halimeda melanesica Halimeda stuposa
X
Section Pseudo-opuntia Halimeda gracilis
15 16 17
Section Opuntia Halimeda copiosa Halimeda minima Halimeda opuntia
X
X
This study; Zainee et al. (2018), Pongparadon et al. (2015), Pham et al. (2011) and Liao et al. (2004) Liao et al. (2004)
Pham et al. (2011)
X
X
X
X
X
X
X
X
X
X
X
Pham et al. (2011) and Liao et al. (2004)
X
Liao et al. (2004) Pongparadon et al. (2015) This study; Zainee et al. (2018), Pongparadon et al. (2015), Pham et al. (2011) and Liao et al. (2004) Pongparadon et al. (2015) Zainee et al. (2018)
X
X
Undetermined Section Halimeda papyracea
X 7
This study; Zainee et al. (2018)a , Pongparadon et al. (2015) and Liao et al. (2004)a Liao et al. (2004)
Pongparadon et al. (2015)
X
1
Zainee et al. (2018) This study; Pongparadon et al. (2015), Zainee et al. (2018), Pham et al. (2011) and Liao et al. (2004) Pongparadon et al. (2015) Zainee et al. (2018) and Liao et al. (2004) This study; Zainee et al. (2018) Zainee et al. (2018), Pham et al. (2011) and Liao et al. (2004)
Zainee et al. (2018)
X
X X
Halimeda renschii Halimeda velasquezii
Species total a
6
X
14
20
5
Reference
X
X
13
18 19
4
X X
X
Section Micronesicae Halimeda micronesica Halimeda fragilis
12
3
X
Halimeda gigas Halimeda macrophysa Halimeda taenicola Halimeda tuna
Halimeda cylindracea Halimeda macroloba
2
Malaysian Borneo, Riau Archipelago
1
4
8
2
5
6
4
7
Pham et al. (2011) 1
5
9
9
10
Reported H. borneensis as H.simulans. See text for elaboration.
Acknowledgements We thank Norfarzana Mohd Zahari for field work assistance, Dr. Heroen Verbruggen for sharing insights into the taxonomy of Halimeda, and Dr. Rose Norman for constructive comments in improving the final version of the manuscript. This research was supported by Universiti Kebangsaan Malaysia through the Research University grant UKM-GUP-2018-031. We also thank and acknowledge the approval from the Marine Park Department of Malaysia (research permit number JTLM 630-7 Jld 9 (71)) to undertake this study. References Aikanathan, S., Wong, F.H., 1994. Marine Park Island Management Conceptual Plan for Peninsular Malaysia. WWF Project MYS256/93. l36 pp.
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