_____________________________________________ *Correspondence: muktipadapanda@gmail.com ISSN 2235-9370 Print/ISSN 2235-9362 Online © University of Sri Jayewardenepura 78 Insect Flower Visitors and their Role in Mangrove Pollination: A Study from East Coast of India M. Panda1,3*, N. Lele2, R.N. Samal3, D. Dalai4, S.P. Parida5 and T.V.R. Murthy2 1Department of Botany, Banki (Autonomous) College, Odisha, India 2Space Application Center (SAC-ISRO), Ahmadabad, India 3Chilika Development Authority, Department. of Forest and Environment, Odisha, India 4Research Scholar, National Rice Research Institute, Odisha, India 5Centurian University of Technology and Management, Odisha, India Date Received: 23-02-2019 Date Accepted: 16-12-2019 Abstract Insects play a critical role in bringing successful pollination in angiosperms. Mangrove pollination is a poorly studied aspect from scientific community. This particular work investigated the insect visitors and other prospective of mangrove flowers. Twenty two species (i.e., 17 true and 5 mangrove associates) from Bhitarkanika Wildlife Sanctuary and Devi estuary of Odisha state (East coast of India) were selected; plants were pre-marked and visiting insects were recorded starting from 07.00 am to 13.00 pm during the flowering period of each species. Fifty three species of insects which belongs to seven orders, twenty five families and forty four genera were recorded. The highest, i.e., 14 sp. of insects had been recorded from Aegiceras corniculatum which is a small tree and riverine mangrove. Among insects, bees were found as the most common flower visitors (in 82% mangroves) and particularly “honey bee”, i.e., Apis dorsata visited to sixteen mangrove species (i.e., 73% mangroves). Bees, particularly Honeybee (A. dorsata), sweet bee (Lasioglossum sp.) and carpenter bee (Xylocopa pubescens) were actively engaged in pollen dispersal. Resident time and visitation rate supported that bees with highest visitation rate and low resident time were powerful candidates in bringing mangrove pollination. Wasps, beetles and butterflies act more to be foraging species. Facilitation of bee management and particularly supporting apiculture will help to increase pollination successes of rare and threatened mangroves at regional and global level. Keywords: Mangrove, flower, pollination, bees, forest conservation 1. Introduction Mangrove ecosystems are well known in terms of productivity, role of coastal protectio n, a habitat for diverse flora and fauna and most importantly as a large carbon pool both in living tissues and in the form of sediments. Mangal loss is over alarming and thus had been legalised in many countries. Long term conservation only possible through maintaining a stable population structure and flora diversity in the ecosystem. This depends on successive reproduction and subsequent regeneration of mangrove species. Pollinators are one such group whose effective management can maximise reproductive success of rare and endemic mangroves. Pollinators depend less on the plants than the plants on them (Tomlinson, 2016). Pollination benefits society by increasing food security, improving livelihoods and act as a key driver in the maintenance of biodiversity and ecosystem function (Pratap, 2011). Generally, pollination is done almost completely by canopy dwellers such as bats, birds, moths, butterflies, bees and other insects (Alongi, 2009). Identification of effective pollinator in forest with large DOI: https://doi.org/10.31357/jtfe.v9i2.4470 mailto:muktipadapanda@gmail.com Panda et al. /Journal of Tropical Forestry and Environment Vol. 9, No. 02 (2019), 78-92 79 canopy like mangrove is difficult. Tomlinson (2016) described pollination in terms of flower visitors that is presumed pollinators. Wild pollinators (mostly bees and flies) can be quite important for plants requiring insect pollination (Capinera, 2010). Not all bees gather nectar and produce honey but all of them gather and store up pollen grains and do cross pollination in flowering plants (Mani, 1995). The plants at most risk of loss which are dioecious and self-incompatible, and those that propagate only by seeds (Kearns and Inouye, 1997). The floral and pollination biology of mangrove plants has been moderately studied (Raju, 1990, Raju et al., 1994, Mitra et al., 2013). Mangroves have both self-pollinating and cross-pollinating mechanisms that vary with species (Kathiresan and Bingham, 2001, Tomlinson, 2016). These pollinators are a group of animals which includes birds, bats and insects like butterflies, bees, beetles, flies and wasps etc. (Azuma et al., 2002; Ghosh et al., 2008; Ghosh and Chakrabarti, 2012; Hogarth, 2015; Tomlinson, 2016). The flowers of family Rhizophoraceae display three different pollination mechanisms i.e., Rhizophora spp.:wind pollinated, Ceriops decandra: insect pollinated and explosive pollen release in Ceriops tagal and Bruguiera spp. (Ghosh et al., 2008; Hogarth, 2015; Tomlinson, 2016). Ghosh and Chakrabarti (2012) reported bee, wasp, moth and flies are capable of pollinating in C. decandra. Large flowered species of Bruguiera are pollinated by birds and small flowered species of Acanthus, Aegiceras, Avicennia, Excoecaria, and Xylocarpus are probably by butterflies and various types of bees (Noske, 1993; Hogarth, 2015). Some wasps and flies are highly dependent on mangroves for nesting and are particularly important pollinators of C. decandra, Kandelia candel and Lumnitzera racemosa (Tomlinson, 2016). In Avicennia marina, the most common visitor was the honeybee, Apis mellifera, which is apparently attracted to the nectar-like secretion found toward the base of the corolla tube (Clarke and Myerscough, 1991). The present study is undertaken to investigate the diversity of insect visitors and their ro le in pollination of twenty two mangroves (i.e., 17 true and 5 associate species) from Bhitarkanika Wildlife Sanctuary and Devi estuary (Odisha), along East Coast of India. 2. Methodology 2.1 The study area Two mangrove ecosystems, Bhitarkanika Wildlife Sanctuary (BWS) and Devi estuary (DE) of Odisha state, along the East Coast of India were selected for present study. BWS comes under legal protection and a part of it having the mangrove forest is declared also as a National Park (86 45 to 87 03 E Longitude and 20 30 to 20 48 N Latitude) in the view of better protection of mangrove species, with special reference to residing salt water crocodiles (i.e., Crocodylus porosus), Olive ridley sea turtle (i.e., Lepidochelis olivacea) and many other threatened fauna and flora residing inside and in connection to the ecosystem. It is a deltaic ecosystem established in the evolutionary process from deposition of the Brahmani and Baitarani rivers in Rajnagar coastal block of Kendrapara District. Mangrove of DE (86 18 to 86 20 E and 19 57 to 19 58N) is thought to be of recent formation that got established along the river bank of Devi (a distributaries of river Mahanadi). The climate of these sites is almost tropical and subtropical type. Max. rainfall in July-August (200-450 mm) and Min. in December-January (0-10 mm); Max. temperature in April-May (38 C) and Min. in January (15 C) and Relative humidity ranges from 60-88 as received data from Indian Meteorological Department (IMD, Bhubaneswar) for the specified time period. 2.2 Data collection Twenty two mangal species i.e., 17 true and 5 associates (Table 1; Supp. Table 1 and 2) were selected and study conducted during calendar year of 2016-2017. Five flowering twig of each species 80 were pre-marked during flower bud stage. One day visual study was conducted from morning 07.00 am to 13.00 pm during flowering time of each mangrove species. Not a single insect was captured or harmed by any means; photographs were taken using the camera, Sony Alfa SLT 58Y, DSLR (Plate 1). Insects were identified through experts’ knowledge and using literatures (Mani, 1995; Chinery, 2007; Resh and Carde, 2009; Singh, 2011; Smetacek, 2017). Table 1: Selected true mangrove and mangrove associates from two sites. True mangroves Mangrove associates Aegiceras corniculatum (L.) Blanco, Acanthus ilicifolius L., Aegialitis rotondifolia Roxb, Avicennia alba Blume, Avicennia marina (Forsk.)Veierh, Avicennia officinalis L. Bruuiera cylyndrica (L.) Blume, Bruguiera sexangula (Lour.) Poir, Bruguiera gymnorrhiza (L) Lamk, Excoecaria agallocha L., Heritiera fomes Buch-Ham. Kandelia candel (L) Druce, Lumnitzera racemosa Wild, Rhizophora mucronata Lamk. Sonneratia apetala Buch. – Ham., Xylocarpus granatum Koenig, Caesalpinia crista L., Cerbera odollam Gaertn, Excoecaria indica (Willd.) Mull. Arg., Salvadora parsica L. Tamarix troupii H.  Species selected from DE Pollinating efficacy was determined by comparing dynamic behavior of visitors, i.e., visitation rate (Landry, 2013) and resident time with consideration of morpho-structural characteristics of the visited insects. Other aspects like, host specificity, host range and pollination syndrome were also studied. Rate of visitation (20 min.) = number of particular species (insect)visits Number of flowers studied Resident time = Time spend by visitor on a single visit to a particular flower A Jaccard index (Cj) was calculated to compare species similarity between the two study sites. 𝐶𝑗 = 𝑎 𝑎 + 𝑏 + 𝑐 where: a=The number of species common to both sites b=The number of species in DE, but not in BWS c=The number of species in site BWS, but not in DE 3. Results A total of 53 species of insects were identified from flowers of studied mangrove species (Table 2; Supp. Table 1 and 2). The result excludes very small insects that were insignificant of carrying pollens. Identified insects belong to 7 orders, 24 families and from 44 genera. The representative orders were Coleoptera, Diptera, Hymenoptera, Lepidoptera, Orthoptera, Hemiptera and Odonta (Table 2 and Figure 1). Lepidoptera and Hymenoptera showed highest species diversity then others (22 spp. and 18 spp., respectively). Diptera and Coleoptera had only 5 and 4 species, respectively. Two species were from Hemiptera and one species each recorded from Orthoptera and Odonta. Out of the total, butterflies:19 spp., bees:8 spp., ants:6 spp., flies:5 spp., wasps and beetles:4 spp. each, moths:3 spp., bugs:2 spp. and one species each of crickets and dragonfly (Table 2 and Figure 2). The flowers of different mangrove species attract insects but variation exists between host range visited by a specific insect. Apis dorsata (Honeybee), Micraspis discolor (Ladybird beetle), Crematogastor spp. (Ant) and Cochliomyia macellaria (Flies) had wide host range then others (Figure 3). Maximum 15 insects were recorded from A. corniculatum and 12 recorded from E. agallocha (Figure 4). C. crista, a mangrove associate (climber) was found visited by 9 insects but most of them were moths and butterflies. The result showed flowers of four mangals, A. rotondifolia, A. marina, K. candel and E. indica were visited by eight insects each. Only, (1) (2) (3) Panda et al. /Journal of Tropical Forestry and Environment Vol. 9, No. 02 (2019), 78-92 81 3 insect species had been recorded from flowers of H. fomes and B. gymnorhiza (Figure 4). Among insects, bees were the most frequent visitors and they visited to 18 mangal species (82% of studied mangroves) and particularly “Honeybee”, i.e., Apis dorsata visited to sixteen mangrove species (i.e., 73% mangroves) (Figure 3 and Figure 5). Dragonfly and crickets were very rare flower visitors. Figure 1. Insect order wise number of insect species. Figure 2. Insect group wise number of species. 82 Figure 3. Showing host range of recorded insects (number of mangrove taxa visited by insects). The comparison of resident time among insect groups showed a large variation. Bees and wasps were found more dynamic and frequent flower visitors. Similarly, study of visitation rate showed high rate for bees, wasps, flies and butterflies, respectively in comparison with other recorded insect groups (Table 3). Moths had more residing time on flowers than others. The increasing trend of resident time is as BeeButterflyWaspFliesDragonflyBeetleCricketsBugsAntsMoth. Figure 4. Mangrove species wise recorded number of visited insect species. Figure 5: Insect group and their visited number of mangrove species. Panda et al. /Journal of Tropical Forestry and Environment Vol. 9, No. 02 (2019), 78-92 83 Table 2: Recorded insects from mangrove flowers and their classification (spp=species). SI.No. Name of insect Order Family Insect class 1 Apis dorsata Hymenoptera Apidae Bee 2 Ceratina simillima Hymenoptera Apidae Bee 3 Componotus spp.1 Hymenoptera Formicidae Ant 4 Componotus spp.2 Hymenoptera Formicidae Ant 5 Componotus spp.3 Hymenoptera Formicidae Ant 6 Crematogaster spp.1 Hymenoptera Formicidae Ant 7 Crematogaster spp.2 Hymenoptera Formicidae Ant 8 Delta campaniforme Hymenoptera Vespidae Wasp (Yellow potter) 9 Halictus ligatus Hymenoptera Halictidae Bee 10 Lasioglossum spp.1 Hymenoptera Halictidae Bee 11 Lasioglossum spp.2 Hymenoptera Halictidae Bee 12 Nomia spp. Hymenoptera Halictidae Bee (Sweet bee) 13 Polistes olivaceus Hymenoptera Vespidae Wasp 14 Polistes spp. 2 Hymenoptera Vespidae Wasp 15 Solenopsis spp. Hymenoptera Formicidae Ant 16 Trigona spp. Hymenoptera Apidae Bee 17 Vespula vulgaris Hymenoptera Vespidae Wasp 18 Xylocopa pubescens Hymenoptera Apidae Bee 19 Aulacophora spp. Coleoptera Chrysomelidae Beetle 20 Canthon viridis Coleoptera Scarabaeidae Beetle 21 Coccinella septempuncata Coleoptera Coccinellidae Beetle (Lady bird) 22 Micraspis discolor Coleoptera Coccinellidae Beetle (Lady bird) 23 Amata sperbius Lepidoptera Arctiinae Moth 24 Appias lyncida Lepidoptera Pieridae Butterfly 25 Atrophaneura latreillei Lepidoptera Papilionidae Butterfly 26 Pachliopta aristolochiae Lepidoptera Papilionidae Butterfly 27 Catochrysops strabo Lepidoptera Lycaenidae Butterfly 28 Catopsilia pyranthe Lepidoptera Pieridae Butterfly 29 Chilasa clytia Lepidoptera Papilionidae Butterfly 30 Crocidolomia biotalis Lepidoptera Crambidae Moth 31 Danaus chrysippus Lepidoptera Nymphalidae Butterfly 32 Danaus genutia Lepidoptera Nymphalidae Butterfly 33 Euploea core Lepidoptera Nymphalidae Butterfly 34 Everes lacturnus Lepidoptera Lycaenidae Butterfly 35 Helicoverpa armigera Lepidoptera Noctuidae Moth 36 Junonia lemonias Lepidoptera Nymphalidae Butterfly 37 Oriens gola gola Lepidoptera Hesperiidae Butterfly 38 Papilio demoleus Lepidoptera Papilionidae Butterfly 39 Papilio polytes Lepidoptera Papilionidae Butterfly 40 Parantica melaneus Lepidoptera Nymphalidae Butterfly 41 Precis almana Lepidoptera Nymphalidae Butterfly 42 Tirumala limniace Lepidoptera Nymphalidae Butterfly 43 Tirumala septentrionis Lepidoptera Nymphalidae Butterfly 44 Vanessa cardui Lepidoptera Nymphalidae Butterfly 45 Chrysomya megacephala Diptera Calliphoridae Flies 46 Cochliomyia macellaria Diptera Calliphoridae Flies 47 Eristalinus spp. Diptera Syrphidae Flies 48 Rhyncomya spp. Diptera Calliphoridae Flies 49 Sarcophaga spp. Diptera Sarcophagidae Flies 50 Chrysocoris spp. Hemiptera Scutelleridae Bugs 51 Dysdercus spp. Hemiptera Pyrrhocoridae Bugs 52 Crocothemis erytbraea Odonata Libellulidae Dragonfly https://en.wikipedia.org/wiki/Hymenoptera https://en.wikipedia.org/wiki/Ant https://en.wikipedia.org/wiki/Ant https://en.wikipedia.org/wiki/Ant https://en.wikipedia.org/wiki/Ant https://en.wikipedia.org/wiki/Ant http://eol.org/pages/648/overview http://www.discoverlife.org/mp/20q?search=Hymenoptera http://www.discoverlife.org/mp/20q?search=Hymenoptera http://www.discoverlife.org/mp/20q?search=Hymenoptera http://www.discoverlife.org/mp/20q?search=Hymenoptera https://en.wikipedia.org/wiki/Ant https://en.wikipedia.org/wiki/Hymenoptera http://www.discoverlife.org/mp/20q?search=Hymenoptera https://en.wikipedia.org/wiki/Coccinellidae https://en.wikipedia.org/wiki/Coccinellidae https://en.wikipedia.org/wiki/Lepidoptera https://en.wikipedia.org/wiki/Lepidoptera https://en.wikipedia.org/wiki/Lepidoptera https://en.wikipedia.org/wiki/Lepidoptera https://en.wikipedia.org/wiki/Lepidoptera https://en.wikipedia.org/wiki/Lepidoptera https://en.wikipedia.org/wiki/Lepidoptera https://en.wikipedia.org/wiki/Lepidoptera https://en.wikipedia.org/wiki/Lepidoptera https://en.wikipedia.org/wiki/Lepidoptera https://en.wikipedia.org/wiki/Lepidoptera https://en.wikipedia.org/wiki/Lepidoptera https://en.wikipedia.org/wiki/Lepidoptera https://en.wikipedia.org/wiki/Lepidoptera https://en.wikipedia.org/wiki/Lepidoptera https://en.wikipedia.org/wiki/Lepidoptera https://en.wikipedia.org/wiki/Lepidoptera https://en.wikipedia.org/wiki/Lepidoptera https://en.wikipedia.org/wiki/Lepidoptera https://en.wikipedia.org/wiki/Lepidoptera https://en.wikipedia.org/wiki/Lepidoptera https://en.wikipedia.org/wiki/Lepidoptera https://en.wikipedia.org/wiki/Diptera https://en.wikipedia.org/wiki/Dragonfly 84 53 Metrioptera spp. Orthoptera Tettigoniidae Crickets Table 3: Resident time and Visitation rate of each insect class. Flower visitors Resident time (S) (MeanSE) Visitation rate (m) (MeanSE) Bee 14.172.11 35.835.68 Beetle 34.673.28 4.171.23 Flies 23.083.42 5.331.25 Wasp 20.581.96 6.001.47 Butterflies 19.922.01 3.600.66 Ant 53.754.83 2.670.67 Moths 97.0012.27 2.400.66 Bugs 50.174.04 3.000.82 Dragonflies 28.002.56 2.500.41 Crickets 45.672.31 1.670.33 4. Discussion Mangrove flowers are not much eye-catching as like many terrestrial angiosperms. They also lack significant provisions in the form of pollinator rewards. In comparison to other forest or garden plants, few and specific insects do pollination in mangroves. Mangrove community contains species that are both generalists and specialists (Azuma et al., 2002). Our result showed similarity with many previous studies on aspects of pollinator diversity and role in mangrove species pollination (Clarke and Meyerscough, 1991; Pandit and Choudhury, 2001; Azmi et al., 2012; Raju et al., 2012; Raju et al., 2014, Hermansen et al., 2014; Tomlinson, 2016). The report towards visitation of ants, wasp, bugs, flies, bees, cantharid beetles and moths to flowers of A. marina by Clarke and Meyerscough (1991) showed similarity to this study. Hermansen et al. (2014) identified 38 species that visited to flowers of A. marina but only A. mellifera was a significant pollinator. We found A. dorsata as a potential pollinator of 16 mangrove species under our study. They had not reported butterfly visits which had been recorded during this particular investigation. In L. racemosa, three groups of flower visitors were found which include bees, wasps and butterflies (Raju et al., 2014). Our study had recorded beetle and ant visitation along with bees and butterflies from flowers of L. racemosa. K. candel is a riverine mangrove, occur along the river banks and influenced by freshwater input. The flowers of this plant produce a chemical (methyl anthranilate) that is known to repel species of birds and insects like bees and butterflies (Azuma et al., 2002). We recorded beetle, wasp and moth along with previously recorded bee and butterflies from flowers of K. candel. Pandit and Choudhury (2001) studied a 3 day (both day and night) flower visitors of mangrove species, A. corniculatum and S. ceseolaris at Bhitarkanika. They recorded 17 species of Lepidoptera, 7 species of Hymenoptera, 3 species of Diptera, 5 species of birds and 3 species of mammals from S. ceseolaris and 16 species of Lepidoptera, 9 species of Hymenoptera, 2 species of Diptera, 1 species of Coleoptera and 3 species of birds from A. corniculatum. The genus, ‘Bruguiera’ show specialised pollination through birds. They have large flowers and peculiar tube shape which attracts birds. In B. gymnorrhiza, the calyx is red, a colour attractive to birds (Tomlinson, 2016). In this particular study we recorded wasp, bee and ant visitation to B. sexangula; bee and ant from B. gymnorhiza (Table 4). Bees because of their structural adaptations for the collection of pollen are considered to be the most efficient pollinators (Abrol, 2012). Bees as a flower visitor have been observed in many species of the genera like, Acanthus, Aegiceras, Avicennia, Excoecaria, Rhizophora and Xylocarpus (Tomlinson, 2016). Xylocopa varipuncta (carpenter bee) has been identified to carry pollens of exclusive mangroves like, A. alba, L. racemosa, S. caseolaris, S. ovata and R. apiculata in the mangrove community of Setiu Wetlands, Terengganu (Azmi et al., 2012). Bumble bee visited flowers show increased seed set than when plant excluded from it (Miller-Struttmann, 2017). Carpenter bees have long tongue which gathers mainly Panda et al. /Journal of Tropical Forestry and Environment Vol. 9, No. 02 (2019), 78-92 85 pollen, but not nectar. Carpenter bee is one among the most efficient agents for cross pollination in mangrove flowers (Mani, 1995). We found it’s strong association with flowers of E. agallocha and A. Corniculatum (Plate 1). This bee is very dynamic and flies actively back and forth to flowers which help in pollen dispersal and deposition. The sweet bees (Lasioglossum spp.) are recorded from mangroves like, A. corniculatum, A. rotondifolia, B. gymnorhiza, K. candel and R. mucronata (Supp. Table 1). They were regular visitors in flowers of A. corniculatum (Plate 1). Their hind legs help and make them a good candidate for pollen dispersal. Comparison of host range showed bee, ant, beetles, butterfly, flies and wasps were more general flower visitors than moths, bugs, crickets and dragonfly which were rare and occasional visitors (Figure 5). Previously, no beetle pollinated flowers had been recorded from mangroves, which are considered to be “primitive” pollinators and typically associated with large flowers or inflorescences of much generalised type (Tomlinson, 2016). This particular study had recorded lady bird beetle (Micraspis discolor) visitation from 12 mangroves (54%) and thought to have a major contribution and bringing pollination in species like A. corniculatum, B. cylindrical, S. apetala, A. ilicifolius, C. decandra and K. candel (Figure 3, Plate 1). R. mucronata primarily wind pollinated but insect visitation also reported which supports our work. Table 4: Mangrove species and their flower visitor class identified in the present study. True mangroves Visitor class True mangroves Visitor class 1 A. corniculatum (L.) Blanco Bee, Flies, Wasp, Beetle, Ant, Bird 13 K. candel (L) Druce Bee, Beetle, Wasp, Butterfly, Moth 2 A. ebracteatus Vahl. Bee, Beetle, Wasp, Moth, Spider 14 L. racemosa Willd. Bee, Beetle, Ant, Butterfly, Bird 3 A. ilicifolius L. Bee, Beetle, Butterfly, Ant, Spider, Bird 15 R. mucronata Lamk. Bee, Beetle, Ant 4 A. rotondifolia Roxb. Bee, Wasp, Ant 16 S. apetala Buch. - Ham. Beetle, Moth, Bird 5 A. alba Blume Bee, Beetle, Dragonfly, Flies, Butterfly 17 X. granatum Koenig Bee, Beetle, Moth, Bugs, Ants, Bird 6 A. marina (Forsk.)Veierh Bee, Beetle, Moth, Flies, Wasp, Butterfly, Bird Mangrove associates 7 A. officinalis L. Bee, Beetle, Ant, Flies, Butterfly, Bird 18 C. crista L. Butterfly, Crickets, Moth, Bird 8 B. cylyndrica (L.) Blume Beetle, Ant, Flies 19 C. odollam Gaertn Ant, Butterfly, Moth, 9 B. sexangula (Lour.) Poir Bee, Ant, Wasp, Bird 20 E. indica (Willd.) Mull. Arg. Bee, Flies, Ants, Butterfly, Bugs 10 B. gymnorrhiza (L) Lamk Bee, Ant, Bird 21 S. parsica L. Bee, Beetle, Flies, Ant, Bird 11 E. agallocha L. Bee, Wasp, Flies, Bugs, Butterfly 22 T. troupii H. Bee, Butterfly, Bird 12 H. fomes Buch-Ham. Bee, Ant, Spider Ant and honey bee visitation to flowers of H. fomes showed their role in pollination of this south Asian endemic species. High resident time indicates it to be a forging species. An insect having high visitation rate and low resident time is a good pollinator (Landry, 2013). Our study showed, bees, butterflies, and wasps are efficient mangrove pollinators with low resident time and high visitation rate (Table 3). The species of former group with highest visitation rate, low resident time and with structural adaptation placed them a potential candidate in bringing mangrove pollination. Bugs, moths and ants were forging species and contribute little to the mangrove pollination as lack structural adaptation to carry pollens from flowers. We reviewed literature of eighteen mangrove species that showed all species were more or less associated with biotic pollinators like insects more commonly from family Hymenoptera, Diaptera, Coleoptera and Lepidoptera (Marshall, 1983; Clarke and Meyerscough, 1991; Raju et al., 1994; Sun et al., 1998; Naskar and Mandal, 1999; Pandit and Choudhury, 2001; Raju et al., 2006; Ghosh et al., 2008; Nagarajan et al., 2010; Ghosh and Chakraborti, 2012; Raju et al., 2012; Pandey and Pandey, 2013; Hermansen et al., 2014; Raju and Raju, 2014; Raju et al., 2014; Tomlinson, 2016) (Table 5). The latter two groups spend enough time for nectar foraging. Mangrove flowers are not much attractive but still able fascinate few unique insects that bring successful pollination. 86 The work of Faegri and Pijl (1979) and Abrol (2012) on pollination syndrome (characters which attracts or favors for pollination) also supported our findings (Table 6). The yellow/brown coloured flower of Avicennia sp. and B. sexangula; Blue colour in A. ilicifolius are commonly visited by bees. White flowered species of A. corniculatum and A. rotondifolia with ample nectar were found to be frequently visited by bees, i.e., Honeybee and Losioglossum spp. (Supp. Table 1; Plate 1). Thus, attracting pollinators is a prerequisite for reproductive success in angiosperms (Moyroud and Glover, 2017). Past work showed the genus, Sonneratia have night blooming flowers which attract bats for foraging and pollination (Table 5). Beetle and moth visits to flowers of Sonneratia spp. had been recorded from this study (Table 4). Butterfly visitation to T. troupii; flies visitation to E. agallocha and E. indica; beetle visitation to A. corniculatum, A. rotondifolia, K. candel and R. mucronata etc., bird pollination in B. sexangula and B. gymnorhiza; moth visitation of mangrove associates like, C. odollam and C. crista; ant visits to A. corniculatum and A. rotondifolia, X. granatum and H. fomes were supported by previous studies on pollination syndrome (Faegri and Pijl, 1979; Abrol, 2012). Table 5: Result of literature review showing studies on flower visitors and pollinators of different mangrove species. Mangrove Wind Insect Bird Bats (H/D/C) Butterfly (L) A. corniculatum (L.) Blanco - 3, 5, 6, 12 6, 12 6, 12 - A. rotondifolia Roxb. - 5 - - - A. illicifolius L. - 3 - 3 - A. alba Blume - 11 11 - - A. marina (Forsk.)Veierh - 2, 10, 11, 13 2 - - A. officinalis L. - 3,11 11 - - R. mucronata Lamk. 3,5,8,16 8*, 10 - - - B. cylindrical (L.) Blume - 16 3, 5 - - B. gymnorhiza (L.) Lamk. - 9 - 3, 5, 16 - B. sexangula (Lour.) Poir - 9 - 3, 5, 16 - C. crista L. - 5,14 14 - - C. decandra (Griff.) Ding Hou - 8, 7, 10, 16 - - - E. agallocha L. - 5 - - - K. candel (L) Druce - 3, 4, 5, 16 4, 5 - - L. racemosa Willd. - 3, 15, 16 15 - - Sonneratia sp. - - - 1, 16 X. granatum Koenig - 5* - - - H. fomes Buch.-Ham. - 5* - - - Note: 1: Marshall, 1983; 2: Clarke and Meyerscough, 1991; 3: Raju et al., 1994; 4: Sun et al., 1998; 5: Naskar and Mandal, 1999; 6: Pandit and Choudhury, 2001; 7: Raju et al., 2006; 8: Ghosh et al., 2008; 9: Nagarajan et al., 2010; 10=Ghosh and Chakraborti, 2012; 11: Raju et al., 2012; 12: Pandey and Pandey, 2013; 13: Hermansen et al., 2014; 14: Raju and Raju, 2014; 15: Raju et al., 2014; 16: Tomlinson, 2016 [H: Hymenoptera, D: Diaptera, C: Coleoptera, L: Lepidoptera and =Honeybee, = Bumble bee] Among the four bee species i.e., honey bee, carpenter bee, sweet bee and bumble bee, we observed that honey bees were more common and visited inflorescence in group. A single inflorescence of Salvadora parsica was noted to host approximately about 10-15 honey bees at a particular time. Similar results were recorded from mangroves like, A. corniculatum, A. marina and B. sexangula. Carpenter bees were the second most sociable after honey bees and recorded in groups of approximately 3-4 from the flowers of A. corniculatum and E. agallocha. Bumble bee and sweet bee were rare and single individuals had been recorded from the visited flowers. During this particular work we noted anti-herbivory role of Micraspis discolor (Ladybird beetle) which prevents leaf herbivory and damage in many mangrove species. Leaf area loss by herbivores is a common phenomenon in mangroves like genera Avicennia, Kandelia, Cerops and Rhizophora. Presence of Micraspis discolor on mangrove leaves protect leaves from herbivory damages along with play a critical role in pollination (Plate 1). Honey bee not only brings Panda et al. /Journal of Tropical Forestry and Environment Vol. 9, No. 02 (2019), 78-92 87 successful pollination, it also supports the earnings of local livelihood through high quality honey production. About 200 tons of honey and 50 tons of beeswax are harvested annually from reserve forest of Sundarbans (Gani, 2001). This is 50 percentage of total honey production of Bangladesh. In Bhitarkanika, honey is collected by the local people largely to sell in the market as resource for their livelihood (Hussain and Badola 2010). 88 Table 6: Pollination syndromes: Traits of flowers pollinated by different pollinators, (Adapted after, Faegri and Pijl, 1979; Abrol, 2012). Pollinator class Floral morphology Colour Scent Nectar tube Primary attractants Toughness Floral opening Insects (Entomophily) Differs with type of pollinators Yes Yes Yes Not enough Day and night Bees (Melitophily) Zygomorphic with great depth effect, mechanically strong adequate landing facility Blue, yellow, purple (except red) Sweet smell Nose size or Long body width Nectar hidden deep; sucrose rich; abundant pollen Not enough, have a landing platform or lip Day and night Flies (Myophily) Actinomorphic, regular, simple, funnel-like Light or dull, whitish Imperceptible Open cups Nectar Not tough Day and night Butterflies (Psychophily) Actinomorphic, flowers in group, erect radial, good landing facilities Dull brown, white, blue and purple Weak Long narrow Nectar in ample quantities, hidden at base of pollen tubes Not tough, no landing platform Day and night Moths (Phalaenophily) Actinomorphic or Zygomorphic, horizontal Pale, purple, white Strong sweet, nocturnal Long narrow Nectar in large but hidden in tubes Not tough, no landing platform Night Ants (Myrmecophily) Small, sessile, close to ground White, purple, blue Faint Hidden deep Nectar and Pollen ------------ Day and night Beetles (Cantharophily) Actinomorphic, large shallow, often bowl shaped blossoms Dull white, purple or brown Strong fruity No Mostly pollen, Sometimes nectar Not enough Day and night Wasp (Sphecophily) Dull brown Nectar Day and night Birds (Ornithophily) Large container like, tubular or funnel like strong supports for perch. Red, yellow or orange No (birds can’t smell) Long wider Nectar, insects sitting flower, rarely pollen Tough, leathery, plenty of nectar Day and night Wind (Anemophily) Regular, small, Unisexual (either monoecious or dioecious species), highly reduced perianth, anthers and stigmas exerted Yellow or brown, may be absent or reduced No No ------- Not tough, big anthers, plenty of pollen. Stigmas feathery to catch the pollen Day and night  From present study Panda et al. /Journal of Tropical Forestry and Environment Vol. 9, No. 02 (2019), 78-92 89 Plate 1: Flower visitors and presumed pollinators in different mangrove species of BWS and DE. [Note: 1-4: A. dorsata (Giant honey bee) on flowers of A. rotondifolia, R. mucronata, S. parcica and A. officinalis, respectively; 5: Vespula sp. on flower of A. rotondifolia; 6-7: Euploea core and Tirumala limniace on flowers of T. troupii, respectively; 8: Lasioglossum sp.1 on flower of A. corniculatum; 9-10: Lasioglossum sp.2 on flower of A. corniculatum; 11: Amata sperbius feeding on flowers of X. granatum; 12: Xylocopa pubescens visiting flowers E. agallocha; 13: Nomia sp. on E. indica; 14: Micraspis discolor sitting on flower of A. corniculatum; 15 & 16: Dysdercus sp. (bug) & Ant visitation on flowers of X. granatum, respectivly; 17: A bug (Aulacophora sp.) sitting 1 2 3 4 8 7 6 5 11 10 9 14 13 12 15 16 17 18 19 90 on A. corniculatum; 18: Herbivory of mangrove leaves; 19: Undamaged leaves in presence of Micraspis discolor on K. Candel] 5. Conclusion Mangroves are exclusively seed propagated plants. Excluding Rhizophora spp. which bears predominantly wind pollinated mangroves, all other species more or less depend on biotic agents/pollinators for effective pollen transfer. Habitat degradation, conversion to aquaculture land, use of pesticides in agriculture, introduction of exotic plant species are strongly affecting the existence and action of natural pollinators. ‘Bhitarkanika’ being the second large single mangrove patch in India, presently experiencing loss of species diversity for which it was previously known throughout the globe. Impact of climate change on pollinator availability and specialist pollination in mangroves can further studied towards effective management of fragile ecosystem like mangrove. Giving more emphasis on bee keeping can help to increase the reproductive success and seed output in many mangroves. Not only the honey bee but others like Carpenter bee (Xylocopa spp.), Sweet bee (Lasioglosum spp.) may need to be given priority for increase of their population. Conservation of associate mangrove species will give additional advantage to maintain true mangrove diversity as they provide alternative forage during non flowering period of true mangrove species. Making policies and law to prevent use of harmful chemicals in peripheral agriculture land will help to prevent further loss of these natural pollinators. The anti-herbivory role of the predatory ladybird beetle and effect of climate change on pollinator availability in this fragile coastal ecosystem may be further investigated and can be used towards long term management. Acknowledgment We are thankful to PCCF, Wildlife (Odisha), DFO- Rajnagar and staffs of mangrove forest division of BWS for their support and valuable contribution during our field survey. References Abrol, D.P., 2012. 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