Keywords

15.1 Introduction

Spirobranchus or colloquially known as Christmas Tree Worm (CTW) is a tube-building polychaete worm belongs to family Serpulidae. The worms obtained its common name ‘Christmas Tree Worm’ from its exposed colourful two radiolar crowns that shaped like small conifer trees, which usually associated with Christmas celebration. At the moment, genus Spirobranchus consists of 37 species and can be found in all coral reef regions in the world (Polychaeta 2021). Spirobranchus is considered a host generalist; the worms can live in almost all stony corals, including Scleractinia (anthozoan) and Hydrozoa (Millepora) (Rowley 2008; Hoeksema et al. 2020). Nevertheless, recent studies also reported that CTW could also live in various secondary hosts including mushroom coral, zoantharian, ascidian, octocorallia (soft coral), sponges, and live bivalve shells (Hoeksema and ten Hove 2014, 2017; van der Schoot et al. 2016; García-Hernández and Hoeksema 2017; Hoeksema et al. 2020).

Apart from its unique shape, the colour polymorphism of CTW is also making the genus distinctive in the coral reef ecosystem. Colour diversity in animal serve various purposes including protection from predators (camouflage, warning), attractants for potential prey (bait maiming) and to attract the opposite sex for reproduction (Bond and Kamil 2002; Hanlon et al. 2013; Stevens et al. 2014; Duarte et al. 2017). Moreover, colouration also might indicate environmental stress (Troïanowski et al. 2015). Nevertheless, the study on colour polymorphism in Polychaeta is limited compared to other taxa. For example, in scaleworm Harmothoe imbricata (Nygren et al. 2011). One of the earliest studies on CTW was done by Dales (1962), which characterised the colouration pigment in Sabellide and Serpulidae. Since then, there was a temporal void of knowledge until Song (2006) listed S. giganteus colourations in French Polynesia, which consisted of five colours (blue, brown, marigold, purple and white). Interestingly, colour variations in CTW are high even in a small area. Individuals CTW can have different radiolar crown colours although live relatively next to each other on the same coral colony. Nevertheless, the purpose of having different colours in individual level of CTW is still not fully understood by researchers until today.

The Indo-Pacific region, which includes southeast Asia, Indian Ocean, central Pacific and northern Australia is the habitat locality for Spirobranchus corniculatus (Grube 1862). Initially, three Spirobranchus species (S. corniculatus, S. gaymardi, and S. cruciger) which form the S. corniculatus complex were reported from the region (ten Hove 1994). However, recent molecular work revealed that the so-called three species actually belong to a single species which is S. corniculatus (Willette et al. 2015).

In Malaysia, no study has been conducted on the host and colour diversity of S. corniculatus. Hence, the purpose of this study is to identify the preferred host, and colour polymorphism of S. corniculatus at Pantai Pasir Cina, Bidong Island, South China Sea.

15.2 Materials and Methods

The study was conducted between August and September 2018 on the reef flat at Pantai Pasir Cina, Bidong Island (Fig. 15.1). This site was chosen because of accessibility for researchers to conduct SCUBA diving from shore until 8–10 m (depending on the tide) of reef flat that consists of different coral communities that allows depth comparison to being done (Safuan et al. 2020).

Fig. 15.1
figure 1

Sampling sites (a and b) at Pantai Pasir Cina, Bidong Island, South China Sea

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The reef flat was divided into two sites which are A and B, separated by a coral rubble patch made for boat landing to facilitate underwater data collection. At each site, three sampling depths were chosen including 3 m, 6 m and 9 m. Each sampling depths included ±1 m range and were determined using a dive computer (Mares Puck Pro, Italy). All samplings were done during the high tide of the neap tide.

At each sampling depth, a belt transect method (Hill and Wilkinson 2004) was adapted. A 100 m of transect tape was deployed on the reef. A pair of divers then swam along the belt transect (covering 1 m to both left and right of the transect tape) to count the S. corniculatus and identifies the host, at the same time digitally captured (Olympus Stylus Tough 8000 with underwater casing without the light strobe) the image of each everted CTW (.jpeg format) for colour correction. The 2 m width (1 m left and right) was decided because the general size of CTW is small which require small observation area to give sufficient time for SCUBA divers to collect data and photograph. Hermatypic (reef building) corals were identified until genus level using Coral Finder (Byoguides, Australia) based on the digital images taken.

The occurrence of CTW was categorised according to the coral genera and depth; and presented in percentage. Images of radiolar crown of S. corniculatus (.jpeg format) were colour corrected using Adobe Photoshop software to enhance the true colour of CTW (Fig. 15.2). The colour correction is needed because seawater absorbs the light wavelength at different depths; red and orange colours are the first to be absorbed, followed by yellow, green and lastly, blue (Anthoni 2005). The RGB (red, green and blue) layers were applied on each image using Adobe Photoshop software to reveal the true colours of CTW (Pateman 2009). The colour correction was done according to the steps suggested by Probst (2009).

Fig. 15.2
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Comparison image of radiolar crown of Spirobranchus corniculatus before and after colour correction: a Before and b after colour correction

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The colour variations Spirobranchus corniculatus have been determined to its radiolar crown (the Christmas tree shape). The colour classification was designated according to the primary colour of RGB values which are Red, Green, Blue. Moreover, other colours were classified visually in the corrected images: Yellow, Purple, Brown, Orange and White (Song 2006). In addition, variations in the colour pattern were also recorded (i.e. banded, striped, dotted).

Data on CTW occurrence and colour diversity were analysed based on depth and coral preferences and presented in percentage. Due to technical and logistical issues, no replicates were done at each transect and depth. Hence data from the similar depth from sites A and B were combined for descriptive analyses.

15.3 Results

A total of 274 S. corniculatus was recorded from all depth profiles in Pantai Pasir Cina, Bidong Island. The majority of CTW was found with 4–6 m depth (60.2%), followed by 2–4 m (25.9%) while the deepest depth (8–10 m) only represented by 13.9% of total found (Fig. 15.3).

Fig. 15.3
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Distribution abundance (%) of Spirobranchus corniculatus at Pantai Pasir Cina, Bidong Island, South China Sea

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The hermatypic (reef building) corals that have CTW as symbionts are Astreopora spp., Montastrea spp., Montipora spp. and Porites species (Fig. 15.4). Porites spp. has the highest number of CTW symbionts (90.2%), followed by Montipora spp. (4.9%), while Astreopora spp. and Montastrea spp. only recorded 2.4% of recorded CTW each (Fig. 15.5). However, no CTW was found live as a symbiont with Acropora spp. at Pantai Pasir Cina, Bidong Island. Furthermore, among stony coral species (Astreopora spp., Montastrea spp., Montipora spp. and Porites species) that were found along the transects, 56.2% were found with at least one CTW that lived as a symbiont.

Fig. 15.4
figure 4

Diversity of Spirobranchus corniculatus hosts at Pantai Pasir Cina, Bidong Island, South China Sea. a Astreopora spp., b Montastrea spp. (within yellow circle), c Montipora spp., and d Porites species

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Fig. 15.5
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Preferred coral hosts by Spirobranchus corniculatus at Pantai Pasir Cina, Bidong Island, South China Sea

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Figure 15.6 shows the colour diversity of CTW found at Pantai Pasir Cina. A total of five plain colours and four striped colours were recorded. The plain colours are blue, green, orange, white, and yellow; while striped colours are blue, brown, purple and white. Among these colour patterns, plain blue was the primary colour (43.8%), followed by yellow (16.9%) and striped brown (13.1%) (Fig. 15.7). Other colour patterns were recorded occurrence below 10%. Additionally, not all colours are available at all depth, with shallow depth (2–3 m) recorded the lowest (seven colours) while the intermediate (5–7 m) and deep (8–10 m) have eight colours each.

Fig. 15.6
figure 6

Colour and pattern diversity of Christmas Tree Worm, Spirobranchus corniculatus at Pantai Pasir Cina, Bidong Island, South China Sea. a Yellow, b white, c green (arrow pointed), d striped brown, e blue, f orange (arrow pointed), g striped blue (arrow pointed), h striped purple, and i striped white

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Fig. 15.7
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Distribution of colours in radiolar crown of Spirobranchus corniculatus at Pantai Pasir Cina, Bidong Island, South China Sea

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Detail of colour variations according to the depth, is shown in Fig. 15.8. Blue was the dominant colour of S. corniculatus in all depth ranges (2–10 m). However, the second dominant colours in shallowest depth (2–4 m) was striped brown (28.1%), while yellow was the second dominant colours for rest of the depth (5–7 m, 24.2%; 8–10 m, 16.7%).

Fig. 15.8
figure 8

Colour diversity in radiolar crown of Spirobranchus corniculatus at different depth (during high tide) at Pantai Pasir Cina, Bidong Island, South China Sea. a 2–4 m, b 5–7 m, c 8–10 m

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15.4 Discussion

15.4.1 Spirobranchus corniculatus Host at Pantai Pasir Cina

The highest percentage of S. corniculatus found in this study live as a symbiont with Porites spp. The growth pattern of Porites is slower compared to other hard coral general and in enlarging pattern (Razak et al. 2019). The slow growth rate allows the CTW to extend its burrowing tube according to the growth rate of the coral host and adjusting the opening position to gain more advantage during filter feeding (Nishi and Nishihira 1999). Although both Astreopora spp. and Montastrea spp. are massive corals, the numbers of CTW are lower compared to Porites species, probably because the length of tentacles of both genera are longer than later. Also, each individual has larger corallites on the surface of the colony, which probably hindering CTW larvae from settling down and growing, as suggested by Scaps (2011). Besides, Montipora spp. which have small corallites like Porites yet low percentage of CTW as symbionts may caused by the horizontal and encrusting growth, resulting in thinner colony compared to the thick Porites. In this study, no CTW was found as a symbiont with staghorn coral Acropora sp. and other secondary hosts such as zoanthids, ascidians and soft corals. The absence of CTW on Acropora sp. is expected as other recent studies also exempting Acropora species among the list of CTW host (Song 2006; Rowley 2008; Perry et al. 2018) or recorded a very low number of individuals (Dai and Yang 1995). Interestingly, a high number of S. corniculatus larvae was recorded on live Acropora prolifera compared to other substrates (Marsden 1987). Nevertheless, the survival rate of S. corniculatus that settled on Acropora spp. maybe low because of the relatively fast growth rate of the coral in the genus (Anggara et al. 2020). Moreover, the branching shape of Acropora spp. as they grow will gradually make the opening of CTW tube to be located further down to the base of coral and in between the coral branches. This condition will reduce the current flow, subsequently limiting the number of suspended food particles available for CTW, which may lead to death. Moreover, branching corals are more susceptible to physical damage caused by storm or cyclone (Safuan et al. 2020).

Although not the main focus in this study, no CTW was observed live on artificial substrates as discovered by Perry et al. (2018) in the Red Sea. The absence of CTW on artificial substrates (rubbish or man-made materials) at Pantai Pasir Cina is probably due to the condition of the study site. Pantai Pasir Cina is located in front of the Marine Research Station, Universiti Malaysia Terengganu (UMT). The area is mostly restricted for public or tourists except for researchers. Thus, a limited number of people will be at the station at any given time. During the monsoon period, which lasts for 4–5 months, all structures in the water that belongs to the station will be kept on land except for large, heavy structures and for research purpose. Once the monsoon is over, these structures will be placed back in the water together with beach and underwater clean-ups. Hence, the repetitive removal of structures either because of monsoon or rubbish clean-ups probably prohibiting the CTW to settle and live (if settled) on the artificial substrate at Pantai Pasir Cina. Nonetheless, some large and heavy artificial structures such as an overboard backhoe have overgrown hermatypic corals with CTW as symbionts. Although reproductive biology of S. corniculatus is not yet understood, another CTW, S. tetraceros in Abu Kir Bay, Egypt only spawn in a limited period, i.e. between May until September (Selim et al. 2005). If S. corniculatus at Bidong Island also have the same spawning period, larvae that settled on artificial substrates especially small and removable items like discarded plastic material will have very low survivability to live through the monsoon season.

The outcomes from this study also indicate that a high percentage of CTW at Pantai Pasir Cina was found at the intermediate depth (5–7 m) of the reef flat. This depth range is suitable for S. corniculatus because of lower wave action and temperature compared to the shallow depth range (2–4 m) that is highly affected by intertidal cycle, even though the percentage of massive coral at 2–4 m was high. The deepest depth range (8–10 m) of the reef flat is adjacent to a sandy plain outside the bay, which impose a risk of abrasion due to sediment suspension. Also, the current around Bidong Island moves from north to south with the maximum speed of 0.22 m/s (Daud and Akhir 2015), which may reduce the opportunity for trochophore larvae of S. corniculatus to settle on a potential host at 8–10 m. Thus, the ‘Goldilock’ depth (5–7 m) for CTW to live is characterised by moderate wave action, lower water temperature compared to the shallow depth and less abrasive sediment presence with slow current flow compared to deeper depth area. The outcome is slight contradict from a study done by Rowley (2008) in Indonesian reefs at Wakatobi Marine National Park, Indonesia. However, all sampling sites in the Indonesian study are located at the exposed fringing reefs subjected to high sedimentation, moderate-high wave action and strong current. Hence, it is believed that larvae S. corniculatus has local adaptations for selecting preferable habitat to settle down.

15.5 Colour Polymorphism of Spirobranchus corniculatus at Pantai Pasir Cina

The outcome from the current survey shows that a total of nine colour and pattern variations can be seen in the S. corniculatus population at Pantai Pasir Cina. The number of colours is higher than another study done by Song (2006) in French Polynesia, which was five. The higher number is probably because of the classification used in the present study, which includes colouration pattern. A total of four colour patterns was observed on S. corniculatus in this study, while none was reported in French Polynesia (Song 2006). It is believed that striped colours were also present during the 2006 study at French Polynesia, as shown in the publication (Song 2006: Fig. 3). However, they were clumped together based on the primary colour of the radiolar crown. Also, the French Polynesia study did not employ colour correction approach, and only representatives of S. giganteus with different colours were photographed; whereas in this study, images of each everted S. corniculatus within the sampling belt were taken for colour correction analysis. Hence, the marigold colour in Song (2006) is probably yellow and orange, while purple and brown might consist of a plain and striped pattern of the same colour and may include green as revealed in the current study.

Blue is the dominant colour for S. corniculatus across the reef flat at Pantai Pasir Cina. Interestingly, white was the dominant colour for S. giganteus in French Polynesia (Song 2006). Although the number of colours recorded is high, the difference (in percentage) between dominant and the least dominant colour at Pantai Pasir China is huge (42%) compared to 13% at French Polynesia. Nevertheless, as suggested by Nygren et al. (2011), the cause of evolution and maintaining of colourmorph in polychaete is still speculative as no possible explanation can be made for the colourful character. Other polychaete species that have colour polymorphisms including H. imbricate (Polynoidea) and Pomatoceros spp. (Serpulidae) (Føyn and Gjøen 1954; Nygren et al. 2011). The crossbreed experiment between blue and yellow Pomatoceros sp. produced infertile offspring with blue was the dominant colour (Føyn and Gjøen 1954).

15.6 Conclusion

The Christmas tree worms from Pantai Pasir Cina are in symbiosis with hermatypic coral species from genus Porites. Other potential hosts reported from other studies are minimally chosen by S. corniculatus, which may indicate this species has preferred local host. Blue was the primary colour of radiole crown and can be found in all depths. However, the reasons for host preferences and colour variation in the CTW population in Pantai Pasir Cina are still unknown and warrant for further investigation.