Species Diversity and Distribution of Mangroves in Andaman and Nicobar Islands, India

Botanica Marina 2014; 57(6): 421–432

M.P. Goutham-Bharathi*, S. Dam Roy, P. Krishnan, M. Kaliyamoorthy and Titus Immanuel Species diversity and distribution of mangroves in Andaman and Nicobar Islands, India

Abstract: Despite extensive studies on mangrove ecosys- Introduction tems of Andaman and Nicobar Islands since the 1870s, knowledge of exact species composition is far from com- About 71% of India’s mangroves are found in the east coast plete, and there is a lack of comprehensive locality data. (Forest Survey of India 2013) and the largest areas are those The present study was designed to review the existing of the Indian part of the Sundarbans and the Andaman literature and to provide an updated checklist of the true and Nicobar Islands. Mangroves of the Andaman and mangrove species of the Islands. Preliminary surveys Nicobar Islands account for 13% of the total Indian man- were carried out in seven regions (four from the Andaman grove cover (Forest Survey of India 2013), the diversity of group and three from the Nicobar group), and the specific which is similar to the Southeast Asian mangroves (Spald- survey sites for detailed study (n = 51) were selected based ing et al. 1997). With a relative mangrove density of 76.5% on representativeness, importance, and accessibility. Dur- (Mandal and Naskar 2008), the mangroves of Andaman ing 2009–2013, all the selected sites were visited, and and Nicobar Islands are recognized as the best in the mangrove species occurrence was recorded. At present, 25 country in terms of density and growth (Dagar et al. 1991). true mangrove species distributed among 10 families and Despite extensive studies of biogeography, ecology, 14 genera were identified vis-à-vis 17 to 36 species reported and forestry of the mangrove ecosystems of the Andaman in earlier studies. The discernible changes in species num- and Nicobar Islands since the 1870s, considerable dis- bers from earlier studies could mainly be attributed to our parities in species composition still exist, and there is a exclusion of associated littoral vegetation and of species lack of comprehensive locality data. The number of true unlikely to be present among the true mangroves of the mangrove species (plants restricted to intertidal and adja- Islands. Given their limited geographical area, the low cent communities) reported from the Islands ranges from similarity index values between the Andaman and Nico- 17 (Parkinson 1923) to 36 (Debnath 2004). Notwithstand- bar Island groups ( ≤ 0.4) indicate a need for periodical ing the geographical isolation of different islands, many surveys, as mangrove biodiversity is usually homogenous biogeographic studies (for example, Debnath 2004) have in regions where there are no impassable dispersal barri- given imprecise distributional data (Andaman Islands; ers. Further, regular updating of information on the extent Nicobar Islands) for the mangrove species reported in and status of mangroves in the Islands is imperative not their study. Further, mere inclusion of associated littoral only to improve our understanding of phytogeography but vegetation and of species unlikely to be present by several also for better management and conservation. authors based on earlier reports also has contributed to erroneous additions to the mangrove flora of the Andaman Keywords: conservation; floristic affinities; island; phyto- and Nicobar Islands, which emphasizes the importance of geography; species composition; true mangroves. extending our knowledge of mangrove species diversity and distribution in the Islands. DOI 10.1515/bot-2014-0033 Among the 25 countries that have mangrove veg- Received 3 June, 2014; accepted 29 October, 2014 etation in Asia, five viz., Indonesia, Malaysia, Myanmar, Bangladesh, and India, experience intensive logging or conversion to other land uses (FAO 2007). Mangrove forest *Corresponding author: M.P. Goutham-Bharathi, Fisheries Science area in the Andaman and Nicobar Islands continues to Division, Central Agricultural Research Institute (ICAR), decline rapidly, and approximately 369 km2 of mangroves Post Box No. 181, Garacharma (Post), Port Blair 744101, Andaman were lost over a period of 24 years from 1989 to 2013 (Forest and Nicobar Islands, India, e-mail: [email protected] Survey of India 2013). Though not subject to human-driven S. Dam Roy, P. Krishnan, M. Kaliyamoorthy and Titus Immanuel: Fisheries Science Division, Central Agricultural Research Institute land-use changes and urbanization threats, recent reports (ICAR), Post Box No. 181, Garacharma (Post), Port Blair 744101, indicate that there is a dearth of data relating to the det- Andaman and Nicobar Islands, India rimental factors responsible for such continued loss. 422 M.P. Goutham-Bharathi et al.: Mangroves of Andaman and Nicobar Islands

Hence, there is an urgent need to conserve the remaining the Islands. Generally, mangroves are categorized into mangrove area in the Islands. two viz., exclusive species (referred as strict mangrove, The knowledge of exact species composition is imper- obligate mangrove, or true mangrove) and non-exclusive ative not only for understanding the structure and func- species (referred as semi-mangrove, back mangrove, or tion of mangroves and their biogeographical affinities but mangrove associate) based on their habitat and morpho- also to plan strategies for their conservation and manage- logical specialization (Tomlinson 1986). The list given in ment (Jayatissa et al. 2002, Wang et al. 2003). The present Table 1 is not exhaustive, and publications in which no study aimed at assessing the species diversity and distri- categorization was followed (i.e., true mangroves vs. man- bution of mangroves in the Islands, supplemented with a grove associates) were not considered when reviewing critical review of the published literature. The probable mangrove species composition. However, these are briefly reasons for the significant disparities in numbers of man- discussed with regard to the topics studied separately. grove species reported in the earlier studies are also discussed vis-à-vis our field surveys. Floristic similarities

The floristic similarities between the seven regions were Materials and methods examined based on the species presence/absence data using the Sørensen (1948) similarity index. It was calcu- Study area and methods of survey lated as, 2a Mangrove communities across the entire stretch of the Sørensen similarity index(C)= , S (2ab++c) Andaman and Nicobar Islands were surveyed for a period of 5 years at different seasons during 2009–2013. Pre- where a = the number of shared species; b = the number of liminary surveys for identifying specific survey sites were species only in collection 1; c = the number of species only carried out in seven regions (four from the Andaman in collection 2. group of Islands and three from the Nicobar group). The survey sites were selected based on representativeness, importance, and accessibility. The 51 sites selected for conducting comprehensive mangrove surveys are mapped in Figure 1, and the GPS coordinates are given in Table S1. Results and discussion Sites were accessed using both road and boat transport in order to survey the extensive range of tidal reaches. Each Mangrove species reported in earlier studies of the survey sites was visited at least twice, and care was taken to observe both floral and vegetative characters. The numbers of true mangrove species recorded in 18 pub- The mangrove species were identified in the field follow- lications in which mangroves were categorized into true ing Tomlinson (1986) and Giesen et al. (2006), and loca- mangroves and mangrove associates are summarized in tions were recorded. Herbarium specimens for all the true Table 1. There is significant disparity in species numbers, mangrove species were prepared. Because of the conspic- and these have increased from 17 (Parkinson 1923) to 36 uous similarities in floristic characteristics between the (Debnath 2004) in a period of about 80 years. A similar Andaman and Nicobar Islands and Southeast Asian coun- increase in mangrove species diversity over the years has tries, the classification scheme adopted by Giesen et al. been reported from Australia (Duke 1992) and from Sri (2006) for classifying the Southeast Asian mangroves was Lanka (Jayatissa et al. 2002). followed in the present study. In addition to the literature listed in Table 1, mangrove species composition including halophytes and associated littoral vegetation of the Andaman and Nicobar Islands Review of the published literature has also been investigated by a few authors, although without classifying them into true mangroves and man- Mangrove species composition in the published literature grove associates. According to Blasco (1977), the princi- was compared with the present study to help determine pal halophilous nonparasitic species of the Andaman the validity of earlier records and to extend our knowl- and Nicobar Islands amount to a total of 35 species dis- edge of the current distribution of mangrove species in tributed among 22 families and 26 genera. Rajagopalan M.P. Goutham-Bharathi et al.: Mangroves of Andaman and Nicobar Islands 423

Figure 1 Map of the Andaman and Nicobar Islands depicting the survey sites. (A) Andaman group of Islands; (B) Nicobar group of Islands (see Supplementary Table S1 for names and geographical coordinates of sites).

(1987) reported 42 species of typical mangroves and the these, Chengappa (1934) investigated the regeneration of closely associated littoral vegetation distributed among mangrove forests in Andaman, and Gopinathan and Raja- 23 families and 32 genera. Singh et al. (1987a) studied the gopalan (1983) discussed the important mangrove species pattern and process in mangrove forests of the Islands of the Islands. Ellis (1987) studied the floral composition and reported 26 species of exclusive mangroves, though of nearshore vegetation of the Islands, and Jagtap (1992), without giving a species list. Blasco and Aizpuru (1997) in his account of the marine flora of the Nicobar Islands, have reported 37 species of halophytes including grassy reported 10 species of mangroves. In a recent study of re- types and ferns distributed among 22 families and 26 colonizing mangrove species in tsunami-devastated habi- genera, whereas Mandal and Naskar (2008) reported 61 tats, Nehru and Balasubramanian (2011) reported nine species of mangroves and mangrove associates distrib- mangroves and 30 mangrove associates from the Nicobar uted in 30 families and 39 genera in the Islands. Apart from Islands. 424 M.P. Goutham-Bharathi et al.: Mangroves of Andaman and Nicobar Islands

Table 1 Number of true mangrove species in the Andaman and Composition of true mangrove species Nicobar Islands according to 18 publications from 1923 to 2014 in which mangroves have been categorized into true mangroves and mangrove associates. The true mangrove species composition of the Andaman and Nicobar Islands recorded by 16 papers published from No. of No. of No. of true Source 1923 to 2014 is summarized in Table 3. As two of the 18 families genera mangroves references listed in Table 1 viz., Naskar and Mandal (1999) 09 13 17 Parkinson 1923 and Devraj (2001) have provided identical checklists to 13 16 22 Sahni 1958 Dagar et al. (1991) and Balachandra (1988), respectively, 11 14 23 Mall et al. 1985 they were not considered in this review of the species 11 14 25 Singh et al. 1986 composition. Altogether, 51 species have been reported as 13 17 34 Dagar 1987 14 20 33 Balachandra 1988 true mangroves from the Andaman and Nicobar Islands, 12 16 30 Das and Dev Roy 1989 of which only 11 were considered as true mangroves by all 13 17 34 Dagar et al. 1991 authors. 11 14 27 Singh and Garge 1993 Parkinson (1923) reported a total of 17 true mangrove – 17 27 Jagtap 1994 species from the Islands. It is pertinent to note that two 13 17 35 Dagar and Singh 1999 13 17 34 Naskar and Mandal 1999 species widely recognized as true mangroves, viz. Excoe- 14 20 33 Devraj 2001 caria agallocha and Heritiera littoralis were considered by 12 15 25 Dam Roy 2003 him to be terrestrial plants, and two other species, viz., 16 21 36 Debnath 2004 Aegialitis rotundifolia (observed by Kurz 1870 and Brandis 12 15 26 Dam Roy et al. 2009 1907) and Kandelia candel (observed by Brandis 1907), 13 17 34 Yao et al. 2011 were not encountered in the Islands during his surveys. – 18 33 Ragavan et al. 2014 10 14 25 Present study In his account of mangrove forests of the Islands, Sahni (1958) categorized true mangroves into two viz., principal “–” denotes details not available. and subsidiary species. Cerbera manghas, an occasional element of coastal forest and back mangrove communities (Tomlinson 1986), was included in his list of true man- New distributional records groves. Mall et al. (1985) surveyed the mangrove forests of Middle and South Andaman and reported 23 species of A total of five species (four from the Rhizophoraceae and true mangroves. Dagar (1987) reported the presence of A. one from the Lythraceae sensu lato) have been reported as rotundifolia and K. candel from the Islands after a lapse of new distributional records for the Andaman and Nicobar 80 years and, in addition, listed three species viz., Ceriops Islands between 1987 and 2012 (Table 2), of which Son- decandra, Sonneratia griffithi, and Xylocarpus meckongen- neratia ovata (Lythraceae sensu lato) was unknown from sis as “unobserved species”. His subsequent publication elsewhere in India (Kathiresan and Rajendran 2005, FAO (Dagar et al. 1991), however, did not confirm the pres- 2007, Mandal and Naskar 2008). ence of A. rotundifolia or K. candel, but two of the three

Table 2 Mangrove species recorded as new to the Andaman and Nicobar Islands between 1987 and 2012.

Species Locality Region Island group Herbarium reference Source

Rhizophora lamarckii Montr. Havelock South Andaman Andaman – Singh et al. 1987b Rhizophora stylosa Griff. Burmanallah South Andaman Andaman – Singh et al. 1987b Chidiyatapu South Andaman – Carbyn’s Cove South Andaman – Bruguiera cylindrica (L.) Blume Kadamtala Middle Andaman Andaman – Singh et al. 1987b Bambooflat South Andaman – Wright Myo South Andaman – Bruguiera sexangula (Lour.) Poir. Burmanallah South Andaman Andaman – Singh et al. 1987b Sonneratia ovata Backer Havelock South Andaman Andaman – Dam Roy et al. 2009 Havelock South Andaman Andaman s n 25536 PBL Goutham-Bharathi et al. 2012 Katchall Nancowrie Nicobar – Nehru and Balasubramanian 2012

Dam Roy et al. (2009) reported the occurrence of Sonneratia ovata from Havelock in a regional publication following which Goutham-Bhar- athi et al. (2012) provided a comprehensive description of its floral and vegetative characters. “–” denotes details not available. M.P. Goutham-Bharathi et al.: Mangroves of Andaman and Nicobar Islands 425 1 2 ○ ● ● ● ● ● ○ ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ○ ● ● ○ ● ● 16

● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● 15 Reference

○ ● ● ○ ● ● ● ● ● ● ● ● ● ○ ● ● ● ○ ● ● ● ● ● ○ ● ● 14

● ● ● ● ● ● ○ ○ ● ○ ● ● ● ○ ● ○ ● ● ● ● ● ● ● ● ● ○ ● ● ○ ○ ● ○ ● ● 13 ●? ●? ●?

● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● 12

○ ● ● ○ ● ● ● ● ● ● ● ○ ● ● ○ ● ○ ● ● ● ● ○ ● ● ● ○ ● ● ● ● ● ● ○ ○ ● ○ ● 11

● ● ● ● ● ● ● ○ ● ● ● ● ● ● ● ● ● ● ● ● ● 10 ●? ●?

9 ● ● ● ○ ● ● ● ● ● ● ● ● ● ● ○ ● ● ○ ● ● ● ● ● ●

8 ● ● ● ○ ● ● ● ● ● ● ○ ● ● ○ ● ○ ● ○ ● ● ● ○ ● ● ○ ● ● ● ● ● ○ ● ○ ○ ●? ●?

7 ● ● ● ● ● ● ● ● ● ● ○ ● ● ● ● ● ● ● ● ● ● ● ● ● ● ○

6 ● ● ● ● ● ● ● ● ● ● ● ● ● ○ ● ● ● ● ● ● ● ● ● ● ● ● ● ●

5 ● ○ ● ● ○ ● ● ● ● ● ● ○ ● ● ○ ● ● ● ● ● ○ ● ● ○ ● ● ● ● ● ● ● ●?

4 ● ● ● ○ ● ● ● ● ● ● ● ● ● ● ○ ● ● ○ ● ● ● ● ●

3 ● ● ● ○ ● ● ● ● ● ● ● ● ○ ● ● ○ ● ● ● ● ●

2 ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ●

1 ○ ○ ● ○ ● ○ ● ○ ● ● ○ ● ● ○ ● ● ● ● ○ ○ ○ ○ ○ ○ ●? ●?

Wall. Linn. agallocha Excoecaria Sarcolobus globosus Sarcolobus Lour. [ = Lour. trifoliata Derris (Willd.) Backer] heterophylla (Willd.)Derris Benth.; D. uliginosa Griff. stylosa Rhizophora Linn. officinalis Avicennia = [ Schum. K. (L.f.) spathaceae Dolichandrone D. rheedi (Spreng.) Seem.] Lamk. mucronata Rhizophora marina Avicennia (Forsk.) Vierh. Linn. ramiflora Cynometra Mont. lamarckii Rhizophora Blume alba Avicennia Kostel iripa Cynometra Blume [ = apiculata Blume Rhizophora Linn.] R. conjugata Thunberg [ = Thunberg elliptica Ardisia humilis Vahl] Ardisia Roxb.; (Poir.) solanacea Ardisia (Perr.) C.B. Robinson [ = C.B. Robinson (Perr.) tagal Ceriops Arn.] candolleana Ceriops Roxb. paludosa Phoenix (Roxb.) Pellegrin. [ = Pellegrin. (Roxb.) Aglaia cucullata Roxb.] cucullata Amoora (Griff.) Ding. Hou. (Griff.) decandra Ceriops Pemphis acidula J.R. & G. Frost Pemphis = [ (L.) Blanco corniculatum Aegiceras Gaertn.] A. majus L. [ = manghas Cerbera Bl.] odallam Cerbera Thunb. (Wurmb.) [ = (Wurmb.) Thunb. Nypa fruticans Wurmb.] Nipa fruticans Roxb. rotundifolia Aegialitis (Lour.) Merr. [ = Merr. (Lour.) brachiata Carallia lucida Roxb.] Carallia Willd. racemosa Lumnitzera (Lour.) Poir. (Lour.) sexangula Bruguiera Willd. speciosum Acrostichum Jack (Voigt) Jack = [ littorea Lumnitzera & Arn.] Wight L. coccinea (Roxb.) Wight & Arnold ex Griffith & Arnold Wight (Roxb.) parviflora Bruguiera L. aureum Acrostichum (Linn.) Druce [ = candel Kandelia & Arn.] Wight K. rheedi (Linn.) Lamk. gymnorrhiza Bruguiera Wall. volubilis Acanthus Dryand. littoralis Heritiera (L.) Blume cylindrica Bruguiera L. ilicifolius Acanthus L. indica Flagellaria (L.) Kosterm. [ = tersa Brownlowia Benth.] lanceolata B. Outline of the species composition of true mangroves in the Andaman and Nicobar Islands according to various authors. according to various Islands Nicobar and in the Andaman mangroves true composition of the species 3 Outline of Table mangroves true as listed Species Vahl ebracteatus Acanthus 426 M.P. Goutham-Bharathi et al.: Mangroves of Andaman and Nicobar Islands 1 2 ● ● ● ● ● ● ● species claimed “unobserved” in his preceding publica- 16 tion (C. decandra and X. meckongensis) were reported to

● ● ● ● ● ● ● ●

15 be present. Nevertheless, the total number of true man- Reference

grove species was 34 in both publications. Another pub- ● ● ● ● ● 14 lication by Dagar and Singh (1999), however, included all

the doubtful species (A. rotundifolia, Avicennia alba, C. ● ● ● ● ● 13 ●? ●? ●? decandra, K. candel) in the list of true mangroves. Singh

et al. (1986) investigated the mangrove forests of Middle ● ● ● ● ● 12 and South Andaman and reported Bruguiera sexangula,

● ● ● ● ● ● ● ●

11 Rhizophora lamarckii, and Sonneratia apetala as rare. Balachandra (1988) included Ardisia solanacea (actually

● ● ● ● ● 10 Ardisia elliptica), Carallia brachiata, and Dolichandrone

spathacea as true mangroves. Das and Dev Roy (1989) also 9 ● ● ● ● ● ● included A. alba and K. candel in their list of true man-

8 ● ● ● ● ● ● ● groves from the Islands. ●? Like Dagar et al. (1991), Singh and Garge (1993) also

7 ● ● ● ● ● ● reported X. meckongensis from the Islands. It is important

to note that no distributional data were given in either 6 ● ● ● ● ● ● report, despite inclusion of a rare species. Jagtap (1994)

5 ● ● ● ● ● ● also included A. alba, but A. marina, a common species ●? ●? reported in all literature except Parkinson (1923), was not

4 ● ● ● ● ● recorded in his study. Dam Roy (2003) surveyed only the

Andaman group of Islands and considered Flagellaria 3 ● ● ● ● ● indica to be a true mangrove. However, it was reported as

2 ● ● ● ● an associate in his subsequent publication (Dam Roy et al.

2009). 1 ● ● ● ● Debnath (2004) reported the highest number of

mangrove species (36). Brownlowia tersa, Derris trifoliata, and Dolichandrone spathacea were considered as true mangroves according to his classification. A few associate species, which occasionally occur within mangroves, were included as true mangroves by both Bal- achandra (1988) and Debnath (2004). Yao et al. (2011), in their comparative study of the mangrove flora in China and India, included five species whose presence remains uncertain, on the basis of records in Dagar (1987) and Dagar et al. (1991). In a recent account of the floral composition and taxonomy of mangroves, Ragavan et al.

3 (2014) claimed that 33 species of true mangroves were

3 present, but they described only 31 species (excluding Rhizophora hybrids). The adverse impact of including mangrove associates 3 or beach vegetation and species unlikely to be present when reporting the total number of mangrove species in a given area have been discussed in detail by Jayatissa et al. (2002). The inclusion of doubtful species in the mangrove flora of the Islands not only made a few of the past reports extremely unreliable (for example, Dagar et al. 1991, Dagar and Singh 1999, Debnath 2004) but also meant that the exact mangrove species composition of the Islands was 1, Parkinson 1923; 2, Sahni 1958; 3, Mall et al. 1985; 4, Singh et al. 1986; 5, Dagar 1987; 6, Balachandra 1988; 7, Das and Dev Roy 1989; 8, Dagar et al. 1991; 9, Singh and Garge 1993; 10, Garge Singh and 1991; 9, et al. 1989; 8, Dagar Dev Roy 1988; 7, Das and 1987; 6, Balachandra 1986; 5, Dagar Singh et al. 1985; 4, et al. Sahni 1958; 3, Mall 1923; 2, 1, Parkinson to be present. were claimed 33 species (2014), although et al. Ragavan by were described hybrids) Rhizophora (excluding mangroves true of 31 species Only a few authors. by species as three distinct Pierre were considered X. meckongensis and C.E. Parkinson (Prain) X. gangeticus its synonyms (Lamk.) Roem. and moluccensis Xylocarpus (Prain) C.E. Parkinson (Prain) gangeticus Xylocarpus König [ = granatum Xylocarpus obovata Blume] Carapa Sonneratia ovata Backer Sonneratia Kurz. griffithi Sonneratia (L.) Engl. [ = caseolaris Sonneratia acida L.f.] S. Buch. Ham. Buch. apetala Sonneratia (Lam.) M. Roem. moluccensis Xylocarpus ● denotes occurrence; ○ denotes occurrence but not considered as a true mangrove by the author(s);? denotes occurrence to be confirmed. the author(s);? denotes occurrence by mangrove as a true considered not but ○ denotes occurrence ● denotes occurrence; Smith alba Sonneratia Pierre meckongensis Xylocarpus Species listed as true mangroves true as listed Species Gaertn.f. hydrophyllaceae Scyphiphora 1 2 3 Table 3 Continued) ( Table 2014. et al. 2011; 16, Ragavan et al. Yao 2009; 15, et al. 2004; 14, Dam Roy 2003; 13, Debnath Singh 1999; 12, Dam Roy and 1994; 11, Dagar Jagtap uncertain. M.P. Goutham-Bharathi et al.: Mangroves of Andaman and Nicobar Islands 427

Diversity and distribution of mangroves The present distributional status of all the reported in the Andaman and Nicobar Islands true mangrove species in the Andaman and Nicobar Islands was assessed and is summarized below. A total of 25 true mangrove species distributed among 10 families and 14 genera were recorded from the Andaman and Nicobar Islands during the present Acanthaceae study (Table 4), of which 23 were recorded from South Andaman, and 20 each from North, Middle, and Little Acanthus and Avicennia are the only two genera of Acan- Andaman. Among the survey sites in the Nicobar Island thaceae that has representatives in mangrove communi- group, 10 species were recorded from Nancowrie and ties. The genus Acanthus was represented by two species Great Nicobar. Mangrove species diversity was poor in the Islands, viz., Acanthus ilicifolius and Acanthus at Car Nicobar, where only five species were found. ebracteatus, of which the former was found commonly Figure 2 shows the number of species of true mangroves distributed, while the latter was rare and observed only in different families recorded from different regions of from Sippighat and Shoal Bay of South Andaman. In addi- the Andaman and Nicobar Islands. As South Andaman tion, a few Acanthus specimens with unarmed leaves and was the most intensively studied region, the differences trailing stems closely resembling Acanthus volubilis were in species diversity among the survey regions may have observed from Carbyn’s Cove in South Andaman during been influenced by the differences in research effort 2009. Neither fruits nor flowers were observed through- (Nguyen et al. 2013). out our surveys despite repeated visits. A year later,

Table 4 Distribution and Red List Categories of true mangrove species identified in the present study in seven survey regions of the Andaman and Nicobar Islands (four from the Andaman Island group and three from the Nicobar Island group).

Family True mangrove species Survey regions1 Red List Category Andaman Island group Nicobar Island group

NA MA SA LA CN NC GN

Acanthaceae Acanthus ebracteatus ● LC Acanthus ilicifolius ● ● ● ● ● LC Avicennia marina ● ● ● ● LC Avicennia officinalis ● ● ● ● LC Arecaceae Nypa fruticans ● ● ● ● ● ● LC Phoenix paludosa ● ● ● ● ● ● NT Combretaceae Lumnitzera littorea ● ● ● ● ● LC Lumnitzera racemosa ● ● ● ● ● ● LC Euphorbiaceae Excoecaria agallocha ● ● ● ● ● ● LC Lythraceae Sonneratia alba ● ● ● ● ● LC Sonneratia caseolaris ● LC Sonneratia griffithi ● CR Sonneratia ovata ● NT Meliaceae Xylocarpus granatum ● ● ● ● ● LC Xylocarpus moluccensis ● LC Myrsinaceae Aegiceras corniculatum ● ● ● ● LC Rhizophoraceae Bruguiera cylindrica ● ● ● ● LC Bruguiera gymnorrhiza ● ● ● ● ● ● ● LC Bruguiera parviflora ● ● LC Ceriops tagal ● ● ● ● ● ● LC Rhizophora apiculata ● ● ● ● ● ● ● LC Rhizophora mucronata ● ● ● ● ● ● ● LC Rhizophora stylosa ● ● ● ● ● LC Rubiaceae Scyphiphora hydrophyllaceae ● ● ● ● LC Sterculiaceae Heritiera littoralis ● ● ● ● ● LC

CR, critically endangered; LC, least concerned; NT, near threatened. 1NA, North Andaman; MA, Middle Andaman; SA, South Andaman; LA, Little Andaman; CN, Car Nicobar; NC, Nancowrie; GN, Great Nicobar. 428 M.P. Goutham-Bharathi et al.: Mangroves of Andaman and Nicobar Islands

species were commonly distributed in all survey regions from both the Island groups except Car Nicobar.

Combretaceae

Two species viz., Lumnitzera littorea and Lumnitzera racemosa representing Combretaceae were recorded in our surveys of the Islands. The latter occurs widely in Gobind Nagar of Havelock and Lakshmanpur of Neil Island (South Andaman). In none of the survey sites were L. littorea and Figure 2 Number of species of true mangroves from different fami- L. racemosa found to co-exist (for example, Neil Island), lies in seven survey regions of the Andaman and Nicobar Islands. which could be due to their ecological niches excluding SA, South Andaman; NA, North Andaman; MA, Middle Andaman; LA, each other in a given habitat (Giesen et al. 2006). Little Andaman; NC, Nancowrie; GN, Great Nicobar; CN, Car Nicobar.

Euphorbiaceae encroachment of the site by the local communities has rendered further examination of the species impossible. Excoecaria agallocha (Euphorbiaceae) was common in the Acanthius volubilis was recorded nearly three decades Islands and found to inhabit the landward edges of man- ago as a rare species (Dagar 1987, Dagar et al. 1991, Dagar grove forests along with terrestrial vegetation. and Singh 1999) from Middle and South Andaman. It is important to note that Dam Roy et al. (2009) identified the Acanthus species mentioned above as A. volubilis based Lythraceae on spineless leaves and trailing stems. However, A. ilicifolius with entirely spineless leaves was also recorded from Lythraceae sensu lato was represented by four species Sippighat of South Andaman, indicating the significant from the genus Sonneratia viz., Sonneratia alba, Sonnera- variation in leaf forms in relation to the degree of spini- tia caseolaris, Sonneratia griffithi, and Sonneratia ovata, ness (Tomlinson 1986). It is important to note that recently of which only S. alba was reported by all the reviewed lit- Ragavan et al. (2014) reported A. volubilis from Shoal Bay. erature. While Parkinson (1923) had reported S. alba as a Avicennia was found only in the Andaman group of species with restricted distribution at Betapur of Middle Islands and was represented by two species viz., Avicen- Andaman, it was found to be commonly distributed in nia marina and Avicennia officinalis. Its absence from the all the regions across various habitats, either alone (Bur- Nicobar Islands could not be explained. However, Gopi- manallah and Shoal Bay of South Andaman) or together nathan and Rajagopalan (1983) reported A. marina three with stands of Avicennia and Rhizophora (Dugong Creek decades ago from Spiteful Bay of the Nancowrie group of of Little Andaman) in our surveys. Further, the Son- Islands. Das and Dev Roy (1989), Jagtap (1994), Dagar and neratia species reported as Sonneratia acida (actually S. Singh (1999) have added Avicennia alba to the mangrove caseolaris) by Parkinson (1923) had white petals in con- flora of the Andaman and Nicobar Islands, although it trast to their characteristic dark red petals. Nehru and has not been reported in any other studies including the Balasubramanian (2011) reported S. caseolaris from four current one. As no photographs or locality data were pro- re-colonizing mangrove habitats viz., Kamorta, Katchall, vided, this species could not be verified. However, Mandal Nancowrie, and Trinket of Nicobar Islands, although the and Naskar (2008) also included A. alba (a “+” sign indi- corresponding photograph (figure 3D, p 255) in the article cating its presence in table 2, p 140) in the mangrove flora suggests that S. alba has been misidentified as S. caseola- of the Andaman and Nicobar Islands in their review. ris for the following reasons: 1) mucro with no re-curved point, 2) white staminal filaments, 3) dull pericarp, and 4) cup-shaped hypanthium. Sonneratia apetala has not Arecaceae been recorded during the present study, although it has previously been reported from the Islands by several Arecaceae was represented by two species viz., Nypa fru- authors (Table 3). A few trees of Sonneratia griffithi were ticans and Phoenix paludosa in the Islands. These two observed at Betapur (Middle Andaman) during our M.P. Goutham-Bharathi et al.: Mangroves of Andaman and Nicobar Islands 429 surveys, as recorded by Ragavan et al. (2013). Subsequent et al. (2009) at Burmanallah (South Andaman) was con- to the new record of S. ovata from Radhanagar of Havelock firmed to be a variegated form of B. gymnorrhiza during in the Andaman group of Islands (Dam Roy et al. 2009, our surveys. As B. gymnorrhiza and B. sexangula are mor- Goutham-Bharathi et al. 2012) and from tsunami-impacted phologically similar, the number of colleters (finger-like mangrove habitats of the Nicobar Islands (Nehru and Bal- glandular structures inside the base of stipules) could be asubramanian 2012), our surveys revealed its presence at a useful diagnostic character (Sheue et al. 2005). Wandoor (South Andaman), thus, indicating that regional Although two species of Ceriops viz., Ceriops tagal and endemics may have a wider distribution in the Islands. Ceriops decandra have previously been reported from the Islands, only the former was found in the present study. Dagar et al. (1991) reported C. decandra from Chidiyatapu Meliaceae (South Andaman) two decades ago as a very rare species. Dagar and Singh (1999), Debnath (2004), and Yao et al. Tomlinson (1986) recognized three species of Xylocar- (2011) have also reported C. decandra from the Andaman pus (Meliaceae) viz., Xylocarpus granatum, Xylocarpus and Nicobar Islands but without giving a description or meckongensis ( = Xylocarpus gangeticus), and Xylocarpus locality data. moluccensis on the basis of habitat, trunk, fruit size, Of the four previously reported Rhizophora species, and root elaboration, of which only the former two are only three viz., Rhizophora apiculata, Rhizophora mucro- regarded as true mangrove species. Parkinson (1934), too, nata, and Rhizophora stylosa were found in our studies. recognized three different species of Xylocarpus and high- Identification of mangrove hybrids is problematic (Duke lighted the problems in differentiating X. granatum from et al. 2002). Singh et al. (1987b) was the first to record X. meckongensis. However, there is a great deal of ambi- Rhizophora lamarkii (a sterile hybrid between R. stylosa guity in Xylocarpus species due to deficient taxonomic x R. apiculata) from Havelock amidst R. apiculata and descriptions (Tomlinson 1986, Jayatissa et al. 2002). Two R. mucronata stands (Table 2). It was subsequently species of Xylocarpus viz., X. granatum and X. moluccensis added to the mangrove flora by several authors (Table 3). ( = X. gangeticus and X. meckongensis), were found in our However, our present study revealed the presence of Rhiz- surveys. Of these, the former was commonly distributed, ophora hybrids at Havelock (South Andaman) and Kimious whereas the latter was rare and found only at Baratang Bay (Car Nicobar), which stresses the importance of peri- of Middle Andaman. However, X. moluccensis was also odic surveys in mangrove stands where parental species observed at Havelock (South Andaman) and at Karmatang of Rhizophora taxa typically co-occur (Duke 2007) as there of Mayabunder (North Andaman) by the investigating are major taxonomic problems with Rhizophora (Duke et al. team during a pre-tsunami period (2003). 1998) despite its ubiquitous occurrence throughout the tropical world (Tomlinson 1986, Duke et al. 2002). Further, it is important to note that hybrids of Rhizophora were pre- Myrsinaceae viously reported by Ragavan et al. (2011) from Havelock. The inclusion of Kandelia candel in the mangrove One species representing Myrsinaceae, Aegiceras cornicu- flora of the Islands by several authors (Table 3) could not latum, was commonly encountered in our surveys. be explained as it has not been observed since Brandis (1907).

Rhizophoraceae Rubiaceae Three species of the genus Bruguiera viz., Bruguiera cylindrica, Bruguiera gymnorrhiza, and Bruguiera parviflora Scyphiphora hydrophyllaceae was common in the were reported in our surveys, among which B. gymnor- Andaman Islands, but it could not be located in the rhiza was found to be the most common in the middle Nicobar Islands in our surveys. and upper intertidal zones. Singh et al. (1987b) were the first to record Bruguiera sexangula in the Andaman and Nicobar Islands, and it was reported in all subsequent Sterculiaceae studies. However, it was not encountered during our surveys across the Islands. It is important to note that the Sterculiaceae was represented by Heritiera littoralis Bruguiera species reported as B. sexangula by Dam Roy along the landward edge of mangrove forests, often with 430 M.P. Goutham-Bharathi et al.: Mangroves of Andaman and Nicobar Islands

Table 5 Sørensen similarity index, CS, of the true mangrove flora among all seven regions surveyed in the Andaman and Nicobar Islands.

Survey regions Sørensen similarity index (CS)

North Middle South Little Car Nancowrie Great Andaman Andaman Andaman Andaman Nicobar Nicobar

North Andaman 0.487 0.482 0.487 0.286 0.4 0.4 Middle Andaman 0.469 0.487 0.286 0.4 0.4 South Andaman 0.469 0.263 0.377 0.377 Little Andaman 0.286 0.4 0.4 Car Nicobar 0.347 0.286 Nancowrie 0.412 Great Nicobar

terrestrial plants (for example, at Burmanallah and Sip- Five species viz., Acanthus volubilis, Sonneratia case- pighat of South Andaman, Kalipur of North Andaman) in olaris, Sonneratia griffithi, Sonneratia ovata, and Xylo- the Islands. carpus mekongensis are found to be rare in the Islands with restricted distribution. As the rural population in the Islands has traditionally used mangroves as a source Similarity in floristic composition between of wood and non-wood forest products, they should be survey regions informed about rare species and the importance of their conservation.

The Sørensen similarity indices were low (CS < 0.5; Table 5), The shortfalls of the present study are the inadequate indicating distant floristic affinities between the survey floristic exploration of western coasts of the Islands and regions. However, given the limited geographical area, the of some of the crocodile-infested areas (for example, low similarity index values between the Andaman and the Dugong creek of Little Andaman, Campbell Bay of Great Nicobar Island groups ( ≤ 0.4) suggests the need for period- Nicobar), which should be addressed in the future for ical surveys, as mangrove biodiversity is usually homog- precise documentation of species diversity. Though these enous in regions where there are no impassable dispersal Islands are part of the Indian subcontinent, the mangrove barriers (Spalding et al. 2007, Nguyen et al. 2013). flora present here exhibits greater affinities to the South- east Asian flora (for example, Sonneratia ovata) due to their geographical proximity. Hence, a detailed study of the diversity and distribution of mangroves in the Islands Conclusion would not only improve our understanding of phytogeography but may also lead to additions to the mangrove flora Until recently, the mangroves of the Andaman and of India. Further, this study stresses the significance of Nicobar Islands had remained intact and untouched by regular updating of information on the extent and status humans, but this situation is now changing quite rapidly of mangroves of the Andaman and Nicobar Islands for (Spalding et al. 2010), and the current incomplete knowl- better management and conservation. edge of exact species composition and lack of implemen- tation of adaption-centric conservation strategies could Acknowledgments: The authors thank Space Applications be damaging. The present study was designed to review Centre, Ahmedabad, India, for funding the research pro- the existing literature and to provide an updated checklist ject on Coastal Zone Studies, as a part of which this study of the true mangrove species of the Islands. At present, was carried out. 25 true mangrove species distributed among 10 families and 14 genera could be identified vis-à-vis 17 to 36 species reported in earlier studies. While the discernible changes in species numbers in earlier studies could be attributed to numerous reasons, the disappearance of a few rare References species reported in earlier studies remains unexplained, Balachandra, L. 1988. A comprehensive account of the mangrove which emphasizes our limited knowledge of their location vegetation of Andaman and Nicobar Islands. Ind. Forester 114: and the urgent need for conservation. 741–751. M.P. Goutham-Bharathi et al.: Mangroves of Andaman and Nicobar Islands 431

Blasco, F. 1977. Outlines of ecology, botany and forestry of the Forest Survey of India. 2013. India state of forest report. Forest Sur- mangals of Indian sub-continent. In: (V.J. Chapman, ed.) vey of India, Ministry of Environment and Forests, Dehradun, Ecosystems of the world 1: wet coastal ecosystems. Elsevier, India. p. 252. Amsterdam. pp. 241–260. Giesen, W., S. Wulffraat, M. Zieren and L. Scholten. 2006. Mangrove Blasco, F and M. Aizpuru. 1997. Classification and evolution of the guidebook for Southeast Asia. RAP Publication 2006/07: Bang- mangroves of India. Trop. Ecol. 38: 357–374. kok, Thailand, FAO Regional Office for Asia and the Pacific and Brandis, D. 1907. Indian trees. Constable, London. p. 767. Wetlands International. p. 769. Chengappa, B.S. 1934. Andaman forests and their reproduction, Gopinathan, C.P. and M.S. Rajagopalan. 1983. Mangrove resources. Part 1 Ind. Forester 60: 53–64. CMFRI Bulletin 34: 44–46. Dagar, J.C. 1987. Mangrove vegetation, its structure, ecology, Goutham-Bharathi, M.P., M. Kaliyamoorthy, S. Dam Roy, P. Krishnan, management and importance with special reference to Anda- Grinson-George and C. Murugan. 2012. Sonneratia ovata man and Nicobar Islands. In: Proceedings of the symposium (Sonneratiaceae) – a new distributional record for India from on management of coastal ecosystems and oceanic resources Andaman and Nicobar Islands. Taiwania 57: 406–409. of the Andamans, 17–18 July 1987, Andaman Sci. Ass., Central Jagtap, T.G. 1992. Marine flora of Nicobar group of islands in Anda- Agricultural Research Institute, Port Blair. pp. 8–23. man Sea. Ind. J. Mar. Sci. 21: 56–58. Dagar, J.C. and N.T. Singh. 1999. Plant resources of the Andaman Jagtap, T.G. 1994. Marine flora of Andaman and Nicobar group of and Nicobar Islands Vol. I. Bishen Singh and Mahendra Pal Islands, Andaman Seas, India. In: (V. Suryanarayan and Singh, Dehradun, India. p. 271. V. Sudarsan, eds) Andaman and Nicobar Islands: challenges of Dagar, J.C., A.D. Mongia and A.K. Bandyopadhyay. 1991. Mangroves Development. Konark Publication, Delhi. pp. 133–143. of Andaman and Nicobar Islands, Oxford and IBH Publishing Jayatissa, L.P., F. Dahdouh-Guebas and N. Koedam. 2002. A review Co., Pvt. Ltd, New Delhi, India. p. 166. of the floral composition and distribution of mangroves in Sri Dam Roy, S. 2003. A Compendium on mangrove biodiversity of Lanka. Bot. J. Linn. Soc. 138: 29–43. Andaman and Nicobar Islands. Shri Vignesh Prints, Chennai. Kathiresan, K. and N. Rajendran. 2005. Mangrove ecosystems of the p. 196. Indian Ocean region. Indian J. Mar. Sci. 34: 104–113. Dam Roy, S., P. Krishnan, Grinson-George, M. Kaliyamoorthy and Kurz, S. 1870. Report on the vegetation of the Andaman Islands. M.P. Goutham-Bharathi. 2009. Mangroves of Andaman and Superintendent of Government Printing, Calcutta. p. 75. Nicobar Islands. Central Agricultural Research Institute, Port Mall, L.P., V.P. Singh, A. Garge and S.M. Pathak. 1985. A new Blair. p. 65. approach towards the mangrove forest flora of Andaman Das, A.K. and M.K. Dev Roy. 1989. A general account of the man- Islands Ind. Forester 3: 290–300. grove fauna of Andaman and Nicobar Islands. Fauna and con- Mandal, R.N. and K.R. Naskar. 2008. Diversity and classification of servation areas: 4. Published by the Director, Zoological Survey Indian mangroves: a review. Trop. Ecol. 49: 131–146. of India, Kolkata, India. p. 173. Naskar, K.R. and R.N. Mandal. 1999. Ecology and biodiversity of Debnath, H.S. 2004. Mangroves of Andaman and Nicobar Islands: Indian mangroves. Daya Publishing House, New Delhi, India. taxonomy and ecology. Bishen Singh Mahendra Pal Singh, p. 754. Dehradun, India. p. 133. Nehru, P and P. Balasubramanian 2011. Re-colonizing mangrove Devraj P. 2001. Forests of Andaman Islands. International Book Dis- species in tsunami devastated habitats at Nicobar Islands, tributors, Dehradun, and IBD Publisher & Distributors, India. India. Check List 7: 253–256. p. 402. Nehru, P and P. Balasubramanian 2012. Sonneratia ovata Backer Duke, N.C. 1992. Mangrove floristics and biogeography. In: (Lythraceae): status and distribution of a Near Threatened (A.I. Robertson and D.M. Alongi, eds) Tropical mangrove eco- mangrove species in tsunami impacted mangrove habitats of systems. American Geophysical Union, Washington DC, USA. Nicobar Islands, India J. Threat. Taxa. 4: 3395–3400. pp. 63–100. Nguyen, T.V., N.H. Le, S. Lin., F. Steen, O. De Clerck 2013. Checklist Duke, N.C. 2007. A brief account of the mangroves of New Cal- of the marine macroalgae of Vietnam. Bot. Mar. 56: 207–227. edonia. Interim report, University of Queensland, Brisbane, Parkinson, C.E. 1923. A forest flora of the Andaman Islands. Indian Queensland, Australia. p. 4. Government Central Press, Shimla, India. p. 325. Duke, N.C., M.C. Ball and J.C. Ellison 1998. Factors influencing biodi- Parkinson, C.E. 1934. Indian species of Xylocarpus. Ind. Forester. 60: versity and distributional gradients in mangroves. Global. Ecol. 137–143. Biogeogr. 7: 27–47. Ragavan, P., M. Saxena, T. Coomar and A. Saxena. 2011. Preliminary Duke, N.C., E.Y.Y. Lo and M. Sun. 2002. Global distribution and study on natural hybrids of genus Rhizophora in India. ISME/ genetic discontinuities of mangroves – emerging patterns in GLOMIS Electronic J. 9: 13–19. the evolution of Rhizophora. Trees 16: 65–79. Ragavan, P., K. Ravichandran, P.M. Mohan and A. Saxena. 2013. Ellis, J.L. 1987. Floral composition of the nearshore vegetation Sonneratia griffithii Kurz: status and distribution in Andaman of the Andamans. In: Proceedings of the symposium on and Nicobar Islands. ISME/GLOMIS Electronic J. 11: 5–7. management of coastal ecosystems and oceanic resources Ragavan, P., M. Saxena, A. Saxena, P.M. Mohan, V. Sachithanandam of the Andamans, 17–18 July 1987, Andaman Science and T. Coomar, 2014. Floral composition and taxonomy of Association, Central Agricultural Research Institute, Port Blair. mangroves of Andaman and Nicobar Islands. Ind. J Mar. Sci. 43: pp. 24–27. 1031–1044. FAO. 2007. The world’s Mangroves: 1980–2005. FAO Forestry Paper Rajagopalan, M.S. 1987. Mangroves as component of coastal eco- 153, Rome. (also available at www.fao.org/forestry/site/man- systems of the Andamans. In: Proceedings of the symposium grove/statistics). on management of coastal ecosystems and oceanic resources 432 M.P. Goutham-Bharathi et al.: Mangroves of Andaman and Nicobar Islands

of the Andamans, 17–18 July 1987. Andaman Science Associa- Spalding, M.D., F. Blasco and C.D. Field, eds. 1997. World mangrove tion, Central Agricultural Research Institute, Port Blair. pp. 1–7. atlas. The International Society for Mangrove Ecosystems, Sahni, K.C. 1958. Mangrove forests in the Andaman and Nicobar Okinawa, Japan. p. 178. Islands. Ind. Forester 84: 554–562. Spalding, M.D., H.E. Fox, B.S. Halpern, M.A. Mcmanus, J. Molnar, Sheue, C.R., W.H. J.W.H. Yong and Y.P Yang. 2005. The Bruguiera (Rhiz- G.R. Allen, N. Davidson, Z.A. Jorge, A.L. Lombana, S.A. Lourie, ophoraceae) species in the mangroves of Singapore, especially K.D. Martin, E. Mcmanus, J. Molnar, C.A. Recchia and J. Robert- on the new record and the Rediscovery. Taiwania 50: 251–260. son. 2007. Marine ecoregions of the world: a bioregionaliza- Singh, V.P. and A. Garge. 1993. Ecology of mangrove swamps of the tion of coastal and shelf areas. Bioscience 57: 573–583. Andaman Islands. International Book Distributors, Dehradun, Spalding, M.D., M. Kainuma and Lorna Collins, eds. 2010. World India. p. 181. atlas of mangroves. Earthscan, London, Washington D.C., Singh, V.P., L.P. Mall, A. Garge and S.M. Pathak. 1986. Some ecologi- 2010. ISBN 978-1-84407-657-4 p. 319. cal aspects of mangrove forests of Andaman Islands. J. Bombay Tomlinson, P.B. 1986. The botany of mangroves. Cambridge Univer- Natur. Hist. Soc. 83: 525–537. sity Press, Cambridge. p. 419. Singh, V.P., A. Garge, S.M. Pathak and L.E. Mal. 1987a. Pattern and Wang B., S. Liang, W. Zhang and Q. Zan. 2003. Mangrove flora of the process in mangrove forests of the Andaman Islands. Vegetatio world. Acta. Bot. Sin. 45: 644–653. 71: 185–188. Yao, Y., S. Bera, K. Naskar, W. Liao and C. Li. 2011. A comparative Singh, V.P., L.P. Mall, A. George and S.M. Pathak. 1987b. A new study of mangrove floras in China and India. For. Stud. China record of some mangrove species from Andaman and Nicobar 13: 173–182. Islands and their distribution. Ind. Forester 113: 214–217. Sørensen, T.A. 1948. A method of establishing groups of equal amplitude in plant sociology based on similarity of species con- Supplemental Material: The online version of this article (DOI: tent, and its application to analyses of the vegetation on Danish 10.1515/bot-2014-0033) offers supplementary material, available to commons. Kgl Danske Vidensk. Selsk. Biol. Skr. 5: 1–34. authorized users.