Seagrass in Southeast Asia: a review of status and knowledge gaps, and a road map for conservation

Seagrass distribution and extent by biogeographic region

There are six seagrass bioregions that encompass all the oceans of the world, across both tropical and temperate waters (Short et al. 2007). Southeast Asia lies within the Indo-West Pacific bioregion (Bioregion 5), a vast region stretching from east Africa to the eastern Pacific Ocean, notable for being the largest and most biodiverse (24 species). However, Southeast Asia itself is potentially a distinct biogeographic province within the Indo-West Pacific, as indicated by the cluster analysis by Fortes (1988) for the seagrasses of the Indo-West Pacific. The Philippines and Brunei Darussalam were also shown to be slightly differentiated from other areas because of high seagrass species numbers in the former and low species numbers in the latter (Fortes 1988), which suggests that even finer-scale regions within Southeast Asia may exist, if based on updated distribution data.

In this review, we use the Marine Ecoregions of the World (MEOW) biogeographic scheme to provide the geographical context for seagrass distribution. The MEOW biogeographic scheme classifies all coastal and shelf areas of the world according to benthic and pelagic biota (Spalding et al. 2007), producing a nested system of 12 realms, 62 provinces, and 232 ecoregions. Based on this classification, the seas of Southeast Asia consist of seven provinces and 22 ecoregions (Figure 2), extending from the Bay of Bengal and the Andaman Sea in the west, to the Arafura Sea in the east. The provinces vary in size, with the largest being the Western Coral Triangle Province, which contains seven ecoregions. The Bay of Bengal Province and Sahul Shelf Province are only partly included in what we define as Southeast Asia in this review, which explains their relatively small size in Figure 2.

Figure 2:

Marine provinces and ecoregions of Southeast Asia, based on Spalding et al. (2007).

Provinces are made out of ecoregions with the following codes: 20108 Northern Bay of Bengal; 20109 Andaman and Nicobar Islands; 20110 Andaman Sea Coral Coast; 20111 Western Sumatra; 20112 Gulf of Tonkin; 20114 South China Sea Oceanic Islands; 20115 Gulf of Thailand; 20116 Southern Viet Nam; 20117 Sunda Shelf/Java Sea; 20118 Malacca Strait; 20119 Southern Java; 20120 Cocos-Keeling/Christmas Island; 20126 Palawan/North Borneo; 20128 Sulawesi Sea/Makassar Strait; 20129 Halmahera; 20130 Papua; 20131 Banda Sea; 20132 Lesser Sunda; 20133 Northeast Sulawesi; 20139 Arafura Sea.

Species richness at the province level is highest in the Sunda Shelf and Western Coral Triangle (15 species). Within these provinces, species richness in the individual ecoregions ranges from 3 to 14 species (Table 1), but note that we excluded Halophila gaudichaudii and Halophila tricostata from our dataset because of locational uncertainty. Low species counts were found in the Cocos-Keeling/Christmas Island ecoregion (3 species) and the South China Sea Oceanic Islands ecoregion (4 species). Both ecoregions are fairly isolated, comprising atolls with lagoon seagrass meadows. Low species richness here likely reflects either a limited dispersal pathway between meadows in the greater Southeast Asian region and these remote sites, or a lack of suitable ecological drivers for the majority of species in these lagoons.

In contrast, the Malacca Strait emerges as an ecoregion of special interest in terms of species richness. It is amongst the smallest of the ecoregions but supports 14 seagrass species (Table 1). This narrow strait, measuring 926 km in length, is one of the busiest shipping lanes in the world because it connects the Indian Ocean to the South China Sea (Mokhzani 2004, Ibrahim and Nazery 2007). This may partly explain its high seagrass species richness, as in the case of marine fish (Carpenter and Springer 2005). In an analysis of global shore fish biodiversity, the location of the strait in an area of overlap between Indian and Pacific ocean fauna was suggested as a likely explanation for high species richness (Carpenter and Springer 2005). In terms of gene flow, this ecoregion is recognised as the Indo-Pacific Barrier (Bowen et al. 2016), the equivalent of a marine Wallace line that separates populations of marine fauna on either side of the strait through shifts in sea level during periods of glaciation. This insight is useful in guiding the selection of sampling locations for seagrass phylogeographic studies that address questions about biodiversity distributions in Southeast Asia, and specifically in testing hypotheses about Southeast Asia as a centre of overlap, refuge, accumulation or centre-of-origin for seagrass, such as those suggested by Mukai (1993) and Nguyen et al. (2013), Nguyen et al. (2014). However, we see the need to draw attention to the fact that development in the Malacca Strait due to shipping, port construction, and land reclamation are likely factors that will determine how rapidly seagrasses, as well as other marine ecosystems, are likely to change in the near future (Mokhzani 2004, Ibrahim and Nazery 2007).

The most widespread species in Southeast Asia is Thalassia hemprichii, which had distribution records in all ecoregions, even in locations as remote as the South China Sea Oceanic Islands. Cymodocea serrulata and Cymodocea rotundata are common species as well, occurring in all ecoregions except for the South China Sea Oceanic Islands and the Cocos-Keeling/Christmas Islands. Species that were unique to one ecoregion were Halophila sulawesii (Kuo 2007), with only one record in Samalona Island of the Spermonde archipelago (see also: Taxonomic Highlights, below), and Zostera japonica in the Gulf of Tonkin (Luong et al. 2012). Halophila major and Halophila ovata are also limited to single ecoregions in the Northern Bay of Bengal, and the Andaman and Nicobar Islands, but this may be because these forms are taxonomically difficult to identify (addressed in Taxonomic Highlights below), although recent progress has been made in molecular approaches (Nguyen et al. 2013, 2014).

The extent of seagrass meadows in Southeast Asia is currently 36,762.6 km² (Table 1). The largest areas are in the Palawan/North Borneo (20,115 km²), Eastern Philippines (7159 km²) and Banda Sea (8246.2 km²) ecoregions, all of which are part of the Western Coral Triangle Province. Not all ecoregions are as well-represented in terms of seagrass meadow estimates. The South China Sea Oceanic Islands, Western Sumatera, Northeast Sulawesi, and the Arafura Sea ecoregions, for example, have obvious information gaps. These will be further highlighted in Section “Areal gaps in knowledge and information”.

Seagrass distribution and extent by country

Recent updates now show Southeast Asia to have 21 seagrass species in nine genera and four families, which makes up 29% of the world’s seagrass species (Table 2). Seagrass species diversity is highest in the Philippines (19 species), and lowest in Brunei (7 species), which is the country with the most recent additions to its species list (Lamit et al. 2017).

The nation states of Southeast Asia have a collective coastline of more than 100,000 km that encompass at least 675,824 km² of territorial seas (Flanders Marine Institute 2016). The Philippines has the largest seagrass extent, with seagrass meadows constituting at least 24% of its territorial waters – the largest proportion in the region (Table 3). In contrast, Myanmar and Malaysia have the lowest proportion of known seagrass areas relative to the size of their territorial seas (≤0.02%), while Timor-Leste has yet to produce areal estimates of seagrass meadows. This provides a guide to which countries in particular require greater capacity-building in developing spatial databases for seagrass.

Taxonomic notes

The seagrass species list of Southeast Asia (Table 2) shows 21 species, but some of these are still considered taxonomically uncertain. The genus with the greatest number of unvalidated species is Halophila. This genus has high taxonomic diversity, but its constituent forms appear to have overlapping leaf morphologies that have made validation problematic. The plasticity of this species in response to different substratum, salinity, and light regimes has been demonstrated (Young and Kirkman 1975, Benjamin et al. 1999, Japar Sidik et al. 2010), and is the main reason for taxonomic uncertainty on the basis of morphological traits alone. In Table 2, we show Halophila to consist of nine recognised species and two undescribed species, Halophila sp. 1 (the Philippines) and Halophila sp. 2 (Malaysia and Philippines). Amongst those we list as recognised species, however, we acknowledge that H. major, H. gaudichaudii, H. minor, and H. ovata, which are regarded as being part of the H. ovalis complex (Waycott et al. 2004), which may now include H. sulawesii, are undergoing taxonomic scrutiny in this region, which we briefly summarise below.

In Southeast Asia, Halophila major has been studied in greater detail than other species in its genus, through a combination of morphological and molecular traits. As a result, it has become a recent entry into the species records of Indonesia (Tuntiprapas et al. 2015), Thailand (Tuntiprapas et al. 2015), Malaysia (Japar Sidik pers. obs; see Figure 3), Myanmar (Nguyen et al. 2014), Viet Nam (Nguyen et al. 2013, 2014), and the Philippines (Kim et al. 2017). Halophila minor and Halophila ovata were treated as synonyms for the seagrass flora of Singapore (Yaakub et al. 2013) despite being recognised as two distinct species by Kuo (2000). However, H. ovata was subsequently considered an illegitimate name and proposed as Halophila gaudichaudii by Kuo et al. (2006). As a result, all these confounding species, i.e. H. minor, H. ovata and H. gaudichaudii are present in the species records of this region, and are reported as such in this review on the grounds of maintaining the transparency of these species lists until a taxonomic consensus is reached. We note, however, that H. major appeared in the records of Viet Nam (Southern Viet Nam ecoregion) and Myanmar (Northern Bay of Bengal ecoregion); H. gaudichaudii in the records of the Philippines (ecoregion undetermined); and H. ovata in the Andaman and Nicobar Islands, and the Philippines (ecoregion undetermined).

Figure 3:

Halophila major from Tanjung Adang Laut, Sungai Pulai estuary, Johor (refer also to Nguyen et al. 2014 for morphological and genetic identification of the species).

Photo credit: © Muta Harah.

In Table 2, there are two unidentified Halophila species, i.e. Halophila sp. 1 from Malita, Davao del Sur, the Philippines (Fortes 2013) and Halophila sp. 2, from a mangrove area of Teluk Sepinong, Sandakan, Sabah, Malaysia (Japar Sidik and Muta Harah 2011). Halophila sp. 1 needs further verification. However, Halophila sp. 2 (Figure 4), was also reported as an uinidentified Halophila sp. nov., collected off Molleangan Island, near Banggi Island, Sabah (Rajamani and Marsh 2015), which has recently been described and identified as Halophila tricostata using molecular ITS sequence data in the Philippines (Calumpong et al. 2010, Tiongson 2012). Halophila tricostata is considered endemic to the east coast of Australia (Greenway 1979) and its presence in the species records of Southeast Asia indicates its potential for long distance dispersal from the Great Barrier Reef of Australia to the Palawan/North Borneo ecoregion.

Figure 4:

Halophila sp. 2 collected in 1997 at a mangrove area of Teluk Sepinong, Sandakan, Sabah, Malaysia.

Photo credit: © Japar Sidik.

The genus Halodule is another taxon that has been a source of uncertainty and confusion in species identification because of overlapping morphological characters (leaf width, leaf length dimensions) and species separation through their leaf tips (Phillips 1967, den Hartog 1970, Japar Sidik et al. 1999). Halodule pinifolia is considered to be the narrow-leaved form of Halodule uninervis (Waycott et al. 2004), but these have been shown through genetic analysis on samples in the Philippines to be separate species that have morphological variations in leaf width because of site-specific differences, density and exposure (Wagey and Calumpong 2013). Thus, we have maintained them as different species in Table 2.

Areal gaps in knowledge and information

Information on seagrass in Southeast Asia is geographically unbalanced, with hotspots and coldspots of research effort. Within hotspots, the level of information itself is variable, with some providing reports of species presence, while others provide both species presence and estimates of meadow size. Estimates of meadow size are rarely reported because of the logistical challenges in mapping seagrass meadows. It has only been in recent years that areal estimates for seagrass meadows have begun to emerge more rapidly as a result of advancements in remote sensing technology and well-funded regional projects such as the UNEP/GEF South China Sea Project (UNEP 2008), the Bay of Bengal Large Marine Ecosystem Project (BOBLME 2015), and the JSPS-Asian CORE Project. We consider meadow size data to be particularly critical for moving seagrass conservation and management forward in the region because these provide baselines for understanding ecosystem trajectories, either under natural conditions or in response to environmental change over the long-term, as in the case of the global analysis of seagrass trajectories by Waycott et al. 2009. In this review, information gaps by geographic areas are visualised by plotting locations where data on species presence, meadow size, or both, are available in the region (Figure 5).

Figure 5:

Level of seagrass information available within the Southeast Asian region.

There is quite an even spread of sampling sites and a high level of information (species presence and seagrass areal extent) in the Gulf of Tonkin, the Gulf of Thailand, the Eastern Philippines, Lesser Sunda and the continental part of the Andaman Sea Coral Coast ecoregion (see solid points in Figure 5).

Ecoregions that potentially have seagrass habitats but which are data depauperate include:

1. The South China Sea Oceanic Islands, with merely one data point in the Layang-Layang atoll and no meadow area estimates;

2. The Sulawesi Sea/Makassar Strait, with most of the data points clustered on the southwestern and northeastern coastline of Sulawesi, with no meadow area estimates;

3. The Sunda Shelf/Java Sea, especially on the islands of Borneo and Sumatera;

4. The Arafura Sea, which has just one data point, in the Aru group of islands.

Accessibility to seagrass sites influences the distribution of data points in the region, to a certain extent. Some sites are inaccessible to researchers because they are remote or are under territorial dispute. The South China Sea Oceanic Islands, which include the Spratly Islands, have both characteristics: they lie right in the centre of the South China Sea and have been the subject of multiple overlapping maritime claims by the Philippines, Malaysia, Viet Nam, Brunei, Taiwan and the People’s Republic of China for more than 50 years. Because they are physically isolated, these sites are natural laboratories for testing ideas about allopatric differentiation in seagrass and seagrass-associated species, and to elucidate seagrass dispersal routes in the region. To take the example of fish larvae in the Spratly Islands, larval drift time and vector current charts indicate that the western Philippines, Taiwan, south-eastern China, Brunei, and Malaysia are direct sink habitats for coral reef fish from the Spratlys (McManus 2017). Long-distance dispersal in seagrasses has also been shown to be possible through seeds, fruits, viviparous seedlings and vegetative fragments, all of which have the capacity to move over hundreds of kilometers in distance (Kendrick et al. 2012). However, if seagrass scientists in the region hope to fill in this data gap, rapid action is necessary because of the amount of recent island-building in this ecoregion as a result of intense territorial claims (Southerland 2016). Island-building often involves sand-dredging and land reclamation on shallow coral reefs and in lagoons. To date, two-thirds of currently occupied atolls in the Spratlys have been shown to have proportionally less reef extent than unoccupied atolls, implying the detrimental effects of island-building on reef systems (Asner et al. 2017). Along with these reefs, seagrasses may also be equally damaged before being recorded and studied for science.

Google Earth images of the the Sulawesi Sea/Makassar Strait ecoregion show the presence of soft substrate coastlines, large estuaries, and outlying islands which are often associated with seagrass. Seagrasses appear to be widespread in this ecoregion, and the area of Derawan, east Kalimantan, in particular has been the subject of study (McKinnon et al. 1996, van der Zon 2010). However, the available sources mentioned seagrass in the area in a broad sense, without giving details of locations, full species list, or meadow extent. Similarly, the Sunda Shelf/Java Sea ecoregion has sparse datasets on the Malaysian side of Borneo despite anecdotal evidence for large areas of seagrass along those coastlines (Japar Sidik pers. obs.).

An observation that came up in this effort to review updated seagrass species and meadow information was that these were often categorised according to countries. This is certainly useful from a national point of view, but for seagrass science to be cohesive at the regional level, we need to ensure that information about species and meadow estimates are both sea-specific and country-specific. In this review, we used MEOW bioregions for this purpose. However, other biogeographic schemes may be just as useful, and we regard the use of bioregions as a starting point for scientists in the region to discuss data and information needs when collaborating on regional-scale studies.

Thematic gaps in knowledge and information

Seagrass research in Southeast Asia is increasing based on the number of research papers that have been produced in the last decade (Ooi et al. 2011a), and an update of the number of research articles, reports and studies that have been reported in the region has shown a steady increase in research output decade by decade for most countries (Figure 6). However, there are still noticeable gaps in knowledge in Cambodia, and Myanmar, as well as places like East Timor, Brunei, and the Cocos (Keeling) Islands. There is also an increase in the number of research papers, reports, and theses published by authors originating from or based in the country or region itself, which indicates an increase in research interest and capacity of local scientists. There has been an increase in the number of national or regional journals being made available online, which has increased the visibility of the research being published, along with academic sharing and networking sites, such as ResearchGate™ which allows researchers with a verified profile to share their research output – both in journals as well as in other forms, such as reports, posters, conference proceedings, book chapters, etc. – to be shared publicly and directly with the platform’s audience.

Figure 6:

Research output per decade by country/territory.

Numbers based on searches on Web of Science and updated from Ooi et al. (2011a).

Taxonomic research continues to be a mainstay of the research efforts in this region, with new species – particularly in the Halophila ovalis species complex (Waycott et al. 2004) – being described (see Kuo 2007, Japar Sidik and Muta Harah 2011, Fortes 2013). However, there is an obvious need for traditional morphological seagrass taxonomy to embrace new methods in the field. There is currently already a Global Initiative to Barcode Seagrass (GIBS) based at the State Herbarium of South Australia and the University of Adelaide (GIBS 2018), and more participation from researchers in the Southeast Asian region may be beneficial for the advancement of seagrass taxonomy.

There is an increasing trend of research output for the region as a whole (Ooi et al. 2011a; Figure 6), and there are some distinct trends in the intensity of work within each thematic research area across the decades (Figure 7). There was a surge in the number of seagrass ecology and environment related research from the 1990s onwards, and this is by far the most productive research area in terms of output. There has also been a progression in this field moving away from purely descriptive to more experimental studies examining interactions and cumulative stressors and anthropogenic impacts of the major causes of seagrass decline such as sedimentation (Cabaço and Santos 2007, Manzanera et al. 2011, Ooi et al. 2011b, Han et al. 2012), water quality declines and light reduction (Bite et al. 2007, Leoni et al. 2008, Baden et al. 2010, Collier et al. 2011, Yaakub et al. 2014a), changes in temperature (Campbell et al. 2006, Collier and Waycott 2014, Gao et al. 2017), and competition with macroalgae (Davis and Fourqurean 2001, Taplin et al. 2005, Martinez-Luscher and Holmer 2010, Holmer et al. 2011).

Figure 7:

Research output for the Southeast Asian region by thematic area presented as decadal totals.

New research themes also emerged in the 1990s concerning conservation and management (e.g. Fortes 1991, Kirkman and Kirkman 2002, Unsworth and Cullen 2010), and connectivity of seagrass habitats (e.g. Fortes 1988, Vermaat et al. 2004), likely in response to the trend of habitat loss from the rapid population expansion across Southeast Asia between the mid-90s and the present. There were also some new research areas – such as genetics (e.g. Matsuki et al. 2013, Nakajima et al. 2014, Arriesgado et al. 2015, Hernawan et al. 2017) and blue carbon (e.g. Miyajima et al. 2015, Alongi et al. 2016, Rozaimi et al. 2017) – that have increased in intensity, advancements, and improvements in protocols and methodology. More traditional research areas, such as mapping of areal extent of seagrass habitats, also received a boost in research output with improvements in remote sensing technology, and accessibility of satellite imagery. Continued interest in this field and expansion of research into more remote areas can help improve and continue to address information gaps in areal extent of seagrass meadows in the region, and also start to expand into examining seasonal variation and decline.

Despite the continued increase in research, it is plain to see that a lot of work still needs to be carried out in order to address the gaps in knowledge and information. For example, there is virtually no social science research examining the social, cultural and economic aspects of human-seagrass interactions, and there is research emerging that points to important relationships between coastal populations and seagrass beds (Cullen-Unsworth et al. 2014). Furthermore, while the significance of seagrass fishery activity has been acknowledged globally (Nordlund et al. 2017), the lack of information on seagrass fishery resources and the flow-on benefits from ecosystem services it provides in the Southeast Asian region is a data gap that needs to be addressed (Unsworth et al. 2009). In Table 4, we suggest the direction for existing and new thematic research areas, as well as potential areas for regional research cooperation.

A roadmap for seagrass conservation and research in Southeast Asia

An example of sharing platforms would be the International Seagrasss Biology Workshop (ISBW). The ISBW series is a meeting of research scientists, students, and coastal environment managers focusing on global seagrass issues, improving seagrass knowledge, developing networks and advocating seagrass protection or conservation. Twelve ISBWs have been held and each followed individual themes reflecting both a geographical or institutional interest, and current trends in seagrass research as new knowledge and techniques became available (Coles et al. 2014). The 12th ISBW held in Nant Gwrtheyrn in North Wales focused on securing a future for seagrass. The 13th ISBW, to be held in Singapore in June 2018, will have a theme of “Translating Science into Action”, and will focus on current developments in seagrass science and how it can be effectively developed into actions, programs, and policies that will aid in seagrass conservation and management. These outcomes are important, not just for the Southeast Asian region, but globally as well.

Regionally, there is the option of leveraging on existing platforms to foster sharing and cooperation, such as the Association of Southeast Asian Nations (ASEAN) Cooperation on Environment. This regional organisation holds nature conservation and biodiversity, and the coastal and marine environment as two of its seven strategic priorities (ASEAN Cooperation on Environment 2017). Getting seagrass conservation on the ASEAN environmental agenda would be a big boost in terms of fostering cooperation, collaboration, and knowledge sharing in the region. This in itself, will be an uphill task, especially since there are competing environmental issues, such as transboundary haze, which are more visible and seemingly have wider regional urgency. There are also other ASEAN-related bodies, such as the ASEAN Center for Biodiversity, which could be a smaller and more manageable platform to launch the seagrass conservation and management agenda for the region.

It is likely that the degradation of seagrass ecosystems is expected to continue, despite greater local and region-wide conservation efforts and the promises of programs and projects being implemented and planned. At present, there appear only two likely options left for us: status quo or “business as usual”, wherein coastal development are intensified, but with almost complete disregard of relevant scientific knowledge and pertinent laws; or protect and enhance what remains of the ecosystem, wherein people are given the opportunity to conserve and enjoy them for themselves and the future generations. It is easy to argue in favour of a combination of these approaches, but as the past years have shown, this has been easier said than done. To our knowledge, success along this line in the region has been insignificant – in both temporal and spatial magnitude and scale – in relation to the total area of coastal space utilised and the amount of resources spent. There is an increasing likelihood that coastal environmental change will create a need for adjustments of established ecosystems on spatial and temporal scales that are unprecedented in SE Asian history. Hopefully, these adjustments are not compromises to the detriment of seagrass ecosystems.

Sound conservation and management of our seagrass ecosystems can be realised. Basic human survival as well as robust national and global socioeconomic arguments underline the compelling need for the effort. The specific interventions in improving seagrass management in the world have been spelled out even as early as the 1990s (Fortes 1991, UNEP SCS/SAP 1999) and more recently by UNEP (2012), but even with these, a secure future for the region’s seagrass resources seemingly remains out of sight. Trajectories toward seagrass loss can be reversed if and when all concerned stakeholders contribute positively to the effort in reversing current coastal ecosystem degradation trends. In order to sustain the benefits we all derive from these natural assets, substantial commitments and investments must collectively be made by communities, scientists, local government units, national government agencies, and assisting organisations to effect a change from the current self-destructive course to one of conservation and sustainable use. Indeed, a transdisciplinary approach is required, with each proposed step undertaken in a holistic manner and not separately or compartmentalised. There is a great opportunity and compelling grounds for regional collaboration and cooperation to tackle the issue of seagrass conservation. It would be a tragedy to let it slip.