Pollination Ecology of Clerodendrum Inerme (L.) Gaertn

Journal of Threatened Taxa | www.threatenedtaxa.org | 26 May 2016 | 8(5): 8777–8787

Pollination ecology of Clerodendrum inerme (L.) Gaertn.

(Lamiaceae) in Coringa mangrove ecosystem, Andhra Pradesh, Communication

India ISSN 0974-7907 (Online) ISSN 0974-7893 (Print) A.J. Solomon Raju 1 & Rajendra Kumar 2 OPEN ACCESS 1 Department of Environmental Sciences, Andhra University, Visakhapatnam, Andhra Pradesh 530003, India 2 Ministry of Environment, Forest and Climate Change, Indira Paryavaran Bhavan, Jor bagh Road, New Delhi 110003, India 1 [email protected] (corresponding author), 2 [email protected]

Abstract: Clerodendrum inerme (L.) Gaertn. (Lamiaceae) is bisexual, self-compatible and has a vector-dependent mixed breeding system. They are dichogamous and herkogamous; the day 1 flowers are staminate while the day 2 and 3 flowers are pistillate. The plant blooms in the evening, possesses a white long corolla with a hairy interior to exclude other insects and strong fragrance are adaptations for pollination by the hawk-mothMacroglossum gyrans. The 2nd and 3rd day flowers are nectar-rich and attract hawk-moths during the dawn and dusk hours. The plant is also visited by bees and butterflies. The bees Xylocopa and Anthophora are primary nectar robbers which collect nectar without effecting pollination. C.In inerme, three forms of flowers can be distinguished based on the position of sex organs. The first form is characterized by elongated stamens and a style which occur in close proximity to each other just after anthesis facilitating contact between the stamens and stigma. The second form is characterized by the scattered position of stamens and style. In the third form, the stamens are fully extended while the style is curved away from them, either to the left or to the right; subsequently the stamens curl inward and the style elongates. Interestingly, the three flower forms can be found within a cyme also. These forms of flowers with strong protandry prevent autonomous selfing but not geitonogamy. The fruit is a capsule and breaks open to disperse nutlets. Birds such as Acridotheres tristis, Corvus splendens, Corvus macrorhynchos and Turdoides caudatus disperse nutlets during the early winter season. Seeds germinate in June and seedlings grow gradually to produce new plants.

Keywords: Clerodendrum inerme, hawk-moth pollination, mixed breeding system, nectar robbery, protandry.

DOI: http://dx.doi.org/10.11609/jott.2276.8.5.8777-8787

Editor: V. Sampath Kumar, Botanical Survey of India, Howrah, India. Date of publication: 26 May 2016 (online & print)

Manuscript details: Ms # 2276 | Received 05 September 2015 | Final received 15 April 2016 | Finally accepted 09 May 2016

Citation: Raju, A.J.S. & R. Kumar (2016). Pollination ecology of Clerodendrum inerme (L.) Gaertn. (Lamiaceae) in Coringa mangrove ecosystem, Andhra Pradesh, India. Journal of Threatened Taxa 8(5): 8777–8787; http://dx.doi.org/10.11609/jott.2276.8.5.8777-8787

Copyright: © Raju & Kumar 2016. Creative Commons Attribution 4.0 International License. JoTT allows unrestricted use of this article in any medium, reproduction and distribution by providing adequate credit to the authors and the source of publication.

Funding: Self-funded.

Conflict of Interest:The authors declare no competing interests.

Author Details: Prof. A.J. Solomon Raju is the Chairman, Board of Studies in the Department of Environmental Sciences, Andhra University, Visakhapatnam. He is the recipient of several national and international awards. He is on the editorial board of several international journals. Mr. Rajendra Kumar is currently working as Research Officer in the Ministry of Environment, Forest and Climate Change, Government of India, New Delhi.

Author Contribution:Both the authors contributed to a similar extent overall.

Acknowledgements: We thank the Andhra University, Visakhapatnam for providing us facilities to carry out this work.

8777 Pollination ecology ofClerodendrum inerme Raju & Kumar

INTRODUCTION Sakamoto et al. (2012) reported that C. trichotomum is protandrous and shows two distinct sexual phases. The The genus Clerodendrum comprises about 500 staminate phase begins when the flower opens, and species of small trees, shrubs, lianas, or occasionally this is followed by the pistillate phase. It is effectively perennial herbs. It is found in tropical and warm pollinated by Papilio and Xylocopa species while the temperate regions of the world, with most of the hawk-moth, Macroglossum is not an effective pollinator species in tropical Africa and southern Asia, but with a but may contribute to self-pollination. Primack et al. few in the tropical Americas and northern Australasia, (1981) reported that C. inerme is strongly protandrous and a few extending north into the temperate zone and visited by the hawk-moth during the dusk hours; in eastern Asia (Mabberley 2008). The members of there were no daytime visitors. With this backdrop, the the genus Clerodendrum are widely used in various present study was contemplated to provide the details of indigenous systems of medicine for the treatment of pollination ecology of C. inerme, a prominent landward diseases such as syphilis, typhoid, cancer, jaundice and shrub in the Coringa Mangrove Ecosystem in Andhra hypertension. Different workers have studied a few Pradesh, India. This information is useful to understand species of Clerodendrum for their pollination aspects. the importance of local insects in pollination ecology Keng (1990) reported that C. laevifolium is pollinated and birds in seed dispersal and subsequent recruitment by insects such as bees and butterflies and mentioned within the mangrove cover. that birds feed on its fruits (berries) and in the process may act as fruit or seed dispersal agents for this species. He has also mentioned that this plant species is the MATERIALS AND METHODS larval host for the Fluffy Tit butterfly, Zelthus amasa maximinianus. Reddy & Reddi (1995) reported that C. The Godavari mangrove wetland lies between infortunatum exhibits geitonogamous and xenogamous 16030’–17000’N and 82010’–80023’E in the State of modes of breeding. The Papilionoid butterflies (Papilio Andhra Pradesh, India. In this wetland, C. inerme polytes, P. polymnestor and Atrophaneura hector) grows along the creeks and towards land; it is are the exclusive pollinators and effect pterigotribic distributed sparsely in this mangrove forest. The plant pollination by striking the anthers and stigma with is characteristically deciduous during the dry season, their wings. Meerabai (2014) also reported that in C. displays seed germination, leaf flushing, flowering, infortunatum, the flowers are adapted for pollination fruiting and seed dispersal during the wet season. Field exclusively by butterflies due to non-promiscuity studies and lab-work were made during the period from of floral rewards to other foragers. This pollination February 2011 to June 2014. syndrome is a necessary pre-condition for the rise of The protocols mentioned in Raju & Rajesh (2014) the floral isolating mechanism. Shamim et al. (2010) were followed to examine the flowering season, floral reported that C. viscosum is exclusively cross-pollinated morphological characters, sexual system, anthesis by ants, butterflies and hawk-moths. It does not set fruit schedule, anther dehiscence timing, pollen output, through self-pollination and they experimentally proved pollen-ovule ratio, nectar aspects such as volume, sugar by bagging the flowers. Rohitash & Jain (2010) noted concentration, sugar types, sugar content, amino acids, that C. splendens is pollinated by Xylocopa, Eumenes stigma receptivity, breeding systems, fruiting aspects sp. and Camponotous campestris. The plant produces such as natural fruit set rate, fruit maturation period, fruit and seed set through geitonogamy and xenogamy dehiscence and seed dispersal, insect foragers, their only. McMullen (2011) reported that C. molle produces foraging behavior and pollen carrying efficiency. fruit via open-pollination, autonomous autogamy, facilitated autogamy, facilitated cross-pollination, diurnal pollination and nocturnal pollination. He also RESULTS noted that cross-pollinated flowers showed a significant increase in seed set and is pollinated by nocturnal and A shrub, grows up to 2m (Image 1). It sheds leaves diurnal visitors. Nocturnal visitors include ants, spiders, continually but leaf shedding is prominent during the hawk-moth s, and roaches whereas diurnal visitors dry season and exhibits profuse leaf flushing during include carpenter bees and ants. Mcmullen also stated the rainy season. The flowering occurs from August to that other studied species of Clerodendrum are fully October, profusely during September (Image 2a). The protandrous and incapable of autonomous autogamy. inflorescence is characteristically a 3-flowered cyme

8778 Journal of Threatened Taxa | www.threatenedtaxa.org | 26 May 2016 | 8(5): 8777–8787 Poffinaion ecofogy of Cferodendrum inerme Raju & K umar

© A.J. Sofomon Raju 12: 1. There is a greaf variaion in fhe fengfh of sfamens despife fheir common poinf of origin on fhe coroffa fube. In case of fowers wifh four sfamens, fwo fong and fwo shorf or aff sfamens are equaf in fengfh whife in fhe case of fowers wifh ive sfamens, fwo are fong and fhree are shorf. The anfhers have versaife ixaion, dark-cofoured, difhecous and infrorse. The ovary has fwo carpefs buf if is fefra-focufar due fo fhe formaion of a fafse sepfum (Image 4e, f). The ovufes vary in number from 2–4 buf 4-ovufed fowers are common (Image 4g) and are erecf, anafropous and arranged on axife pfacenfaion. The fofaf fengfh of sfyfe is 45mm in Image 1. Cferodendrum inerme - Habif. 1sf day fowers and 56mm in fhe 2 nd and 3 rd day fowers. The incfuded parf of fhe sfyfe fengfh is 30–33 mm whife fhe exserfed parf of fhe sfyfe fengfh is 15–18 mm. In fhe borne in axiffary posiion and aff fhe fhree fowers have case of fhe 2 nd and 3 rd day fowers, fhe exserfed parf of a common base poinf (Image 2b). Individuaf cymes fhe sfyfe fengfh is 25–28 mm. The sfyfe wifh simpfe biid produce aff fhree fowers eifher on fhe same day or sigma and fobes unequaf (Image 4d). wifhin 2–3 days (Image 2c–d). The producion of fowers wifhin cymes is dependenf on fhe devefopmenfaf sfage Fforaf biofogy of individuaf fowers. Usuaffy, fhe cenfraf fower emerges The mafure buds wifh coifed sfamens inside open irsf foffowed by fhe faferaf fowers. The fowers orienf from 15:00–18:00 hr by fhe spfiing of pefaf fobes compfefefy or parffy erecf. (Image 4a). Pefafs expand and refex immediafefy; fhen fhe sfamens, sfyfe and sigma exfend beyond fhe rim of Ffower morphofogy fhe coroffa fube (Image 4b). The pafern of sfamens and The fowers are pediceffafe, farge (35–40 mm), sfyfe posiions is diferenf and is disinguished info fhree fragranf, zygomorphic and bisexuaf. Cafyx is green, forms. In fhe irsf form of fowers, fhe sfamens and sfyfe gamosepafous consising of ive sepafs, cup-shaped, are efongafed and in proximify fo each ofher soon afer 8mm fong, 3–4 mm wide and vafvafe af fhe ip. Coroffa anfhesis which facififafes confacf wifh each ofher (Image is whife, fubufar (30mm fong), 4–5 fobed af fhe ip; each 3a). In fhe second form of fowers, fhe sfamens and sfyfe fobe 10–12 mm fong and 4–5 mm wide, and refexed. are spfayed (Image 3b). In fhe fhird form of fowers, fhe The raio of 4 and 5 coroffa fobes is 1: 21. On fhe inner sfamens are fuffy exfended, buf fhe sfyfe is curved away surface, fhe coroffa fube is covered wifh shorf ine hairs from fhem; fhe sfyfe in some fowers moves away fo fhe up fo fhe poinf of afachmenf of sfaminaf ifamenfs. fef side (Image 3c) whife in some ofhers, fo fhe righf The sfamens are 4 or 5, epipefafous, exserfed, exfend side (Image 3d). Lafer, fhe sfamens curf inward and up fo 30mm from fhe coroffa moufh when fhe fowers sfyfe is fef efongafed. Aff fhese fhree forms occur even irsf open. The incfuded parf of fhe ifamenfs is whife, wifhin fhe cyme and occur afmosf in equaf numbers af whife fhe exserfed parf of fhe ifamenfs is purpfe. The pfanf fevef. The anfhers dehisce one hour afer anfhesis raio of fowers wifh four sfamens and ive sfamens is by fongifudinaf sfifs exposing fhe gofden yeffow poffen.

Image 2. Cferodendrum inerme : a - Ffowering phase; b - Simuffaneous anfhesis of aff fhe fhree fowers of fhe cyme; c - Two fowers afready dropped from fhe cyme; d - Ffowering cymes.

Journaf of Threafened Taxa | www.fhreafenedfaxa.org | 26 May 2016 | 8(5): 8777–8787 8779 Poffinaion ecofogy of Cferodendrum inerme Raju & K umar

Image 3. Cferodendrum inerme : a - Sfamens and sfyfe in cfose proximify fo each ofher; b - Sfamens and sfyfe are spfayed; c - Sfamens are fuffy exfended and fhe sfyfe is orienfed fo fhe fef; d - Sfamens are fuffy exfended and fhe sfyfe is orienfed fo fhe righf.

Aff fhe sfamens (4 or 5) are ferife and produce afmosf Tabfe 1. Resuffs of breeding experimenfs on Cferodendrum inerme fhe same number of poffen grains. The poffen oufpuf Mode of poffinaion No. of fowers No. of fowers Fruif sef per anfher is 796 ± 51.2. The fofaf poffen producivify poffinafed sef fruif (%) in fowers wifh 4 sfamens is 3,184 and in 5-sfamens Aufonomous 30 0 0 is 3,980. The poffen grains are fricofporafe, profafe, aufogamy (bagged) ecfocofpus fong narrow wifh acufe ends, reicufafe- Facififafed aufogamy 25 0 0 (hand-poffinafed and rugufafe wifh spinufes widefy disfribufed and 66.4 ± 1.32 bagged) µm fong and 52.2 ± 0.8 µm wide (Image 4c). The sigma Geifonogamy 30 9 30 wifh forked fobes is nof recepive af and afer anfhesis Xenogamy 30 25 83 buf if is recepive wifh divergenf fobes on fhe 2 nd and Open-poffinaion 70 27 38 3rd day. Necfar is secrefed during posf-anfhesis period. Ifs secreion is graduaf from anfhesis onwards buf ifs vofume is measurabfe on fhe 2 nd and 3 rd day. A fower produces 3.5±1.2 µf of necfar which is secrefed around 38% in open poffinaions (Tabfe 1). fhe ovary and weff profecfed due fo fhe fubufar nafure of fhe coroffa. The necfar sugar concenfraion is 13–21 Foraging acivify and poffinaion % and fhe common sugars incfude sucrose, gfucose The fowers are speciafized and fhe sfamens and and frucfose. The fofaf sugar confenf in fhe necfar of sigma are exposed when fhe pefafs unfofd and refex. a fower is 0.37±0.06 mg (range 0.24–0.46). The necfar The hawk-mofh Macrogfossum gyrans was fhe irsf amino acids incfude fhe esseniaf amino acids such as visifor fo fhe fowers. If began ifs necfar-foraging acivify isofeucine, vafine, fysine, mefhionine and fhreonine, as soon as fhe fowers open during fhe fafe evening and and non-esseniaf amino acids such as afanine, bufyric dusk hours. Again, fhis mofh foraged during fhe dawn acid, gfufamic acid, hydroxyf-profine, serine and asparic hours from 05:00-07:00 h (Fig. 1). If did nof forage af acid. The coroffa fogefher wifh sfamens and sigma faffs ofher imes of fhe day. The bees ( Xyfocopa pubescens of afer fhree days. The cafyx is persisfenf, graduaffy and Anfhophora bicincfa ) and buferfies ( Pareronia bufges and encfoses fhe fruif in case of ferifized fowers. vaferia, Danaus genuia and Barbo cinnara ) foraged The enire fower fogefher wifh pedicef faffs of if if is nof during fhe day ime from 08:00 fo 17:00 h (Fig. 1), buf poffinafed or ferifized. fhe bees showed more acivify from 08:00–12:00 h whife buferfies from 08:00–11:00 h (Tabfe 2, Fig. 2). Breeding sysfems However, fhe overaff foraging acivify of fhese dayime The resuffs of breeding sysfems indicafe fhaf fhe foragers was nof very infense and afso fheir foraging fowers are seff-compaibfe and seff-poffinaing. The visifs were nof very frequenf. Of fhe fofaf foraging fruif sef is absenf in aufonomous and facififafed visifs, fhe hawk-mofh made 39%, buferfies 38% aufogamy, 30% in geifonogamy, 83% in xenogamy and and bees 23% of visifs (Fig. 3). The body washings of

8780 Journaf of Threafened Taxa | www.fhreafenedfaxa.org | 26 May 2016 | 8(5): 8777–8787 Poffinaion ecofogy of Cferodendrum inerme Raju & K umar

Image 4. Cferodendrum inerme : a - Coifed sfamens in bud sfage; b - Uncoifing of sfamens; c - Poffen grain; d - Biid sigma; e & f - Ovary; g - Ovufes; h & i - Anfhophora bicincfa coffecing necfar by puncfuring fhe coroffa fube; j - Anfhophora bicincfa coffecing poffen; k & f - Xyfocopa pubescens coffecing necfar by puncfuring coroffa fube; m - Pareronia vaferia afemping fo coffecf necfar; n - Danaus genuia coffecing necfar; o - Barbo cinnara coffecing necfar.

Figure 1. Hourfy foraging acivify of buferfies and hawkmofh on Cferodendrum inerme fhese foragers coffecfed from fhe fowers reveafed fhe mofh is an eicienf carrier of poffen and afso consisfenf presence of poffen in diferenf numbers depending on foragers wifh greaf infensify af fhe fowers during fhe frequency of foraging visifs, exfenf and cerfainfy of fhe enire period of fowering. The dayime foragers confacf befween fhe sfamens and sigma and fhe wings were nof eicienf carriers of poffen, nof very frequenf and fhe abdomen of fhe foragers (Tabfe 3). The hawk- foragers and afso nof consisfenf ones during fhe enire

Journaf of Threafened Taxa | www.fhreafenedfaxa.org | 26 May 2016 | 8(5): 8777–8787 8781 Pollination ecology ofClerodendrum inerme Raju & Kumar

Table 2. List of insect foragers on Clerodendrum inerme

Order Family Genus Species Common name Forage sought

Hymenoptera Apidae Xylocopa pubescens L. Large Carpenter Bee Pollen + Nectar

Anthophoridae Anthophora bicincta F. Blue Banded Bee Pollen + Nectar

Lepidoptera Pieridae Pareronia valeria Cr. Common Wanderer Nectar

Nymphalidae Danaus genutia Cr. Striped Tiger Nectar

Hesperiidae Borbo cinnara Wallace. Rice Swift Nectar

Sphingidae Macroglossum gyrans Walker Diurnal hawk-moth Nectar

Figure 2. Hourly foraging activity of bees onClerodendrum inerme period of flowering. nectar by making holes through the corolla tube by The hawk-moth is a very swift flier and spins around bypassing the floral sex organs. Xylocopa pubescens the flowers in quick succession collecting nectar from makes a hole at the mid-part of the corolla tube to a number of flowers on the same plant. It also makes collect nectar (Image 4k,l); the exact point where the inter-plant movements frequently for nectar collection hole is being made is mostly at the origin point of the from the fresh as well as 2nd and 3rd day flowers. This epipetalous stamens covered with short hairs. The moth with a 32.5mm long proboscis, is very successful in flower hanged downwards when this bee species with reaching the nectar location at the corolla base. While its heavy body weight landed on the corolla tube. Then, approaching the flower and collecting nectar from the the nectar freely flowed through the grooves present on flowers, it contacts the stamens and stigma of the same the inside of the corolla tube from the flower base to or different flowers with its wings and abdomen always this fixed position of stamens. The short hairs present and this foraging behavior ends up in pollination. The at the fixed point of stamens prevent the flow of nectar just open flowers available during the dusk hours with beyond this point towards the mouth of the corolla little nectar volume driving the moth to make multiple tube. On the contrary, A. bicincta makes a hole through visits to these flowers as well as 2nd and 3rd day flowers the corolla tube at the flower base and robs nectar in which nectar is richly available, on the same and bypassing the floral sex organs (Image 4h,i). The flower different plants. Such a foraging behavior is considered did not hang downwards when this bee species with to increase opportunities for cross-pollination. light body weight landed and this might be the reason Among the bees, Xylocopa pubescens is an exclusive for the bee to move to the corolla base to rob the nectar forager and Anthophora bicincta is both a pollen nectar. The nectar-robbing by these two bee species do and nectar forager. These two bee species robs the not contribute to effecting pollination. However, these

8782 Journal of Threatened Taxa | www.threatenedtaxa.org | 26 May 2016 | 8(5): 8777–8787 Poffinaion ecofogy of Cferodendrum inerme Raju & K umar

Tabfe 3. Poffen recorded in fhe body washings of insecfs on Cferodendrum inerme

Sampfe size Number of poffen grains Insecf species (N) Range Mean S.D Xyfocopa pubescens 10 13–48 30.3 10.70

Anfhophora bicincfa 10 54–126 85.3 22.87

Pareronia vaferia 10 21–56 38.1 11.63

Danaus genuia 10 14–73 35.9 16.12

Barbo cinnara 10 11– 21 13.6 2.4 Figure 3. Foraging visifs of diferenf cafegories of insecfs on Macrogfossum gyrans 10 131–214 179.1 32.5 Cferodendrum inerme

bees wifh vibraing wings in fighf mode confacfed fhe © A.J. Sofomon Raju sfamens and sigma occasionaffy whife approaching fhe fowers. Such individuaf bees capfured poffen on fheir wings and underside of fhe abdomen and fhese coufd efecf poffinaion. Furfher, A. bicincfa afso coffecfs poffen from individuaf anfhers (Image 4j). Among buferfies, fhe foraging visifs of Pareronia vaferia (Image 4m) and Danaus genuia (Image 4n) are refaivefy frequenf when compared fo fhose of Barbo a b cinnara (Image 4o). In P. vaferia , fhe body fengfh is 25.6mm and fhe proboscis fengfh is 29.5mm, whife in Image 5. Cferodendrum inerme : a - Green mafuring fruifs; D. genuia and B. cinnara fhe body fengfh is 23.9mm b - Mafure and dry fruifs abouf fo shed seeds. and 14.1mm wifh proboscis fengfh of 12.2mm and 17.5mm respecivefy. In P. vaferia and D. genuia , fheir body fengfh facififafes fhem fo have confacf produce mafure fruifs. The fruif is a capsufe, ovaf- befween fhe sfamens and sigma in fighf mode and shaped, 10–15 mm fong, green iniiaffy (Image 5a) and whife approaching fhe fowers and such an approaching bfack when ripe and dry (Image 5b). Dry fruifs spfif or behavior coufd make fhe buferfies capfure poffen onfo break info 2–4 fobes depending on fhe number of ovufes fheir wings as weff as fhe underside of fhe abdomen and ferifized, each wifh a fhick corky waff and a nuffef. Fruif evenfuaffy efecf poffinaion. Such confacfs were found dispersaf occurs from November-December. Birds such fo be refafed fo fhe pafh and posiion fhe buferfies as Acridofheres frisis (Indian Myna), Corvus spfendens fake fo access fhe fowers. In B. cinnara , fhe body fengfh (House Crow), Corvus macrorhynchos (Jungfe Crow) is shorf and ifs confacf wifh fhe sfamens and sigma and Turdoides caudafus (Common Babbfer) feed on fhe is rare whife approaching fhe fowers. Aff fhe fhree nuffefs and in fhe process disperse fhem fo diferenf buferfy species probed fhe fowers by insering fheir pfaces. Nuffefs germinafe during fhe rainy season soon proboscis info fhe fhroaf of fhe coroffa fube. Buf, fhe afer fhe irsf monsoon rains in June. coroffa fube fengfh was far in excess of fhe fengfh of fhe proboscis of fhese buferfies, fhus fowers in erecf or pariaffy erecf posiion deprived fhe foraging buferfies DISCUSSION of necfar. The buferfies however are successfuf in gaining access fo necfar in fhe hanging fowers in which Mangrove species are usuaffy cafegorized as fhe necfar reaches fhe mid-parf of fhe coroffa fube; such “excfusive” species fhaf are fimifed fo fhe mangrove fowers acquired fhis orienfaion due fo visifs fo fhem environmenf and “non-excfusive” species fhaf are previousfy by fhe bee, Xyfocopa pubescens . mainfy disfribufed in a ferresfriaf or aquaic habifaf buf afso occur in fhe mangrove ecosysfem. These non- Fruiing excfusive species are referred fo as semi-mangroves, Poffinafed and ferifized fowers iniiafe fruif back mangroves or mangrove associafes (Tomfinson devefopmenf immediafefy and fake 20–25 days fo 1986; Parani ef af. 1998; Lacerda ef af. 2002). In fhe

Journaf of Threafened Taxa | www.fhreafenedfaxa.org | 26 May 2016 | 8(5): 8777–8787 8783 Pollination ecology ofClerodendrum inerme Raju & Kumar case of Clerodendrum inerme, there is a controversy Yao-Wu et al. (2010) stated that an unusual with reference to its status as a constituent of mangrove pollination syndrome that prevents self-pollination exists forests. Parani et al. (1998) reported that it is a fringe in the genus Clerodendrum. This pollination syndrome species found abundantly both on the landward edge as is functional through dichogamy and herkogamy. The well as deep inside the mangrove environment. Saenger usual floral mechanism is that when the flower opens, (2002) considered it as a mangrove, but Satyanarayana the stamens stand erect, parallel to the central axis et al. (2002) did not consider it as a mangrove species. of the flower, while the style bends over, holding the Wang et al. (2011) reported that C. inerme behaves like stigma beyond the rim of the corolla. After the pollen both a true mangrove and a mangrove associate due is shed, the stamens curl up or bend over, and the style to its largest salinity tolerance. Nevertheless, in this straightens out, bringing the stigma to the center of study, C. inerme is considered as a mangrove associate. the flower. Such a movement and function of floral sex It is a shrub that occurs predominantly in the mangrove organs precludes self-pollination. Keng (1990) reported forests and along the coastlines. It is exposed to a wide that C. laevifolium is pollinated by insects such as bees range of fluctuations in salinity due to its occurrence in and butterflies. Reddy & Reddi (1995) reported that the landward sites as well as in the open sites within C. infortunatum with morning anthesis is exclusively the mangrove zonations at the study area. Therefore, it pollinated by papilionoid butterflies; the pollination plays an important role in the formation and stabilization occurs due to the striking of anthers and stigma with the of the forest floor due to its prolific growth. wings of butterflies. Such a form of pollination is referred C. inerme blooms during the rainy season and to as pterigotribic pollination. Meerabai (2014) reported produces typical 3-flowered cymes which are quite that the typical butterfly pollination C.in infortunatum is prominent and displayed well because of its white flowers because of non-promiscuity of floral rewards to other against the bright green foliage. Primack et al. (1981) foragers. She also noted that this pollination syndrome reported that this species produces 2–8 flowers in each is a necessary pre-condition for the rise of floral cyme and this report does not agree with the present isolating mechanism. Shamim et al. (2010) reported study indicating that each cyme is 3-flowered. Further, that C. viscosum is exclusively cross-pollinated by ants, these authors noted that the flowers in a cyme generally butterflies and hawk-moths. Rohitash & Jain (2010) remain at the same developmental stage, so that the noted that C. splendens is pollinated by Xylocopa sp., flowers in the same cyme are unlikely to pollinate each Eumenes sp. and Camponotous campestris. McMullen other. In the present study, it is found that the flowers (2011) reported that C. molle with night late evening within the cyme show different developmental stages, anthesis is pollinated by nocturnal and diurnal visitors. open whether on the same day or over a period of three Nocturnal visitors include ants, spiders, hawk-moth s, days at the most. This difference in developmental and roaches whereas diurnal visitors include carpenter stages of flower buds is most likely to pollinate each bees and ants. Sakamoto et al. (2012) reported that other if pollinators are available. Further, the cymes of C. trichotomum is pollinated by the carpenter bees, different branches of the same plant also show various Xylocopa species, the butterflies, Papilio species and developmental stages so that the cymes of the same the hawk-moth Macroglossum sp. Primack et al. (1981) plant pollinate each other through geitonogamy if there reported that C. inerme is never visited by daytime is pollinator activity. visitors but is visited by one large hawk-moth during The flowers open during the morning hours in the dusk hours. Clerodendrum infortunatum (Reddy & Reddi 1995) and C. inerme with evening anthesis, white long corolla during the late evening hours in C. molle in which the with hairy interior to exclude other insects and strong flowers are fragrant (McMullen 2011). In C. inerme, the fragrance appear to be adaptations for hawk-moth flowers are fragrant and open during the evening hours pollination (Primack et al. 1981). In the present study, as in C. molle. Primack et al. (1981) also reported that it is visited and pollinated by one large hawk-moth, the flowers are fragrant but they have not mentioned Macroglossum gyrans as soon the flowers are open the time of flower-opening. These authors stated that during the evening hours. It is a nectar feeder but the the calyx cup is covered with an irregular series of raised nectar in just open flowers is almost absent. The new elliptical glands which apparently function as extra- flowers take one to two hours to secrete nectar that floral nectaries and ants commonly feed on them. In the compels the hawk-moth to pay multiple visits to the new present study, C. inerme does not show such glands on as well as old flowers. The flowers opened one or two the calyx cup and also the ants do not visit the flowers. days before are nectar-rich and serve as the principal

8784 Journal of Threatened Taxa | www.threatenedtaxa.org | 26 May 2016 | 8(5): 8777–8787 Pollination ecology ofClerodendrum inerme Raju & Kumar nectar source for the visiting hawk-moths during the it does so at the base of the corolla tube. This is because evening hours. Further, the same hawk-moth is the first its light weight does not bring the flower to a hanging visitor to the flowers on the following day during the position when it lands. Therefore, the two bee species dawn hours by which time the flowers accumulate nectar are typical nectar robbers. Both the butterflies and in considerable amounts. The nectar is in considerable bees however contribute to sporadic pollination while volume, sucrose-rich with a sugar concentration of 13- approaching the flowers during which their wings and 21%, agrees with the report of Cruden et al. (1983). abdomen strike the anthers and style. Further, it is a source of certain essential and non- Nectar robbing is a behavior exhibited by some essential amino acids, and protein content. In the species of bees in which nectar is obtained through present study, the hawk-moth being a swift flier visits holes made by puncturing near the bases of the corolla numerous flowers on the same and different plants in tubes. Nectar robbers are subdivided into primary quick succession in order to quench its thirst for nectar nectar robbers which make the holes and then extract and in effect contributes to both self (geitonogamy) and the nectar and secondary nectar robbers which obtain cross-pollination. Primack et al. (1981) presumed that nectar by using holes made by primary robbers (Inouye the purple color of the filament and style presumably 1983). Carpenter bees are the most notorious primary make them difficult for the hawk-moth to see and nectar robbers (Barrows 1980), make perforations avoid. The versatile anthers with pollen in grooves, with their maxillae (Barrows 1976) and this method allow pollen to be placed precisely on the hawk-moth is probably used by all Xylocopa bees (van der Pijl proboscis. In the present study, Macroglossum gyrans 1954). These bees employ this method when they are approaches the flowers either laterally or from the front unable to access nectar and exists mostly in tubular through the stamens and stigma to insert its proboscis flowers (Barrows 1980). In the present study, species into the corolla tube to collect nectar. In this process, of Xylocopa and Anthophora are considered as primary its contact with the stamens and stigma are random but nectar robbers since they make holes on the corolla not with certainty and also there is no precise placement tube of C. inerme and secondary robbers of nectar are of pollen from the versatile anthers on the proboscis of absent. the moth. The pollen deposition largely occurs on the Nectar robbing is variously interpreted in relation wings and abdomen. Further, the production of a small to host fitness. It has positive or neutral or mutualistic quantity of pollen in individual flowers of C. inerme is effects on host fitness in terms of increase or decrease or another indication that it is adapted for nectar-feeding no effect in seed set rate (Zhang et al. 2009). The removal lepidopteran, in this case M. gyrans. Therefore, M. of floral nectar by robbers decreases the standing crop gyrans is to be considered as the principal pollinator of and in some cases changes the sugar concentration of C. inerme. nectar available to other pollinators (Pleasants 1983). C. inerme is, however, also visited by day-time visitors Longer pollinator flight distances generally translate such as butterflies and bees but their overall foraging into increased pollen flow and increased outcrossing activity is low and also is not consistent throughout rates (Fenster 1991). If nectar robbers are the cause the flowering period. The butterflies with their short of longer flight distances by the legitimate pollinators, proboscis are not capable of collecting nectar from the they could be increasing the fitness of the robbed long tubular corolla but they are successful in collecting plants by promoting outcrossing. The robbers could nectar from the flowers that were previously visited by then be considered as mutualists. Guitian et al. (1994) Xylocopa bees. Such flowers stay in a hanging position observed that nectar robbing by carpenter bees has a and the nectar is accumulated at the attachment positive effect on seed set in Pterocoptis grandiflora. point of staminal filaments covered by internal hairs. Zimmerman & Cook (1985) and Castro et al. (2008, The butterflies access this nectar with their proboscis 2009) stated that nectar robbing besides influencing without any difficulty. TheXylocopa bee makes a hole on host female fitness, could potentially enhance male the mid-part of the corolla tube where the epipetalous fitness and increase the offspring outcrossing rate by stamens take their origin, which are covered by short forcing legitimate pollinators to fly farther in search of hairs inside. When Xylocopa lands on the corolla tube, nectar, thus expanding the pollen dispersal distance the flower hangs downward and as a result, the nectar and neighbourhood size, and reducing geitonogamy. flows to the attached point of stamens; then thebee Nectar robbing by both Xylocopa and Anthophora collects nectar by making a hole on the corolla tube. The could potentially enhance male fitness by driving the Anthophora bee also makes a hole to collect nectar but legitimate pollinator,M. gyrans to fly farther and farther

Journal of Threatened Taxa | www.threatenedtaxa.org | 26 May 2016 | 8(5): 8777–8787 8785 Pollination ecology ofClerodendrum inerme Raju & Kumar in search of nectar. Such a foraging behavior by this in tidal water. As a result, certain floral mechanisms pollinator and expands the pollen dispersal distance and which promote out-crossing with its associated genetic promotes the out-crossing rate in C. inerme. advantages can be expected in established populations Primack et al. (1981) reported that C. inerme is (Primack et al. 1981). In C. inerme, the protandry strongly protandrous but did not explain how it works together with different positions of stamens and style in with reference to the movements of stamens and different sets of flowers would allow fruit set in isolated stigma within the flower. They have also not mentioned or congregated individuals while totally preventing whether there are different forms of flowers based on selfing within individual flowers. Such a dual breeding the position of stamens and style during the life of the system is advantageous for C. inerme to colonize new flower. In this study, three forms of flowers have been areas in mangrove and coastal areas and also the nearby distinguished with reference to the position of floral terrestrial habitats. The prolific growth ofC. inerme with sex organs. The first form is characterized by elongated its extensive root system in these areas is important to stamens and style which occur in close proximity to control land and beach erosion, and stabilize the forest each other just after anthesis; this facilitates contact floor. between the stamens and stigma. The second form is Wheeler et al. (1992) noted that fruit or seed characterized by the scattered position of stamens and dispersal in Clerodendrum genus happens through birds. style. In the third form, the stamens are fully extended Keng (1990) reported that birds are probably involved in while the style is curved away from them, either to dispersal of fruit or seed in C. laevifolium. Lorence and the left or to the right; subsequently the stamens curl Flynn (1997) stated that C. macrostegium is spread by inward and the style elongates. Interestingly, the three fruit eating birds. InC. inerme, the fruit is a capsule and flower forms can be found within a cyme also. Such breaks into different lobes depending on the number flower forms have been reported in C. molle (McMullen of nutlets produced inside. Each lobe contains a nutlet. 2011). These forms of flowers appear to have evolved Birds such as Acridotheres tristis, Corvus splendens, to prevent autonomous and facilitated selfing but C. macrorhynchos and Turdoides caudatus disperse certainly not geitonogamy. The strong protandry in C. nutlets or seeds in the study area, occur during the early inerme does not facilitate individual flowers from self- winter season. Seed germination occurs as soon as the pollinating but it facilitates different flowers on the same monsoon sets in during June. plant to pollinate each other through geitonogamy. This A few workers have reported that Clerodendrum is further substantiated by fruit set in geitonogamous species serve as larval hosts for lycaenid butterflies. pollinations. Although geitonogamy is self-fertilization, C. laevifolium is a larval host for Zelthus amasa in that the pollen fertilizing the ovules originates from maximinianus (Keng, 1990), C. glabrum for Hypolycaena the same parent plant, different parts of branches of philippus philippus (Ivor, 1994) and C. indicum for the plant may diverge genetically through somatic Spindasis vulcanus (Kunte, 2007). In the present study, mutation (Roubik 1995). Such a genetic divergence field observations indicated that C. inerme is another was experimentally proved in Byrsonima crassifolia in larval host for S. vulcanus. Therefore, Clerodendrum which one of five trees used in experiments was initially genus is probably the best larval host plant for found to be self-incompatible produced fruits through lycaenid butterflies. Further studies may provide more self-pollination when the flowering period was nearly information on other butterflies that use this plant over and in Pscidia carthagenensis in which one-day old species as a larval host. artificially self-pollinated flowers did not set fruit but 2-day old flowers set some fruits (Baker et al. 1983). In C. inerme, the protandry is functional partially since REFERENCES fruit set occurs through geitonogamy. The protandry function in this species is important as an out-breeding Baker, H.G., K.S. Bawa, G.W. Frankie & P.A. Opler (1983). 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