Journal of Threatened Taxa | www.threatenedtaxa.org | 26 March 2019 | 11(5): 13617–13621

 

Observations on the female flowers and fruiting of Tape Grass Enhalus acoroides from South Andaman Islands, India

 

Vardhan Patankar 1, Tanmay Wagh 2 & Zoya Tyabji 3

 

1,2,3 Wildlife Conservation Society, 551, 7th Main Road, Rajiv Gandhi Nagar, 2nd Phase, Kodigehalli, Bengaluru, Karnataka 560097, India.

1,2 Tata Institute of Fundamental Research, National Centre for Biological Sciences, GKVK Campus, Bengaluru, Karnataka 560065, India.

3 Andaman Nicobar Environment Team - Centre for Island Ecology, Post Bag 1, Junglighat P.O., Port Blair, Andaman Islands 744103, India.

1 vardhanpatankar@gmail.com (corresponding author), 2 twagh.97@gmail.com, 3 zoya.tyabji@gmail.com

 

 

doi: https://doi.org/10.11609/jott.4253.11.5.13617-13621   

 

Editor: Anonymity requested.          Date of publication: 26 March 2019 (online & print)

 

Manuscript details: #4253 | Received 14 May 2018 | Final received 02 August 2018 | Finally accepted 20 March 2019

 

Citation: Patankar, V., T. Wagh & Z. Tyabji (2019). Observations on the female flowers and fruiting of Tape Grass Enhalus acoroides from South Andaman Islands, India. Journal of Threatened Taxa 11(5): 13617–13621. https://doi.org/10.11609/jott.4253.11.5.13617-13621

 

Copyright: © Patankar et al. 2019. Creative Commons Attribution 4.0 International License. JoTT allows unrestricted use, reproduction, and distribution of this article in any medium by adequate credit to the author(s) and the source of publication.

 

Funding:  Department of Science and Technology, Andaman Nicobar Forest Department

 

Competing interests: The authors declare no competing interests.

 

Acknowledgements: The study was conducted with support from the Department of Science and Technology, Government of India, under the DST-INSPIRE Faculty Programme.  We would like to thank the Andaman and Nicobar Administration and the Department of Environment and Forests, Port Blair, for granting us permits to carry out this work.  The Divisional Forest Officer, Mr Shazi Abraham, and the Deputy Conservator of Forests, Mr Naveen Kumar, provided us with field assistants and a boat for reef surveys.  The Andaman and Nicobar Islands’ Environmental Team (ANET) and Nature Conservation Foundation (NCF) helped with SCUBA equipment and field logistics.  We especially thank range officers, Mr A.K. Singh and Mr Jason John, for field assistance and data collection.

 

 

 

Abstract: Documenting phenologic events is crucial in obtaining deeper insights into the life cycle of seagrasses.  We documented and compared the flowering and fruiting of the seagrass Enhalus acoroides from multispecies seagrass meadows at two sites, Henry Lawrence and Tarmugli islands located inside the marine national parks in South Andaman Islands.  At these two locations, the average density of shoots ranged between 30.9/m2 and 18.16/m2, fruits between 5/m2 and 2.33/m2, and flowers between 6.7/m2 and 3.83/m2, whereas the mean length of the peduncles ranged from 40.59cm at Henry Lawrence to 32.44cm at Tarmugli Island.  We observed significant differences between the densities of shoots and fruits and peduncle lengths in the two sites.  The density of flowers, however, did not vary significantly.  These observations of fruiting and flowering in E. acoroides establish an important reproductive stage in the life cycle of the species and open avenues for further seagrass research in the Andaman Islands.  We describe the findings and emphasize on the need to establish a long-term phenology monitoring program for E. acoroides in the Andaman Archipelago.

 

Keywords: Andaman Islands, flowering, Henry Lawrence Island, marine national park, phenology, seagrass, Tarmugli Island.

 

Seagrasses are marine angiosperms usually confined to sandy substrates in shallow temperate and tropical waters throughout the world (Vermaat et al. 2004; Fortes 2013).  Sixty seagrass species are reported globally, of which 14 species are found in the Indo-Pacific (Short et al. 2007).  Throughout their distribution, seagrasses are threatened by trawl fishing, sand mining, coastal construction, nutrient enrichment, sewage, and other terrestrial pollutants (Duarte 2002; Baden et al. 2003; Short & Waycott 2010).  One of the consequences of these pressures is meadow fragmentation, which lowers seed output and is considered one of the reasons for seagrass declines worldwide (Green et al. 2003; Unsworth & Cullen 2010).  Realizing their ecologic importance, many countries have provided varying degrees of protection to seagrass meadows (Short & Waycott 2010). 

Amongst these, the Tape Grass Enhalus acoroides (L.f.) Royle, which is distributed throughout the Indo-Pacific (Short & Waycott 2010), is the tallest species with leathery leaves which can grow up to 150cm.  Due to its large shoot size, E. acoroides forms one of the major contributors to the productivity and biomass of seagrass meadows (Brouns & Heijs 1986; Rollón 1998).  Clumps of this species form important habitats for juvenile fish, benthic invertebrates, and scores of burrowing organisms (Nakamura & Sano 2004, 2005).  It is a source of nutrients for the Green Sea Turtle Chelonia mydas and a few reports indicate feeding of Dugong Dugong dugon on its shoots(Nair et al. 1975; Erftemeijer et al. 1993; Andre et al. 2005; Adulyanukosol & Poovachiranon 2006; D’Souza et al. 2013).  Enhalus acoroides is dioecious, flowering twice a year from March to July and November to December (Rollón 1998; Rollón et al. 2003; Vermaat et al. 2004).  In view of Enhalus’ hydrophobic mode of pollination (Rattanachot & Prathep 2011), this flowering, when compared to that of other seagrass species, is unique in that the male flowers are released for surface pollination whereas the female flowers have to extend their coiled peduncles (stalk bearing the fruit or flower) to the water surface to capture pollen (Johntone 1979; Rollón et al. 2003).  Once the pollination is complete, the female peduncle coils back towards the bottom (Sulochanan & Korabu 2009).  The length of the peduncle increases with increase in depth (Johnstone 1979; Rollón 1998) and the peduncles terminate into pinkish-green flowers, the ovaries of which pollinate into green, bulbous fruits (Sulochanan & Korabu 2009).

In India, Enhalus acoroides is reported from the Palk Bay and Gulf of Mannar in the state of Tamil Nadu and along the Andaman & Nicobar Islands (Mahalingam & Gopinath 1987; Das 1996; Manikandan et al. 2011).  In the Andaman & Nicobar Islands, before the tsunami of 2004, E. acoroides was reported from Paschim in Bihar, North Reef, Inglis, Henry Lawrence, Havelock, and Cinque islands in the Andaman group and Camorta, Trinket, Nancowry, Katchal, Pilomilow, Little Nicobar, and Great Nicobar islands in the Nicobar group (Das 1996).  Post-tsunami, however, its presence was reported only from Henry Lawrence and Tarmugli in the Andaman Islands and Kamorta and Nancowry in the Nicobar Islands (Thangaradjou et al. 2010; D’Souza et al. 2015).  This could be attributed either to lack of focused studies on the distribution of E. acoroides meadows or the loss of these meadows to natural disturbances (tsunami and cyclones).  Owing to their ecosystem services, documenting and understanding various life cycle events of E. acoroides is necessary to obtain deeper insights into their ecology and to develop effective conservation strategies.

Sexual reproduction (characterized by flowering and fruiting) is an important event in the life history of Enhalus acoroides as they release floating propagules into the water column, which helps in recolonization of new areas (Rollón et al. 2003).  This also helps in mixing of genes, which is an important evolutionary adaptation to cope with environment changes (Marbà & Walker 1999; Alexandre et al. 2006).  Thus, understanding the flowering season in E. acoroides is of particular importance.  There, however, is limited information on the flowering and fruiting of E. acoroides and most studies are limited to taxonomic documentation and distribution of the species across the island chain.  In such a scenario, opportunistic natural history observations of E. acoroides can act as baselines and probe hypothesis-driven studies on the phenology, ecology, and biology of the species.  We report the observations on the flowering and fruiting phenomenon of E. acoroides at two important seagrass meadows, Henry Lawrence and Tarmugli islands in the South Andaman group of islands.

 

Material and methods

Study area

The study was carried out at Henry Lawrence (12.1300N & 93.0990E) and Tarmugli (11.5890N & 92.5310E) islands in the Andaman Archipelago (Fig. 1).  Henry Lawrence Island is part of the Rani Jhansi Marine National Park (RJMNP) in Ritchie’s Archipelago, South Andaman, and covers an area of 54.7km2 (Singh 2003).  The coast is lined by a thick mangrove forest, whereas coral reefs and seagrass meadows are found in the shallow coastal waters surrounding the island.  The seagrass meadow at Henry Lawrence is composed of multiple seagrass species including a large patch of Enhalus acoroides (c. 600m2)Similarly, Tarmugli Island, with a total area of 12.6km2, is part of the Mahatma Gandhi Marine National Park (MGMNP) in Wandoor, South Andaman (Fig. 1).  The island has a dense coastal forest along with coral reefs and nearshore seagrass meadows.  Unlike Henry Lawrence, however, the seagrass meadow at Tarmugli is exposed to the open ocean and the E. acoroides patch is significantly smaller (c. 150m2).  The meadows at both sites are relatively shallow, ranging from 1–3 m at Tarmugli and 2–6 m at Henry Lawrence, and the substrate is sand mixed with coral rubble, which is an ideal habitat for the seagrass associated faunal communities such as sea cucumbers, sea anemones, juvenile fish, and burrowing worms (Image 1).

 

Sampling protocol

We carried out data collection after incidental observation of flowering and fruiting of the species between 02 and 27 May 2016, using snorkelling and scuba gear at depths of 1–6 m at high tide.  We placed 10 random 1m x 1m quadrats in the E. acoroides meadow at Henry Lawrence at depths of 2–4 m and six quadrats at Tarmugli Island at depths of 1–3 m.  Due to the relatively smaller size of the E. acoroides meadow at Tarmugli Island, we limited the number of replicate quadrats to six.  Within these quadrats, we counted the number of shoots, fruits, and female flowers and estimated their density per square metre.  For the morphometric data, we measured the length of the peduncles, i.e., the distance from the base of the peduncle to the base of the fruit, and the female flower using a measuring tape.  The average number of shoots, fruits, and flowers, and the mean lengths of the peduncles were compared between the two sampled sites by performing Welch’s two sample t-test to account for unequal sample sizes.  Data was explored in Microsoft Excel v.2016 and analyzed using R v3.2 (R Development Core Team 2015).

 

Results and Discussion

We observed a significant difference between peduncle lengths and the number of shoots and fruits between the two sites, whereas we did not observe significant difference in the number of female flowers between the two sampled sites (Table 1).  The male flowers were not observed during the sampling.

We observed a wide variation in the number of shoots and fruits and the peduncle lengths of E. acoroides across the two meadows, which can be attributed to several inherent processes.  The meadow at Henry Lawrence Island is considerably larger, deeper, surrounded with mangroves, and shielded from the open ocean, which could be some of the reasons for the longer peduncle lengths and higher density and abundance of the species as compared to Tarmugli Island.  The variation across these two meadows shows the importance of local environment factors (location, meadow size, depth, exposure) in influencing the E. acoroides meadow dynamics (Rollón 1998; Marbà et al. 2005).

As our study was necessarily opportunistic and conducted on incidental observations, we were unable to document the male flowers and monitor the extent of the flowering season of E. acoroides in our study area.  Previous studies carried out on the flowering of E. acoroides from the Philippines and Thailand recorded March to July and November to December as the flowering season (Rollón 1998; Vermaat et al. 2004; Rattanchot & Prathep 2011) whereas in the Gulf of Mannar flowering was reported in June (Sulochanan & Korabu 2009).  Our observation of flowering of the female plant in May is within the flowering season recorded at Philippines, Thailand, and the Gulf of Mannar.

Various studies showed that E. acoroides forms an important refuge for juvenile fish populations (Nakamura & Sano 2004); therefore, protecting these sites should be of utmost importance especially as climate change increases the frequency and intensity of benthic disturbances (Hoegh-Guldberg et al. 2007).  We recommend that extensive surveys be carried out in all potential seagrass meadows of the Andaman & Nicobar Archipelago to understand the phenology of all 11 seagrass species (Das 1996; Savurirajan et al. 2015; Immanuel et al. 2016).  The state forest department in collaboration with research institutions should establish long-term monitoring programs to collect specific data on seagrasses as well as to assess potential seed banks, seed dispersal, meadow connectivity, genetic variability, and gene flow.  The detailed studies and long-term monitoring of E. acoroides meadows in Henry Lawrence and Tarmugli islands will help establish the flowering season and increase our understanding of the factors controlling sexual reproduction, the time of release of male flowers, dispersal abilities, colonisation strategies, and resilience to natural catastrophes.  Such research will not only provide new information on the phenology, ecology, and biology of E. acoroides and other seagrass species, but also provide empirical and technical support for seagrass meadow conservation in the face of rapid climate change and expanding threats to seagrasses and coastal areas in the Andaman Islands.

 

 

Table 1. Difference in the abundance of shoots, fruits, and flowers and the mean length of the peduncles at Henry Lawrence and Tarmugli islands in South Andaman.  Significance between sites was tested using Welch’s two sample t-test (T).

 

 Attributes

Henry Lawrence

Tarmugli

T

df

p-value

 

Mean

 

 

 

Length of peduncle

40.59±1.67

32.44±1.73

3.3866

77.519

0.001114*

No. of shoots

30.9±3.11

18.16±1.53

3.6633

12.568

0.003018*

No. of fruits

5±0.61

2.33±0.55

3.2129

13.476

0.006528*

No. of flowers

6.7±0.76

3.83±0.60

2.9567

13.956

0.01044

 

*Significance at alpha=0.05, P<0.01

All the attributes are expressed as mean±standard error.

 

For figure / image – click here

 

References

 

Adulyanukosol, K. & S. Poovachiranon (2006). Dugong (Dugong dugon) and seagrass in Thailand: present status and future challenges, pp41–50. In: Proceedings of the 3rd International Symposium SEASTAR2000 Asian Bio-logging Science.  Kyoto University, Japan, 50pp.

Alexandre, A., R.S. Cabaco & E.A. Serra (2006). Timing and success of reproductive stages in the seagrass Zostera noltii. Aquatic Botany 85(3): 219–223.

Andre, J., E. Gyuris & I.R. Lawler (2005). Comparison of the diets of sympatric Dugongs and Green Turtles on the Orman Reefs, Torres Strait, Australia. Wildlife Research 32(1): 53–62.

Baden, S., M. Gullström, B. Lundén, L. Pihl & R. Rosenberg (2003). Vanishing seagrass (Zostera marina, L.) in Swedish coastal waters. AMBIO: Journal of the Human Environment 32(5): 374–377.

Brouns, J.J.W.M. & F.M.L. Heijs (1986). Production and biomass of the seagrass Enhalus acoroides (L.f) Royle and its epiphytes. Aquatic Botany 25: 21–45.

Das, H. (1996). Status of Seagrass habitats of the Andaman and Nicobar coast. Report submitted to Sálim Ali Centre for Ornithology and Natural History, Coimbatore, 35pp.

D’Souza, E., V. Patankar, R. Arthur, T. Alcoverro & N. Kelkar (2013). Long-term occupancy trends in a data-poor Dugong population in the Andaman and Nicobar archipelago. PloS One 8(10): e76181.

D’Souza, E., V. Patankar, R. Arthur, N. Marbà & T. Alcoverro (2015). Seagrass herbivory levels sustain site-fidelity in a remnant Dugong population. Plos One 10(10): e0141224.

Duarte, C.M. (2002). The future of seagrass meadows. Environmental Conservation 29(2): 192–206.

Erftemeijer, P.L.A. & W. Moka (1993). Stomach content analysis of a Dugong (Dugong dugon) from South Sulawesi, Indonesia. Marine and Freshwater Research 44(1): 229–233.

Fortes, M.D. (2013). A review: biodiversity, distribution and conservation of Philippine seagrasses. Philippine Journal of Science 142: 95–111.

Green, E.P., F.T. Short & T. Frederick (eds.) (2003). World Atlas of Seagrasses. University of California Press, Berkeley, USA, 324pp.

Hoegh-Guldberg, O., P.J. Mumby, A.J. Hooten, R.S. Steneck, P. Greenfield, E. Gomez, C.D. Harvell, P.F. Sale, A.J. Edwards, K. Caldeira, C.M. Eakin, R. Iglesias-Prieto, N. Muthiga, R.H. Bradbury, A. Dubi & M.E. Hatziolos (2007). Coral reefs under rapid climate change and ocean acidification. Science 318(5857): 1737–1742.

Immanuel, T., M.G. Bharathi, S. Sawhney, P. Ragavan & R.K. Sankar (2016). New record of the pantropical seagrass Halophila decipiens Ostenfeld (Hydrocharitaceae) from the Andaman and Nicobar Islands, India. Botanica Marina 59(1): 1–5.

Johntone, I. (1979). Papua New Guinea seagrasses and aspects of the biology and growth of Enhalus acoroides (L.f) Royle. Aquatica Botanica 7: 197–208.

Mahalingam, R. & K. Gopinath (1987). Ecological conservation of seagrass beds in the Gulf of Mannar, India. Environmental Conservation 14(3): 265–268.

Manikandan, S., S. Ganesapandian & K. Parthiban (2011). Distribution and zonation of seagrasses in the Palk Bay, southeastern India. Journal of Fisheries and Aquatic Science 6(2): 178–185.

Marbà, N., C.M. Duarte, E. Diaz-Almela, J. Terrados, E. Alvarez, R. Martinez, R. Santiago, E. Gacia & A.M. Grau (2005). Direct evidence of imbalanced seagrass (Posidonia oceanica) shoot population dynamics in the Spanish Mediterranean. Estuaries 28: 53–62.

Marbà, N. & D.I. Walker (1999). Growth, flowering, and population dynamics of temperate Western Australian seagrasses. Marine Ecology Progress Series 184: 105–118.

Nair, R.V., R.S.L. Mohan & K.S. Rao (1975). The Dugong (Dugong dugon). Bulletin of the Central Marine Fisheries Research Institute No. 26, Kochi, 42pp.

Nakamura, Y. & M. Sano (2004). Comparison between community structures of fishes in Enhalus acoroides  and Thalassia hemprichii - dominated seagrass beds on fringing coral reefs in the Ryukyu Islands, Japan. Ichthyological Research 51(1): 38–45.

Nakamura, Y. & M. Sano (2005). Comparison of invertebrate abundance in a seagrass bed and adjacent coral and sand areas at Amitori Bay, Iriomote Island, Japan. Fisheries Science 71(3): 543–550.

R Development Core Team (2015). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available online at http://www.R-project.org/.   Accessed on 02nd January 2018.

Rattanachot, E. & A. Prathep (2011). Temporal variation in growth and reproduction of Enhalus acoroides (L.f.) Royle in a monospecific meadow in Haad Chao Mai National Park, Trang Province, Thailand. Botanica Marina 54(2): 201–207.

Rollón, R.N. (1998). Spatial Variation and Seasonality in Growth and Reproduction of Enhalus acoroides (L.f.) Royle Populations in the Coastal Waters off Cape Bolinao, NW Philippines. Wageningen PhD Thesis, 135pp.

Rollón, R.N., E.D.D.R. van Steveninck & W. van Vierssen (2003). Spatio-temporal variation in sexual reproduction of the tropical seagrass Enhalus acoroides (L.f.) Roylein Cape Bolinao, NW Philippines. Aquatica Botanica 76: 339–354.

Savurirajan, M., R.K. Lakra & T. Ganesh (2015). A new record of the seagrass Halophila beccarii Ascherson from the Port Blair coast, Andaman and Nicobar Islands, India. Botanica Marina 58(5): 409–413.

Short, F., T. Carruthers, W. Dennison & M. Waycott (2007). Global seagrass distribution and diversity: a bioregional model. Journal of Experimental Marine Biology and Ecology 350(1–2): 3–20.

Short, F.T. & M. Waycott (2010). Enhalus acoroides. In: The IUCN Red List of Threatened Species: e.T173331A6992567.  Accessed on 4th January 2018, https://www.iucnredlist.org/species/173331/6992567

Singh, H.S. (2003). Marine protected areas in India. Indian Journal of Marine Science 32(3): 226–-233.

Sulochanan, B. & L.S. Korabu (2009). Enhalus acoroides (L.f.) Royle fruits observed in Gulf of Mannar, pp19–21. In: Marine Fisheries Information Service, Technical and Extension, Series, 200pp.

Thangaradjou, T., K. Sivakumar, E.P. Nobi & E. Dilipan (2010). Distribution of seagrasses along the Andaman and Nicobar Islands: a post tsunami survey, pp157–160. In: Raghunathan, C., C. Sivaperuman & Ramakrishna (eds.). Recent Trends in Biodiversity of Andaman and Nicobar Islands. Zoological Survey of India, Kolkata, 542pp. 

Unsworth, R.K.F. & L.C. Cullen (2010). Recognising the necessity for Indo-Pacific seagrass conservation. Conservation Letters 3: 63–73.

Vermaat, J.E., R.N. Rollon, C.D.A. Lacap, C. Billot, F. Alberto, H.M. Nacorda, F. Wiegman & J. Terrados (2004). Meadow fragmentation and reproductive output of the SE Asian seagrass Enhalus acoroides. Journal of Sea Research 52(4): 321–328.