Introduction
Avicennia genus with eight species is the most diverse genera among all the mangroves (Tomlinson, Reference Tomlinson1986; Duke, Reference Duke1991; POWO, 2023). They are also the most cosmopolitan in their distribution; reported from 30°N to 30°S latitude, native to ~120 countries of tropics to temperate, while introduced to the coast of California, United States (POWO, 2023). Alongside broad distribution, the Avicennia genus in general tends to form mixed to monodominant stands virtually located throughout tidal ranges i.e., from seawards to landward zones of mudflats, estuarine, and deltaic coasts (Tomlinson, Reference Tomlinson1986; Duke, Reference Duke1991; Thatoi et al., Reference Thatoi, Samantaray and Das2016). Their adaptability and widespread existence along the equator pose an intriguing question on their propagule dispersal across the continent (Clarke, Reference Clarke1993; Wong et al., Reference Wong, Foong, Lai, Dai, Mao and Wang2020). Avicennia is also among the genera whose species (e.g., Avicennia marina) have a high threshold for the environmental factors which enables them to be a better successional species in the degraded mangroves and new intertidal zones created by soil accretion or erosion (Huxham et al., Reference Huxham, Berger, Skov, Sousa, Bohn, Hawkins, Firth and Williams2018; ShivaShankar et al., Reference ShivaShankar, Purti, Ganta, Mandal, Singh, Kaviarasan, Satyakeerthy and Jacob2022; Zimmer et al., Reference Zimmer, Ajonina, Amir, Cragg, Crooks, Dahdouh-Guebas and Wodehouse2022).
The Andaman and Nicobar Islands (hereafter ANI's) are among the global hotspots for mangrove species richness and are endowed with about 80% (n = 38) of total mangrove species found in India (n = 46) (Ragavan et al., Reference Ragavan, Saxena, Mohan, Ravichandran, Jayaraj and Saravanan2015). Three out of eight Avicennia species namely A. marina (Forssk.) Vierh., Avicennia officinalis L., and Avicennia alba Blume are distributed in India (Kathiresan, Reference Kathiresan2010; Ragavan et al., Reference Ragavan, Saxena, Jayaraj, Mohan, Ravichandran, Saravanan and Vijayaraghavan2016a, Reference Ragavan, Mohan, Saxena, Jayaraj, Ravichandran and Saxena2016b). However, their spread within various mangrove patches of India is inconsistent. For instance, A. officinalis is not distributed in the mangroves of Lakshadweep, and Daman & Diu on the West coast, while, the presence of A. marina in the mangroves of Lakshadweep Islands is doubtful (Ragavan et al., Reference Ragavan, Saxena, Mohan, Ravichandran, Jayaraj and Saravanan2015). Similarly, A. alba is distributed in most parts of the east coast of India, however, their distribution is either absent (Tamil Nadu, Daman & Diu) or doubtful (Kerala, Lakshadweep, ANI's) in Southern India and the Islands (Ragavan et al., Reference Ragavan, Saxena, Saxena, Mohan, Sachithanantham and Coomar2014). A few studies published before the 2004 tsunami have included A. alba in their mangrove flora checklist from the ANI's (Das and Dev Roy, Reference Das and Dev Roy1989; Dagar et al., Reference Dagar, Singh, Mongia, Lieth and Al Masoom1993; Jagtap, Reference Jagtap, Suryanarayan and Sudarsen1994; Dagar and Singh, Reference Dagar and Singh1999; Debnath, Reference Debnath2004). However, recent studies (post 2004 tsunami) have ruled out the occurrence of A. alba in the ANI's and suggested the doubtful records by the previous studies as misidentification of the morphological variants of A. marina (Goutham-Bharathi et al., Reference Goutham-Bharathi, Roy, Krishnan, Kaliyamoorthy and Immanuel2014; Thatoi et al., Reference Thatoi, Samantaray and Das2016; Ragavan et al., Reference Ragavan, Mohan, Saxena, Jayaraj, Ravichandran and Saxena2016b). Also, upon cross-verification with other recently published literature, and the herbarium repository at the Botanical Survey of India, Port Blair, ANI's the authors could not find any relevant specimens, locations, or photographs of A. alba from the ANI's.
Following the 2004 Sumatra-Andaman earthquake and Indian Ocean tsunami, the mangrove forest of ANI's has experienced a loss of ~190 sq. km. of mangrove cover and a constant deterioration owing to alteration in the tidal water regime caused by the coastal uplift and subsidence across the ANI's (Nehru and Balasubramanian, Reference Nehru and Balasubramanian2018; Majumdar et al., Reference Majumdar, Chakraborty, Saha and Datta2019; Ramakrishnan et al., Reference Ramakrishnan, Gladston, Kumar, Rajput, Murali and Rajawat2020; ShivaShankar et al., Reference ShivaShankar, Narshimulu, Kaviarasan, Narayani, Dharanirajan, James and Singh2020). The coastal uplift was recorded highest in the West coast of North Andaman (1.35 m); while the highest subsidence was reported from the Southern tip of Great Nicobar Island (2.85 m) (Malik et al., Reference Malik, Murty and Rai2006; Meltzner et al., Reference Meltzner, Sieh, Abrams, Agnew, Hudnut, Avouac and Natawidjaja2006). The land uplift and subsidence have created vast new intertidal zones suitable for mangrove colonization on the uplift seafloor and subsided terrestrial zones (Nehru and Balasubramanian, Reference Nehru and Balasubramanian2018; Ramakrishnan et al., Reference Ramakrishnan, Gladston, Kumar, Rajput, Murali and Rajawat2020; ShivaShankar et al., Reference ShivaShankar, Narshimulu, Kaviarasan, Narayani, Dharanirajan, James and Singh2020). To understand the pattern of mangrove colonization at respective new intertidal habitats, we conducted an extensive mangrove vegetation survey across the ANI's. Further, Avicennia species being one among the pioneer species and aggressive colonizers on the bare intertidal zones, we expect that these species will colonize better than other mangroves due to their competitive advantage of having high environmental thresholds (e.g., salinity), efficient propagule dispersal and establishment strategies (Clarke and Myerscough, Reference Clarke1993; Friess et al., Reference Friess, Krauss, Horstman, Balke, Bouma, Galli and Webb2012). Therefore, our study aims to explore the spatial distribution, abundance, and colonization patterns among the Avicennia species across the new intertidal zones formed after the coastal uplift and subsidence in ANI's.
Methodology
The vegetation survey was conducted from 2019 to 2023 during the non-monsoon season of each year (January to May) across the Andaman and Nicobar Islands focusing on the new intertidal zones formed due to coastal uplift (i.e., uplift reef bed and seafloor) and subsidence (i.e., drowned terrestrial zones) (Figure 1). Field sites were selected with the help of previous field experiences of the authors (Nehru and Balasubramanian, Reference Nehru and Balasubramanian2012, Reference Nehru and Balasubramanian2018), Google Earth images, and published literature (Majumdar et al., Reference Majumdar, Chakraborty, Saha and Datta2019; Ramakrishnan et al., Reference Ramakrishnan, Gladston, Kumar, Rajput, Murali and Rajawat2020; ShivaShankar et al., Reference ShivaShankar, Narshimulu, Kaviarasan, Narayani, Dharanirajan, James and Singh2020). At each selected site, three belt transects perpendicular to the coastline were laid randomly at a minimum distance of 50 m to cover the site heterogeneity. Further, each belt constitutes at least three vegetation plots of 10 × 10 sq. m at every 50 m for tree enumeration (⩾10 cm Girth at Breast Height (GBH)) with nested subplot of 3 × 3 sq. m for sapling (<10 cm – ⩾1 cm GBH) and 1 × 1 sq. m (<1 cm GBH) for seedling enumeration. The geo-coordinate of the plot and characteristics of soil substratum in the site were noted. Additionally, species exploration was conducted at each site to ensure the documenting of species that were present in the site but not represented in the plot.
Figure 1. Spatial representation of Andaman and Nicobar Islands with representation of total number of sites visited across islands (blue square), and occurrences of Avicennia marina (black circle), A. officinalis (yellow triangle), and A. alba (red plus).
Results
We found three species of the genus Avicennia (A. alba, A. officinalis, and A. marina) colonizing the islands at the new and old intertidal habitat (Figure 1). Out of 79 surveyed sites, the genus Avicennia was present at a total of 55 sites (Relative Frequency (RF) = 70%) including 46 sites (84%) from Andaman Islands and nine sites (16%) from Nicobar Islands (Figure 1). However, only one site in North Andaman was found colonized by all three species of Avicennia, while, overall 19 sites in the Andaman Islands were colonized by two species of Avicennia (A. marina and A. officinalis). Further, we did not encounter A. officinalis from the Nicobar Islands, while only three sites in Great Nicobar were colonized by two Avicennia species (A. alba and A. marina).
Among all the three Avicennia species, considering all the cohorts (trees, saplings, and seedlings) A. marina was the most abundant (Relative Abundance (RA) – 97.92%), and widely distributed species (RF – 68.75%) across the islands, followed by A. officinalis (RA – 1.93%) which was present at 25 sites (RF – 26.25%) (Figure 1). A. alba was the rarest (RA – 0.16%) among all the three species, which was recorded only from four sites (RF – 5%) in ANI's (Figure 1). Similarly, the relative abundance of A. marina tree was highest (RF – 99.66%), followed by A. officinalis (RF – 0.17%), and A. alba (RF – 0.17%). The relative abundance of the recruitment (sapling and seedling) cohort was dominated by A. marina (RF – 96.5%), followed by A. officinalis (RF – 3.4%), and A. alba (RF – 0.16%) (Figure 2A & B). Further, the key features documented to identify and differentiate among the three Avicennia species found in Andaman and Nicobar Islands were their leaf tip, flower size with the arrangement, propagule shape, and bark colour (Figure 3) (Table 1).
Figure 2. A: Relative abundance of all the three Avicennia species found each tree, sapling, and seedling cohort, B: Relative frequency of all the three Avicennia species found in the islands.
Figure 3. Key features to identify three Avicennia species (left – A. alba, middle – A. marina, and right – A. officinalis) occur in the Andaman and Nicobar Islands. A: tree crown; B, C, & D: leaf shape and tip; E, F, & G: propagules shape and beak; H, I & J: flower; K, L, & M: bark.
Table 1. Key identification features to be observed in the field to identify and differentiate among the three Avicennia species found in the mangroves of ANI's
During the March 2022 vegetation survey, A. alba was found colonizing the uplift site, on the west coast of North Andaman Islands (13° 26′ 38.04″ N — 92° 52′ 41.88″ E) (Figure 4A). This particular site has experienced land uplift up to ~1.3 m, and the new intertidal habitat was formed at seaward that receives tidal water inundation during most of the high tides. Due to acute uplift, the substratum was predominantly consisting of calcareous dead coral boulders, reef beds, and coarse sand. There was no remnant mangrove patch close to the site except for some fringing mangroves and isolated trees along the creeks. The two A. alba trees colonized at this site were located beside a small water channel. The trees were in the flowering stage (March) with multiple branches of ~30 cm GBH and ~8 m in height. Avicennia alba was also accompanied by other two Avicennia species (A. marina and A. officinalis) with copious saplings, and seedlings of all three species (Figure 4A). A voucher specimen of the A. alba materials collected from North Andaman is submitted to the herbarium at Wildlife Institute India, Dehradun (Voucher specimen no. 12905, Anoop Raj Singh & Nehru Prabakaran).
Figure 4. A. alba colonizing in the new intertidal habitat created post tsunami due to land uplift and subsidence. A: All the three Avicennia species colonizing at seaward zone on the uplift sites of North Andaman Islands, B & C: A. alba colonization at the landward zone in the subsided sites of Nicobar Islands along with Nypa fruticans and planted Cocos nucifera.
We encountered five individuals of A. alba from three sites of Great Nicobar Island (Swaroop Nallah: 6° 49′ 17.00″ N – 93° 53′ 53.16″ E, Jogindar Nagar (13 km): 6° 56′ 56.31″ N – 93° 54′ 32.41″ E, and Galathea Bay: 6° 50′ 21.19″ N – 93° 51′ 22.03″ E) (Figure 4B & C). Avicennia alba at Swaroop Nallah was found alongside A. marina with abundant seedlings. Whereas, in 13 km, the A. alba was growing along with the A. marina in the landward zone adjacent to the Nypa fruticans and planted Cocos nucifera. In Galathia Bay, it is growing in the seaward fringes where the mangrove colonization was sparse; the single tree encountered here with a girth size of 45 cm and 10 m in height was in flowering and fruiting stage (July) (Figure 4B & C). The A. alba trees were thickly dense, with multiple branches and broad crowns. All three sites in Great Nicobar having vast intertidal zones may facilitate aggressive colonization of Avicennia species in the future.
Discussion and conclusions
Avicennia species are one among the aggressive colonizers during mangrove succession in the degraded/disturbed mangrove forests and new intertidal zones formed due to soil accretion (Friess et al., Reference Friess, Krauss, Horstman, Balke, Bouma, Galli and Webb2012; Huxham et al., Reference Huxham, Berger, Skov, Sousa, Bohn, Hawkins, Firth and Williams2018; Zimmer et al., Reference Zimmer, Ajonina, Amir, Cragg, Crooks, Dahdouh-Guebas and Wodehouse2022). Their ability to tolerate a euryhaline range of soil and water, prolonged tidal water inundation, and cryptovivipary (embryo fatten to break the seed coat while remaining attached to the mother tree) allows them to quickly establish and outcompete their competitors (Burchett et al., Reference Burchett, Field and Pulkownik1984; Duke, Reference Duke1991; Clarke and Myerscough, Reference Clarke and Myerscough1993). These characteristics together are also responsible for their widespread distribution across the globe (Smith, Reference Smith1987; Duke, Reference Duke1991; Clarke, Reference Clarke1993). However, Avicennia distribution in the mangrove forest is noticeably restricted mostly to seaward and landward zones and does not form stand in mid-zone (Smith, Reference Smith1987). We also observed a similar pattern in the mangrove forest of ANI's where Avicennia was either present towards the seaward zone or landward zone. Avicennia's are characteristically photophilic species that require a high amount of sunlight (shade intolerant) for their growth and development, which is usually abundant at landward and seaward zones compared to mid-zone where the canopy is saturated (Smith, Reference Smith1987). Also, the mid-zone habitat is aggressively used by Grapsid crabs that profusely predate on the propagules of Avicennia species limiting the regeneration of Avicennia stand in the mid-zone (Smith, Reference Smith1987). Hence, the formation of new intertidal habitat at the landward zone in subsided sites and seaward zone in the uplift site due to coastal subsidence and uplift across the ANI's becomes the perfect habitat for Avicennia to colonize (Thirumurugan et al., Reference Thirumurugan, Singh and Prabakaran2022).
A. marina was found colonizing aggressively on the new intertidal zones across the ANI's and created monodominant stands in the new intertidal zones. Also, this species is particularly the most abundant in the seaward new intertidal zones in North Andaman (sites characteristics of loose and fine sediments of sea floor exposed due to uplift) and on the extreme south of Great Nicobar Island (sites characteristic of subsided terrestrial zones with fine to coarse sandy substratum). A. marina has peculiar root-shoot growth specification where the root grows at a much faster rate compared to the shoot, allowing Avicennia propagules to quickly hold on to the substratum and colonize despite the short window of opportunity offered by the new intertidal habitat formed especially at seaward zone, where the propagule establishment is restricted by frequent and long-duration of tidal water inundation (Balke et al., Reference Balke, Bouma, Horstman, Webb, Erftemeijer and Herman2011). Hence, due to their root-shoot specification, they could successfully colonize across the ANI's and are likely to spread at a much faster rate in the near future. Further, amongst three Avicennia species, A. marina possesses the highest degree of salinity tolerance causing their high abundance, and wide distribution from hypersaline habitat (seaward/mid-zone – range 15 to 25 ppt) to hyposaline habitat (landward – range 5 to 15 ppt), across the islands (Downton, Reference Downton1982). Contrarily, A. officinalis exclusively prefers high salinity areas and barely colonizes at landward zone (no salt habitat) (Downton, Reference Downton1982). Their occurrence in the Andaman Islands before the 2004 tsunami might have facilitated them to colonize the new intertidal habitat created in the Andaman Islands. While, the occurrence of A. officinalis in the mangroves of the Nicobar Islands has not been reported despite the vast intertidal area available for colonization post land-subsidence (Prabakaran et al., Reference Prabakaran, Bayyana, Vetter and Reuter2021). Naturally A. officinalis is not very successful in colonization in the islands, and rare to form monodominant stand which indicates they may have a relatively lesser threshold to disturbances. So, even if the propagules of A. officinalis might have managed to reach the Nicobar Islands, they may have found it difficult to colonize and proliferate compared to the other two Avicennia species.
The disjunct presence of A. alba on the northern extreme (North Andaman west coast) and southern extreme (Great Nicobar east coast) followed by their complete absence across the stretches of the ANI's is scientifically intriguing. Though there were unconfirmed reports of A. alba in the ANI's (Das and Dev Roy, Reference Das and Dev Roy1989; Dagar et al., Reference Dagar, Singh, Mongia, Lieth and Al Masoom1993; Jagtap, Reference Jagtap, Suryanarayan and Sudarsen1994; Dagar and Singh, Reference Dagar and Singh1999; Debnath, Reference Debnath2004), the recent more comprehensive exploration across the ANI's during 2009–2015 by Nehru and Balasubramanian (Reference Nehru and Balasubramanian2011), Goutham-Bharathi et al. (Reference Goutham-Bharathi, Roy, Krishnan, Kaliyamoorthy and Immanuel2014), and Ragavan et al. (Reference Ragavan, Saxena, Mohan, Ravichandran, Jayaraj and Saravanan2015) could not locate this species in the islands. Moreover, Ragavan et al. (Reference Ragavan, Saxena, Mohan, Ravichandran, Jayaraj and Saravanan2015) ascertained that the earlier unconfirmed reports of A. alba were misidentification of the morphological variants of A. marina by the earlier studies. Also, the current study documented a maximum GBH of 45 cm A. alba trees and did not find any old trees that would have had before the 2004 tsunami origin. The extensive survey between 2009–2011 by Nehru and Balasubramanian (Reference Nehru and Balasubramanian2018) and subsequent surveys by Ragavan et al. (Reference Ragavan, Saxena, Mohan, Ravichandran, Jayaraj and Saravanan2015) and Goutham-Bharathi et al. (Reference Goutham-Bharathi, Roy, Krishnan, Kaliyamoorthy and Immanuel2014) during 2012–2014 in Great Nicobar Islands did not report A. alba. Therefore, we assume that A. alba either occurred rarely or was absent in ANI's before the tsunami. Also, extreme events like cyclones and tsunamis in the Indian Ocean and Bay of Bengal may have facilitated propagule dispersal into ANI's from the neighbouring coastal lines. For example, the monsoonal current pattern of Indian Ocean Rim Countries (IORC) like Indonesia, Singapore, Thailand, Myanmar, and Bangladesh – where A. alba is abundantly found – are closely allied with ANI's (Turner and Yong, Reference Turner, Yong, Briffett and Chew1999; Imai et al., Reference Imai, Takyu and Nakamura2009; Chandran et al., Reference Chandran, Raj, Ravindran and Narayana2018; Setyadi et al., Reference Setyadi, Pribadi, Wijayanti and Sugianto2021; Aye et al., Reference Aye, Tong and Tun2022). Thus, these events may have led to the establishment of a new population in the new intertidal zones of Great Nicobar and North Andaman Islands. Also, it is noteworthy that we have found numerous seedlings of A. alba colonizing the seaward zones of its present locations in Great Nicobar and North Andaman. This species is also observed by the authors to form monodominant stands in the mangroves along the seaward zones across the eastern coast of India (e.g., Sundarbans, Bhitarkanika, Coringa). Therefore, the presence of A. alba is arguably recent in the ANI's, like Sonneratia ovata (Nehru and Balasubramanian, Reference Nehru and Balasubramanian2012), A. marina (Thirumurugan et al., Reference Thirumurugan, Singh and Prabakaran2022) and Aegiceras corniculatum (Thirumurugan et al., Reference Thirumurugan, Singh, Gnanasekaran and Prabakaran2023) in the Nicobar Islands. However, A. alba is expected to spread faster in the seaward zones of the new intertidal habitat and soon establish monodominant stands over the course of mangrove succession. A long-term monitoring of this succession would be required to understand the future patterns.
As per the IUCN Red List, the three Avicennia species found in ANI's are under the ‘Least Concern’ category, but their population status is declining consistently throughout the globe (IUCN, 2023). Concerning the global trend, it is very likely that the population status of Avicennia species would increase several folds due to the formation, and availability of vast new intertidal areas post coastal uplift and subsidence throughout the ANI's. Hence, it is recommended that the Avicennia species being one of the suitable species for the colonization of the new intertidal area should be strongly endorsed by the forest manager for a better success rate of mangrove plantation drive in the islands. Further, A. alba being the least abundant and rare species among all the three Avicennia needs an extensive exploration in the remaining mangrove patch of the islands to better understand the A. alba population status. Also, further studies focusing on the long-term monitoring of mangrove succession in the new intertidal zones, population genetics to ascertain the potential source of newly established populations of A. alba, and creating habitat suitability model to predict the futuristic spread of Avicennia spp. across the ANI's would be important to scientifically manage the plantation drives by the forest managers and local administration in the ANI's.
Acknowledgements
We are highly thankful to the DST-Inspire Faculty Programme (DST/INSPIRE/04/2018/001071/FA18-LSPA111) by the Department of Science and Technology, Government of India, and the Rufford Small Grant (grant ID – 32387-1) by The Rufford Foundation for financial support of the research work. We acknowledge encouragement by the Director, Dean, and Faculties at the Wildlife Institute of India. We extend our heartfelt thanks to the Department of Environment and Forest, Andaman and Nicobar Islands for field permission, manpower, and logistics support for the smooth conduct of fieldwork.
Authors’ contributions
CRediT authorship contribution statement
ARS: Funding acquisition, Conceptualization, Methodology, Data collection & curation, Validation, Visualization, Writing – original draft, Writing – review & editing. TMV: Methodology, Data collection & curation, Validation, Writing – review & editing. NP: Project administration, Supervision, Funding acquisition, Conceptualization, Methodology, Data collection & curation, Validation, Visualization, Writing – review & editing.
Financial support
1. DST-Inspire Faculty programme (Grant ID: FA18-LSPA111)
2. 1st Small grant by The Rufford Foundation (Grant ID: 32387-1)
Competing interests
None.
Data availability
Data will be provided on request.
