Thalassia hemprichii (Sickle Seagrass)

Introduction



Similar to the grass in the field or on your lawn, seagrasses grow to form homogeneous looking patches of greenery. Everything looks consistent and similar – you can barely tell an individual plant from another (Figure 1).
DSC_0355.jpg
Figure 1: A typical seagrass patch. (Photo taken by Cheok Zi Yu)
As you imagine a big continuous expanse of grassland – it is not difficult to imagine cows on the field, contentedly munching away. Similarly, seagrass patches have their own grazers – the sea cow or Dugong (Figure 2)!
The cows.png
Figure 2: From left, the domesticated cow and its marine counterpart, the sea cow, or Dugong both grazing on their favourite foods. Images under Creative Commons license
However, the seagrass is not a grass – the two are very distantly related groups. This is due to evolutionary reasons: Seagrasses, of the Alismatale family, are considered one of the basalmost group of monocots and are considered "primitive" compared to true grasses. With the advent of genetic studies, it was proven that seagrasses form a group on their own, separate from true grasses[1] .

So, what is a seagrass?

A seagrass is:
  1. An angiosperm
  2. Has acquired tolerance to submergence and salinity
  3. Hydrophilous
  4. Clonal
  5. Able to compete effectively in marine environments
Out of all the coastal ecosystems in the world, seagrass ecosystems are the least well-known, in terms of both scientific knowledge as well as public awareness of the habitat[2] . However, as the human population grows, the coasts are increasingly under anthropogenic pressure, leading to large scale, devastating declines in seagrass habitats[3] . Coupled with lack of research and public awareness, conservation of seagrass ecosystems remains limited and lacking compared to other coastal ecosystems[2] .
This page strives to educate about seagrass habitats and their conservation, with a focus on the island-state of Singapore and an important but under-studied seagrass species, Thalassia hemprichii. In this section, we emphasize the importance of seagrass habitats and the anthropogenic reasons behind their decline, with a focus on seagrass meadows in Singapore.

Thalassia hemprichii

TH image.jpg
Figure 3: Thalassia hemprichii when submerged. Image courtesy of Ria Tan (Wildsingapore)
Thalassia hemprichii is a species of seagrass native to the island-state of Singapore (See distribution). It is considered relatively rare in the country, and listed as “Critically Endangered” in the Singapore Red List Databook[4] . However, T. hemprichii in an important component of mature seagrass habitats due to its biological characteristics. It has the following biological properties of a climax species:
Thalassia hemprichii dominated meadows tend to be in close proximity with mangroves and coral reefs *[7] , forming an intricate network of biological and chemical relationships with these habitats[8] [9] and creating a stablising effect on the coastal environment[10] .

Habitats to Ocean Life

The following video gives you a glimpse into the variety of wildlife found in a temperate seagrass habitat, imagine how much richer a tropical seagrass meadow could be!
Video courtesy of Aquaworks Underwater Films
Within the meadow lies a thriving ecosystem of invertebrates, fishes and organisms seeking shelter within the canopy of leaves and the dense root and rhizome network within the soil[11] . Infauna bury and feed off the soil, amongst the seagrass roots, which is rich in organic matter[7] . Above the soils, epiphytes anchor themselves to the leaves of seagrasses to feed and fishes, mature and juveniles of various species[12] , weave themselves amongst the leaves[2] . In turn, carnivores at the top of the food chain, such as seastars feed on the rich array of invertebrates found in the habitat (Figure 4). Particularly in T. hemprichii dominated meadows, a variety of other primary producers such as calcerous, fleshy, rooted or free floating algae also inhabit the meadows.
Seagrass organisms.png
Figure 4: From left, Hippocampus comes, Tiger Tail Seahorse (image courtesy of Ria Tan (Wildsingapore)) and Pentaceraster mammillatus, Pentaceraster Sea Star (taken by Cheok Zi Yu) found on seagrass patches in Singapore
Seagrass meadows are also host graceful visitors such as the Dugong, or the Sea Cow (Dugong dugon), and sea turtles. Dugongs consume large amounts of seagrass everyday. Their tendency to chomp as they move over the meadow often leads to the formation of feeding trails (Figure 5) – clear lanes of bare sediment where the seagrass has been pulled up. Seagrasses are also major food sources of sea turtles[13] .
Dugong - WildSingapore.jpg
Figure 5: A dugong feeding trail
Without seagrass ecosystems, an estimated 70 species of fishes and invertebrates are in danger of losing their homes and becoming extinct[6] .

Ecosystem Services

Seagrass medows provide numerous ecosystem services, summarised in Figure 6 below, cumulating to a value of USD $19,004 per hectare per year! This value is almost twice that of other coastal ecosystems, where each has values of between USD $6,000-10,000 [1] .
Seagrass Ecosystem Services_v2.png
Figure 6: Ecosystem services provided by seagrass meadows, information from Barbier et al., 2011

 Seagrass meadows are home to commercially important species such as Giant Tiger Prawns (Peneaus monodon and P. semisulcatus), Whitings (Merlangius merlangus), Snappers (Lutjanus synagris, L. apodus etc.) and more. Decline of seagrass meadows has been predicted to cause significant economic losses in the fishery industy[12] .

Seagrass meadow's high productivity and canopy cover are important in counteracting two key aspects of global warming: unprecedented levels of carbon dioxide in the air and sea level rise. Seagrasses consume carbon dioxide in the water as they grow, storing carbon and acting as a carbon sink[14] . This is particularly true of the persistent climax seagrass species such as T. hemprichii, which are long lived[15] . The leaves of seagrasses slow down wave velocity during storms and their roots stablise sediments, protecting coasts from erosion, which is important as the sea level continues to rise[16] . T. hemprichii meadows are also thought to experience enhanced deposition relative to meadows where other species dominate[7] , an added benefit of having this species around!

Human Impacts on Seagrass Meadows

Throughout the world, seagrass habitats are declining at devastating rates[3] . The reduction in percentage of seagrass cover in the world has already decreased by 30% and habitats continue to decline at a rate of 7% per year. If this estimated rate continue unabated, seagrass habitats will disappear within a few decades.
Large scale coastal modification activities such as land reclamation bury whole seagrass meadows[17] and increases sediment content in local waters[18] , blocking sunlight reaching the surface of seagrass leaves. Uncontrolled nutrient input from discharges into rivers also cause eutrophication in coastal waters, further lowering light availability[19] . Other mechanisms leading to seagrass loss include mechanical damage by boats [2] and their susceptibility to rising sea levels.

Seagrass Habitats in Singapore

Seagrass meadows in Singapore are usually multispecific, comprising of multiple species, due to the richer seagrass diversity here in the Indo-Pacific region[7] . Singapore's Northern shores have greater freshwater influence compared to the exposed Southern shores due to their proximity to the Johor River in the North. Hence, the meadows in Singapore support high biodiversity due to different combinations of abiotic and biotic factors that make up each individual patch[20] .
However, seagrass habitats in Singapore have undergone drastic changes since the start of her development. Land reclamation has radically transformed the country's coasts (Chou 1998); The island of Singapore has grown by 22.9% since 1819[21] . An estimate of past seagrass extent using herbarium records by Yaakub et al. (2014)[22] found that there used to be numerous seagrass patches on the eastern coast of Singapore (Figure 7). Today, that intertidal zone is now land, and there are all but 3 patches left in the area. But there is hope yet! These 3 patches are considered newly formed since land reclamation, and without any purposeful restoration on our part! And one of them, near the Tanah Merry Ferry Terminal, contains Thalassia hemprichii!
Figure 1_edited.png
Figure 7: Seagrass meadows in Singapore in the 1950s and 2000s. Note the island's growth in size and a number of newly emerged seagrass patches on the East coast. Edited with permission from Yaakub et al., 2014
Even after the study in 2014, seagrass researchers from the Experimental Marine Biology Lab (EMEL) in the National University of Singapore (NUS) are still discovering new seagrass meadows on Singapore's coasts (Figure 8)! Recent research efforts are looking into the connectivity of seagrass patches in contributing to reslience and the potential restoration of seagrass habitats in Singapore (pers.comm.).
DSC_0345.jpg
Figure 8: This is a re-emerged (and newly discovered) patch located on the southeastern coast of Singapore. It had yet to be recorded when Yaakub et al. (2014) was published

Biology

This section covers the methods of propagation of T. hemprichii (clonal growth and sexual reproduction) before highlighting its dispersal strategies. At the community level, succession in a meadow and T. hemprichii’s global distribution relative to its sister species is examined.

Clonal Growth (Asexual reproduction)

Clonal growth is the growth of the plant from the same parent cell, meaning that new individuals or ramets are genetically identical to the parent cell. This growth mode of of T. hemprichii cannot occur without its apical meristems (see description). If the meristems are damaged, there are no known specialised responses in the plant. Only the sister species, T. testudinum has been observed to undergo 'twinning', the emergence of two foliar (leaf) tissues from a vertical shoot. Interestingly, as T. hemprichii undergoes asexual growth, the rhizome apex are known to be able to adjust their depth in the sediment in response to erosion or sedimentation[23] . When physical damage of seagrass occurs, it can lead to the formation of fragments that act as potential dispersal vectors (see dispersal).

Sexual Reproduction

Thalassia hemprichii and all other seagrass species (except for Enhalus acoroides) are hydrophilous, i.e pollination is carried out using water as the dispersal medium. This is a unique biological characteristic of all seagrasses, which is better discussed from the evolutionary point of view[24] .
Thalassia hemprichii seeds have to germinate soon after fertilisation, due to a lack of dormancy period (see dispersal). This precludes the formation of a seed bank, which is the presence of seeds in the soil that can remain dormant but viable over long periods. Research on T. hemprichii seeds found that almost all of them died within six days after burial. The high mortality is thought to be due to high oxygen respiratory requirements of the seeds[25] .

Dispersal

At high densities, population growth is limited due to competition for resources[26] . Water is an abiotic media used by many plants for dispersal[27] .
Sexual propagules (fruits and seeds of T. hemprichii) stay buoyant in the water for a few days. In contrast, naturally released T. hemprichii seeds float for a median value of 0.3h - approximately 20 minutes! The floating time is important as positively buoyant propagules are freely dispersed by ocean currents. Once the propagule's buoyancy becomes negative, the features on the bottom of the seafloor becomes an additional obstruction factor[28] . Therefore, the distances travelled by T. hemprichii fruits are longer than that of its seeds:
Estimated distance travelled
 T. hemprichii[29]
 T. testudinum[30]
Seed
 less than 5km
 0.06-3km
Fruit
 23km
 less than 1-15km
The dispersal potential of the seeds, coupled with a lack of dormancy, has therefore raised questions about the importance of sexual reproduction of T. hemprichii. Do they merely serve to increase genetic diversity[7] ?
Fragments have long been speculated to be an asexual method of dispersal for seagrass. Recently, there has been a number of publications on T. hemprichii fragments as potential dispersal vectors. Wu et al. (2016)[31] , found that T. hemprichii fragments with an apical meristem have a long viability period of up to 3 months, and can potentially act as dispersal vectors. While observed colonization of new habitats by fragments of this species has yet to be reported, Rollon (2001)[32] has documented the emergence of a young T. hemprichii meadow on an isolated Pacific island, a distance floating seeds are unlikely to travel. Combined with local discoveries of re-emerged seagrass meadows containing T. hemprichii, such as the patch in Figure 8, this hints at the possibility of the species being able to disperse via vegetative fragments.

Succession in Seagrass Meadows

Within a meadow, small, round-leaved species dominated closest to the shore. Towards the ocean, narrow leaved species follow before they are replaced by T. hemprichii and other large-leaved species.
This zonation is the result of the community succession process - initially, the pioneer species Halophila ovalis rapidly colonises an appropriate patch of barren land, either via seed banks or fragment settlement. H. ovalis will then alter the soil composition, facilitating its own replacement as the dominant species by narrow-leafed species (Halophila uninervis), and finally by climax species such as T. hemprichii[7] .

Distribution

Thalassia hemprichii is mainly found along the coasts in the Indo-Pacific region, while T. testudinum is native to the Carribean sea, extending to the Bermudas.
Worldwide Dist - Sister species.png
Figure 9: From top, a) distribution of Thalassia hemprichii; b) distribution ofThalassia testudinum. From Discover Life[33][34] . Note that the lone demarcation of T. testudiunum in the east coast of Africa is due to a preserved specimen and is not indicative of the distribution of the species.
Since the two sister species have non-overlapping global distributions, they are thought to be the result of allopatric speciation (see evolution).

Taxonomy

This sections provides a detailed description of T. hemprichii and its diagnosis. We provide insight into its formal name, type specimen and finally, its unique evolution.

Description

Detailed descriptions of seagrass morphology and growth habit for the Thalassia genus were only published in the 20th century. Prominent ones include papers by den Hartog (1957[35] & 1970[36] ), Tomsonlin (1974[37] ) and Tomsonlin and Vargo (1966[23] ). Tomlinson (1974) admitted that his conclusions were merely based on "superficial dissection", and called for more studies on seagrass morphology. However, the advent of DNA sequencing and other molecular methods after his publication likely resulted a further decrease in emphasis on morphology descriptions in taxonomical studies.
The habit descriptions below were described for the sister species of T. hemprichii - T. testudinum. Morphologically, both species are essentially similar (see diagnosis and [[Thalassia hemprichii#Evo|evolution).
Figure 5.png
Figure 10: Key morphological characters of T. hemprichii. The scars on the rhizome and thick sheath are diagnostic traits that differentiate this species from other seagrass species in the region. Photographs taken by Cheok Zi Yu
The general habit of T. hemprichii is depicted in Figure 10. The thick horizontal rhizome has numerous vertical shoots separated by an odd number of scale leaves. The vertical shoots bear foliage-leaves, which are encompassed in a thick sheath, the leaves are curved and rounded at the tip[36] . The membranous scale leaves encompass the younger portions of the rhizome but can be counted as they fall off and leave behind triangular scars on the rhizome. The scars are a diagnostic feature of the species. The apical meristem gives rise to vertical shoots. Some vertical shoots may branch into a new horizontal rhizome and apical meristem, however the intervals at which this happens is difficult to predict and hence considered "irregular". The production of a new meristem from vertical shoots is thought to be function of the age of the shoot[23] .
Thalassia hemprichii is known to be highly organised and meristem-dependent in its growth due to the following reasons[23] :
TH Reproductive Structures_v2.png
Figure 11: Reproductive structures of T. hemprichii. 1) Fruit; 2) Flower; 3) Seed. Drawing is under creative commons license Wikipedia page and image of the seed is courtesy of Ria Tan (Wildsingapore)
Flowers of T. hemprichii are dioecious. Female flowers have six styles and occur singly, while male flowers have between three to 12 stamens and occur in groups. Flowers usually occur seasonally[7] , and pollination occurs via hydrophilly[24] . The fruit is globular and prickly. The seeds are rich in proteins and starchy, and are cryptoviviparious. They lack a dormancy period and have to germinate soon after release from the parent plant[37] .

Diagnosis

TT image - CC.jpg
Figure 12: Thalassia testudinum, which looks very similar to Thalassia hemprichii
T. hemprichii and its twin species, T. testudinum are two morphologically very similar species - it is difficult to tell them apart except at a macro-scale. One can use their flowers to differentiate the two organisms:
Flower structure (sex)
 T. hemprichii
 T. testudinum
Number of styles (female)
 6
 7-8
Stigmatic branches (female)
 Shorter then its sister species
 Longer than its sister species
Number of stamens (male)
 3-12
 9
Thankfully, the native ranges of these two species do not overlap (see distribution).

Classification and Nomenclature

Kingdom
 Plantae







Phylum
 Tracheophyta







Class
 Liliopsida







Sub class
 Alismatidae








Order
 Hydrocharitales







Family
 Hydrocharitaceae







Genus
 Thalassia







Species
 Thalassia hemprichii
Higher ranks of T. hemprichii are different for different sites (see further information) - implying the arbitrariness or lack of use of such rankings. The highest ranking commonly used by seagrass scientists is the subcalss Alismatidae or family Hydrocharitacea.
Common names: Sickle Seagrass, Dugong grass, Turtle grass (shares this name with its twin species, T. testudinum)
Species name: Thalassia hemprichii (Ehrenb. ex Solms) Asch. 1871
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Original taxonomical document by Ascherson[38]Read online
Thalassia is a genus with only 2 members, which are sister species. They are often coined “twin” species, due to a lack of obvious features to differentiate the two[7] .
Synonym: Schizotheca hemprichii Ehrenb. ex Solms 1834
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A snapshot (incomplete) of the original description of the species (in German)[39]Read online
Ehrenberg was the first to name the species, placing it under the genus Shizotheca[39] . Subsequently, Ascherson redescribed the species under genus[38] . Shizotheca hemprichii is therefore now a synonym.

Type Information

The original holotype collected by Ehrenberg cannot be located and appears to have been lost. Ferrer-Gallego and Boisset (2015) subsequently selected what they called a “lectotype” for T. hemprichii after evaluating all the herbarium sheets that have been referenced for the species. The “lectotype” is currently designated as: Eritrea, Massaua, Mare rubrum, Ehrenberg s.n. (BM barcode BM000922237!; isolectotypes: K barcode K000911822!, L barcodes L1203715! & L1203710!, P barcodes P02074514! & P02074520!)[40] .
Before explaining why this new type was designated as a “lectotype” as opposed to a “neotype”, let us examine the definitions of each term for animals (under the International Commission on Zoological Nomenclature, ICZN) and plants (International Association for Plant Taxonomy, IAPT).

 ICZN
 IAPT[41]
Neotype
 To replace a missing holotype[42]
 Serves as a holotype “as long as all of the material on which the name of the taxon was based is missing”
Lectotype
 Becomes the holotype, chosen from a set of syntypes[43]
 A specimen/illustration of the original material if no holotype was indicated at the point of publication, or if holotype is missing – it takes precedence over the neotype
Ferrer-Gallego and Boisset (2015) stated in their article that they were considering “original” specimens, implying that the they were all collected as by Ehrenberg the first author of the name. Alternatively, Ehrenberg might not have clearly stated the holotype in his original publication. When considering the IAPT rules, it us unsurprising that the new type specimen was designated as a "lectotype". However, if T. hemprichii were to be named under the rules of the ICZN, then the correct term for the chosen specimen would be the “neotype” instead.

Evolutionary origin

The phylogenetic study by Les et al. (1997) was carried out using a chloroplast gene rbcL. From Figure 13, 2 possibilities on the evolution of seagrasses can be deduced: there were either 2 (set of red arrows in Figure 13) or 3 (set of orange arrows) independent evolutions that gave rise to seagrasses. The paper eventually concluded that it was likely to be three independent invasions. If there were only 2 independent evolutions, a reversal back to the freshwater adapted state for the Zannichelliaceae/Potamogetonaceae clade will be required, a process that they thought was highly unlikely.
Final Phylo.png
Figure 13: Strict consensus phylogenetic tree depicting evolutionary relationships between aquatic angiosperms, species within light blue boxes are "seagrasses" with T. hemprichii marked with a black arrow, and non-seagrass hydrophilic species are boxed in dark blue. Orange and red arrows mark two hypothetical origins of "seagrasses". Used with permission from Les et al. (1997)
The paper also examined the evolution of hydrophily in seagrasses. Hydrophily is known to be an extreme divergence from the pollination process of a typical flowering plant. This is because water disrupts contact between the pollen and the stigma, hence preventing pollination. The state of hydrophily, which uses water for pollination, would therefore require major structural and biochemical modifications to the plant’s reproductive system[44] . Since seagrasses are usually fully submerged in the ocean, hydrophily is the required adaptive trait for continued sexual reproduction[45] . As such, the evolution of hydrophily and the ability to colonise marine habitats are therefore thought to have “evolutionary affinity” (Les 1997). Les et al. (1997)’s phylogenetic tree also shows this, because even amongst aquatic plants, seagrass make up more than half of the hydrophilous species (Figure 13) .
Hence, seagrasses are an ecological group as they are not monophyletic. Instead, they are grouped together for the convenience of their distinctive ecological niche [46] .
Figure 13 also shows that salinity tolerance seagrasses did not evolve in a step-wise manner, i.e. are not evolved from a "'mangrove-like' saltwater plant". The bootstrap support for the seagrass clades within Hydrocharitaceae and Zosteraceae are 100%. For the Cymodoceaceae family the value is lower, at 40%. However, all are nested within freshwater species. Hence, seagrasses are likely to have descended from a freshwater angiosperm ancestor (Tomlinson 1974).
Specifically for the Thalassia genus , it is a clear monophyletic group within the Hydrocharitaceae family, with 94% bootstrap support. Within the genus, there are only very small-scale differences between the morphologies of the two sister species, but clear divergence was found when their DNA sequences were compared [47] . The species are hence thought to have been the result of allopatric speciation, when continental drift more than 24 million years ago split the populations of the Thalassia ancestor into two[7] , giving rise to the two sister species.

Glossary of terms

Angiosperm
 a flowering plant
Asexual Reproduction
 Incliudes seed production without fertilisation and 'selfing' (clonal growth)
Carbon sink
 a natural environment that stores carbon for a long period of time
Cryptoviviparious
 the embryo within the seed grows to become a seedling while the seed is still attached to the parent plant
Diagnosis
 Unique descriptions on a species enabling you differentiate from other species
Dioecious
 male and female reproductive organs are found on separate individuals
Epiphytes
 sessile organisms that grow on plant. Compare to the terrestrial definition Wikipedia
Habit
 the general shape or appearance of the plant
Holotype
 a single type specimen upon which the description and name of a species is based on
Hydrophilous
 a pollination system where pollen grains are transported on or below the surface of water (Les 1988), thought to be a requirement for invasion of marine habitats
Infauna
 a group of animals which live within the sediments of aquatic habitats
Lectotype
 a subsequent type chosen to serve as the holotype of a species
Monocots
 a group of flowering plants with seeds that contain one embryonic leaf
Monophyletic
 a group of organisms (clade) that consists of an ancestor and all of its descendants
Nomenclature
 The naming of a species
(Primary) productivity
 rate at which energy gets converted into organic carbon via photosynthesis
Taxonomy
 the traditional definition, which encompasses species descriptions (alpha) and assigning them into higher classifications (beta)

Further Information

Differentiating seagrass species in Singapore: Ribbon-like seagrasses
Monitoring seagrasses along Singapore's shores: Team Seagrass
Type specimen: Type specimen of //T. hemprichii//
Informative pages on the Sickle Seagrass: Algaebase; IUCN; ITIS

References

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