PLATINUM The Journal of Threatened Taxa (JoTT) is dedicated to building evidence for conservaton globally by publishing peer-reviewed artcles online OPEN ACCESS every month at a reasonably rapid rate at www.threatenedtaxa.org. All artcles published in JoTT are registered under Creatve Commons Atributon 4.0 Internatonal License unless otherwise mentoned. JoTT allows allows unrestricted use, reproducton, and distributon of artcles in any medium by providing adequate credit to the author(s) and the source of publicaton.

Journal of Threatened Taxa Building evidence for conservaton globally www.threatenedtaxa.org ISSN 0974-7907 (Online) | ISSN 0974-7893 (Print) Communication Pollination ecology of Brownlowia tersa (Malvaceae), a Near Threatened non-viviparous true mangrove shrub

Aluri Jacob Solomon Raju

26 July 2019 | Vol. 11 | No. 9 | Pages: 14119–14127 DOI: 10.11609/jot.4906.11.9.14119-14127

For Focus, Scope, Aims, Policies, and Guidelines visit htps://threatenedtaxa.org/index.php/JoTT/about/editorialPolicies#custom-0 For Artcle Submission Guidelines, visit htps://threatenedtaxa.org/index.php/JoTT/about/submissions#onlineSubmissions For Policies against Scientfc Misconduct, visit htps://threatenedtaxa.org/index.php/JoTT/about/editorialPolicies#custom-2 For reprints, contact

The opinions expressed by the authors do not refect the views of the Journal of Threatened Taxa, Wildlife Informaton Liaison Development Society, Zoo Outreach Organizaton, or any of the partners. The journal, the publisher, the host, and the part- Publisher & Host ners are not responsible for the accuracy of the politcal boundaries shown in the maps by the authors.

Partner Member

Threatened Taxa

Journal of Threatened Taxa | www.threatenedtaxa.org | 26 July 2019 | 11(9): 14119–14127

Pollination ecology of Brownlowia tersa (Malvaceae), a Near Threatened non-viviparous true mangrove shrub Communication

Aluri Jacob Solomon Raju ISSN 0974-7907 (Online) ISSN 0974-7893 (Print) Department of Environmental Sciences, Andhra University, Visakhapatnam, Andhra Pradesh 530003, India. PLATINUM [email protected] OPEN ACCESS

Abstract: Brownlowia tersa is a low-ground semi-evergreen shrub species. The phenological events occur sequentally—leaf fall, leaf fushing, fowering and fruitng from April to November. It is hermaphroditc, protandrous, self-compatble, facultatve xenogamous, and melitophilous involving worker honey bees, small male and female carpenter bees and male and female cuckoo bees. Of these, worker honey bees and female carpenter bees forage for both pollen and nectar while male carpenter bees and both sexes of cuckoo bees forage exclusively for nectar. Cuckoo bees are very important for cross-pollinaton because they are swif fiers and visit many fowers from diferent plants in the shortest tme. Carpenter bees and honey bees are largely important for self-pollinaton as they are not fast fiers and tend to spend more tme at each fower for forage collecton. The fowers have a specialized pollinaton mechanism to resort to autonomous autogamy if not pollinated but this mode of pollinaton is subject to the availability of pollen in its own anthers. Fruit is a 1-seeded follicle produced from a single carpel of the fower. It is indehiscent and foats in tdal water when detached from the plant. When setled in muddy substratum, it breaks open to expose the seed which germinates and produces a new plant in quick succession. The study reports that the plant is highly threatened due to diferent human economic actvites taking place in the area and hence immediate in situ conservaton measures are required for its protecton and propagaton.

Keywords: Facultatve xenogamy, hermaphroditsm, melitophily.

DOI: htps://doi.org/10.11609/jot.4906.11.9.14119-14127

Editor: Cleofas Cervancia, University of Philippines Los Baños College Laguna, Philippines. Date of publicaton: 26 July 2019 (online & print)

Manuscript details: #4906 | Received 18 February 2019 | Final received 31 May 2019 | Finally accepted 16 June 2019

Citaton: Raju, A.J.S. (2019). Pollinaton ecology of Brownlowia tersa (Malvaceae), a Near Threatened non-viviparous true mangrove shrub. Journal of Threatened Taxa 11(9): 14119–14127. htps://doi.org/10.11609/jot.4906.11.9.14119-14127

Copyright: © Raju 2019. Creatve Commons Atributon 4.0 Internatonal License. JoTT allows unrestricted use, reproducton, and distributon of this artcle in any medium by adequate credit to the author(s) and the source of publicaton.

Funding: UGC, New Delhi, India and Society for Conservaton Biology, Washington DC, USA.

Competng interests: The author declares no competng interests.

Author details: Prof. A.J. Solomon Raju is the recipient of several natonal and internatonal awards. He has more than 300 research papers in internatonal and natonal Journals.

Acknowledgements: The work reported in this paper was carried out with the fnancial support received under BSR Mid-Career Award insttuted by the University Grants Commission, New Delhi, and Marine Secton - Small Grants Program insttuted by the Society for Conservaton Biology, Washington DC, USA.

14119 Pollinaton ecology of Brownlowia tersa Raju

INTRODUCTION true mangrove species (Duke 1992; Giesen et al. 2007; Polidoro et al. 2010) though it has not been included The Malvaceae family contains herbs and shrubs in the Indian mangrove fora in certain natonal and (Tang et al. 2007). Flowers of this family are usually internatonal status reports (Kathiresan & Bingham hermaphroditc and entomophilous (Ruan 2010). 2001; Kathiresan & Rajendran 2005; Anonymous 2008; Wind pollinaton in the species of this family is unlikely Mandal & Naskar 2008). But, it is reported as a true because the pollen grains are stcky and tend to clump mangrove species in the mangrove fora of Andaman together. Pollinators are mostly bees and buterfies; & Nicobar Islands (Sahni 1958; Debnath 2004). In the however, other pollinators are species-specifc and IUCN Red List, it is included in the Near Threatened include hawk moths, hummingbirds, and other birds category (Kathiresan 2010; Polidoro et al. 2010) and the (Rathcke 2000; Ruan 2010). In this family, the sub- reasons stated for this status include habitat loss from family Brownlowioideae consists of eight genera with coastal development, erosion and the constructon of 70 species distributed in palaeo-tropical lattudes. shrimp and fsh ponds throughout its range. Further, it This sub-family is characterized by sepals fused into a is also stated that this species may qualify for threatened campanulate tube (Burret 1926), many stamens either category in the near future due to its occurrence only on unfused or slightly fused into fascicles at their base with the landward margin where it is the most vulnerable to or without staminodia (Ridley 1922; Hutchinson 1967), coastal development and human actvites (Kathiresan and ovaries sessile or borne on a short-stalk representng 2010). B. tersa has been in use as a traditonal folk gynophore. Among these genera, Brownlowia consists remedy for diarrhoea, dysentery, wounds and boils. of about 30 species widely distributed in southeastern Roots possess antbacterial actvity while leaves possess Asia through Malaysia and the Pacifc Islands (Tomlinson ant-infammatory, antoxidant, analgesic and ant- 1986). Diferent authors reported that Brownlowia is a diarrhoeal actvites (Hossain et al. 2013). Despite its genus of trees, comprising about 25 species in southern threatened status, there have been no studies on the and southeastern Asia with Borneo as centre of its reproductve biology of this species in any part of its distributon where it is represented by 17 species of which distributon. Further, the other species B. argentata has 15 are endemics. Many species of this genus grow along also not been investgated for its reproductve biology so rivers, in swamp forests and mangroves (Kostermans far. Tomlinson (1986) noted that the pollinaton biology 1965; Turner 1995; Bayer & Kubitzki 2003). This genus is of Brownlowia is unknown. Since then, no one has ever distnguished from other genera by its apocarpous fruits atempted to report on the pollinaton biology of any and loosely connected carpels (Bayer & Kubitzki 2003). species of this genus. Only two shrub hermaphroditc species B. argentata The study is aimed at providing certain details of and B. tersa have been reported as occurring in swamp foral biology and pollinaton in B. tersa which is currently forests and river banks, and mangroves inundated by the in threatened status at Coringa Mangrove Forest (CMF), highest tdes (Tomlinson 1986). These two species have Andhra Pradesh, India. This informaton is useful been classifed as true mangrove species by diferent to understand the sexual, breeding, and pollinaton authors (Duke 1992; Giesen et al. 2007; Polidoro et al. systems and fruitng ecology. Further, it provides clues 2010). B. tersa is distributed from India to southeastern to understand why it atained threatened status not only Asia where it has been recorded in Myanmar, Cambodia, at this forest and also at other mangrove forests where Thailand, Malaysia, Brunei, Singapore, the Philippines, it is distributed. Indonesia (Giesen et al. 2007). In India, its distributon is restricted to the east coast where it is common in West Bengal and Odisha but rare in the Godavari estuary of MATERIALS AND METHODS Andhra Pradesh, and the Andaman & Nicobar Islands (Venu et al. 2006; Kathiresan 2010; Bhat et al. 2011). CMF covering an area of 188km2 lies at 16043’47.413”N This species is distnguishable in the feld based on and 82012’54.864”E. It is located in the delta in East certain characters such as the presence of brown-scaly Godavari District; it is created by the river Godavari. twigs, lanceolate leaves with dull silvery undersurface Freshwater fows into the mangrove wetlands of the and pear-shaped, 2-valved fruits. It ofen grows in Godavari delta for a period of six months and peak fow stands along the banks, remains almost half-submerged normally occurs during July to September, coinciding during high tde, and withstands the tdal surges due with the southwest monsoon season. During this period to its intricate root system. Globally, it is reported as a the entre delta, including the mangrove wetland is

14120 Journal of Threatened Taxa | www.threatenedtaxa.org | 26 July 2019 | 11(9): 14119–14127 Pollinaton ecology of Brownlowia tersa Raju submerged under freshwater, since penetraton of sea fower was determined and expressed in µl. The fowers water is completely blocked by the large amount of used for this purpose were bagged at the mature bud incoming freshwater. Brackish water conditons prevail stage, opened afer anthesis and nectar squeezed into from October to February and sea water dominates the micropipetes to measure the volume of nectar. Nectar entre mangrove wetland from March to May due to sugar concentraton was also simultaneously determined the absence of freshwater discharge. In recent tmes, using a hand sugar refractometer (Erma, Japan). however, freshwater discharge from the river system is Fify fowers each from 10 randomly selected plants low due to insufcient and erratc rainfall during monsoon were used for each mode of the breeding system. The seasons. stgmas were pollinated with the pollen of the same Field studies were carried on the populatons of fower manually by using a brush; they were bagged for Brownlowia tersa (L.) Kosterm. in the areas of Ratkalva fruit set through manipulated autogamy. The fowers Reserve Forest which falls under non-sanctuary area were fne-mesh bagged without hand pollinaton for fruit of CMF. Observatons regarding the organizaton of set through spontaneous autogamy. The emasculated inforescences, the spatal positoning of fowers, and fowers were hand-pollinated with the pollen of a their positon on the plant were made since these diferent fower on the same plant; they were bagged features are regarded as important for foraging and and followed for fruit set through geitonogamy. The efectng pollinaton by fower-visitors. The fower emasculated fowers were pollinated with the pollen of a longevity was recorded by marking 20 just open fowers diferent individual plant and bagged for fruit set through and following them untl fall of. Anthesis was initally xenogamy. All these modes of pollinaton were followed recorded by observing 10 marked mature buds in the for one month for calculatng the percentage of fruit set feld. Later, the observatons were repeated fve tmes in each mode. Twenty inforescences consistng of 125 on diferent days, each day observing 10 marked mature fowers were tagged on 20 plants prior to anthesis and buds in order to provide accurate anthesis schedule. The followed for fruit set rate in open-pollinatons. Fruit same marked mature buds were followed for recording maturaton period, fruit dehiscence, seed dispersal and the tme of anther dehiscence. The presentaton patern establishment were observed in detail. of pollen was also investgated by recording how anthers The insects visitng the fowers were bees only and dehisced and confrmed by observing the anthers under they had their nestng sites close to B. tersa populatons. a 10x hand lens. The details of fower morphology such They were observed carefully for 10 hours a day for 15 as fower sex, shape, size, colour, odour, sepals, petals, days in diferent weeks during the fowering season. The stamens and ovary were described. hourly foraging visits of each bee species were recorded Twenty-fve mature but un-dehisced anthers were on 10 diferent days for which 30 inforescences were collected from fve randomly chosen plants and placed in selected. The data obtained was used to calculate the a petri dish. Later, each tme a single anther was taken out percentage of foraging visits made by each bee species and placed on a clean microscope slide (75 x 25 mm) and per day in order to understand the relatve importance dabbed with a needle in a drop of lactophenol-aniline- of each bee species. Simultaneously, the bees were blue. The anther tssue was then observed under the observed for their foraging behavior such as mode of microscope for pollen, and if pollen grains were not there, approach, landing, probing behaviour, the type of forage the tssue was removed from the slide. The pollen mass they collected, contact with essental organs to result in was drawn into a band, and the total number of pollen pollinaton, and inter-plant foraging actvity. The bees grains was counted under a compound microscope (40x were captured from the fowers during 10.00–12.00 h on objectve, 10x eye piece). This procedure was followed fve diferent days for pollen analysis in the laboratory. for countng the number of pollen grains in each anther For each bee species, 10 specimens were captured and collected. Based on these counts, the mean number each specimen was washed frst in ethyl alcohol and the of pollen produced per anther was determined. The contents stained with aniline-blue on a glass slide and characteristcs of pollen grains were also recorded. The observed under a microscope to count the number of stgma receptvity was observed by H2O2 test as given in pollen grains present. In the case of pollen collectng Dafni et al. (2005). bees, pollen loads on their corbiculae/scopae were The presence of nectar was determined by observing separated prior to washing them. From pollen counts, 50 mature buds and open fowers collected at random from the average number of pollen grains carried by each 10 plants. Individual volumes of nectar were recorded bee species was calculated to know the pollen carryover for 20 fowers and then the average volume of nectar per efciency of diferent bees.

Journal of Threatened Taxa | www.threatenedtaxa.org | 26 July 2019 | 11(9): 14119–14127 14121 Pollinaton ecology of Brownlowia tersa Raju

RESULTS below and light yellow with brown dots all over. Corolla is cream-coloured with light yellow base, 2–3 mm longer Habit and phenology than calyx, 5-petalled, free and apex rounded. Stamens Brownlowia tersa is a semi-evergreen bushy and are many, free, present in fve bundles and free from spreading shrub distributed in sunny locatons along calyx and corolla. Anthers are petaloid and atached to tdal creeks and brackish water creeks where mud is the flament by the base. Ovary sits on a well-developed accretng (Image 1a). A green snake (unidentfed) uses stalk. It has four carpels which are partally joined and the habitat of this plant in all locatons where the plant each carpel has two reniform ovules (Image 2k–n). All occurs (Image 1b,c). It grows up to two meters in height four carpels are joined by a common style tpped with a without any above ground roots. It is fast growing, simple stgma. much-branched and forms pure stands. The branches are grey, smooth and marked with lines and grooves Floral biology along their length. Leaves are petolate, lanceolate to Mature buds are globose and open during 09.00– elliptc-lanceolate and leathery with a rounded base and 11.00 h with peak opening at 10.00h (Image 2a–g). The a pointed tp; the upper surface is glossy and smooth stamens show anther dehiscence by longitudinal slits while the lower surface is grey-green and covered with during anthesis. In mature buds, the stgma is below the a dense layer of tny, hairy scales. Leaf fall occurs during height of stamens but stands straight and erect beyond late April to late May, leaf fushing during June–July and the height of the anthers during anthesis. The stgma fowering during late July to second week of September remains so for 6 hours and gradually curves towards at populaton level. Individual plants fower for about the anthers of the same fower and eventually contacts four weeks only. Inforescence is terminal and axillary; its own pollen. It atains receptvity three hours afer it is a paniculate cyme with several fowers which open anthesis and remains so for fve hours. The pollen over a period of about a week. (Image 1e,f). Cauliforous grains are oblate-spheroidal, yellow, 3-colporate, sexine fowers are also borne on main stems and woody trunks. thinner than nexine and 27–29 μm in size (Image 2h–j). They are initally stcky but later turn powdery with a Flower morphology gradual increase in temperature and fall as single grains. Flowers are pedicellate, 5–7 mm long, 5-6 mm wide, Individual anthers produce 890.6 ± 52.83 pollen grains creamy-brown coloured, mildly odoriferous, bisexual and and the total pollen output by a fower depends on the actnomorphic. Calyx is bell-shaped, 5-sepalled, connate number of stamens produced. The stgma terminates

Image 1. Brownlowia tersa: a - Habitat | b&c - Habitat for Green Snake | d - Thyreus histrio restng on the stem | e - Twig with early stage of inforescence | f - Inforescence with maturing buds. © A.J. Solomon Raju.

14122 Journal of Threatened Taxa | www.threatenedtaxa.org | 26 July 2019 | 11(9): 14119–14127 Pollinaton ecology of Brownlowia tersa Raju

its receptvity by the end of the day. Nectar is produced Table 1. Results of breeding systems in Brownlowia tersa. in minute volumes around the base of the carpels and is No. of No. of protected by the basally connate calyx; it amounted 1.2 fowers fruits Fruit set Pollinaton mode pollinated formed (%) ± 0.23 µl per fower and the sugar concentraton stood Autogamy (unmanipulated) 50 7 14 at 28 ± 1.5%. The fowers fall of by noon of the second Autogamy (manipulated) 50 17 34 day. Geitonogamy 50 25 50 Breeding systems Xenogamy 50 36 72 Hand-pollinaton tests showed that the plant Open-pollinaton 125 43 34 produces fruit through self and cross-pollinaton. Fruit set rate varied from 14–34 % in unmanipulated and manipulated autogamy, 50% in geitonogamy, 72% in bees of the hive nearby in the same forest. In other bee xenogamy and 34% in open-pollinaton. These results species, both male and female bees visited the fowers. indicate that fruit set is the highest in xenogamy and The male carpenter bee foraged for only nectar while lowest in unmanipulated autogamy among hand- female bee foraged for both pollen and nectar. The male pollinaton tests. Fruit set evidenced in open-pollinaton carpenter bee collected nectar for its own consumpton is taken as the product of auto-, geitono- and xeno-gamy while female carpenter bee used the nectar collected (Table 1). by it for its own consumpton and also mixed it with pollen to make bee bread to feed the larvae. The Flower visitors and pollinaton female carpenter bee collected pollen and packed it as The fowers were foraged exclusively by bees during honey bees did but they packed it into the weak scopa 09.00–17.00 h with peak actvity during 10.00–13.00 surrounded by sparse body hairs located on the tbia of h coinciding well with the availability of more fresh hind legs. The male and female cuckoo bees foraged fowers (Fig. 1). The bees belong to Apidae family and for only nectar for their own consumpton. The foral included honey bees (Apis cerana F. and A. forea F.), a architecture facilitated the bees to probe for the forage small carpenter bee (Ceratna binghami Cockerell) and with great ease and during probing they contacted the a cuckoo bee (Thyreus histrio F.; Image 1d). In honey stgma and stamens efectng pollinaton. Worker honey bees, only worker bees visited the fowers and foraged bees and the female carpenter bees tended to spend for both pollen and nectar. Worker bees collected more tme at each fower, plant and patch as they were pollen, groomed and brushed it down towards the involved in collectng both pollen and nectar while male hind legs and packed the pollen into the corbiculae or carpenter bees and both sexes of cuckoo bee tended to pollen baskets which are located on the tbia of the same spend less tme at each fower, plant and patch as they legs. They used nectar collected by them for their own were involved in collectng only nectar. All four bee consumpton and also for feeding the queen and male species made inter-plant and inter-patch fower visits in

45 45 4045 Apis cerana 40 Apis cerana 4035 Apis floreacerana 35 Apis florea 35 CeratinaApis florea binghami 30 Ceratina binghami 30 ThyreusCeratina histrio binghami 3025 Thyreus histrio 25 Thyreus histrio 2520 20 2015 15

No. of foraging visits of foraging No. 1510

No. of foraging visits of foraging No. 10 No. of foraging visits of foraging No. 105 5 05 0 0 8:00 9:00 10:00 11:00 12:00 13:00 14:00 15:00 16:00 17:00 18:00 8:00 9:00 10:00 11:00 12:00 13:00 14:00 15:00 16:00 17:00 18:00 8:00 9:00 10:00 11:00 12:00 13:00 14:00 15:00 16:00 17:00 18:00 Time (h) Time (h) Figure 1. Hourly foraging actvity of bees on BrownlowiaTime (h) tersa. Figure 1. Hourly foraging activity of bees on Brownlowia tersa Figure 1. Hourly foraging activity of bees on Brownlowia tersa Figure 1. Hourly foraging activity of bees on Brownlowia tersa Journal of Threatened Taxa | www.threatenedtaxa.org | 26 July 2019 | 11(9): 14119–14127 14123 Pollinaton ecology of Brownlowia tersa Raju

Image 2. Brownlowia tersa: a–g - Diferent stages of anthesis | h - Dehisced anthers with yellow powdery pollen | i&j - Pollen grains | k&l - Ovary, style and stgma | m - Simple stgma | n - Ovules | o - Fruitng | p - Cauliforous fruits | q - Seed germinaton | r - Seedling | s - New plant. © A.J. Solomon Raju.

Table 2. Pollen recorded in the body washings of insect foragers on 26.5 Brownlowia tersa. 26 Sample Insect species Range Mean S.D. 25.5 size (N) 25 Apis cerana 10 54–208 115.4 50.08 24.5 Apis forea 10 93–156 99.1 19.44 24 Ceratna smaragdina 10 95–129 98.1 12.23 23.5

Thyreus histrio 10 67–304 162.3 75.49 23 Apis cerana Apis florea Ceratina binghami Thyreus histrio

FigureFigure 2. Relatve 2. Percentage percentage of foraging of visits foraging of bees visits on Brownlowia of bees on tersa Brownlowia tersa. quest of more forage and in the process they efected both self- and cross-pollinatons. Among all four bee species, T. histrio made 26%, A. forea and C. binghami, Fruitng ecology and seed dispersal each 25% and A. cerana 24% of total visits recorded at In fertlized fowers, calyx remains for about a the fowering patch (Fig. 2). The pollen recorded in body week without any further development and falls of washings of sampled specimens of bees indicated that all subsequently. A single carpel produces fruit in fertlized of them carry and transfer pollen to other fowers either fowers. Fruits mature in about four weeks; remain in the same or diferent patches. The average number greyish-green from fruit initaton and untl dispersed of pollen grains recorded was 115.4 for A. cerana, 99.1 (Image 2o,p). Individual fruit is a woody, fbrous heart- for A. forea, 98.1 for C. binghami and 162.3 for T. histrio shaped follicle, 12–15 mm long and bi-lobed with a (Table 2). single seed. It is indehiscent while on the plant, falls of when due, foats due to its fbrous husk of fruit carpel, imbibiton of water by it; this foatng state of fruits

14124 Journal of Threatened Taxa | www.threatenedtaxa.org | 26 July 2019 | 11(9): 14119–14127 Pollinaton ecology of Brownlowia tersa Raju facilitated their dispersal by tdal water. When it setles stgma above the anthers facilitate the occurrence of on the muddy substratum and upon imbibiton, it breaks only geitonogamy and xenogamy for a brief period; in open exposing the seed but fruit carpel remains intact additon, vector-mediated autogamy also occurs upon untl seed germinaton. With initaton of root growth the commencement of stgma receptvity. Finally, the and development, the cotyledons shed the fruit carpel fowers resort to autonomous autogamy by gradually and show contnued growth to form seedlings and curving the style and stgma towards the anthers; this subsequently new plants (Image 2q–s). pollinaton mode is a “fail-safe” strategy evolved by the plant to ensure pollinaton in fowers that have not been pollinated by pollinator bees. Its occurrence, however, DISCUSSION is subject to the availability of pollen in the anthers of the same fower. Ruan et al. (2010) reported on style Brownlowia tersa is a shrubby, spreading plant curvature and its role in efectng self-pollinaton in 52 and forms patchy distributon along the tdal creeks species of Malvaceae. These authors classifed the studied connectng the landward zone at the study area. An species into two types: species with style curvature unidentfed green snake has been found to use this before pollen shedding, and species with style curvature gregarious shrub at all locatons of its occurrence for its afer pollen shedding. In the former type, the styles shelter but why it uses the habitat of this partcular plant remain erect if stgmas are pollinated or cease to curve is unknown. In B. tersa, fowering and fruitng seasons if pollinaton occurs in the process of style curvature or are variously reported by diferent authors. Kathiresan contnue to curve downwards towards the anthers if not (2010) noted that it fowers and fruits during July– pollinated. In the later type, the styles curve eventually October but he has not mentoned the locaton where it bringing stgmas down to establish contact with the was recorded. Ragavan et al. (2016) noted that it fowers anthers. The style curvature and eventual occurrence during February–March and fruits during April–July in of self-pollinaton in B. tersa represents the second type, India and Andaman & Nicobar Islands. The present study sensu Ruan et al. (2010). Therefore, B. tersa is a perfect made at CMF India showed that all phenological events hermaphroditc species with facultatve xenogamous occur sequentally—leaf fall, leaf fushing, fowering, matng system. and fruitng—from April to November. Flowering starts Ruan (2010) stated that anemophily is unlikely in in late July and contnues for about seven weeks while Malvaceae because the pollen grains are stcky. Spira fruitng during October–November at populaton level, (1989) reported that H. moscheutos with stcky pollen however, individual plants fower for less than a month. grains is not anemophilous and a vector other than wind The fowers are borne in terminal and axillary paniculate is needed for successful pollinaton. The present study cymes as well as on main stems and woody trunks shows that B. tersa pollen is also stcky and in efect, indicatng that the plant with shrubby habit perhaps the bees foraging on the fowers collect pollen slowly evolved to compensate the brief period of fowering indicatng that the plant is not anemophilous. Further, by producing cauliforous fowers in order to atract the stcky nature of the pollen enables the plant to pollinators and maximize fruit set at plant level. avoid anemophily during non-receptve phase of the Diferent authors provided taxonomic characters stgma to maximize cross-pollinaton and minimize self- of B. tersa but certain characters have been incorrectly pollinaton. Feng (1984) and Rachcke (2000) reported reported. Judd & Manchester (1997) reported that that many species of Malvaceae are entomophilous and Brownlowia fowers have fve elongate antpetalous pollinated by bees, buterfies, hawk moths and birds. staminodia while Chung & Soepadmo (2017) noted Faegri & van der Pijl (1979) and Proctor et al. (1996) that B. tersa fowers have lanceolate staminodes and reported that bee-pollinated fowers vary in their size, persistent androgynophore. The present study showed shape and colouraton; they may be open and bowl- that B. tersa lacks staminodia and androgynophore but it shaped (radially symmetrical) or more complex and has gynophore on which the ovary is well seated. Further, non-radially symmetric (zygomorphic), and ofer nectar the stamens are bundled, anthers petaloid which dehisce and pollen as rewards. The present study reports that by longitudinal slits, and the carpels with reniform ovules B. tersa displays a radially symmetrial fower shape, are partally joined by a common style terminated with dull-coloured corolla, mildly odoriferous and also ofers a simple stgma. The foral details of B. tersa clearly nectar and pollen as rewards to pollinators; in line with indicate that the plant is morphologically and functonally this, the plant is pollinated exclusively by bees and hermaphroditc. Protandry and the erect positon of the hence it is melitophilous. Among bees, Apis spp. carry

Journal of Threatened Taxa | www.threatenedtaxa.org | 26 July 2019 | 11(9): 14119–14127 14125 Pollinaton ecology of Brownlowia tersa Raju pollen in pollen baskets located on their hind legs for situated towards landward zone, the fallen fruits do not use subsequently by their colony while female bees of disperse longer distances and soon they setle in muddy C. binghami carry pollen in the scopae located on their substratum. Gradually, the seed inside the fruit imbibes hind legs for brood provisioning. The pollen collecton water and breaks the fruit open exposing the seed which actvity by these bees signifcantly decreases pollen soon germinates and produces a seedling and then a new availability for pollinaton purpose although pollinaton plant. The fruit pericarp, however, remains enclosing is efected by them, and also it mostly undermines the the cotyledons untl the initaton of root formaton by occurrence of autonomous autogamy towards the end of the seedling. Similar process of fruit foatng and seed the day. The producton of many fowers in paniculate germinaton is reported in B. peltata by Rachmadiyanto cymes, on main stem and woody trunk daily, individual et al. (2017). fowers with several stamens and each stamen producing Gopal & Chauhan (2006) noted that B. tersa copious pollen appear to enable the plant to compensate populatons are experiencing severe loss at the range the pollen loss caused by Apis and C. binghami bees, margins due to human actvites and coastal development however. Male bees of C. binghami and both sexes of T. and hence has become an endangered species in India histrio act exclusively as nectar feeders and play principal while Kathiresan (2010) mentoned that B. tersa is Near role in the pollinaton of B. tersa. Further, T. histrio is a Threatened. Field studies conducted in this mangrove swif fier, collects nectar from as many fowers as it could forest area for the last 12 years for the reproductve in a single visit and hence is very important in efectng ecology informaton on diferent mangrove plant species cross-pollinaton. Apis bees build their colonies on the showed a gradual decrease in the populaton size of B. peripheral branches of Excoecaria agallocha while C. tersa due to deforestaton and modifcaton for fuel wood binghami has its nests in the stems of Acanthus ilicifolius; collecton, catle shelter and eco-tourism actvites. This these plant species occur 5–10 m away from B. tersa. situaton is to be corrected otherwise this species would T. histrio does not have its own nest but it uses the face the risk of genetc erosion and become extrpated in underground nests of Amegilla sp. which occur nearby the course of tme. Therefore, immediate and efectve on the landward side of the mangrove forests. Since in situ conservaton measures are necessary for its the nests of all these bee species occur near B. tersa, protecton and propagaton. they display a situaton of foral constancy and efect pollinaton due to massive fower producton by the plant during the fowering season. CONCLUSIONS In the present study, hand-pollinaton tests on B. tersa indicated that the plant is self-compatble and Brownlowia tersa is a low-ground semi-evergreen fruits through all modes of pollinaton with varying shrubby species. It displays phenological events levels of reproductve success, however, fruit set rate sequentally—leaf fall, leaf fushing, fowering, and in open-pollinatons is not commensurate compared fruitng—from April–November. It is hermaphroditc, with the ability of the plant to fruit through autogamy protandrous, self-compatble, facultatve xenogamous with or without involvement of pollinators and through and melitophilous. It has the ability to fruit with or geitonogamy and xenogamy with the involvement without pollinator actvity but fruit set rate is the highest of pollinators. Further, the fowers characteristcally with pollinator actvity. Pollinators are exclusively bees produce 1-seeded fruits only from a single carpel consistng of honey bees, small carpenter bees, and indicatng that only one out of four carpels forms fruit and cuckoo bees of which the last one is very important for only one of 2-ovules of the carpel forms seeds. The fruits cross-pollinaton due to their swif fying behavior and are indehiscent and foat in tdal water upon detachment ability to collect nectar from many fowers of diferent from the plant. Diferent authors noted that Brownlowia plants. Fruit is a 1-seeded follicle and produced from a species are ofen dispersed by water indicatng that they single carpel of the fower. It is indehiscent and foats in foat in tdal water (Kostermans 1965; Turner 1995; Bayer tdal water when detached from the plant. When setled & Kubitzki 2003). Similarly, Rachmadiyanto et al. (2017) in muddy substratum, it breaks open to expose the seed reported that B. peltata also produces 1-seeded fruits which germinates and produces a new plant. The study from a single carpel but the fruits dehisce into carpels to reports that the plant is highly threatened due to land expose the seeds; the fruits foat and disperse by water. use changes and regular human and catle actvity, and The fruits of B. tersa foat because fruit pericarp is fbrous hence immediate in situ conservaton measures are and imbibe water. Since the locatons of the plant are required for its protecton and propagaton.

14126 Journal of Threatened Taxa | www.threatenedtaxa.org | 26 July 2019 | 11(9): 14119–14127 Pollinaton ecology of Brownlowia tersa Raju

REFERENCES Kathiresan, K. & B.L. Bingham (2001). Biology of mangroves and mangrove ecosystems. Advances in Marine Biology 40: 81–251. Anonymous (2008). Mangroves for the future: natonal strategy and htps://doi.org/10.1016/S0065-2881(01)40003-4 acton plan, India. Ministry of Environment and Forest, Government Kathiresan, K. & N. Rajendran (2005). Mangrove ecosystems of the of India, 63pp. Indian Ocean region. Indian Journal of Marine Sciences 34: 104– Bayer, C. & K. Kubitzki (2003). Malvaceae, pp225–311, In: Kubitzki, 113. K. & C. Bayer (eds.). The Families and Genera of Vascular Plants Kostermans, A.J.G.H. (1965). Miscellaneous botanical notes 5. Bulletn Volume V, Flowering Plants Dicotyledons Capparales, Malvales and of Botanical Survey of India 7: 128–131. Non-betalain Caryophyllales. Springer, Berlin, I–IX+418pp. htps:// Mandal, R.N. & K.R. Naskar (2008). Diversity and classifcaton of doi.org/10.1007/978-3-662-07255-4_28 Indian mangroves: a review. Tropical Ecology 49: 131–146. Bhat, J.R., J.D. Macintosh, T.S. Nayar, C.N. Pandey & B.P. Nilratna Polidoro, B.A., K.E. Carpenter, L. Collins, N.C. Duke & A.M. Ellison (Eds.) (2011). Towards conservaton and Management of Mangrove (2010). The loss of species: mangrove extncton risk and geographic ecosystems in India. Ministry of Environment and Forest, New Delhi, areas of global concern. PLoS ONE 5: e10095. htps://doi. 278pp. org/10.1371/journal.pone.0010095 Burret, M. (1926). Beietrage zur Kenntnis der Tiliaceen. Notzblat des Proctor, M., P. Yeo & A. Lack (1996). The Natural History of Pollinaton. Botanischen Gartens und Museums zu Berlin-Dahlem 9: 592–880. Timber Press, Portland, 487pp. Chung, R.C.K. & E. Soepadmo (2017). Brownlowia latfana (Malvaceae- Rachcke, B.J. (2000). Birds, pollinaton reliability and green fowers Brownlowioideae), a new species from Terengganu, Pensinsular in an endemic island shrub, Pavonia bahamensis (Malvaceae). Malaysia. Phytotaxa 298: 134–146. htps://doi.org/10.11646/ Rhodora 102: 292–414. phytotaxa.298.2.3 Rachmadiyanto, A.N., Peniwidiyant & P.W.K. Hutabarat (2017). Fruit Dafni, A., P.G. Kevan & B.C. Husband (2005). Practcal Pollinaton descripton and evaluaton of fve treatment to break seed dormancy Biology. Enviroquest Ltd., Ontario, 583pp. of Brownlowia peltata Benth, pp46–53. In: ICBS Conference Debnath, H.S. (2004). Mangroves of Andaman and Nicobar Islands: Proceedings, Internatonal Conference on Biological Science, 2015, Taxonomy and Ecology. A Community Profle. Bishen Singh KnE Life Sciences, Dubai. htps://doi.org/10.18502/kls.v3i4.686 Mahendra Pal Singh. Dehradun, 133pp. Ragavan, P., A. Saxena, P.M. Mohan, R.S.C. Jayaraj & K. Ravichandran Duke, N.C. (1992). Mangrove foristcs and biogeography, pp63– (2016). The rediscovery of Brownlowia tersa (L.) Kosterm. 100. In: Robertson, A.I. & D.M. Alongi (eds.). Tropical Mangrove (Malvaceae), from the Andaman Islands, India - a Near Threatened Ecosystems - Vol. 41. American Geophysical Union, Washington DC, mangrove species. Check List 12: 1–5. 329pp. htps://doi.org/10.1029/CE041 Ridley, H.N. (1922). The Flora of the Malay Peninsula, Volume I, Faegri, K & L. van der Pijl (1979). The Principles of Pollinaton Ecology. Polypetaleae. L. Reeve & Co., Ashford, Kent, 918pp. htps//doi. Pergamon Press, New York, 244pp. org/10.5962/bhl.ttle.10921 Feng, K.M. (1984). Flora. Science Press, Beijing. 49: 1–238. Ruan, C-J. (2010). Review and advances in style curvature for the Giesen, W., S. Wulfraat, M. Zieren & L. Scholten (2007). Mangrove Malvaceae. Internatonal Journal of Plant Developmental Biology 4: Guide Book for Southeast Asia. FAO and Wetlands Internatonal, 98–111. Dharmasarn Co., Ltd., Bangkok, 781pp. Sahni, K.C. (1958). Mangrove forests in the Andaman and Nicobar Gopal, B. & M. Chauhan (2006). Biodiversity and its conservaton in Islands. Indian Forester 84: 554–562. the Sundarban mangrove ecosystem. Aquatc Science 68(3): 338– Spira, T.P. (1989). Reproductve biology of Hibiscus moscheutos 354. htps://doi.org/10.1007/s00027-006-0868-8 (Malvaceae), pp247–255. In: Bock, J.H. & Y.B. Linhart (eds.) The Hossain, H., I.A. Jahan, S.I. Howlader, J.H. Shilpi, S.K. Dey & A. Hira Evolutonary Ecology of Plants. Westview Press, Boulder, Colorado, (2013). Ant-infammatory and antoxidant actvites of ethanolic 614pp. leaf extract of Brownlowia tersa (L.) Kosterm. Oriental Pharmacy Tang, Y., M.G. Gilbert & L.J. Dorr (2007). Flora of China. Vol. 2. Science and Experimental Medicine 13: 181–189. Press & Missouri Botanical Gardens Press, Beijing, 264–298pp. Hutchinson, J. (1967). The Genera of Flowering Plants (Angiospermae). Tomlinson, P.B. (1986). The Botany of Mangroves. Cambridge Clarendon Press, Oxford, 660pp. University Press, New York, 413pp. Judd, W.S. & S.R. Manchester (1997). Circumscripton of Malvaceae Turner, M. (1995). A catalogue of the vascular plants of Malaya. (Malvales) as determined by a preliminary cladistcs analysis of Gardens’ Bulletn Singapore 47: 1–757. morphological, anatomical, palynological, and chemical characters. Venu, P.W., Arisdasan, C.R. Magesh & T. Sathyamurthy (2006). Britonia 49: 384–405. htps://doi.org/10.2307/2807839 Brownlowia tersa (L.) Kosterm. (Tiliaceae) in India. Rheedea 16: Kathiresan, K. (2010). Globally threatened mangrove species in India. 111–114. Current Science 98: 1551.

Threatened Taxa

Journal of Threatened Taxa | www.threatenedtaxa.org | 26 July 2019 | 11(9): 14119–14127 14127 PLATINUM The Journal of Threatened Taxa (JoTT) is dedicated to building evidence for conservaton globally by publishing peer-reviewed artcles online every month at a reasonably rapid rate at www.threatenedtaxa.org. OPEN ACCESS All artcles published in JoTT are registered under Creatve Commons Atributon 4.0 Internatonal License unless otherwise mentoned. JoTT allows allows unrestricted use, reproducton, and distributon of artcles in any medium by providing adequate credit to the author(s) and the source of publicaton.

ISSN 0974-7907 (Online) | ISSN 0974-7893 (Print)

July 2019 | Vol. 11 | No. 9 | Pages: 14087–14246 Date of Publicaton: 26 July 2019 (Online & Print) www.threatenedtaxa.org DOI: 10.11609/jot.2019.11.9.14087-14246

Artcle Short Communicatons

Species richness and abundance of monogonont rotfers in relaton to An updated checklist of Indian western Himalayan gymnosperms and environmental factors in the UNESCO Sakaerat Biosphere Reserve, Thailand lectotypifcaton of three names – Nataporn Plangklang, Chaichat Boonyanusith & Sujeephon Athibai, – Jibankumar Singh Khuraijam & Jaideep Mazumdar, Pp. 14204–14211 Pp. 14087–14100 New record of Blue Perch Badis badis (Anabantformes: Badidae) from Communicatons Godavari River basin of Telangana State, India – Kante Krishna Prasad & Chelmala Srinivasulu, Pp. 14212–14215 Distributon and habitats of Paphiopedilum Pftzer (Orchidaceae) known to occur in Bhutan First record of the Small Bamboo Bat Tylonycteris fulvida (Peters, 1872) – Dhan Bahadur Gurung, Nima Gyeltshen, Kezang Tobgay, Stg Dalström, (Mammalia: Chiroptera: Vespertlionidae) from Nepal Jangchu Wangdi, Bhakta Bahadur Ghalley, Lekey Chaida, Phuntsho, Ngawang – Basant Sharma, Anoj Subedi, Bandana Subedi, Shristee Panthee & Gyeltshen, Kelzang Dawa, Tandin Wangchuk, Rebecca Pradhan, Thomas Hoijer & Pushpa Raj Acharya, Pp. 14216–14219 Choki Gyeltshen, Pp. 14101–14111 Is canine distemper virus (CDV) a lurking threat to large carnivores? A case Diurnal Serianthes nelsonii Merr. leafet paraheliotropism reduces leafet study from Ranthambhore landscape in Rajasthan, India temperature, relieves photoinhibiton, and alters nyctnastc behavior – Nadisha Sidhu, Jimmy Borah, Sunny Shah, Nidhi Rajput & Kajal Kumar Jadav, – Thomas Edward Marler, Pp. 14112–14118 Pp. 14220–14223

Pollinaton ecology of Brownlowia tersa (Malvaceae), a Near Threatened Notes non-viviparous true mangrove shrub – Aluri Jacob Solomon Raju, Pp. 14119–14127 Extended distributon of the vulnerable Cooper’s Stone Flower Corallodiscus cooperi (Gesneriaceae) in India A note on the taxonomy and natural history of the Summer Clicker – Vikas Kumar, Samiran Panday, Sudhansu Sekhar Dash, Bipin Kumar Sinha & Lahugada dohertyi (Distant, 1891) (Insecta: Hemiptera: Cicadidae) along with Paramjit Singh, Pp. 14224–14227 its distributon in northern West Bengal, India – Vivek Sarkar, Pp. 14128–14136 Extended distributon record of two bellfower species of Codonopsis (Campanulaceae) from the Indian state of Arunachal Pradesh Observatons on nestng actvity, life cycle, and brood ball morphometry of – Khilendra Singh Kanwal, Umeshkumar Lalchand Tiwari, Lod Yama & the Bordered Dung Beetle Onitcellus cinctus (Fabricius, 1775) (Coleoptera: Mahendra Singh Lodhi, Pp. 14228–14231 Scarabaeidae) under laboratory conditons – Amar Paul Singh, Kritsh De, Shagun Mahajan, Ritwik Mondal & First record of the Blue-and-white Flycatcher Cyanoptla cyanomelana Virendra Prasad Uniyal, Pp. 14137–14143 (Temminck, 1829) (Aves: Passeriformes: Muscicapidae) from Bhutan – Kado Rinchen, Kinley Kinley, Chhimi Dorji & Dorji Wangmo, Pp. 14232– Spiders of Odisha: a preliminary checklist 14234 – Sudhir Ranjan Choudhury, Manju Siliwal & Sanjay Keshari Das, Pp. 14144– 14157 Buterfies collected using malaise traps as useful bycatches for ecology and conservaton Status of water birds in Haripura-Baur Reservoir, western Terai-Arc landscape, – Augusto Henrique Batsta Rosa, Lucas Neves Perillo, Frederico Siqueira Utarakhand, India Neves, Danilo Bandini Ribeiro & André Victor Lucci Freitas, Pp. 14235–14237 – Tanveer Ahmed, Harendra Singh Bargali, Deepa Bisht, Gajendra Singh Mehra & Affullah Khan, Pp. 14158–14165 Notes on the hairstreak buterfies Euaspa Moore, 1884 (Lepidoptera: Lycaenidae) with new distributon records to the Indian eastern Himalaya Bird diversity in the coastal talukas of Sindhudurg District, Maharashtra, India – Gaurab Nandi Das, Subrata Gayen, Motoki Saito & Kailash Chandra, – Golusu Babu Rao, Santhanakrishnan Babu, Goldin Quadros & Pp. 14238–14241 Vijaykumar Anoop, Pp. 14166–14186 First report of the Australian gall midge Actlasioptera tumidifolium Greater One-horned Rhinoceros Rhinoceros unicornis (Mammalia: Gagné, 1999 (Diptera: Cecidomyiidae) from Andaman Islands, India Perissodactyla: Rhinocerotdae) populaton census in the Rajiv Gandhi Orang – Duraikannu Vasanthakumar & Radheshyam Murlidhar Sharma, Pp. 14242– Natonal Park, Assam, India 14243 – Deba Kumar Duta & Parikshit Kakat, Pp. 14187–14193 New record of Blanford’s Fox Vulpes cana (Mammalia: Carnivora: Canidae) in Crowding, group size and populaton structure of the Blackbuck central Oman: a connecton between the northern and southern populatons Antlope cervicapra (Linnaeus, 1758) (Mammalia: Cetartodactyla: Bovidae) – Taimur Alsaid, Abdulrahman Aluwaisi, Sultan Albalushi, Zahran in the semi-arid habitat of Haryana, India Alabdulsalam, Said Alharsusi & Steven Ross, Pp. 14244–14246 – Deepak Rai & Jyot, Pp. 14194–14203 Publisher & Host

Partner Member

Threatened Taxa